Parasitology

in Veterinary Medicine
 Parasitology
in Veterinary Medicine

Peter Deplazes
Johannes Eckert
Alexander Mathis
Georg von Samson-Himmelstjerna
Horst Zahner

Wageningen Academic
• Publishe rs
Authors

Pete r Deplazes, Professor Dr. med. vet., EVPC

Director, Institute of Parasitology
Vetsuisse Faculty and Medical Faculty, University of Zurich
Winterthurerstr. 266a, 8057 Zurich, Switzerland

Johannes Eckert, Emeritus, Prof. Dr. med. vet., Dr. h. c., EVPC
Institute of Parasitology
Vetsuisse Faculty and Medical Faculty, University of Zurich
Winterthurerstr. 266a, 8057 Zurich, Switzerland

Alexander Mathis, Professor Dr. sc nat ETH

Institute of Parasi_tology
Vetsuisse Faculty and Medical Faculty, University of Zurich
. Winterthurerstr. 266a, 8057 Zurich, Switzerland

Georg von Samson-Himmelstjerna, Professor Dr. med. vet., EVPC

Director, Institute of Parasitology and Tropical Veterinary Medicine
Department of Veterinary Medicine, Freie Universitat Berlin
Robert von Ostertag Str. 7-13, 14163 Berlin, Germany

Horst Zahner, Emeritus, Professor Dr. med. vet.

Institute of Parasitology
BFS - Biomedical Research Center Seltersberg, Justus Liebig University Giessen
Schubertstr. 81, 35392 Giessen, Germany

Graphics

Salome Ehrat (c/o IPZ), Marianne Mathys, Anne Seeger, Jeanne Peter and Sandra Amrein (VetCom, Vetsuisse
Faculty, Zurich, Switzerland)

Important note
The authors have made every effort to ensure that the information on control strategies and on the use of antiparasitic
drugs, including dosage and application forms. is in accordance with current knowledge and legal regulations,
but no liability can be accepted by the authors or the publisher. Therefore, every reader is encouraged to examine
carefully the leaflets accompanying each drug - possibly after consultation of n specialist - to determine whether
the dosage schedules recommended therein or contrnindications with respect to the indication differ. Special
attention must be payed to the legal regulations for the use of drugs in food-producing animals.
Preface
'Parasitology in Veterinary Medicine' is an updated
English version of the German textbook 'Lehrbuch der
Parasitologie fi.ir die Tiermedizin: published by Enke
Verlag(MVS Medizinverlage, Stuttgart) in three editions
(2005, 2008, 2013). The book was conceived and written
by a team of authors with J. Eckert, K.T. Friedhoff, H.
Zahner and P. Deplazes(1 st and 2nd ed.), and P. Deplazes,
J. Eckert, G. von Samson-Himmelstjerna and H. Zahner
(Yd ed.). Requests for an English version suggested to
translate and revise the book. For this project Alexander
Mathis was invited to join the team of authors. The
translation work has been generously supported by a
financial contribution from Bayer HealthCare Animal
Health.
In the authors' view the book is suited both for basic
and advanced studies and as reference source for the
veterinary practice. Although focused on the European
situation, the book also deals with important parasitic
diseases occurring in other regions.
The main part is organised by parasite groups(protozoa,
helminths, arthropods, etc.). It provides information
on the parasites' biology, epidemiology, immunology,
pathogenesis, clinical signs, diagnosis, therapy and
control. Summaries allow for a quick overview.
Another part is arranged according to animal species
(cattle, sheep and goats, pigs, horses, dogs and cats,
rabbits, poultry, bees). It contains tables listing the
parasites of the organ systems and showing antiparasitic
drugs. Furthermore, practical instructions on the
control of parasitic diseases are given. A list of trade
names of selected antiparasitics and vaccines should
help in practice to select suitable medicines for various
animal species. Since the trade names in the various
countries may be different, the data in this list are
to be considered only as examples. Registrations of
antiparasitics and vaccines and instructions on dosage
and applications may change over time. Therefore, the
user is requested to examine carefully the manufactures
leaflets accompanying each product.
Further chapters deal with general parasitology,
zoonoses, parasites in food, diagnostic procedures, and
essentials of therapy and control of important parasitoses.
A detailed glossary with etymological notes is intended
for a better understanding of parasitological terms. The
book contains numerous tables and is illustrated with
421 figures, including many instructive drawings of
parasite life cycles.
The authors would like to thank all colleagues and co­
workers for their contributions and support. Special
thanks go to Mrs. Esther Zi.ist (secretary, Institute of
Parasitology, Zi.irich), the editorial team of Wageningen
Academic Publishers, the graphic design staff of the
Vetsuisse Faculty Zi.irich, and the persons, institutions
or publishers who generously provided pictures and the
printing permission(► p. 633).
Zi.irich, Berlin, Giessen - February 2016
Peter Deplazes
Johannes Eckert
Alexander Mathis
Georg von Samson-Hi1mnelstjerria
Horst Zahner
 Table of contents

Preface....................•. 7

Abbreviations, symbols and country indicators ... 12

PART I.
GENERAL PARASITOLOGY . 15

1. Parasite-host relationships 16 1.4 Parasite-host relationships 21

1.1 Parasitism and other lnterspecific relationships 16 1.4.1 Host-finding 21
1.2 Parasites and their properties 17 1.4.2 Infection and infestation 22
1.2 .1 Origin of the term 'parasite' 17 1.4.3 Development of parasites in or on a host 22
.
1 .2 2 Medically Important groups of parasites 17 1.4.4 Pathogenicity, virulence and adverse effects
1.. 2 3 Nomenclature , taxonomy and systematics of of parasites 24
parasites 17 1.5 Immunology of parasitoses 25
1.2.4 Evolution of parasitism 8
1 1.5.1 Innate and adaptive immunity 25
.
1 .
2 5 Genes and genomes of parasites 19 1.5.2 Parasite antigens 30
1.2.6 Categories of parasites 19 1.5.3 Immune effector mechanisms against parasites 30
1.2.7 Properties of parasites 19 1.5.4 Immune evasion strategies of parasites 36
1.3 Hosts and their properties 20 .
1 .
5 5 lmmunopathology of parasitic infections 39
1.6 Parasitoses: general aspects 40

PART II.
PARASITES AND PARASITOSES: P ROTOZOA .........43

Protozoa.......... . .. 44

2. Phylum Metamonada 47 5.2 Class Haematozoea 127

2.1 Class Trepomonadea 47 5..1
2 Order Haemosporida 127
2.1.1 Order Diplomonadida 47 Family Plasmodiidae 127
Family Hexamltidae 47 .
5 2.2 Order Piroplasmlda 129
Family Babesiidae 1 29
3. Phylum Parabasala 52 Family Thelleriidae 140
3.1 Class Trichomonadea 52 - Subphylum Ciliophora 147
3.1.1 Order Trichomonadida 52 5.3 Classes Lltostomatea and Oligoh ·,phorea 147
Family Monocercomonadidae 52 5.3.1 Orders Vestlbuliferida and others 147
Family Trichomonadidae 54 Family Balantidiidae 147
Family Pycnotrichidae 149
4. Phylum Euglenozoa 59 Families lchthyophthiriidae and Ch Jae 149
- Subphylum Klnetoplasta 59 .
5 .
3 2 Orders Sessilida and Mobilida 150
4.1 Class Kinetoplastea 59 Families Epistyiidae and Trichodin:u 150
4.1.1 Order Trypanosomatida 59
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Family Trypanosomatidae 59 6. Phyla Amoebozoa and Perco.
.
4 .1 2 Order Bodonida 78 151
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Family Bodonidae 78 6.1 Classes Entamoebidea, Lobosea and
Heterolobosea 151
� 5. Phylum Alveolata 79 6.1.1 Order Entamoebida 151
co - Subphylum Apicomplexa 79 Family Entamoebidae 151
C
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Q) 5.1 Class Coccidea 79 6.1.2 Order Centramoebida and other orders 153
5.1.1 Order Adeleida 81 Family Acanthamoel:lidae and other families 153
C Family Hepatozoidae 81
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Further families of the order Adeleida 82 7. Phylum Microsporidia (syn. Microspora) 155
0 5.1.2 Order Eimeriida 82 7.1 Class Microsporea 155
Family Eimeriidae 82 7..1 1 Order Microsporida 155
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co Family Sarcocystidae 98 Family Nosematidae 157
co 160
n. 5.1.3 Order Cryptosporlda 122 Family Pleistophoridae
Family Cryptosporldiidae 122
 Table of con1ents

PART Ill.
PARASITES AND PARASITOSES: METAZOA. 163

8. Phylum Myxozoa 164 8.1.2 Order Malacovalvulida 167

8.1 Classes Myxosporea and Malacosporea 164 8.1.3 Order Multlvalvulida 168
8.1.1 Order Bivalvulida 165

Helminths ..... . . 169

9. Phylum Platyhelminthes (flatworms) 173 Family Molineidae 302

- Subphylum Trematode (flukes) 173 Families Amidostomaticfae and Omithostrongyfidae 303
9.1 Class Olgenea 173 Family Dlctyocaulidae 303
9.1.1 Order Echlnostomlda 175 ■ Superfamily Metastrongyfoidea 312
Family Fasciolldae 175 Family Metastrongyfidae 312
Family Echlnostomatldae 186 Family Protostrongyfidae 313
9.1.2 Order Amphlstomlda 188 Family Crenosomatidae 318
Family Paramphlstomldae 189 Family Anglostrongyfidae 320
9.1.3 Order Plaglorchllda 191 Family Fllaroldidae 324
Family Dlcrocoellidae 191 10.1.3 Order Ascarldlda 326
9.1.4 Order Oplsthorchllda 197 ■ Superfamlly Ascaridoidea 326
Family Oplsthorchlidae 197 Family Ascarididae 327
Family Heterophyldae 199 Family Anisakldae 339
9.1.5 Order Strlgeatida 200 ■ Supertamily Heterakoidea 341
Family Strigeidae 200 Family Heterakidae 341
Family Diplostomidae 200 Family Ascaridildae 342
Family Schistosomatidae 201 10.1.4 Order Oxyurida 343
9.2 Class Monogena 205 Family Oxyuridae 343
9.3 Class Cestoda 206 10.1.5 Order Spirurida 346
Subclass Eucestoda 206 - Suborder Camallanina 346
9.3.1 Order Pseudophylllda 208 - Suborder Splrurina 346
Family Diphyllobothriidae 208 ■ Superfamily T helazloidea 346
9.3.2 Order Cyclophyllida 212 Family Thelazlldae 346
Famlly Mesocestoldidae 213 ■ Superfamily Spiruroidea 349
Family Anoplocephalidae 215 Family Spirocercidae 349
Families Davalneidae, Dilepididae and ■ Superfamlly Habronematoidea 349
Hymenolepldidae 220 Family Habronemalldae 349
Family Dlpylidiidae 222 ■ Superfamily Filarioldea 352
Family Taenildae 224 Family Filarlldae 353
Family Onchocercidae 357
10. Phylum Nematoda (syn. Nematozoa) 10.2 Class Adenophorea (Aphasmidia) 368
(threadworms or roundworms) 254 10.2.1 Order Enopllda 368
10.1 Class Secernentea 258 ■ Superfamily Trlchineiloidea 368
10.1.1 Order Ahabdltlda 258 Famlly Trlchuridae 368
Family Strongyloldldae 259 Family Trichinellidae 376
Families Rhabdltidae and Cephalobidae 263 ■ Superfamily Dioctophymatoidea 383
10.1.2 Order Strongylida 264 Family Dioctophymatidae 383
■ Superfamily Strongyloidea 264
Family Strongylidae 264 11. Phylum Acanthocephala (thorny- ·u
Family Chabertiidae 275 headed or spiny-headed worms) 384 Q)

Family Syngamidae 278 �

■ Superfamily Ancylostomatoidea 280 12. Phylum Annelida (segmented worms) 387
Family Ancylostomatidae 280 ·.::
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■ Superfamily Trichostrongyloidea 287 13. Phylum Pentastomida (incertae sedis)
Family Trichostrongylidae 287 (so-called tongue worms) �
389
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 Table of contents

14. Phylum Arthropoda (arthropods) 392 Family Psoroptidae 435

- Subphylum Amandibulata 395 Family Sarcoptidae 442
14.1 Class Arachnida 395 Other families of the order Astigmata 448
Subclass Acari (mites s.1.) 395 - Subphylum Mandibulata 449
14.1.1 Order Metastigmata (lxodida, ticks) 396 14.2 Class Crustacea (crustaceans) 449
Family lxodidae 399 14.3 Class Insects (insects) 449
Family Argasidae 415 14.3.1 Order Blattaria (cockroaches) 449
■ Subfamily Ornithodorinae 418 14.3.2 Order Phthiraptera 450
14.1.2 Order Mesostigmata (syn. Gamasida) 420 14.3.3 Order Heteroptera (true bugs) 457
Family Dermanyssidae 420 14.3.4 Order Coleoptera (beetles) 457
Family Macronyssldae 422 14.3.5 Order Diptera (flies) 458
Family Halarachnidae 423 .· Suborder Nematocera ('thread-horn flies') 458
Family Rhinonyssidae 424 Family Culicldae 459
Family Laelaptidae 424 Family Psychodidae 463
Family Varroidae 424 Family Simuliidae 465
14.1.3 Order Prostlgmata (syn. Trombldlformes) 426 Family Ceratopogonidae 469
Family Demodicidae 426 c::.1 Suborder Brachycera ('short-horn flies') 472
Family Cheyletiellidae 430 Family Tabanidae 472
Family Syringophilidae 431 Family Braulldae and Drosophilidae 474
Family Tromblculidae 431 Family Muscidae and Fanniidae 475
Family Psorergatldae 433 Family Glosslnidae 481
Family Myoblidae 433 Families Calliphoridae and Sarcophagidae 483
Family Pyemotidae 433 Family Oestridae 489
Family Tarsonemidae 434 Family Hippoboscidae 498
14.1.4 Order Astigmata (Sarcoptiformes) 435 14.3.6 Order Siphonaptera (fleas) 500

PART IV.
ZOONOSES AND PARASITES IN FOOD. . .. 507
15. Zoonoses and parasites in food 508
15.1 Zoonoses 508
15.2 Parasites in food 515

PART V.
DIAGNOSTICS . . . . . . . . . . . . . . . . . . . 519

16. Diagnostics 520 16.1.7 Examination of environmental san- 536

16.1 Laboratory procedures 520 16.1.8 Preservation of helmlnths and arth,, 536
16.1.1 Introduction 520 16.2 Diagnostic plates 538
16.1.2 Diagnostic samples 521 16.2 .1 Ruminants 538
16.1.3 Diagnostic laboratories 521 16.2.2 Equldae 544
16.1.4 Procedures for intravital parasite detection 521 16.2.3 Pig 547
16.1.5 Methods for post mortem parasite detection 533 16.2.4 Dog and cat 548
16.1.6 Hints for microscopic identification of 16.2.5 Poultry 551
parasite stages 536 16.2.6 Characteristics of tick genera 552
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 Table of contents

PART VI.
PRINCIPLES OF THERAPY AND CONTROL OF PARASITOSES . 555

17. Therapy 556 18. Control 566

17.1 Categories of therapy 556 8
1 .1 Control methods 566
17.2 Antiparasitic drugs 556 18.1.1 Technical and operational control methods 566
7
1 .2.1 Use of antiparasitics 557 8
1 .1.2 Legal and regulatory measures 566
17.2.2 Chemical groups of antiparasitic drugs 557 8
1 .1.3 Physical measures 566
1 .3
7 Drug resistance 563 8
1 .1.4 Use of antlparasitics 566
8
1 .1.5 Biological parasite control 566
8
1 .1.6 Immunological control of parasites 567
8
1 .1.7 Sterilisation and disinfection 571
18.2 Control strategies 572

PART VII.
PARASITOSES OF DIFFERENT ANIMAL SPECIES AND ORGAN SYSTEMS, ANTIPARASITIC
DRUGS AND STRATEGIC CONTROL . . . • I • ♦ t • t • • • • o • o t • t • • • • • • • • • o o
. 575

19. Parasitoses of different animal species 9

1 .4.1 Parasltoses of organ systems, antiparasitics
and organ systems, antiparasitic drugs and vaccines 597
and strategic control 576 9
1 .4.2 Strategic control of Important parasitoses of
19.1 Parasitoses of cattle, sheep and goats 576 dogs and cats 599
9
1 .1.1 Parasitoses of organ systems and antiparasitics 576 9
1 .4.3 Parasitoses and companion animal travel 606
9
1 .1.2 Strategic control of important parasitoses of 19.5 Parasitoses of rabbits 607
cattle 576 19.6 Parasitoses of poultry 608
9
1 .1.3 Strategic control of important parasitoses of 9
1 .6.1 Parasitoses of organ systems, antiparasitics
sheep and goats 584 and vaccines 608
19.2 Parasitoses of pigs 587 19.6.2 Strategic control of important parasitoses of
9
1 .2.1 Parasitoses of organ systems and antiparasitics 587 poultry 610
91 .2.2 Strategic control of important parasitoses of pigs 587 19.7 Parasitoses of the honey bee 612
19.3 Parasitoses of horses 590
19.3.1 Parasitoses of organ systems and antiparasitics 590 20. Trade names of antiparasitics and
9
1 .3.2 Strategic control of Important parasitoses of vaccines 615
the horse 590 Antlparasitics (endo-, ecto- and
9
1 .3.3 Export and import of horses 597 endectoparasitics) 615
19.4 Parasitoses of dogs and cats 597 Vaccines 617

PART VIII.
APP ENDIX. 619

21. Glossary ..... . 620

22. Graphics and sources of pictures 0 0 t O I O O O O O O O O I O I O t O O O O o o O o o O o 0

633

23. Index ............. • • • .............................. 634

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Abbreviations, symbols and country indicators

Abbreviations GM-CF Grnnuloq1t'•macrophage colony-

stimulating factor
Art. Tc Activatt'd T c-dl GPS Global positioning s tcm
A DO Antihiod)'·d�ndt'nl cl'll-mcdta1f!'J h Hour
C)'tuto..•dcit)1 H&E Ha,matoxylin & co in htalnin�J
� AnUgc.-n IFAT lndirecl Ouorescent antibody lMI
ALT Alan,lnr aminolramfel'Ut' IFN lnttrferon
AP Anligl'n-ptt$entlng cdl lg lmmunoglobu.lin
AR Anthdmintlc re�i,tanct IC lmmunochromatogruph)'
A.!ff A!p.1r1at"£ amlno1r.1niftra� It lnterltukin
BAL Broncho.ih-oolar hwagt i.rn. 1ntnunuscular
b.w. Bod)• Wt'lglu IP8 Institute or P-11rasitology. Bern/
8Z llenz.lmilt.uolt Swlt1.erland
Complement IPG In titule of Panisitology, fiits�tnl
CAPC Companlo . n Aulmal l.'al'll!ihc Council Gcrmiln)'
D lus,�r of JlfTcrenH111iun/dc1trmlnaot ll'H In litut, of PuraJilolngy. llannovc,/
T
CF Complement Oxatlon le.l Cernumy
Crcathw kinase l l'TVB Institute or P11rnsltology and Trorical
•type lec-lln re,cptor Vc:terlmuy Mvc.Jlc-inc:. Berlin/Getman;
entnil nervous i)!Slem IPZ Institute o( Para�li-ology. ZOrl h/
Ccrcbrosplnal fluid Swlt1.crlnnd
Ct,mputitd tomography ITS Internal trnmcribed spacer
C}'lotoxk lymphocytes i.v. Intravenous
Day kbp Kllobasc pairs
Da Dalton L Latin
DALY Disability adjusted life year Ll, L2, etc. Larva 1, Larva 2 ( I", 2nJ larval Jlaf,f of
DNA Deoxyribonucleic acid helminths or arthropods)
DR Drug resistance LAMP Loop-mediated isothermal amplifica.tion
ECG Electrocardiogramme LCS Liquor cerebrospinalis
EDTA Ethylene diamine tetraacetk acid LOH Lactate dehydrogenasc
e.g. For example (lat.: exempli gratia) LDT Larval development test
EHEC Enterohaemorrhagic Escherichia coli LMT Larval migration test
EHT Egg hatch test Lpg Larvae per gram (of faeces)
EFSA European Food Safety Authority MALDl-
ELISA Enzyme•linked immunosorbent assay TOF MS Matrix-assisted laser desorption/
EM Electron microscopy ionisation time of flight mass
EMA European Medicines Agency spectrometry
EPEC Enteropathogenlc Escherichia coli Mbp Mega base pairs (one million bast pairsJ
Epg Eggs per gram MHC Mayor histocompatibility complex
E/S antigen Excretory/secretory antigen ML Macrocydic lactones
ESCCAP European Scienllfic Counsel Companion MPS Mononuclear phagocytic system
(I)
Animal Parasites n Number, e.g. number of animals
C ETEC Enterotoxic Eschericllla coli NET Neutrophil extracellular trap
·t5
FAD Flea allergy dermatitis NG Neutrophil granulocyte
(l)
� FAMACHA ► Glossary, p. 620 NK cells Natural killer cells
cro FAO Food and Agriculture Organization NLR Nucleotide-binding oligomerisation
FECRT Faecal egg count reduction test domain like receptors
·c
xg Gravitational force (at centrifugalion) OIE Office InternationaJ des Epiiooties ( =
G Greek World Organisation for Animal Health)
.6 GABA Gamma-aminobutyric acid Opg Oocysts per gram
GALT Gut associated lymphoid tissue PAM Pathogen associated molecular patterns
GGT Gamm1:1•glutamyl transferase PAS Periodic acid-Schiff reaction
GIN Gastrointestinal nematodes PCR Polymerase chain reaction
·GLQH Glutamate dehydrogenase PG Prostaglandin
p.l. Post infectiollf'.till
 Abbrev1allons. symbols and country indicators

Country indicators 1

pl. Plural EU European Union

p.o. Per os AL Albania
ppm Parts per million = mg/kg, e.g. mg drug/ AT Austria
kg feedstuff AU Australia
PRR Pattern recognition receptors BA Bosnia-Herzegovina
PV Parasitophorous vacuole BE Belgium
qPCR Quantitative PCR ( ► PCR) BG Bulgaria
r.h. Relative humidity BY Belarus
RNA Ribonucleic acid CA Canada
SAFC Sodium acetate-acetic acid-formalin- CH Switzerland
concentration CY Cyprus
s.c. Subcutaneous CZ Czech Republic
SEM Scanning electron microscopy DE Germany
sG Specific gravity (of flotation solutions) DK Denmark
SI Safety index EE Estonia
sgl. Singular ES Spain
s.l. Sensu lato, in a broader sense Fl Finland
SNOPAD Standardised Nomenclature of Parasitic FR France
Diseases GR Greece
sp. (spp.) Species (plural) HR Croatia
SPF Specific pathogen free HU Hungary
ssp. (sspp.) Subspecies (plural) IE Ireland
S.S. Sensu stricto, in a narrow sense IS Iceland
St. 5 5 th stage = preadult stage of nematodes IT Italy
syn. Synonym LI Liechtenstein
Tc Cytotoxic T cell LT Lithuania
TEM Transmission electron microscopy LV Latvia
TGF Transforming growth factor LU Luxembourg
Th T helper cell MD Moldova
TLR Toll-like receptor ME Montenegro
TNF Tumour necrosis factor MK Macedonia
TReg Regulatory T cell NL The Netherlands
TT Targeted treatment NO Norway
TST Targeted selective treatment PL Poland
UN United Nations PT Portugal
us Ultrasonography RO Romania
var. Varietas RS Serbia
VCAM Vascular cell adhesive molecule RU Russian Federation
VSA Variable surface antigen SE Sweden
VSG Variable surface glycoprotein SI Slovenia
WAAVP World Association for the Advancement SK Slovakia
of Veterinary Parasitology TR Turkey
WB Western blot UA Ukraine Q)
C
WHO World Health Organization UK United Kingdom ·c3
'5
USA United States of America Q)

Symbols
cu
C
Females ·;:::

aa
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Males
Symbol for zoonotic significance of a _s;
parasite species or groups of parasites >.
0)
comprising such agents 0
0
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1 Source: ISO (International Organization of Standardization)
cu
3166-1, except USA. Q_
 1. Parasite-host relationships
A parasite is an organism that lives in a more or less
close association with an organism of another species
(the host), derives sustenance from it and is pathogenic,
although this potential is not always expressed. In a wider
sense, the term 'parasite' refers to all organisms with
such characteristics (bacteria, protozoa, fungi, animals).
However, in the medical field, this term is traditionally
used in a narrower sense and designates eukaryotic
organisms belonging to the Protozoa and Metazoa
( ► Table 1.1 ). The pathogenic potential discriminates
parasites from partners in other biocoenoses, such as
commensalism, mutualism and symbiosis ( ► Glossary,
p. 620). In veterinary and human medicine, parasitology
relates to infectious diseases, together with virology,
bacteriology and mycology.
Parasites are causative agents of infectious diseases
in humans, such as malaria, sleeping sickness,
toxoplasmosis, schistosomosis or echinococcosis.
Also, domestic and wild animals are often infected with
parasites that can cause impairment of performance,
other adverse effects, diseases and death. Therefore,
parasites are of worldwide importance for animal
husbandry i n addition to veterinary and human
medicine as:
• causative agents of diseases of the skin and internal
organs in all groups of animals that are under the
care of humans (cattle, sheep, goats, pigs, poultry,
other livestock, horses, small animals, pet animals,
laboratory animals, zoo animals, wild animals, fish,
bees);
• vectors of infectious agents (viruses, bacteria,
protozoa, helminths};
• causative agents of zoonoses (diseases whose
causative agents are naturally transmitted between
vertebrate animals and humans};
• problems in food hygiene (human and animal
pathogenic or nauseating parasites in food of animal
origin);
• pathogens to be considered in trade (import or
export) of animals and animal products;
• factors in animal welfare, since parasites can cause
(l)
C annoyance and suffering of animals;
·c3 • economic factors, because parasites can cause
'6
(l) significant losses in animal production (impaired
�
performance, diseases, etc.) worldwide, and incur
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high costs for control of parasitic diseases. In areas
·;::
(l)
with favourable conditions for parasite develop­
ment and transmission (e.g. in the tropics) or
-� with inadequate food supply for animals (e.g. arid
>- regions), parasites may particularly affect animal
0)
0 husbandry.
0
·wco In veterinary education, parasitology focuses on
co problems caused by parasitic diseases, their diagnosis
0..
and control. However, the study of parasitology also
offers fascinating insights into the widespread biological
phenomenon of'parasitism' with its complex interactions
between parasite, host and the environment.
1.1 Parasitism and other
interspecific relationships
Summary
• A parasite Is an organism that lives on or in an organism
of another species (the host), derives sustenance from
It and Is pathogenic, although the pathogenic potential
Is not always expressed.
• In the medical field the term 'parasite' is restricted to
eukaryotic organisms belonging to the Protozoa
(unicellular organisms) and Metazoa (Animalia).
Parasites are divided into different categories, e.g.
ectoparasites or endoparasites.
• Parasites, originally derived from free-living ancestors,
have special features due to adaptations to the
parasitic life, including specialised morphological
structures and metabolic pathways, often high
reproductive rates and large population densities, as
well as specialisation to life in certain host species
(host specificity) and their organ systems (skin, blood,
respiratory tract, intestine, etc.).
• In their mostly complex life cycles, parasites occur
in various stages with different characteristics. These
stages are often exposed to extremely diverse living
conditions inside or outside the hosts. The life cycles
may be associated with one or several changes of
hosts and with alternations of sexual and asexual
reproduction (alternation of generations).
• Pathogenesis of parasitic diseases Is characterised
by parasite-related factors (Including cell and tissue
damage, withdrawal of substrates, Influences on
host metabolism, etc.) and by host-related reactions
Qnflammatlon, Immune defence, lmmunopathology).
Every organism interacts with its environment and with
individuals of the same species (autecology). In addition,
there are relationships between different species of
organisms (synecology), including certain forms of life
which are characterised by physical contact between
dissimilar partners (biosystems). Commensalism is a
biosystem in which a guest (commensal) benefits from
the host without harming it. In mutualism dissimilar
organisms live together (mutualist and host) to their
common advantage, but without interdependence.
Symbiosis is a relationship between organisms of
different species (symbiont and host) in which both
partners complement each other physiologically and are
interdependent. Parasitism is characterised by the fact
that parasites do not kill their hosts (at least not directly},
but they can significantly affect vital functions of hosts
and cause diseases and deaths. Further biosystems are
parasitoidism (predatory parasitism) and predation

(► Glossary, p. 620). A clear distinction of certain
biological systems, especially of commensalism and
parasitism, is often not possible because there are
indistinct transitions, and the win-loss balance from
the partnership cannot always be determined.
From an ecological perspective it should be emphasised
that although parasites live at the expense of their
hosts, they do not usually jeopardise their host animal
population under natural conditions. This is due to the
ecological host-parasite balance which has developed
during evolution. As a result of human interference
with the ecosystem, for example habitat changes of wild
animals or certain forms of livestock husbandry, these
equilibria can shift in favour of the parasites, resulting
in illness and death of the host animals.
1.2 Parasites and their properties
1.2.1 Origin of the term 'parasite'
The term 'parasite' is derived from the Greek word
parasitos [para: beside; sitos: food] meaning a person
who eats at the table of another. Originally, people who
participated as officials in ritual meals for deities were
called parasites. Later, people were assigned this term
if they were associated with rich nobles and - invited
or uninvited - procured access to the table societies
and tried by flattery and buffoonery to get something
from the table. This type then found its way into Greek
comedy. The term 'parasite' in a scientific context has
been used since the middle of the 17 th century.
1.2.2 Medically important groups of
parasites
Parasites, important in veterinary and human medicine
as pathogens or vectors of pathogens, belong to different
groups of the Eukaryota, which are listed in ► Table
I. I. The classification and ranking shown in the table is
simplified and conservative; a new classification, based
on phylogenetic relatedness, has recently been proposed
(► Adi et al. 2012, p. 41).
1.2.3 Nomenclature, taxonomy and
systematics of parasites
Nomenclature is concerned with naming of organisms
which is governed by internationally agreed codes of
rules (International Code of Zoological Nomenclature).
They prescribe a binominal name for every living
being (binomial or binary nomenclature), of which
the first denotes the genus and the second the species,
e.g. Fascia/a hepatica. The higher systematic categories
(genus, family, order, etc.) are uninominal, e.g. genus
Fasciola, family Fasciolidae. According to the rules of
nomenclature, names of a genus or species may not be
connected by a h yphen, not even in compound words.
I Parasite-host relationships
Table 1.1. Important groups of parasites.
Subregnum 1 Phylum
Protozoa2 Metamonada, Parabasala, Euglenozoa,
Percolozoa, Alveolata, Amoebozoa,
Mlcrospora3
Metazoa Myxozoa
(Animalia, Helminths2 :
(.)
C
animals) - Platyhelmintha (flatworms) (I)
E
- Nematoda (round- or threadworms) 0
- Acanthocephala (thorny-headed worms) z
Annelida 0ointed worms)
Arthropoda, including Pentastomida (so-
called linguatulids)
1 Lalin names of the taxa ► Table 1.2.
2 Collective name without phylogenetic significance ► p. 169.
3 Uncertain taxonomic position as there are relationships with fungi.
Wrong: Fasciola-hepatica infection; right: Fasciola
hepatica infection.
Based on their (genetic) relationship and common
characteristics, species of living organisms are merged
into genera or higher groups (categories), which are
referred to as taxa (singular: taxon). Accordingly,
taxonomy is the science that deals with the classification
of organisms.
As shown in ► Table 1.2, some taxa can be recognised
by the ending of the taxon.
Systematics describes peculiarities and characteristics
of organisms; it characterises species and examines the
phylogenetic relationships between different species.
Today, genomic analyses provide valuable information
in this respect. According to the classical definition, a
species is characterised by the fact that individuals form
a reproductive community. However, this is hard to
verify in some of the parasites, e.g. in parasitic protozoa
or helminths. Therefore, genetic features are increasingly
used besides morphological and biological criteria to
characterise a species. However, genetic analyses are only
suitable for characterising a new species if significant
special features in the genome are identified. A species
can comprise several variants, called strains, having
specific characteristics and properties. Variants with
distinct genetic features are referred to as genotypes
(► Glossary, p. 620).
New knowledge, especially in the genetic studies of
relationships between living organisms, and existing
or newly emerging ambiguities often lead to changes
in systematics and taxonomic classification. As a result,
different classification systems of parasites can be found
in the international literature. This textbook contains
selective and simplified taxonomic compilations (for
more information, see Adi et al., 2012, and further
specialised literature).
 Part I. General parasitology

Table 1.2. Taxonomic categories for classification of living organisms.

... -- ., .. .,,;::.,,:, '•·
-, ., - --
�categories 'l1E�dlng Sub- or. supercategor,ies Ending

Regnum -a subregnum -a
Phylum -a subphylum -a
- --'
Classis -ea, -a superclassis -a
·-
subclassis -ia
-- ---
Ordo -ida, -a superordo -idea
subordo -ina
-
Familia -idae superfamilia -oidea
-
subfamilia -inae
Genus see 1 subgenus see 1
Species see1 subspecies see 1
1 Names of species and genera are determined and fixed by internationally agreed codes of binominal nomenclature. Distinct endings are
prescribed internationally for the taxa subfamilia, familia and superfamllia. There are no international rules regarding all the other taxa. In
this book the endings listed in the table are used, except some traditionally accepted endings,

1.2.4 Evolution of parasitism evolved in various groups of eukaryotes during different

Parasitism is a common life style of eukaryotic
organisms (protozoa, fungi, plants, animals). Currently,
approximately 1.8 million eukaryotic species are
described; about 30% have adopted a parasitic life style.
The number of actually existing, not yet identified species
is estimated at 3-30 million. Protozoans and metazoans,
which are of interest in this textbook, comprise different
proportions of parasites, as exemplified by the following
data (approximate number of species in parentheses):
insects 39% (about 950,000 to 1 million), Arachnida 17%
(75,000), Nematoda 60% {26,646), Trematoda (Digenea)
100% (18,000), Cestoda 100% (5,000), Alveolata 40%
(17,050) and Kinetoplastida 97% (600). Parasites have
periods of the earth's history. Thus, free-living organisms
or their developmental stages have passed to various
forms of parasitism ( ► Table 1.3). In the course of
their joint evolution (co-evolution), hosts and their
parasites have adapted to each other to some degree.
In advanced phases of co-evolution, a balance can be
reached that ensures survival and reproduction of the
parasite without significant adverse effects to the host.
On earth, which is approximately 4.5 billion years old,
prokaryotes emerged as the first living beings about
3-3.5 billion years ago, and unicellular eukaryotes 2-2.5
billion years ago. In the Proterozoic Eon (beginning 2.5
billion years ago) and the Cambrian period (beginning

Table 1.3. Important categories of parasites.

Site on or In a host ectoparasltes parasites living on or In the skin or in cavities directly connected
with the external environment (e.g. external auditory canal, gills
of fish)
endo arasltes parasites of Internal or ans of a host
Organ localisation on or In a parasites of skin, distinct organs, tissues and blood
host
Degree of dependence from organisms depending on their host
Q)
T5
C host facultatlve parasites organisms living only occasionally as parasites
opportunistic parasites organisms which infecVinfest a host under favourable conditions
(e.g. impaired immune defence), possibly causing damage
� Duration of host contact temporary parasites parasites living only a short period on or in a host
co
-
C stationary parasites
·;;:: parasites living all the time on or in a host
Parasitic phases In life cycle permanent parasites all developmental stages are parasitic
periodic parasites only certain stages are parasitic
-�
Host spectrum monoxenic parasites parasites with one obligatory host species

-
>,

0 heteroxenic parasites parasites able to use several obligatory host species

0
'in Host range narrow host range
co broad host range

545 million years ago), numerous species of multicellular
organisms evolved. This period is associated with the
first appearance of protozoa (- 750 million), flatworms
(- 570 million), arachnids (- 530 million) and insects
(- 400 million). Some molecular datings place the
development of arthropods earlier (about 720 million
years).
Palaeoparasitological findings document that parasitic
forms of life developed early in the course of the history
of the earth, as indicated by some examples: fossil
pentastomids, approximately 500 million years old from
the Cambrian, show body structures exhibiting a high
degree of adaptation to parasitism with great similarities
to structures of recent endoparasitic pentastomids. In
amber from the Cretaceous period (- 65 to 145 miUion),
well-preserved inclusions were found, for example, of a
larva of a hard tick (identified as genus Amblyomma),
numerous blood-feeding sandflies and a larva of a
parasitic nematode (Mermithidae), which emerges from
the abdomen of a non-biting midge (Chironomidae).
Even nematophagous fungi ( ► p. 567), together with
their prey (small nematodes), were preserved for
posterity in about 100 million-year-old amber. Ascaris
eggs were found in about 30,000 year-old sediments in a
cave in France; Egyptian mummies of different dynasties
contained eggs of schistosomes, a Taenia species or
other parasites (e.g. Dracunculus, Ascaris). A more
recent example is the finding of Trichuris eggs in a 3,300
year-old glacier mummy (known as 'Otzi'), detected
in 1991 in the Otztal Alps (South Tyrol, Italy). This
and many other findings demonstrate that humans and
animals were already infected or infested with parasites
in ancient times.
1.2.5 Genes and genomes of
parasites
Compared to the prokaryotic bacteria, most eukaryotic
parasites have larger genomes, as shown by the following
examples (haploid genome sizes in millions of base pairs
[Mbp]): bacteria: Escherichia coli: 4.2; Protozoa: Giardia
duodenalis: 11.7; Trypanosoma brucei: 25; 1bxoplasma
gondii: 87; Babesia bovis: 9.4; Metazoa: Schistosoma
mansoni (Trematoda): 270; Echinococcus granulosus
(Cestodea): 150; Haemonchus contortus (Nematoda):
50; Onchocerca volvulus (Nematoda): 150; Anopheles
gambiae (Insecta): 280; for comparison mouse: 2,700.
The free-living nematode Caenorhabditis elegans plays
a special role as a model organism in genetic research. It
has six chromosomes, about 19,000 genes and a genome
of 97 Mbp, and exhibits many morphological and
biological similarities with parasitic nematodes. Today,
genetics, genomics and molecular biology play an
important role in many areas of parasitology, including
molecular phylogeny, pathogenesis (parasite-host
interactions), immunology (e.g. identification antigen
coding genes and genetic engineering of antigens for
vaccine production), in diagnos tics (e.g. PCR, DNA
1 . Parasite-host relationships
sequence analysis) and epidemiology (e.g. genetic
characterisation of parasite and host populations or
detection of parasite stages in the environment).
1.2.6 Categories of parasites
Cl)
Parasites are allocated to different categories, based on Q)
certain criteria ( ► Table 1.3). Pseudoparasites are free­
tQ)
Q.
living organisms which are randomly associated with a 0
host. Examples are non-parasitic insects that have been 0...
caught in the coat of animals, or larvae of flies which
were accidentally ingested by a host and are excreted
unchanged in the faeces.
1.2.7 Properties of parasites
Parasites have characteristics that distinguish them more
or less from free-living organisms, depending on the
degree of their adaptation to parasitic life. Some of these
properties are mentioned here.
Adaptations of structures. Structural adaptations
are manifested in metazoan parasites (helminths,
arthropods) in certain body shapes (dorsoventral or
lateral flattening); loss of wings in parasitic insects;
development of special organs for attachment, clasping
or penetration and special mouthparts ( ► Figure
1.1); reduction or absence of light sensory organs;
specialised adaptations of mechano- and chemosensors
and frequently also in the development of efficient
reproductive organs, which are a prerequisite for high
reproduction rates. Tapeworms, living in the intestine
of a vertebrate host and 'swimming in a sea of food:
have no digestive tract. They absorb nutrients through
the body surface, which is equipped with microvilli-like
structures ( ► Figure 9.32, p. 207).
Physiological adaptations. Physiological
adaptations enable parasites to live in a wide range
of external environments, host species and host
Q)
T5
C
'6
�
c
('O
C
·;::
.s
Figure 1.1. Adaptations to the parasitic life. (a) Scolex of >,
0)
a tapeworm of the genus Taenia with hooks and suckers 0
as attachment organs; (b) anterior end of a hookworm 0
·u5
(Ancy/ostoma caninum) with tooth-like structures at the mouth �
opening (SEM photographs, coloured) (Photos: H. Mehlhorn). &
 Part I. General parasitology
environments (cells, various organ systems). These
adaptations allow developmental stages of parasites
to alternate between dissimilar hosts (e.g. vertebrate
- insect), different organ systems in the host (e.g.
intestine - liver - lung), and the outside world. Thus,
free-living stages of parasitic nematodes have an aerobic
metabolism and are able to break down carbohydrates
into CO2 and water by the usual steps of glycolysis and
the tricarboxylic acid cycle. In contrast, adult parasitic
nematodes switch to an anaerobic energy metabolism
and excrete incompletely degraded products of the
carbohydrate metabolism, such as succinate, pyruvate
and volatile fatty acids (e.g. Ascaris) or predominantly
lactate (mostly blood and tissue parasite). Parasitic
nematodes are not strictly anaerobic and can use mrygen
when available. Generally, the metabolism of parasites
is characterised by diverse peculiarities, regarding inter
alia generation of energy, nucleotide synthesis, lipid
metabolism, antioxidant and detoxification mechanisms.
There is some evidence that the metabolism goes
through an intermediate phase during the transition
of parasites from an aerobic environment to one with
low oxygen tension. For example, young stages of
Fasciola hepatica rely on aerobic energy metabolism in
the liver parenchyma, while older singes in bile ducts
rely on anaerobic processes (for detnils, see Barrett,
2011; Kohler, 2006).
Host specificity. Host specificity is defined as
the restriction of a parasite in a particular stage of
development to one or more host species, which offer
the necessary living conditions. Depending on whether
a parasite has a wide or narrow host range, it is called
euryxene or stenoxene, respectively ( ► Table 1.3). Host
specificity is a genetically fixed properly of each parasite
species and an expression of molecular, morphological,
physiological and immunological adaptations to a
specific host or a group of hosts. The physiological and
molecular basis of host specificity is poorly understood.
Host finding. Parasites use different strategics for
finding suitable hosts and to infect/infest them. Vectors
can be involved in these st ratcgies ( ► Chapter 1.4.1).
Reproduction rate. Many parasite species arc
characterised by high reproduction rates and population
Q)
densities. For example, a single meronl of malaria
·u
C
'6 parasites localised in human liver contains up to I 0 5
Q)
� developmental stages (merozoites). A tapeworm of
� and birds.
co
C
·;;::
Q)
j
-�
>,
-
0)
0
0
·v;
co
co
Cl.
the genus Taenia can release daily up to I 06 eggs, a
roundworm of the genus Ascaris 2x 10 5 and the large
liver fluke (Fasciola hepatica) 2x 104 eggs. Through
asexual reproduction of Fasciola or other parasites in
intermediate hosts, the number of descendants can be
further increased.
Life cycles. Parasites pass through complex life
cycles, in which various stages with different properties
are formed. Therefore, parasites are able to live and
develop in different habitats. Life cycles can be direct or
indirect. In direct development, only one host species
is involved. Thus, infectious stages of the parasite are
transmitted directly between two host individuals of
the same species, often after a longer development and
persistence in the external environment. Several hosts of
different species are involved in indirect development,
for example a vertebrate animal as definitive host and an
invertebrate (e.g. mollusc, arthropod) as intermediate
host. Besides obligate host changes, optional hosts
changes may also occur in certain parasites species.
Alternations of generations may be included in the
development, i.e. an alternation of sexual and various
forms of asexual reproduction ( ► Glossary, p. 620).
Further properties. Other properties of parasites
with special relevance to medical aspects are their
pathogenicity (or pathogenic potential) ( ► Chapter
I .4.4) and the ability to elicit and evade immune
responses of the host ( ► Chapter 1.5).
1.3 Hosts and their properties
Like parasites, hosts are divided into different categories,
some of which are listed in ► Table 1.4. In principle,
hosts can be susceptible or unsusceptible for one or more
parasite species. Due to their genetic constitution and
anatomical-physiological conditions, unsusceptible
hosts do not provide living conditions for certain
parnsitcs. In contrast, susceptible hosts offer suitable
conditions for the development to one or more stages
of a parnsite. for cxnmplc, humnns are the onl}' natural
definitive hosts of the tnpcworms Taenia sagi,wta and
Tawla soliwn, living in the small intestine. Sexual
development ofthe protozoon 'foxoplasma gondii occurs
only In the small intestine of the cat and some other
felid species, but asexual tissue stages find favourable
conditions for development in a wide range of mammals
 1. Parasite-host relationships

Table 1.4. Categories of hosts (selection).

Definitive host host in which sexual reproduction occurs (e.g. ruminants for Fascia/a hepatica)
Intermediate host host in which the parasite passes obligatorily through part of its development; in this phase
asexual multiplication may occur (e.g. fresh-water snails with laNal stages of Fascia/a O'l
C
hepatica) TI
C
Patatenlc host (transport host)
host harbouring laNal parasite stages (usually Infective stages) which do not develop ..=
further or multiply (e.g. mice with Infective laNae of Taxaca_ra _c_a n is_)
_ _ __________. 0
Main host ( preference host) host In or on which a parasite species is most frequently found (e.g. in Europe: red foxes I
-----½Ior Echinococcus multilocularis)
Side host host in which a parasite species is less frequently found (e.g. cats with Echinococcus
multilocularis)
Accidental host host, In which a parasite can settle and develop but does not play a role in transmission
(e.g. humans as hosts for metacestodes of Echinococcus granulasus and Echinocaccus
i------ ________,_!!lultitocutaris)
Aberrant host (dead end host) host in which a parasite cannot persist for a longer period or develop (e.g. humans with
juvenile stages of Dlrofilarla immltls

1.4 Parasite-host relationships 1.4.1 Host-finding

'Summary Parasites reach their hosts either actively or passively.

Parasite-host relationships are discussed here under
various aspects, including host-finding, infection/
Infestation, parasite development on or in a host,
pathogenicity, and immunology (for the latter, ► Chapter
·1.5).
• Host-finding can be an active process of parasites or
their vectors using different strate gies and modes of
orientation (e.g. ticks, insects, helminths); alternatively
parasite stages are transmitted passively to a host
through food or drinking water (e.g. oocysts, cysts,
eggs, laNae). If parasite stages develop in a vector,
transmission is called cyclic, otherwise acyclic or
mechanical.
Infection of a host can occur In several ways: orally,
through other body openings, percutaneously, or
via the placenta or the lactic gland (dlaplacental or
transmammary transmission, respectively). After
transmission to a host, the Infective stages perceive
diverse signals for seeking suitable habitats and for
further development, but the respective knowledge
is limited. Intracellular parasites recognise host cells
initially by molecular Interactions with cell surface
receptors to enter a host cell or to be Incorporated
'into a cell.
• Life in various host habitats requires special
properties, including adaptations of metabolism and
the ability to escape the Immune response of the host
(► Chapter 1.5.3). Migrations of parasites through host
tissues and organ systems are fascinating biological
phenomena with relevance to parasite pathogenicity
and pathogenesis of parasitic diseases ( ► Chapter
Active host-finding is common in certain insect and
tick species. Various diurnal mosquitoes and flies locate
their hosts primarily olfactorily and visually. Optical
orientation rarely plays a role in ticks (e.g. in the camel
tick Hyalomma dromedarii), but the ability to orientate
through chemical signals predominates ( ► Chapter
14.1). Also, certain stages of helminths exhibit active host
finding strategies. Miracidia of Fasciola hepatica, hatched
from eggs in water, show initially long-range dispersal
behaviours and display random (undirected) swimming
movements, but later they orientate themselves to light
and the water surface and are thus guided to habitats
in which their intermediate hosts (fresh-water snails)
live. At short distances miracidia are attracted to several
glycoproteins and other substances secreted by the
snails. Infective larvae of skin-penetrating nematodes
(Strongyloides spp.) increase their crawling speed in
response to thermal stimulation, possibly to improve
tJ1e likelihood of finding a host. Larvae of Strongyloides
stercoralis (predominantly a parasite of humans) are
attracted to several odours emitted by human skin.
Host-finding strategies are lacking in other groups of
parasites whose infectious stages are accidentally and
Q)
passively ingested by a host (immotile, protozoan cysts C
or oocysts of Giardia, Entamoeba, Eimeria, Toxoplasma ·o
TI
etc.; eggs of tapeworm and nematode species and Q)
the motile infectious larvae of strongyles). However, �
special behaviours and strategies of nematode larvae cu
C
·;:::
can promote their uptake by a host. For example,

l 1.4.4 ). infectious larvae of trichostrongyles migrate from

the site of their development (faeces of ruminants) to
plants, thus increasing the chance of being picked up
C
>,
O'l
by a grazing animal. It has been shown that infectious 0
larvae of Haemonchus contortus are attracted by the smell ·u5
of grass and 5% CO2_ This suggests that the larvae may
cu
be stimulated by CO 2 exhaled by ruminants in similar Cl.
 Part I. General parasitology
concentrations. Infectious larvae of the bovine lung
worm (Dictyocaulus viviparus) or of trichostrongylid
species use the capsule-like sporangia of a fungus(genus
Pilobolus) which grows in cattle faeces, as a transport
vehicle. The larvae attach to the sporangia to be catapulted
away from faeces to reach forage crops. The strategy of
direct and passive transition of parasite stages to a host
requires a high reproductive potential and is favoured
by the fact that stages of certain parasites can survive
up to weeks or even years i n the external environment.
Many parasite species pass through predation into a new
host. Infectious larvae of certain tapeworm species that
develop in rodents are ingested together with the prey by
carnivores in which adult tapeworms develop(peroral
transmission). Similarly, infectious stages of certain
species of protozoa(e.g. cysts of Toxoplasma gondii) or
helminths(e.g. larvae of Trichinella, other nematodes,
cestodes and trematodes) that develop in animals can be
transferred by ingestion of raw muscle tissue or organs to
humans or other susceptible hosts. Frequently, vectors
transmit infectious parasite stages to a host, either by
inoculation during feeding(inoculative transmission) or
by faeces or other excreta(contaminative transmission).
If parasites develop in a vector, transmission is called
cyclic; if this does not happen, the transmission is
referred to as acyclic or mechanical. In some cases,
vector behaviour favours the transmission of infectious
parasite stages to a host. For example, a larval stage of
the small liver fluke (Dicrocoelium dendriticum) settles
in the nervous system('brain worm') of the intermediate
host, an ant, and causes behavioural changes. Ants
infected with a 'brain worm' attach firmly with their
mouthparts to plants at cooler temperatures during
evening hours and are unable to return to their nests. In
this fixed position they 'offer' themselves for ingestion
by ruminants grazing during the night or early morning.
1.4.2 Infection and infestation
Pathogenic or apathogenic microorganisms reach a
host via different ways of transmission( ► Glossary,
p. 620). This contact leads to colonisation or infection.
Colonisation is the presence of a microorganism on skin
or mucous membranes without apparent consequences.
Infection refers to the establishment of a pathogenic
agent on or iJ1 a host with subsequent host reaction,
Q)
T5
C often with multiplication of the agent. Formerly, the
'5 term invasion was used for agents that do not multiply
Q)
in a host(e.g. the majority of helminth species). Today,
�
infection is the term commonly used for endoparasites,
C'
co while infestation refers to ectoparasites.
C
·;::
Q)
j For entry into a host, parasites use different infection
routes, e.g. peroral(through the mouth), percutaneous
-�
>­ (through the skin), transplacental(through the placenta),
OJ
0 and transmammary transmission(via the mammary
0
:t= gland), the latter with subsequent transfer of agents
Cf)
co via the milk to a new host (lactogenic transmission).
co Furthermore, pathogens can use other body orifices as
a...
portals of entry, e.g. the genital tract (venereal or sexual
infection), the nostrils (nasal infection) or the ear
(otogenic infection). Special attention should be paid
to the possibility of iatrogenic transmission of agents,
for example by using contaminated needles employed
for blood specimen collection, by blood transfusion or
other medical procedures. With reference to the time of
infection, a distinction is made between prenatal(before
birth), perinatal(during birth) and postnatal(after
birth) infection, and with regard to the propagation of
an agent in a host population between horizontal and
vertical infection(► Glossary, p. 620).
1.4.3 Development of parasites in or
on a host
The establishment of a parasite in or on a vertebrate host
is associated with transition into a new habitat, which
differs in its physicochemical and molecular conditions
from a previous habitat ( external environment,
intermediate or transport host). This is particularly
evident in endoparasites which are faced with a variety
of challenges in the new habitat:
• Perception of signals indicative of environmental
changes, providing stimuli for further development.
• Recognition of appropriate species-specific
habitats in the host, e.g. gastrointestinal tract, liver,
lung, blood vessels or body cells. Many species of
parasites migrate through different organ systems - e.g.
some nematode species from the intestine via liver and
lung back to the gut - before they settle in their target
habitat where mature stages develop. These migrations
are species- or genus-specific and require mechanisms
of the parasites for finding suitable habitats and niches.
Intracellular parasites must first identify suitable host
cells by molecular interactions before they penetrate
into the cell. Various groups of protozoa have developed
different strategies for infecting host cells(see below).
• Metabolic adaptation to conditions in the
host. Nematodes, previously living in an external
environment with high oxygen content, have to adapt
their oxidative metabolism to an anaerobic glycolytic
pathway for living in an oxygen-poor environment, e.g.
the intestinal lumen of a vertebrate host(► Chapter
1.2.7). This requires a metabolic plasticity of various
developmental stages of the respective nematode species.
In addition, the products of reproduction(eggs, larvae)
must be programmed in a way that survival in the
outside environment or in an intermediate or transport
host is secured.
• Adaptation to adverse habitat conditions.
Developmental stages of parasites are partly exposed
to effects of an aggressive environment(e.g. hydrochloric
acid and pepsin in the stomach) and the defence

mechanisms of the host, requiring adjustments to these
conditions.
• Integration into complex biocoenoses. Certain
parasites must be able to live in complex biocoenoses.
For example, in the large intestine of horses, numerous
organisms form a community, consisting of many
nematode species (e.g. small strongyles) and a wide
spectrum of species of symbiotic or commensal bacteria
and protozoa. Only recently, more detailed studies of the
multifold interactions in such biocoenoses are possible
due to genetic and molecular approaches.
• The search for mating partners. In dioecious
. parasites, for example in nematode species, males and
females have to get together for mating. Furthermore, the
offspring (eggs, larvae) must reach the environment or a
vector in sufficient numbers. Chemo-attraction between
males and females of Schistosoma mansoni, inhabiting
blood vessels in the host, has been demonstrated in vitro,
and seems to play a role in the natural habitat.
• Habitat selection and development. A
fascinating and important question addresses the
physiological and molecular mechanisms involved in
habitat selection and development of endoparasites
in vertebrates or other hosts. Considerable knowledge
exists on protozoa, but information on helminths is
'
still scarce.
Nematodes. Free-living nematodes can use
chemical gradients for orientation in the
environment. Caenorhabditis elegans is not only able
to perceive water-soluble substances in micromolar
and volatile molecules in picomolar concentrations
but also to differentiate various and structurally
very similar substances. In parasitic nematodes
such an orientation is unlikely, because chemical
gradients would be unlikely to build up, for example,
in the gastrointestinal tract with its peristalsis and
turbulences.It seems that, rather than using chemical
gradients for orientation, helminths can perceive and
follow individual signals, which constantly occur
at certain positions of the migration path as a kind
of signpost. The reactions of the parasites to such
signals are referred to as 'fixed action patterns', which
are genetically determined and are stereotypically
induced when certain key signals occur. This is
supported by some experimental evidence. After
peroral infection of rats, larvae of the nematode
Heligmosomoides polygyrus penetrate the intestinal
mucosa and encyst subserously in the intestinal wall.
The triggering signal to penetrate into the mucosa
is the contact with bile, which is supplied through
the common bile duct in the anterior duodenum.
In this zone, in which the 'bile' signal occurs, most
larvae penetrate into the mucosa. However, in rats
in which the opening of the common bile duct is
experimentally displaced distally, the majority of the
larvae penetrate the intestinal mucosa more distally,
1 . Parasite-host relationships
even in the colon. For this nematode species, a single
constant signal is apparently sufficient as trigger
and guide for habitat selection. Similar observations
(/)
were made for Tr ichinella spiralis. The fixed action a,
patterns can also be triggered by a signal chain,
for example in the liver fluke Fasciola hepatica. -�Ctl
0.
Infectious, encapsulated metacercariae are activated
0
after ingestion by the high CO2 concentration in the
forestomach system. They hatch from the capsule
c
in the anterior small intestine under the influence E
0.
0
of bile acids, which simultaneously act as signals for a5
the parasites to pass through the intestinal wall. In a;
the peritoneal cavity the juvenile parasites migrate to
the liver, but the mode of orientation is not known.
The data mentioned above provide some clues to the
mechanisms of habitat selection, but many aspects
are not yet understood.
Protozoa. Intracellular protozoa must find and
enter suitable target cells without destroying them.
Toxoplasma gondii is used here as an example. In
a susceptible intermediate host the parasite stages
(zoites) infect nucleated host cells. Infection is an
active process, which starts with an initial loose
attachment of the parasite to the cell wall by means
of surface proteins (so-called SAG family) and ends
when the parasite has entered the cell and is enclosed
in a parasitophorous vacuole in which it multiplies
asexually. Phases of this process are schematically
shown in ► Figure 1.2. After initial attachment (1),
proteins are secreted by micronemes and the 'neck' of
rhoptries by means of which the parasite adheres to
the cell with its apical complex located on its anterior
pointed end (2-4). With the support of the conoid,
the cell membrane is invaginated and an annular
structure is simultaneously formed by proteins
derived from rhoptries and micronemes. With the
progressive penetration of the parasite into the cell,
this structure moves on the parasite's surface to the
blunt pole as a 'moving junction' which eventually
seals the penetration site at the cell membrane (5-6).
Simultaneously, proteins are secreted from rhoptries
into the cytoplasm. Finally, the parasite enters the
cytoplasm where it persists in a parasitophorous
vacuole, surrounded by a membrane which consists
of host cell and rhoptry components (7). The whole
process lasts about 1-2 minutes. The parasitophorous
vacuole allows the intracellular survival of the
parasite; it avoids a fusion with lysosomes and
thus the intracellular destruction and is connected
with organelles of the host cell (lysosomes,
endoplasmic reticulum, mitochondria). Soluble
factors (hypervariable kinas es) of the rhoptries
(ROP16, ROP18) are released during the invasion
process into the host cell plasma and influence signal
pathways, which control cell activation by cytokines.
Thus, Toxoplasma, unlike the closely related species
Neospora caninum, can influence the response of
the infected host cell directly at the transcriptional
level. The resulting deregulation ofINF-y andIL-12
 Part I. General parasitology

2 4
3 5

6
7

Toxoplasma -tachyzoite
0
Rhoptry body
Nucleus
Rhoptry neck
Cell plasma

Micronemes Conoid
Inner membrane complex Parasitophorous vacuole

Figure 1.2. Scheme of cell invasion by Toxop/asma: (1) Initial adhesion of the parasite to cell surface; (2-4) apical adhesion; (5)
cell invasion; (6-7) formation of parasitophorous vacuole and detachment from cell membrane (for details, see text) (Graphics:
IPZ, M. Mathys; after Carruthers and Boothroyd 2007). TTTT: proteins.

expression contributes significantly to virulence and
pathogenesis. Signal transduction by Toxoplasma
can act on apoptosis of the host cell, thus prolonging
the survival of the cell. The emergence of zoites
(products of intracellular multiplication) from host
cells is an active process, triggered by increases in
intracellular Ca ++ . Zoites, which had been released
by active emergence or after cell disruption, infect
other cells and thus initiate further multiplication
of the parasite.
• Migrations of endoparasites In hosts. How
parasites navigate during their complicat.ed migrations
through host tissues and organs and which st,imuli
are necessary for further development, is still largely
unknown. Another open question ls why certain
endoparasites undertake extraordinary, 'adventurous'
migrations through the body (e.g. Strongy/us v11/garis
► Figure JO.I 2, p. 269; Toxocara canis ► p. 333) which
are thought to be advantageous for the parasite with
regard to survival. His assumed that such migrations are
Legacies of ancestral phases of the evolution. According
to a more recent hypothesis, body migrations and
temporary residence of developmental stages in tissues
may allow certain helminths to bypass Th2 immune
responses of the host, which take place mainly in mucous
membranes of the digestive tract and can lead to an
elimination of the parasite. Indeed, adult stages of
Tricltine/la spiralis are eliminated after a relatively short
period from the intestine by a classical Th2 response,
while larvae survive for years in the muscles. A similar
situation exists in Toxocara canis.
• Ectoparasites. In ectoparasites the transition from
a free-living phase to parasitic life appears to be simple at
first glance, but again biologically complex and efficient
strategies play a role (e.g. ticks, ► p. 396). Ectoparasites,
especially those that are in close contact with a host and
persist there for long time, are confronted with various
defence mechanisms ( ► Chapter 1.5.2).
1.4.4 Pathogenicity, virulence and
adverse effects of parasites
By definition, parasites have a pathogenic potential
which is not always expressed because pathogenic
effects in a parasite-host relationship are influenced
by susceptibility, immune status and general condition
of the host.
Pathogenicity and virulence. Pathogenicity is a
property of a species. Within a species various strains
can exist with different degrees of virulence, ranging
from low to high. These properties of the pathogen face
the couterparts of the host. A host species is susceptible
or unsusceptible to a certain pathogen due to its genetic
constitution. Within a basically susceptible host species,
subpopulations or individuals may exist that are fully

susceptible or partially resistant. This resistance is an
innate property and needs to be distinguished from
immunity ( ► Chapter 1.5).
Parasite species vary widely in their pathogenicity.
For example, the large liver fluke, Fasciola hepatica, is
highly pathogenic for sheep, but the small liver fluke,
Dicrocoelium dendriticum, is much less pathogenic.
Furthermore, various developmental stages of a
pathogenic species may differ significantly in virulence.
Adults of the tapeworm Echinococcus multilocularis,
living in the intestine of carnivores, do not induce disease
even in massive infections. In contrast, E. multilocularis
metacestodes can cause fatal infections in intermediate
and accidental hosts (rodents, humans).
Mechanisms of pathogenicity. The adverse effects
that parasites exert on their hosts are extremely diverse
and complex, and represent the result of parasite-host
interactions. Basically, the following types of adverse
effects can be distinguished: (a) direct damage by the
parasite (e.g. mechanically by the bite of an insect);
(b) indirect effects induced by parasite signals and
substances with subsequent host reactions. These
interactions require somatic contact between parasite
and host which makes communication via signals
possible.
A basic mechanism of pathogenicity, common to all
groups of pathogens (viruses, bacteria, eukaryotes) is
the triggering of an inflammatory response, which is
a first line of defence of the host as part of the innate,
non-specific defence. Mechanical insults (e.g. tick bite)
and body components of parasites or substances secreted
by them can induce inflammatory reactions, acting as
signals for further reactions. As a result of the parasite
action on the host, mast cells are recruited, which secrete
the cytokine TNF-a. At the same time macrophages
and dendritic cells incorporate parasite-derived
molecules or small pathogens (protozoa) and are thus
activated. Activated macrophages can kill phagocytised
parasites by means of reactive oxygen and nitrogen
species (e.g. H202, NO) and attract granulocytes.
These cells degranulate near larger parasites and thus
release reactive substances as a defence. Since such
inflammatory reactions and their effects can also damage
the host, an anti-inflammatory response is engaged in
parallel, involving TNF-a as messenger substance and
the anti-inflammatory cytokine IL-10. Furthermore,
in the course of parasitic infections or infestations,
immune responses are stimulated which serve to defend
pathogens, but can also damage the host (immuno­
pathology, ► p. 39). In addition to inflammation and
immunity, many other mechanisms play a role; these are
very briefly summarised in ► Table 1.3 and considered
in parts II and III ( ► p. 44 and p. 146).
·1. Parasite-host relationships
Direct damage caused by parasites (e.g. mechanical
damage to tissues, blockade and compression of organs,
destruction of parasitised cells) is usually less important
than indirect adverse effects resulting from the basic ·c::::,
reactions mentioned above. This also applies to the E
deprivation of food substances by parasites that are E
Q)
nutritionally fully or partially dependent on their hosts. >
:;::;
Quantitatively, such direct losses of nutrients usually 0.
co
play a minor role considering the mass ratios of the -0
co
parasite burden and the host. However, parasites can -0
C
cause significant indirect losses of nutrients, for example co
coC
Q)
by inducing inflammatory and immune reactions in
the intestinal mucosa, resulting in reduced uptake, C
absorption and utilisation of nutrients and losses of
host components (albumin, blood, etc.) into the digestive
tract (examples: trichostrongyles, hookworms). Blood
loss due to various causes can lead to anaemia ( ► Table
1.5). Toxins in the classical sense ( ► Glossary, p. 620)
play a role as pathogenic factors in some parasites (e.g.
toxins of ticks or blackflies), but cytotoxic substances,
produced by parasites (e.g. pore-forming proteins)
or emerging during inflammatory or immunological
reactions, are of greater relevance. Finally, it should be
noted that - as mentioned above - the adverse effects
result from of an interplay between parasite and host
involving genetic factors.
1.5 Immunology of parasitoses
Summary
• Vertebrates are equipped with two functionally closely
related defence systems to fight pathogens, a non­
specific innate immune system and a specific,
acquired or adaptive immune system. Principles of
these systems In relation to parasitoses are described
In the following chapter.
1.5.1 Innate and adaptive immunity
The innate immune system of vertebrates includes, as a
first non-specific line of defence, physical and chemical
barriers (e.g. skin, mucosa! surfaces in, for example,
the nasal and gastrointestinal tracts and the lungs, pH,
etc.) and secretions (e.g. saliva, sweat, tears, digestive
Q)
enzymes, bile acids, mucus, defensins) that prevent many
·u
C
potential infectious organisms from establishing in the '5
body. Should a bacterium, virus or parasite evade these Q)
�
barriers, then cellular components (phagocytes, natural
killer cells [NK cells], natural killer T cells [NKT cells] co
C
and others) and complement pathways are activated. ·.::::
Cells of the innate immune system are activated when .S
they recognise 'pathogen associated molecular patterns' >,
Ol
(PAMPs), molecular structures that are not present in/ 0
on the host. Various organisms - not just vertebrates but
·u;
also lower animals and even plants - possess cells that
have receptors named 'pattern recognition receptors' co
CL
 Part I. General parasitology

Table 1.5. Mechanisms of parasite pathogenicity (selection).

- "'
I ,., . ..
·1
' I !Meehanlsm
ye ·� - T
,A'dv.er:se eff,ect to,tfi� !host
. � "'.,;%,,. "· ""
Inflammation primary inflammation through direct effects of parasites -+ cell and tissue damage in various
organs
lmmunopathological effects induction of T cell-dependent immunopathies (e.g. intestinal villus atrophy), of inflammation
(e.g. in intestinal mucosa or liver parenchyma) or allergic reactions (e.g. in skin); impairment
of blood coagulation cascade, induction of immunocomplex diseases -+ various
pathophysiological consequences, e.g. kidney disorders; immune modulation -+ alterations of
defence capacity; induction or immunosuppression -+ impaired defence capacity of the host
(► Chapter 1.5)
Cytopathogenicity protozoa with intracellular multiplication -• alterations or cell structures and functions -•
destruction of host cells; immunologically based, T cell-dependent, cytotoxic effects to host
cells -+ cell death, necrosis, reactive inflammation
Tissue destruction mechanical damage caused by attacl1menI organs or helmlnt11s or mouth parts of arthropods,
damage through migrating activities and enzymes of parasite stages -+ bleedings, tissue
destruction, primary inflammation, regenerative processes; tissue damage t11rough
cytopathogenic eflects (see above); tumour-like prollferatlon of Echlnococcus multilocularis
metacestodes -+ tissue destruction, metastasis formation
Blockade and compression blockade or intestine or air passages by masses or I1elmlnths -+ disturbances of gut and lung
functions; compression or bile ducts or blood vessels by helminths (e.g. Echinococcus cysts)
_, cholestasis, disturbances or blood circulation
Withdrawal and loss of blood withdrawal of blood by blood-feeding helminths (e.g. Haemonchus, hookworms) or arthropods
(e.g. ticks, fleas); damage to bile ducts (e.g. Fasciola) or intestine (e.g. Eimeria species,
hookworms) and blood loss though mucosa -+ anaemia
Withdrawal and loss of withdrawal of nutrients by parasites -► mostly minor losses; withdrawal of vitamins, e.g.
substrates vitamin 8 12 by Diphyllobothrium -+ anaemia; damage to the gastro-intestinal mucosa -+
loss of water, minerals, proteins -► diarrhoea, dehydration, emaciation -+ compensatory
degradation or muscle proteins
Effects of pharmacologically excretion of cytotoxic substances or anticoagulants in saliva of blood-sucking arthropods
active substances -► local bleeding, inflammation, allergic reactions; excretion of toxins by ticks or blackflies
-+ local and general toxic reactions (tick or Simulium toxicoses; release of eicosanoides
(mostly prostaglandins, thromboxanes und leukotrienes) with multirold pharmacological und
immunological effects.
Transmission of pathogens parasitic arthropods are important vectors of numerous species of viruses, bacteria, protozoa
and helminths; helminths are rarely vectors (Heterakis gal/inarum transmits Histomonas
meleagr!dis) .... inrectlous diseases

(PRRs), which bind PAMPs as ligands, triggering diverse
biochemical pathways in cells and activating various
defence measures.
An important group of PRRs are the Toll-like receptors
(TLRs; named after a homologous protein, Toll,
which was first discovered in the fruit fly, Drosophila
melanogaster). TLRs are transmembrane proteins
in and on specialised cells of the immune system,
namely, antigen-presenting cells (APCs: monocytes,
Q)
C macrophages, dendritic cells). There are an estimated
·c3
'6 I0-15 different TLRs in vertebrate species, which
Q)
� recognise different PAMPs; for instance, peptidoglycans
and (triacyl) lipoproteins on Gram-positive bacteria
cu are recognised by TLR-1, whereas lipopolysaccharides
C
·.::
Q) (LPS) on Gram-negative bacteria are recognised by
TLR-4, and flagellin (a protein of the motor complex of
C bacterial flagellae) is recognised by TLR-5. Only a few
>, parasite structures have, to date, been shown to serve
CJ)
0 as ligands for TLRs. One example is profilin, a protein
0
·u5 that regulates the polymerisation of actin and, thereby,
cu is an essential factor in the motility of the protozoan
cu
Q_ parasite Toxoplasma gondii, and which is critical for its
ability to invade host cells. It is recognised, in mice, by
TLR-11. Other groups of PRRs that recognise structures
of pathogens include transmembrane or soluble CLRs
(C-type Lectin Receptors) and intracellular NLRs
(Nucleotide-binding O/igomerisation Domain-Like
Receptors).
Recognition of PAMPs first occurs at, or near to,
the site of infection and is, therefore, a function of
'resident' immune cells such as tissue macrophages
and dendritic cells. These resident cells must be able to
communicate with other components of the immune
system to recruit help to where it is needed. They achieve
this by producing mediators called chemokines and
cytokines. Chemokines are small (7-15 kDa), relatively
uniform proteins acting chemotactically ( e.g. MCP-1
or IL-8) to attract, for instance, phagocytic cells like
neutrophils and circulating macrophages to the site
of infection. Cytokines, on the other hand, represent
a multitude of heterogenous proteins that may be
classified as interleukins (ILs), interferons (IFNs),
colony stimulating factors (CSFs), and tumour
necrosis factors (TNFs). Some are synthesised by

many different cell types (e.g. IL- I, lL-6. IFN-a, TNF-a,
TNF-P), others only by one or a few cell types (e.g.
JL-2, IL-4, IFN-y). They can play important roles in a
variety of biological functions including regulation of
the immune response, growth stimulation and pro­
or anti-inflammatory effects. Often, a single cytokine
may have multiple (or pleiotropic) effects, resulting in
highly complex interrelations.
One of the earliest and most important effects of
chemokines and cytokines is to induce inflammation
as part of the innate immune response. In this context,
they not only act to attract other immune cells but also
aid their recruitment by causing vasodilation, increasing
blood flow and vascular per meability, facilitating
access to the infection site of circulating phagocytic
cells (neutrophils and macrophages) and complement
proteins. For instance, eicosanoids like leukotriene 84
and prostaglandin E2, along with cytokines like IL-land
TNF-a, combine to enhance the expression of so-called
adhesion molecules (selectins, VCAM-1) on endothelial
cells, which causes the adhesion of phagocytes
(neutrophils and macrophages) to endothelial cells
of blood and lymph vessels, a precondition for their
emigration from the blood into the surrounding tissues.
Activated endothelial cells, along with macrophages, also
release nitric oxide (NO), which is a potent vasodilator.
The end-result of this process are redness, heat, swelling
and pain that characterise inflammation.
The primary task of phagocytes is the phagocytosis
of unicellular pathogens or, in case of multicellular
(metazoan) pathogens, extracellular killing via ADCC
reactions ( ► p. 32). The complement system plays an
important role in assisting phagocytosis. Its antibody­
independent activation via the alternate pathway or the
lectin pathway (activation by mannose-binding proteins)
results in the formation of opsonizing components
(C3b). Neutrophils also produce chemokines and
cytokines to maintain the inflammatory reaction and,
moreover, several cleavage products of the complement
system act as potent pro-inflammatory mediators and
are chemoattractants for a variety of effector cell types
of the innate immune system, including neutrophils,
macrophages and mast cells. In this way, inflammatory
responses can be greatly amplified. Macrophages and
dendritic cells, meanwhile, are important early sources
of IL-12, which helps to activate NK cells, which are
important bridges between innate and adaptive immune
responses (see below). Last but not least, in continuation
of the complement cascade, a pore forming, membrane
binding complex (C5b6789) is generated on the surface
of pathogens, leading to their lysis.
Neutrophils are potent producers of reactive oxygen
species (ROS), lytic enzymes and antimicrobial peptides,
all of which are able to kill pathogens. They are, as a result,
short-lived soldiers in the innate immune response.
But, even after death, they continue to fight because,
1 . Parasite-host relationships
upon their death, netlike fibrils (NETs; Neutrophil
Extracellular Traps) are released into the surroundings.
These consist predominantly of nucleic material (DNA,
histones) that can trap, immobilise and kill bacteria,
fungi and protozoa.
Q)
Further cellular components of the innate immune >
�
system are NK/NKT cells, which account for 2% and 0..
ro
0.1 % of the mononuclear cells in the blood, respectively. -g
NK cells are able to induce apoptosis or necrosis within "O
C
'altered' cells (e.g., tumour cells or virus infected cells), ro
Q)
which are not expressing Major Histocompatibility
C
Complex-I receptors (MHC-1) on their cell surface. C
NK cells can, furthermore, kill free pathogens directly
by the exocytosis of granzymes and perforins. NK
cells detect a variety of signals that indicate that host
cells are under stress, for instance due to intracellular
infection. They are also able to recognise PAMPs, e.g.
lipophosphoglycans from Leishmania, which activate
TLR-2. NKT cells are a heterogeneous group of T cells
with minimally diversified T cell-receptors so that,
unlike other T cells, they recognise lipids and glycolipids,
not peptide-MHC complexes. Despite these important
innate immune functions, however, arguably the main
role of NK/NKT cells is to provide a rapid, early supply of
cytokines (IFN-y and TNF-a in the case of NK cells and
a much broader spectrum in NKT cells) that helps in the
initiation and direction of adaptive immune responses.
If an infectious agent eludes the various effectors of
innate immunity, then a more specific adaptive immune
response is activated. Adaptive immune reactions
regulate and control the course of primary infections
and protect an organism completely or partially from
re-infection (anti-infectious immunity) or from the
clinical consequences of an infection (protection from
disease). The reactions start with the processing of
antigens and the presentation of epitopes (peptide
sequences of an antigen) by antigen-presenting cells
(APCs: dendritic cells, B lymphocytes, macrophages
and, in the intestinal tract, so-called M cells) to specific
immune cells (mainly T cells). Subsequent responses
then occur at two broad levels: (a) in the form of cellular
immune reactions by T lymphocytes; and (b) in the
form of humoral immune reactions by B lymphocytes
and B lymphocyte derived plasma cells, which produce
antibodies (immunoglobulins, i.e. IgM, IgG, IgA, IgE,
etc.). Both reaction types are linked at several levels but
on occasion may act separately; e.g. B cells are able to
produce antibodies against some antigens independently
of T cell help, recognising so-called T-independent
antigens, often repetitive carbohydrate components,
whereas, mostly, generation of antibodies to other
(mainly protein-derived) antigens relies on cooperation
between B and T cells.
Cellular immune reactions are conveyed by CDs +
cytotoxic T lymphocytes (Tc) or T helper lymphocytes
(T h lymphocytes, CD4+ lymphocytes) (► Figure
 Part I. General parasitology

1.3). Tc recognise antigenic epitopes in connection particular PRRs on which type of APCs react with which
with MHC-1 molecules on the surface of target (e.g. specific PAMPs. In a simplified statement, intracellular
infected) cells(MHC-1 molecules are found on almost pathogens and their PAMPs and antigens provoke the
all nucleated cells and they react with and present highly synthesis of IL-12 by APCs, which stimulates early IFN-y
specific peptides that have been proteolytically cleaved production by NK cells, steering the reaction towards
from pathogens inside host cells). Presentation of Thi, whereas helminths and, sometimes, also arthropod
antigens toTh cells depends on connections with MHC­ antigens induce predominantly the expansion ofTh2 via
II molecules(MHC-II molecules are only found on the the early expression of IL-4. There are, however, many
surface of so-called professional APCs, which are able to open questions concerning such regulatory processes,
endocytose pathogen proteins that are extracellular). Th and also host species differences probably play a role.
cells consist of various subsets(e.g. Thi, Th2, Th3, ThS,
Th9, Thi 7 and more), which differ by their cytokine Adaptive immune reactions play crucial roles in both
production patterns and, thus, have distinct, though primary parasitic infections and subsequent infections.
sometimes overlapping, functions. However, it must be The latter implies - particularly when a long period
noted, that the classification ofTh subsets relies on data of time has elapsed between primary infection and,
obtained mainly in mice and humans and cannot be for example, secondary infection - some kind of an
uncritically assigned to other species, but it nevertheless immunological memory, because many B or T cells
seems to be a somewhat universal system. become eliminated by apoptosis at the end of a primary
immune response when an antigen becomes limiting.
A special role in parasitic infections is played by the Carriers of immunological memory are specific memory
so-called Th l/Th2 dichotomy. Th1 cells are especially B and T ceIJs, which escape the apoptosis that occurs
involved in cellular and inflammatory immune reactions, at the end of a primary response. In the case of B ceIJs,
processes that are stimulated by activation of macrophages the activation of a special 'survival gene: bcl-2, in the
and other effector cells, and accordingly, their cytokine respective cell may play a role for long-term survival. In
profile reflects these functions (► Figure 1.3). They the case ofT cells, several subtypes of memory cells are
are important for effective defence against intracellular known for both CD4 + and cog+ cells. Memory cells are
infections, e.g. as caused by many protozoan parasites. able to proliferate quickly and respond in an enhanced
In contrast, cytokines produced by Th2 cells rather act manner when reconfronted with their cognate antigen.
in an anti-inflammatory manner and enhance antibody
synthesis, in particular IgE. Correspondingly, they play Immune reactions may directly or indirectly inhibit
a significant role in immediate type hypersensitivity the development of parasites or may kill and eliminate
reactions. In addition,Th2 associated mediators enhance them from the host's body and they very often harness
propagation and activation of eosinophils and mast cells. the armaments of the innate immune system but in
They affect predominantly extracellular pathogens, in a very focused, specific manner. If immunity persists
particular metazoa, by complex mechanisms(see below). after complete elimination of the parasites, it is called
Thl and Th2 show mutual negative influences by their sterile immunity. In case of concomitant immunity
dominating cytokines IFN-y and IL-4, respectively. (also called preimmunity), antiparasitic efficacy ceases
after elimination of the parasites, i.e. it depends on
In recent years, further subsets of T helper cells with continuous antigenic boosters by living agents. Which
specific properties have been described, such as ThS, type of immunity takes place depends on the particular
Th9 and, most particularly, Th17. Th17 cells are seen host-parasite relationship (see the various chapters of
as pro-inflammatory cells, acting prior to adaptive this book).
immune responses, and have marked regulatory effects
on neutrophils (but not on eosinophils)(► Figure 1.3). Immune responses to pathogens are not exclusively
Both IFN-y and IL-4 impair Thi 7 proliferation. beneficial to the host, since they may provoke pathological
processes, for instance by overflowing reactions in the
In addition, general regulatory T celJ subpopulations course of inflammation processes, hypersensitivity
exist (TReg: Tri, Tr3), which stand out by virtue of reactions or even autoimmune processes. Common
strong IL-10 andTGF-� synthesis, two cytokines with consequences of parasitic infections are, furthermore,
clear anti-inflammatory effects(► Figure 1.3). parasite induced antigen specific or general immuno­
suppression. These respective topics will be discussed
The decision of which T cell subset will prevail in the in the following chapters.
course of an immune response may depend on the
PAMPs and antigens involved; it seems probable that
cytokine patterns are regulated, at least in part, by which

-
 1 . Parasite-host relationships

·c::J
E
E
>
:;::;
Q)

a.
co
-0
co
-0
C:
co
Q)

C:
C:
Antigen
presentation I
11.:2
I
IFNy
I
Tr-l!Fo
IL•4
Stimulating/
inhibitory ILJ13
cytokines
rdrn

Th cell subsets

IFNy IL-4 IL-17 IL-10

IL-2 IL-5 IL-21 TGFB
Secreted cytokines IL-13 IL-22
I

♦ "' "'
I I

Effector cells

Effector molecules/ NO, RO, enzymes, Antibodies, allergic Lytle enzymes, RO, Granzymes, perforins etc.,
mechanisms cytokines/chemo- reactions, lysis, cytokines/chemokines, lysis and induction of
kines, phagocytosis, opsonisatlon of acute inflammation, apoptosis of infected
chronic inflammation, extracellular phagocytosis with cells to kill intracellular
killing of intra- pathogens killing, NET formation pathogens
cellular pathogens for killing extra­
cellular pathogens

Figure 1.3. Simplified scheme of interactions between cells, cytokines and reactive molecules in immune reactions (Graphics:
IPZ, A. Seeger; after Zahner, IPG).
APC: antigen presenting cells, which present antigens with MHC molecules of class I (MHC I) or class II (MHC II) to naive T
helperO cells (Tho) or cytotoxic T cells (Tc).
Th cells differentiate into various subsets (e.g. T helper 1 [fh1], T helper 2 [fh2], T helper 17 [fh17], T regulatory cells
[rReg], which synthesise different cytokine patterns (interleukins: IL-1, etc., IFN-y), and can activate, stimulate or inhibit
themselves and other cells (macrophages [M0], B cells [BJ, neutrophil granulocytes [NGC]).
Activated cells synthesise cytokines and effector molecules like antibodies, various cytolytic enzymes, nitric oxide (NO) and
oxygen radicals (RO) or granzymes and perforins.
Part I. General parasitology
1.5.2 Parasite antigens
mlslng:tfle
oreover, so�e;"para
antigenic variation, thereby evad
Immune reactions of a host respond to antigens
whereby antigenic determinants, epitopes, are based
on their primary, secondary, tertiary or even quaternary
structures. Due to the complex developmental and
metabolic processes of parasites, parasite antigens show
marked diversity and are often post-translationally
m odified. They are commonly grouped into
somatic (structural) and excretory-secretory (EIS)
antigens. Somatic antigens may be surface antigens
of endoparasites with which the host is confronted,
or internal antigens, to which the host is not exposed
until degradation of the parasite occurs. In the case of
gastrointestinal nematodes that are not disintegrated
by the host after their death but are excreted, internal
structural antigens may be completely hidden from the
host. E/S antigens are released by helminths, for example
by migrating nematode larvae. In protozoa, they may be,
e.g. molecules that are exocytosed in the course of cell
ipvasion by infectious stages of Apicomplexa. Antigens
of ectoparasites to which the host is exposed, are mostly
saliva components but can also be ingredients of the
parasite's faeces and may be equated with E/S antigens.
The molecular structures of many parasite antigens
have been elucidated. In principle, they are typically
proteins and glycoproteins, but may also be glycolipids.
Modern techniques of proteomic analyses have, for
example, characterised the larval E/S products of
important gastrointestinal nematodes of ruminants or
of infectious stages of chicken coccidia and will definitely
clarify the composition and structure of other parasitic
structures in future, too. Additionally, the functions
of parasitic components are often verified by analyses
of homologies with molecules whose function has
been experimentally determined in other species. For
example, proteins released by micronemes of coccidia
show thrombospondin-like motives and sequences that
correspond to conserved regions in vertebrate proteins
with adhesive properties, i.e. they seem to initiate an
attachment of the parasites to the potential host cell;
many microneme proteins are strongly immunogenic.
Structural relationships of antigens may span genera
and may be responsible for immunological cross­
reactions. In other cases, cross reacting post-translational
modifications are observed. Phosphorylcholine (PC) on
helminth proteins is an important example. PC is a small,
haptenic epitope that is linked to carbohydrates and
proteins. It appears to have strong immunomodulatory
properties.
Cross-reacting antigens generally do not induce cross­
immunity and represent only a small proportion of the
antigenic spectrum of eukaryotic organisms, which is
characterised by a broad diversity and many peculiarities
including, e.g. the ability of particular parasites to vary
their antigenic profile. A well-known example is the
change of surface antigens in the Trypanosoma brucei
group ( ► Chapter l.5.3). In addition to this specific type
of antigenic variation as an immune evasion adaptation,
antigens that are presented to the immune system of
the host may differ between the various developmental
stages of parasites, e.g. the different stages (sporozoites,
merozoites, gamonts) of Apicomplexa. Stage-specific
antigens are also found in helminths; for example all
developmental stages of Trichinella spi ralis are equipped
with stage specific surface antigens. This adds another
dimension of complexity for immune control of parasitic
infection.
1.5.3 Immune effector mechanisms
against parasites
l-fsummary
• Olvtl"II Immune effector mechanisms may affect the
dtvelopment, prollferatlon and lifespan of parasites,
or may klll them,
• peolfto humorel antlbodlea can Induce lysls or
'' opeonlze paraeltea, partlcularly protozoa, with and
without Involvement of complement.
• Cellular Immune reaction, by Th1 cells result lr:i the
eyntheala Qf cytotoxic host factors or In various other
antlpan131tlc effect& depending on the effector cell type.
CytotQxlc T cells that recognise parasite antlger:,s on
the host cell surface may eliminate parasites by killing
the host cell.
• Tissue helmlnths are predominantly sontrolled by
•nUbody dependent cellular cytotoxic reactions
Vd)OC reactions), whereas gastrointestinal helmlnths
may be ellmlnated by self-cure reactions promoted
by immediate (type I) hypersensitivity. Immunity to "
arthropod parasites may be Influenced by the intensity
of their relationship with their host.
• In many parasitic infections, a type of immunity
develops that does not affect the established parasite
population but controls superinfections (concomitant
immunity).
 1 . Parasite-host relationships

The antigenic character of parasites induces immune
reactions with distinct impacts on clinical manifestations
and epidemiology that may substantially influence the
course of a primary infection and the susceptibility of
the host to superinfections. The effects may be manifold
and range from impaired development and reproduction
and shortening of lifespan to killing and elimination of
the entire parasite population or of particular stages.
Filariae are a good example of the latter, as infected hosts
show frequently a selective immunity to the first stage
larvae, the microfilariae, whereas the adult worms persist
(► p. 361).lmmunity may have several outcomes: sterile
immunity, resulting in elimination of the immunising
parasite population; partial immunity, resulting in
a certain level of control of the parasite population,
mitigated by immune evasion strategies of the parasite;
or concomitant immunity - which is relatively common
in parasitic infections - the result being persistence of
the established parasite population but effective control
of superinfections, dependent on a continuous antigenic
booster by the persisting parasites (this may be the
basis of an enzootic stability, e.g. in bovine babesiosis
(► p. 135)). The variety of developmental steps and
localisations of parasites in or on a host means that types
and mechanisms of immunity may vary from parasite
to parasite, though some generalities for protozoan,
helminth and arthropod infections can be ascribed.
Immune effects against protozoa. Protozoa live
as extracellular or intracellular parasites and, therefore,
show quite different vulnerability to immunological Cl)
E
attacks in a host. Extracellular parasites are usually
accessible to humoral mechanisms. They may be
·c
(\j
.c
lysed or phagocytosed. Cellular immune mechanisms (.)
Q)
play a more important role in the case of intracellular E
parasites, either by direct effects by cytotoxic T cells +-'
(CDs + , Tc) or indirectly through helper T cells (CD4+ (.)
Q)
Th cells), particularly Thl and Th17 subpopulations :i:::
Q)
(► Figure 1.4). Q)
C
::::,
E
• Lysis is a complement dependent process. The E
necessary activation of the complement cascade occurs
after antigen-specific binding oflgM or IgG antibodies
onto the parasite surface via the Fe-receptor (classical
pathway) or, in an antibody-independent manner (i.e.
via the alternative pathway, lectin pathway, see above),
through reactivity with particular surface structures. In
both scenarios, a membrane binding and pore forming
complex (C3b6789) is formed, which damages the cell
membrane of the parasite.
• Phagocytosis, after opsonization by complement
and/or specific antibodies, is an important immune
mechanism against extracellular protozoa. After
internalisation of the parasite within a membrane-

Humoral reactions Cell-mediated reactions

NKcell
Lysis mediated by antibodies and complement
Free parasites in 1
tissues and �
body cavities
,....,_�
Cytotoxic
cell

Phagocytosis after opsonisation

by antibodies (+ complement)

Activated monocyte
Infected cell with parasite
antigens on surface

Figure 1.4. Immunological effector mechanisms against protozoa. Free parasites in tissue or body cavities (tachyzoites of
Toxoplasma gondii and trypanosomes are depicted) may be lysed via antibodies and complement, or phagocytosed by
macrophages and granulocytes after opsonisation. This applies also to infected cells (e.g. Babesia infected erythrocytes),
which carry parasite antigens on the surface. In case of intracellular agents, the host cell represents the target that can be
eliminated by natural killer (NK) cells and cytotoxic T cells. Th1 and NK cells activate macrophages as effector cells by IFN-y.
Macrophages, serving as host cells (e.g. for Leishmania spp.), may be activated to kill the intracellular parasites (Graphics:
IPZ, A. Seeger; after Zahner, IPG).
 Part I. General parasitology
enclosed phagosome, coupled with fusion with a
lysosome to form a phagolysosome, the parasite may
be killed by H202, 02 and OH radicals, NO, lysozymes
and hydrolytic enzymes. The elimination of infected
cells is also possible. For example, in response to Babesia
or Plasmodium infection, invaded erythrocytes display
parasitic elements on their cell membrane, rendering
them susceptible to recognition, phagocytosis and lysis
by immune cells.
• Mechanisms associated with CD4 + T cells.
Thl associated cytokines, in particular IFN-y, induce,
e.g. in Leishmania infected macrophages, the synthesis
of reactive N- and 0-metabolites, which may kill the
intracellular pathogens. Thl mediated cytotoxic effects
by N- and 0-metabolites are a generally important
means of defence against infectious agents. They control
primary infections, e.g. the proliferation of Plasmodium
spp. i n mouse models and the course of many other
protozoa! infections. The zoonotic parasite Toxoplasma
gondii represents a special example of Thl influence.
Under increasing immune pressure from the host, this
cyst-forming coccidium converts from rapidly dividing
stages, tachyzoites, to slowly proliferating bradyzoites,
which subsequently persist in cysts inside muscle and
brain cells for long periods ofome, apparently sheltered
from immune reactions. This stage conversion is at least
partly induced by IFN-y of T. gondii specific Th1 cells,
which mediates the synthesis of NO in macrophages.
NO binds covalently to intracellular iron and thereby,
may inhibit Fe-dependent enzymes of the mitochondrial
respiration chain of the aerobic tachyzoites. Bradyzoites,
i n contrast, are anaerobic stages, i.e. the parasite
seems to evade NO effects by stage conversion. N­
and 0-metabolites are also secreted by macrophages,
granulocytes and other cells and may display their effects
extracellularly, too (see ADCC reactions below).
• Cytotoxic lymphocytes. cos + T lymphocytes
(Tc cells) get cytotoxic when they recognise peptides
of intracellularly generated antigens in connection
with MHC-I on cell surfaces. For instance, they
play an important role in immunity to Eimeria spp.
by affecting early intracellular stages deriving from
challenge infections. Intra-erythrocyte stages of Babesia
spp. and Theileria spp., however, are not affected since
Q)
C erythrocytes, if at all, exhibit very few MHC-I molecules.
·c3
'6
�
Q)
Immune effects against helminths. Immune
reactions against helminths are basically determined
co
C by T helper cells. In case of gastrointestinal helminths,
·;;::
Q) Th2 reactions are dominating. The steering cytokines
j are synthesised within hours after infection in response
-� to EIS antigens in Peyer's patches, i.e. are initially
>- independent of CD4+cells.In the case of tissue helminths,
0)
0 stage-dependent differences are known. For example,
0 schistosomes (► p. 201) induce predominantly Thi
·w
co associated cytokines in the early phase of infection until
co
a. the beginning of patency. Subsequently, a switch-over to
Th2 and Thl 7 dominated responses occurs under the
influence of soluble egg antigens. In many cases, the Th2
dominance is a prerequisite for protective effects against
helminths. For example, continuing infections with
small amounts of infective larvae of intestinal nematodes
result in the establishment of a stable, chronic infection,
associated with a prevailing Thl response.
Effector mechanisms against helminths are mainly
cell mediated. The in vivo protective effect of humoral
antibodies has been well documented against
invading Taenia and Echinococcus oncospheres, but
the antibody-mediated mechanisms against other
helminths are unclear. Indeed, early stages of trematodes
(schistosomes, Fascia/a hepatica) are killed in vitro by
antibodies and complement, and larval stages of ascarids
bind specific antibodies to their surface, however, it
is doubted that such mechanisms are really able to
eliminate the parasites in vivo. Furthermore, although
protective effects of colostrum against some helminths
has been noted, the involvement of T cells contained
in the colostrum cannot be excluded. Additionally,
different localisations of the parasites may account for
different defence strategies. In fact, such differences have
emerged with ADCC reactions (see below) appearing
to be important against helminths residing in tissue
or body cavities, versus self-cure reactions (see below)
against gastrointestinal nematodes.
• Antibody dependent cellular cytotoxicity
(ADCC) reactions. Helminths cannot be phago­
cytosed like protozoa, simply due to their size.
Tissue dwelling helminths, including extra-intestinal
stages of gastrointestinal parasites (e.g. of ascarids),
are therefore predominantly eliminated by ADCC
reactions. ADCC reactions are virtually an extracellular
equivalent of phagocytosis (► Figure 1.5). Antigen­
antibody complexes, generated either with or without
participation of complement on the surface of parasites,
are brought into narrow contact with effector cells via
binding to Pc- and/or complement-receptors on the
cell; cells are activated and release effector molecules
onto the parasite surface. All cell types bearing Fe- or
complement-receptors may be involved (macrophages,
neutrophils, eosinophils, platelets and others); however,
the binding of effector cells occurs predominantly via
IgG and IgE antibodies, since macrophages, eosinophils
and platelets are equipped with IgE-Pc-receptors.
The participation of IgE antibodies, which are often
produced in relatively large amounts due to the Th2-
biased responses to helminth infections, is probably of
particular importance in the immune elimination of
juvenile trematodes. These stages express Pc-receptors
on their surface (as an immune evasion strategy, see
below), which recognise the Fe-part of IgG but not
that of IgE.
The diversity of cell types involved in ADCC reactions
accounts for a plurality of effector molecules, e.g.

(Eosinophilic) granulocyte
Surface antigen-anti­
body complex
Major basic protein,
cationic protein,
peroxidases, phospho­
lipidases, etc.
Figure 1.5. Immunological effector mechanisms against tissue stages of helminths, e.g. the elimination of a microfilaria of
Dirofilaria immitis by Antibody Dependent Cellular Cytotoxicity (ADCC) reactions. Effector cells (granulocytes, macrophages,
platelets, etc.) attach to antigen-antibody (red) complexes on the parasite surface via Fe-receptors (yellow). They secrete effector
molecules, which damage the cuticle of the parasite. Additionally, they release toxic metabolites (NO, RO [reactive oxygen
intermediates]). Box: microfilaria with attached cells (Graphics: IPZ, A. Seeger; after Zahner, IPG).
hydrolytic enzymes, reactive 0- and N-intermediates,
defensins (small cytotoxic peptides), as well asTNF-a
andTNF-P that may affect helminth parasites.These
molecules damage directly the parasite or attract and
activate additional effector cells. The efficacy of some
effector molecules as 0- and N-radicals does not
depend on a direct cell-parasite contact, i.e. also cells
of the second line may collaborate. Other cells, which
are not directly involved in cytotoxic operations like
mast cells, Band CD4+T lymphocytes may enhance
the damaging process by the release of mediators
(histamine, leukotrienes, cytokines), so that a concert
of many humoral and cellular components is generated
including the crosslinking ofThl andTh2 associated
components.
• Self-cure reactions. Self-cure reactions are a
particular type of immune elimination of helminths
by rapid expulsion of still living larvae or adults from
the gastrointestinal tract of hosts (► Figure 1.6 and 1.7).
TheseTh2-mediated reactions may differ depending on
the respective host-parasite relationship.They may be
induced by challenge infection or happen independently
of a re-infection, and may result in the expulsion of
1 . Parasite-host relationships
Macrophage
en
E
en
·c
C'CS
.c
()
Q)
E
,._
0
()
Q)
Q)
C
::i
E
E
Lysozyme, proteases,
collagenases, estera­
ses, etc.
larvae or adults. In every case, however, it requires an
intactTh2 system and includes a local immediate (type
I) hypersensitivity reaction in the infected part of the
gastrointestinal tract. In most cases, self-cure reactions
are independent of other mechanisms that may be
involved in protection against reinfections.
The classical self-cure reaction is observed in
trichostrongyle infections in sheep and represents an
important mode of regulation of the worm burden. Self­
cure reactions in Haemonchus contortus infected sheep
frequently start after a homologous heavy superinfection.
It results in a batch-wise elimination of the adult worm
population within a period of 2-4 days, which may also
contain larvae of the challenge population. Studies in
Teladorsagia circumcincta infected sheep suggest that
in particular specific IgA antibodies of the intestinal
mucus are involved in larval expulsion. However, in
most cases, part of the larval population establishes and
develops into a new adult worm population.The self­
cure reaction is associated with oedemas and enhanced
mucosal secretion at the localisation site of the parasites
in the gastrointestinal tract and increased histamine
levels in the blood. Considering the often distinct
 Part I. General parasitology

•
Superinfection

Egg shedding

0 1 2 3 4 5 6
Day after superinfection

Figure 1.6. Time course of self-cure reaction In Haemonchus contortus Infected sheep. Sheep with patent infection are challenged
by homologous third stage larvae (L3). With the beginning (3 days p.l.) of their moulting to fourth stage larvae (L4), an expulsion
of adult worms (�, a) from the abomasum starts, associated with a sudden decrease of egg excretion. The reaction coincides
with a distinct increase of histamine levels in the blood and an oedematisatlon of the mucosa In the parasitised region of the

r;
abomasum (Graphics: IPZ, A. Seeger; after Zahner, IPG).

r
(D Degranulating
mast cell

Vasoaclive molecules
co lead to increased
1/) permeability of vessels

•• •
0
0
::,
E
.J:J

• ··
•••
::,
1/)
"C

•'
C

. , .·,
co
co
1/)
0
0
::,
:E

I •• I
antibodies
• slon of adult parasites
associated
with Increased Intestinal
l motility

,df////J--.....�
Q) C . ,.
C
·o
'6
Q)
� \
C'O
C
·c
Q)
Moulting L3 ->l4
1,1.'
.
�-
Figure 1.7. Mechanism of self-cure reaction in sheep infected with gastrointestinal nematodes (simplified). Mast cells invade the
C wall of the gastrointestinal tract of infected animals (mastocytosis). High levels of specific lgE antibodies (1) sensitise the mast
>, cells. After homologous superinfection, third stage larvae (L3) moult to fourth stage larvae (L4) and release moulting antigens
0)
0 (2), which bind to lgE molecules on mast cells. Subsequently, mast cells release vasoactive molecules (histamine, serotonin),
0
'in
which increase the permeability of blood vessels of the intestinal wall and lead to oedematisation of the wall of the infested
part of the gastrointestinal tract and to extravasation of antibodies and cells (3). Adult worms are expelled in cooperation with
co
a. enhanced peristalsis (4). (Graphics: IPZ, A. Seeger; after Zahner, IPG).

mucosal mastocytosis in infected animals, this type of
response suggests a local allergic reaction. The provoking
allergens are released in the course of moulting from
L3 to L4 of the superinfecting larvae ( ► Figure 1.6 and
1.7) It is of epidemiological importance that the ability
of ,heep to respond in self-cure reactions is impaired
ir the course of the last phase of pregnancy and during
tli lactation period.
n several nematode infections (Trichuris spp., Trichinella
,pp., and also Ascaris suum), self-cure reactions occur
after heavy primary infections without challenge
infections. In case of Trichuris suis infections of pigs,
for instance, the adult worms are expelled approximately
9-10 weeks after infection. The mast cell-dependent
reaction is regulated by IL-4 and IL-13, i.e. shows traits
similar to the self-cure reaction in trichostrongyle
infections. Reactions in A. suum infected pigs resemble
this type of self-cure. However, in this case, the larvae,
which arrive after the migration through the host's body
in the small intestine, are rapidly eliminated whilst most
of the adult worms persist.
The intrinsic mediators responsible for worm expulsion
have not yet been determined. They seem to be released
via increased mucosal secretion into the abomasal/
gut lumen and operate non-specifically. The latter is
documented by the observation that the expulsion of
a worm species established in the proximal part of the
gastrointestinal tract (e.g., Haemonchus contortus in the
abomasum) can simultaneously affect a more distally
localised species (e.g. Trichostrongylus colubriformis
in the small intestine). In contrast, the expulsion of
T. colubriformis does not influence the proximally
established H. contortus population. Factors affecting
the worms are seen in mucosal inflammation, which
might create an environment unsuitable for the parasites
and direct effects of mast cell products (biogenic amines
damage nematodes in vitro). It is also possible that
specific antibodies accumulate in the mucosa! mucus
layer due to the increased permeability of blood vessels
in the course of allergic reactions. These antibodies may
then directly interact with the parasites. An increased
peristalsis due to inflammatory processes may play a
further role. IL-13, for instance, strongly influences
peristalsis and goblet cells. Studies in mice also suggest
an essential participation of MucSac in immune
expulsion of intestinal nematodes. MucSac, a mucin
component, is normally expressed in the respiratory
tract but not in the intestinal epithelium; it has,however,
been detected in the gut wall of Trichuris suis infected
pigs,( ► p. 368) but it is not associated with protection
against nematodes in cattle.
1. Parasite-host relationships
• Impaired parasite development. Immune
mechanisms that impair helminth development and
fertility have not been investigated in depth. However, it Cl)
is a regular phenomenon in gastrointestinal nematodes E
·cco
Cl)
that, although able to establish in 'immune' hosts,
..c
they show delayed fertility, retardationn growth and (..)
CD
produce fewer eggs when compared with worms in E
,_
naive hosts. These effects appear to depend on an intact 0
T cell responsiveness but the triggering mechanisms
are unknown. CD
CD
C
The hypobiosis of larval stages of gastrointestinal ::J
E
nematodes, which is of epidemiological importance E
in ruminants ( ► p. 293), seems to be at least partially
dependent on host immunity. Thus, hypobiotic L4 of
Teladorsagia circumcincta complete their development
after treatment of the hosts with corticosteroids.
Immunity to arthropods. Parasitic arthropods
differ markedly by the intensity of their contacts with
hosts. This relationship may, for example, be permanent
and close as in the case of Sarcoptes mites, may be
temporary but rather intensive due to the release of
saliva as in the case of ticks or blood sucking diptera,
or may be quite superficial as in the case of biting lice
(Mallophaga). These differences are at least partially
reflected in immune responses to the infestation.
Sarcoptes infestations induce a predominantly cellular
type of partial immunity and are associated with intense
immunopathological alterations. The success of blood
sucking of some tick species is impaired on hosts that
have been previously infested, and this type of partial
antibody-mediated immunity to ticks can be transferred
with serum to na'ive animals. A further role is probably
played by an accumulation of, predominantly, basophils
around the inserted mouth parts of the ticks. These
basophils are coated by homocytotropic antibodies (IgE;
cutaneous basophil hypersensitivity), and allergens in
the tick saliva induce basophil degranulation and the
release of histamine, which has been shown to inhibit
tick salivation and blood uptake. It may be pivotal that
ixodid ticks persist on their hosts for 5-7 days whereas
other ectoparasites, which complete blood meals quite
rapidly(e.g. fleas), do not induce any kind of protective
immunity. The reaction to biting lice (Mallophaga) in
sheep indicates that immune reactions to arthropods
may arise also in cases of relatively loose contacts;
Mallophaga feed exclusively on components of the
superficial layers of the stratum corneum of the skin
but infested sheep still develop humoral and cellular
hyp ersensitivity - with clinical impacts - to biting
lice allergens and, thereby, control the lice population
immunologically. The responsible allergens are assumed
to be in the saliva and faeces of the lice.
Part I. General parasitology
.5.4 lmlllune evasioll strategies of
parasites
Ion.
J"9 a po.,.la - An efficient evasion strategy is the change of antigenic
ptosls of Immune cells or Inhibition of apoptosls
eel host cells.
strategies - hypoblosls (e. g. of nematode
), formation of dormozoltes or hyp nozoltes In
e aplcomplexan species.
The often long-lasting persistence of parasites in or on
a host implies its ability to evade host defence reactions.
Consequently, many parasites have developed immune
evasion strategies in the course of co-evolution with
their hosts. ► Table 1.6 provides a synopsis.
The sequestration of parasites is a common pheno•
menon. Parasites may retreat into safe refugia as tissue
capsules or cysts, either induced or generated by
themselves (Echinococcus spp. cysts in inner organs,
larvae of Trichinella spp. in capsules in muscle cells,
bradyzoites of Toxoplasma gondii in tissue cysts) or
into immunologically privileged organs (e.g. cysticerci
in the brain). The inside of cells serves as a common
immunological hideaway for protozoa. Indeed, some
protozoa are phagocytosed by host cells, but they evade
the phagosome, successfully residing in the cytoplasm of
the host cell (e.g. Leishmania spp.). Erythrocytes, which
are infected by Haematozoa (Babesia, Plasmodium,
Theileria), represent relatively safe habitats at least
until parasite molecules are incorporated into the cell
membrane. In addition, erythrocytes have a limited
synthesis capacity and do not express MHC molecules.
Theoretically, the most effective immune evasion strategy
of a parasite would be a completely inert surface, making
it immunologically unrecognisable. This would conflict,
however, with the function of protozoa! cell membranes
or the syncytial surface of platyhelminths in nutrient
exchange. Even the acellular cuticle of nematodes is
partially involved in resorption of nutrients. Anyhow,
the surface of tissue nematodes is covered by lipid or
glycolipid layers in several species, which could protect
it from immunological recognition.
Alternative evasion strategies include masking and
immunological mimicry. Masking is achieved by, e.g.
the absorption of host albumin and immunoglobulins
onto the surface of schistosomes and nematode larvae.
These probably conceal antigenic determinants of the
parasites, although direct proof of this has not yet been
demonstrated. More conclusive evidence is given when
host-analogue, functional molecules are generated as
gene products of the parasites and are expressed on the
surface like Fe- and complement receptors on juvenile
trematodes. In these cases, IgG molecules (not IgE!) are
bound the wrong way to these Fe-receptors and become
ineffective. Binding of C3b to complement-receptors
blocks the complement cascade. In addition, trematodes
secrete proteases, which fragment antibodies bound to
the Fe-receptors.
structures. Thus, the various developmental stages
of parasites may be equipped with differing antigens
(stage-specific antigens). Particularly in cases of rapid
switchovers as, for example, in most Eimeria spp., the
immune response of the host lacks behind these events
with delayed efficiency. From an immunological point of
view, the stepwise development and associated moulting
of nematode larvae may have similar effects.
Other parasites may vary their antigenic patterns
(antigenic variation). This phenomenon is best
investigated in African trypanosomes, where the whole
cell surface is covered by a variant surface glycoprotein
(VSG). The VSG is bound to the cell membrane via
glycosylphosphatidylinositol anchors and can easily
be cleaved and replaced by a new VSG to which the
host has not yet been confronted. Parasites with the
new VSG on the surface evade the otherwise efficient
humoral defence of the host and build up a new
population. The number of genes encoding VSGs is
large (10% of the whole genome are exclusively used
to express VSGs). The expression of these genes
indeed follows a hierarchical order of succession, but
this sequence cannot be predicted in a trypanosome
population. Furthermore, since trypanosomes are able
to create new VSGs by genetic recombination, the VSG
spectrum in a parasite population is inexhaustible. In
the case of Giardia duodena/is, an intestinal flagellate,
the persistence in the host probably also depends on
the ability to vary surface antigens (variant surface
protein: VSP). The VSP covers the parasite including
the flagellae and, as for trypanosomes, always only one
gene out of a multigene family (encoding for 100-300
proteins) is expressed. Another example is the variant
(erythrocyte) surface antigens (VESA) of Babesia
 1. Parasite-host relationships

Table 1.6. Immune evasion strategies of parasites (selection).

Obaervecl In �oa
r:n
Q)
Sequestration: retreat into intracellular parasites: piroplasms, plasmodiae formation of capsules (Trichlnella spiralls) or ·a:,
Q)
'safe niches' �n erythrocytes), Trypanosoma cruzl, Theileri8 cysts (Echlnococcus spp.); retreat into CNS
sp. (evasion into the cytoplasm); encystatlon (Coenurus cerebralis, Cysticercus cellulosae) �
(Toxoplasma, Neospora, Sarrocystis) t5
C:
Antigen shedding 1 Plasmodium, BabesiB., Giard/a spp. Fasciola hepatics, Toxocara canis 0

Immunological mimicry trematodes (F. hepatics, schistosomes), "gj

Ascaris suum
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Expression of special trematodes (F. hepatica, schistosomes) C
::,
surface receptors (Fe-, C-) E
Antigen variation trypanosomes (VSG2), Glardia (VSP3), .£
Plasmodlum falciparum (var-antigens4),
Babesia (VESAs4)
Stage specific antigens Coccldla, other Aplcomplexa nematodes (ascarids, filariae, Trichinel/a spp.)
Genetic regulation (e.g. Leishmania spp., Trypanosoma cruzl,
inhibition of iNOS-expression)5 Toxoplasma gondll
Release of detoxifying Leishman/a spp. (gp63, others) filariae (antioxidants)
components
Release of lmmuno­ trypanosomes, Leishman/a spp. many helmlnths (schistosomes, Echinococcus
modulating components6 spp., ascarids, filariae) and arthropods (ticks,
others)
Pro-apoptotic effects on trypanosomes, plasmodia filariae
immune cells
Anti-apoptotic effects on Trypansoma cruzi, Eimeria bovis, Toxoplasma
host cells gondii, Theileria spp.
Hypobiosis dormozoites of Cystoisospora spp. numerous nematode species (e.g. Osterlagia
osterlagi, Dictyocaulus viviparus)
1 Some parasites possess highly antigenic surface antigens that may be shed after binding of antibodies to complexes.
2 Variant surface glycoproteins.
3 Variant surface protein.
4 Antigens expressed on the surface of infected erythrocytes.
5 Inducible NO synthetase (catalyses NO synthesis).
6 Components with various effects (e.g. inhibition of antigen presentation or lymphocyte proliferation).

bovis, the most pathogenic species within the group
of bovine babesiae. VESA are found on the surface of
infected erythrocytes and provide the ability to adhere
to the capillary endothelium, preventing the cells
from being directed to the spleen and degraded. The
antigenic variation is the precondition for the long­
range function of this principle. VESA are encoded by
a multigene family, whereby >300 ves genes encode just
for the antigen subunit VESAla. Remarkably, the same
strategy is employed by Plasmodium Jalciparum, the
most pathogenic agent of human malaria, with the so­
called var genes, although the genetic and biochemical
background of the two parasite genera are completely
different.
In other cases, the parasites expose their surface
antigens to recognition. They even show the host
highly antigenic (often containing repetitive amino
acid sequences) surface structures that, however, can be
shed after binding to antibodies (antigen shedding and
smokescreen antigens). Examples of this phenomenon
are present in Babesia and Plasmodium species, the
'smokescreens' allowing them to survive in the blood
plasma before they reach their safe habitat, the cytoplasm
of erythrocytes.
In cases of intracellular protozoa! infections where,
according to schedule, the parasites are phagocytosed
and the phagosome and lysosome fuse, the parasites
inhibit the synthesis of toxic components (for instance
the inhibition of inducible NO synthesis in infected
macrophages by Leishmania spp.) or they synthesise
detoxifying compounds (e.g. glycoproteins of Leishmania
donovani, gp63 and others, which reduce 02 and H202).
The same function can be attributed to antioxidative
enzymes of helminths. As far as investigated, it appears
that parasites always employ at least one of the relevant
antioxidative enzyme systems (superoxide-dismutase,
catalase, glutathione-dependent enzymes). Additionally,
peroxidoxines, highly conserved antioxidants, which are
especially synthesised under oxidative stress, play a role.
Many parasites modulate or suppress immune react­
ions of the host. Interventions may be non-specific or
specific, and the spectrum of measures of intervention
is broad. It ranges from an impairment of antigen
processing up to the blockade of effector functions.
 Part I. General parasitology
Recently, various parasitic components with respective
properties have been characterised, e.g. particular
protease inhibitors and glycans. Inhibitors of proteases
are encoded by a conserved gene family and interfere
with the immune system of vertebrates. Several
homologues with immunomodulatory properties have
been found in nematodes, for instance the cystatin
homologous cysteine protease inhibitors in filariae.
Vertebrate cystatins, among other functions, regulate
antigen processing in dendritic cells. The filarial
molecule impairs the antigen processing and, thereby,
the activation ofT cells and stimulates IL-10 synthesis.
The immunomodulatory capacity of glycosylated
antigens of various helminths also attracts increasing
interest. Such glycans, which are often modified in a
very specific manner, are partly T cell independent
and immunodominant in the humoral system. Their
expression may be stage specific like glycolipids of eggs
of Schistosoma mansoni, which induce the synthesis of
IL-10, IL-6 and TNF-a and participate in the transition
of the initially Thl dominated response to a Th2
governed type of reaction. They have even been used
as experimental adjuvants to stimulate aTh2 response to
particular antigens. A relatively broad role is also played
by the common phosphorylcholine (PC) modification
of helm in th antigens, which is responsible for frequent
serological cross-reactions between helminth antigens.
Detailed studies with PC-modified molecules offilariae
(e.g. 'PC-ES-62') showed that they favourTh2 responses
by interactions with APCs, uncouple signal chains inT
and B cells, and inhibit the synthesis of pro-inflammatory
cytokines in macrophages.
Furthermore, parasites often induce pronounced
polyclonal B cell activations, which may lead to
massive increases in IgM and IgG plasma concentrations
(mostly in protozoa! infections, see Nagana [ ► p.
62] or leishmanioses [ ► p. 721) or high IgE levels in
helminth infections). These reactions are also triggered
by mediators released by the parasites. Such misguided
responses probably compete with the synthesis of
effective antibodies and, therefore, impair target­
oriented defence measures. Moreover, some parasites
secrete molecules that resemble host cytokines. For
example, proteins have been found in nematodes and
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metacestodes that have structural similarities toTGF-�
·u
C
'6 or macrophage inhibition factor (MIF).These cytokines
�
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are immunosuppressive and act as multipotent activators
� of immune cells. The functionality of the parasite
co
C
molecules has yet to be proven.
·;::
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lmmunomodulating components are also known from
.£ the saliva of blood sucking arthropods (ticks, simuliids).
>-
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Larvae of Hypoderma spp. secrete proteases, so-called
0
0
·u;
co
co
0...
hyp odermins, which cleave antibodies, inhibit the
proliferation of T and B cells and downregulate the
synthesis ofThl cytokines. Generalised Demodex canis
infections in dogs are always associated with severe
impairment of T cell responsiveness.
A further aspect of evasion strategies of parasites is
their influence on apoptotic processes in the host.
Apoptosis, a genetically programmed cell death, is
a physiological process for gentle elimination of no
longer required or disfunctional cells and recycling of
constituents. Parasites are able to induce and to prevent
host cell apoptosis. In the first case, mostly immune cells
are affected, leading to impair defence mechanisms.
Thus, Toxoplasma gondii, plasmodia and Leishmania
donovani cause an enhanced apoptosis of co4+ T cells.
L. donovani predominantly affects Thl cells, i.e. cells
that are associated with abortive infections. Regarding
the prevention of apoptosis, intracellular parasites may
inhibit apoptosis of their host cells to prevent their
untimely death. This is evident in parasites like Eimeria
bovis, which requires >2 weeks to complete the first
merogony in endothelial cells. Similar manipulations
are mainly directed at central pathways of apoptosis. For
example, macromeronts of T heileria parva activate the
transcription factor NF-KB in lymphatic cells, a factor
that is involved in the transcription of many genes and
inhibits apoptosis. Infected cells may therefore persist
in vivo and in vitro.
Hypobiosis may also be classified as an evasion strategy.
Larval stages of gastrointestinal nematodes bypass the
period of time of unsuitable conditions to develop in
the environment within the host. It seems at least partly
immune initiated, but the molecular mechanisms are
not yet understood.
Ectoparasites modulate the host's immune response to
their advantage as well. Products of the salivary glands
of various ixodid ticks and antigens of the warble
fly, Hypoderma lineatum (hypodermins), inhibit the
proliferation of B and T cells in vitro, downregulate
the cytokine synthesis of macrophages (and, thereby,
of T cells too) and suppress inflammatory processes.
Salivary gland products of ixodid ticks block the
alternate pathway of complement activation and prevent
the formation of C3a (anaphylotoxin), i.e. inhibit
inflammatory reactions in the tissue surrounding their
mouthparts.The inhibiting effect of salivary components
of Dermacentor reticulatus on T cells also weakens the
resistance of the host against pathogens transmitted by
ticks. A selective inhibition of Th 17 proliferation by
salivary constituents of ticks is conspicuous, and may
represent an anti-inflammatory measure by the parasite.
 1. Parasite-host relationships

1.5.5 lmmunopathology of parasitic can thus become involved in clinical manifestations of

infections parasitoses or even may determine them.

Summary Irnmunopathological consequences of parasitoses may be

• In addition to parasite-Induced Inflammation (see
above), many parasltoses are aesoclat&d with or
determinecl by immunopathologlcal reactions. They can
be generally classlfled according within the common
scheme of hypersensitivity reaction• (typH MV):
mixed forms are the rule, e.g. In flea allergy In dogs.
High lgE levels may lead to anaphylactlo reactions.
• Another Important lmmunopathologlcal phenomenon
Is the T cell dependent lnteatln•I vlllou• atn,ptly
In gastrointestinal helmlnth Infections. Addltlonally,
autoimmune reaction, due to crou-reacttng anti�
between parasite and host are conaldered reep0nalble
for collateJ81 tlnue damagea In par:tlcular paraslto188.
• In some cases, lmmunopathologlcal reactlont of the
host are an Integral part of the devetopmenlal strategy,
of the parasite, e.g. during the release of Schlstosoma
eggs Into the Intestinal lumen.
Immune reactions aim to neutralise and eliminate
pathogens. They are generally directed to specific
antigens, but effector mechanisms are often broadly
acting and do not differentiate between the real target
organism and surrounding host tissue. Thus, Thi cells
will specifically recognise antigen epitopes, however,
this may activate macrophages to release, for instance
NO, which acts non-specifically. Thus, NO may indeed
kill parasites but may also affect neighbouring, non­
involved host cells. Immunopathological reactions
classified within the common scheme of hypersensitivity >,
0)
reactions ( ► Table 1.7), but are often mixed forms. An 0
0
example is the flea allergy of dogs and cats; in most cases .c
it represents a mix of type I and type IV. Hypersensitivity 0.
reactions are involved in the pathogenesis and clinical 0
C
manifestation of all mange diseases. The exudative ::,
E
dermatitis at the fetlocks of Chorioptes infested horses, E
sheep and goats is an allergic response to mite antigens
and faeces. Sarcoptes infestations show a clear sequence
in hypersensitivity reactions: early after infection, a type
IV response dominates; IgE mediated reactions develop
2-3 weeks after infestation; and, subsequently, a mix of
practically all types of hyp ersensitivity reactions may
be found in infected animals.
A complex of alterations occurring in the helminth
infected intestinal tract and consisting of villus atrophy,
goblet cell hyperplasia and inflammatory infiltration
of the mucosa are, predominantly a consequence of
immunopathological processes. Since athymic animals
lack these alterations, they must be regarded as T cell
mediated. They are rather independent of IFN-y but,
in accordance with the preference of Th2 responses in
helminth infections, are triggered by IL-4 and TNF-a.
Mast cells, induced by IL-4, seem to be the source of
TNF; the damaging component itself is NO, induced by
TNF-a. In addition, TNF-a seems to induce the synthesis
of particular matrix metalloproteinases, which affect

Table 1.7. Hypersensitivity reactions in parasitoses.

Type I - Immediate type allergy (classical local or generalised (shock): flea allergy (dog, cat); shock
allergy): binding of lgE 1 antibodies to Fe-receptors Increased permeablllty of vessels, after rupture of Echinococcus
on mast cells and basophlls, tr1ggerlng of exocytosls extravasatlon of plasma proteins cysts; stings of biting midges
of biogenic amines by binding of allergens and reactive cells Qnflammation), (horses); self-cure reactions in
contraction of smooth muscles gastrointestinal nematode infections
(sheep)
Type II -Antibody dependent cytotoxlclty: opsonlsatlon and lysls of concerned trypanosomes, babesiae (anaemia)
parasite antigens may be adsorbed to host cells or cells
transported to the cell surface, binding of antibodies
with or without complement activation
Type Ill - Immune complex mediated complexes activate glormerulonephritis (e.g. in dogs
hypersensitivity (Arthus reaction): soluble antigens complement; C5a, also C3a, infected with Leishman/a, Babesia
form complexes with antibodies and adhere to C4a (anaphylatoxins), enhanced or 'Direfiiaria immitis), endarteritis in
endothelial cells (particularly small complexes formed vessel permeability: extravasation the lungs (0. immitis infection)
in antigen excess) of proteins and reactive cells
(inflammation)
lype IV - Delayed type hypersensitivity (DTH2): infiltration of reactive cells; extravasation of schistome eggs;
specific T cells release cytoklnes after contact with granuloma formation with flea allergy (mixed form with
antigen (IFN-y, others) subseC!luent fibrotlc conversion type I); scabies; Jones-Mote
reaction (cutameous basophilic
,iQersensitiyjty 2
1
Apart from lgE, also various lgG subclasses are homocytotropic, i.e. bind to homologous mast cells and basophils.
2 A special form in infestations with ectoparasites (licks).
 Part I. General parasitology
the matrix of the L amina propria. Finally, bacterial
components like lipopolysaccharides(LPS) also appear
to be involved in this enteropathy, since gnotobiotic
animals fail to develop these alterations.
Strongly increased IgE levels are generally associated
with helminth infections but are usually of little clinical
relevance(an exception may be, e.g. the rupture of an
Echinococcus cyst). They are caused by polyclonal B
cell activation and are only partially parasite specific.
They do not dispose to allergies as once supposed.
Rather, human allergies are rarer in areas where humans
frequently carry helminth infections than in countries
with high hygienic standards. Experimental studies
in animals indicate that particular helminth-induced
T regulatory cells(TReg) seem to be responsible.
The question of autoimmune reactions in parasitic
infections has only been marginally studied, although
autoantibodies are frequently found in chronic infections.
Obviously, autoimmune processes are responsible
for the damage of ganglions in human Trypanosoma
cruzi infections(Chagas disease), since cross-reacting
epitopes exist in ganglion cells and the parasites. As a
consequence of damaged ganglia, enormous dilatation
of hollow organs(megacolon, megacor) may develop
in the course of chronic Chagas disease.
Diseases are of particular interest when immuno­
pathological reactions are part of the developmental
strategy of parasites. This is considerably striking in
the case of schistosomes, which infect blood vessels
in the bladder or intestinal wall and have to get their
eggs passed into the lumens of bladder or intestine.
The eggs, containing a larva(miracidium), are released
by female worms into the vessels, are swept into the
capillaries where they get stuck. Antigens secreted by
the miracidium interact with specific T cells, resulting
in the release of lymphokines, which attract and activate
a variety o f effector cells in the sense of a type l V
hypersensitivity reaction. Finally, the egg is enclosed in
an active granuloma, which may - provided it is situated
near enough to the mucosal surface - break through into
the lumen of the hollow organ. Since this process also
takes place around eggs that have been swept off into
the liver, brain and other organs, multiple granulomas
Q)
may develop and cause severe tissue damage; this is an
·u
C
'6 important factor in the pathogenesis of schistosomosis.
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�
Last but not least, immunopathological reactions in the
co course of parasitoses may also benefit the host, as shown
C
·c by the self-cure reaction in gastrointestinal nematode
Q)
j infections(see above).
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0)
0 and to plan control measures in an effective, cost-saving
0 and sustainable manner. Control measures., not based
'iii
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co
(l_
1.6 Parasitoses: general aspects
Definitions and nomenclature. Parasitosis (pL:
parasitoses) is a term for an infection or infestation
caused by parasites, regardless of whether it is associated
with clinical symptoms or not. The nomenclature of
parasitoses is handled differently in the literature.
For example, the infection with Fascio la is referred
to as fascioliasis, fascioliase or fasciolosis. The World
Association for the Advancement of Veterinary
Parasitology (WAAVP) has recommended in its
Standardised Nomenclature of Parasitic Diseases
(SNOPAD) to construct the name of a parasitic disease
by adding the suffix '-osis' to the stem of the name
of the parasite taxon(e.g. trypanosom + osis; taeni +
osis; hypoderm + osis)(for exceptions, see Kassai et al.,
1988). ln this book we follow this recommendation.
The term subclinical parasitosis refers to an infection
which causes damage to the host(poor feed conversion,
impaired weight gain, etc.), but n o obvious clinical
symptoms. Opportunistic infections are caused
by facultatively pathogenic agents under conditions
favourable(opportune) for an infection, for example in
immunocompromised hosts. Among infectious diseases,
zoonoses represent a special group. According to a
definition by WHO, zoonoses are diseases and infections
whose causative agents are naturally transmitted between
ver tebrate animals (not animals in general!) and man.
A somewhat wider definition designates zoonoses as
infectious diseases whose causative agents can occur
both in vertebrate animals and humans.
Tenns related to course and other parameters of
parasitoses. Parasitoses predominantly take a chronic
course(gradual onset, duration week or months), rarely
a subacute, acute or peracute. To characterise different
phases of infections, the terms incubation, prepatent
period (prepatency), patent period (patency) and
postpatency are used(► Glossary, p. 620). Infections
can be distinguished in primary infection, reinfection
and superinfection. The term reinfection refers to an
infection of a host which was once infected with a certain
parasite species, but does not harbour the same agent at
the time of a new homologous infection. Superinfection
denotes an infection of a host which is already infected
with a homologous causative agent
Epidemiology, diagnosis and control of
parasitic diseases. One of the main objectives of
veterinary parasitology is to provide the knowledge
necessary for diagnosis, prevention and control of
parasitic diseases. In this context epidemiology plays
a special role as a basis for rational control measures.
Accurate epidemiological knowledge allows a targeted
attack on !ife cycles and transmission ways of parasites,

on epidemiological facts, and the excessive application
of parasiticides to animals according to a 'watering
can principle' include considerable risks, such as the
development of drug-resistant parasite strains and
contamination of animal products (meat, milk, etc.)
or the environment with drug residues; furthermore,
it represents a waste of resources.
Modem epidemiological research includes, in addition
to classical techniques, geographical, mathematical
and molecular methods for evaluating and modelling
epidemiological relationships. It is to be expected that,
due to global climate change, epidemiological conditions
and distribution ranges of parasites may change in the
future. The first signs are already obvious (e.g. ticks,
► Chapter 15.1.1, mosquitoes,► Chapter 14.3.5). Due
to the expanding globalised trade with goods or animals
and tourist traffic, the risk oflong-distance spread and
endemisation of pathogens and vectors is increasing.
Therefore, in addition to research, permanent
monitoring is required to identify epidemiological
changes and emerging infectious diseases in due time.
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Carruthers V, Boothroyd JC (2007) Pulling together: an
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Kassai T, Cordero del Campillo M, Euzeby J, Gaafar S, Hiepe
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Kohler P (2006) Stoffwechselphysiologie von Parasiten. In: Hiepe
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-
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 Part I. General parasitology

Mantovani A, Cassatella MA, Constantini C, Jalllon S (2011)

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Biol Chem 278: 16941-16951.

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Protozoa
Zoonotic pathogens or groups of parasites containing
such pathogens are marked with II
Protozoan derived from protos (G): first; zoon (G):
animal, living being.
Protozoa are a diverse g
eukaryotlc microorganisms with free-lMng, sym
parasitic modes of catJon
the Protozoa to
Excavata, and SAR [Stramenoplles. Alveolata,
and considers the tenn 'Protozoa'• a
without phylogenetic and taxonomic
However, this tenn 18 still used for prao"
• Parasitic protozoa (> 17,000 apeclel)
agents of Important ln1I
for example trypanoaornosla, lellhrnanloela,
toxoplasmosls and cocckllolll. The cellullrstructln
parasitic protozoa la similar to that of other
but they possess some particular cell owvanell
In some groupa, reproduction la asexual (binary or
multiple ftaslon), although the life cyele of most para1ltlc
protozoa Includes an alternation between ISMU8I and
aaxual reproduction.
Morphology. Protozoa are free-living, symbiotic or
parasitic, unicellular, eukaryotic microorganisms of
variable shape and size (approximately 1-300 µm).
Organelles and structures of protozoan cells are
similar to other eukaryotic cells, but some are specific,
particularly in parasitic species. These include the apical
complex of the Apicomplexa (which plays a role in host
cells invasion), the kinetoplast (DNA structure in the
mitochondrion) of Kinetoplasta and specific metabolic
organelles, such as hydrogenosomes, glycosomes and
mitosomes. Likely in adaptation to parasitism, certain
organelles are partially or completely regressed in some
Protozoa. Furthermore, functional adaptations may
occur, e.g. reductive evolution of plastids to apicoplasts
and of mitochondria to hydrogenosomes or mitosomes
( ► Glossary, p. 620). As a result of secondary loss
of structural and functional components, typical
mitochondria are absent in some groups of parasitic
Protozoa (e.g. Giardia, Trichomonas).
Protozoans are enclosed in a thin, double-layered
cell membrane (unit membrane), often with an outer
glycocalix. Some protozoan stages have a thicker, more
robust pellicle (e.g. zoites) making extracellular phases
of life possible, or a wall (e.g. cysts, oocysts) that enables
survival in the external environment.
General life cycle patterns. Some groups of
Protozoa multiply asexually (binary or multiple fissions),
but the multiplication mode of the majority is an
alternation between asexual and sexual reproduction
(agamogony and gamogony, respectively). The life cycles
of Protozoa are mostly complex, including one or several
host species, partially with phases of life outside a host
in the environment.
Protozoa have adapted to diverse habitats and
live in the sea (from deep sea to surface water),
in polar ice, fresh water, soil, or in association with
other organisms as ecto- or endoparasites (> 17,000
parasitic species). Terrestrial and parasitic protozoa
can survive unfavourable environmental conditions
in an encapsulated state as cysts or oocysts. Parasitic
protozoa are heterotrophic, nutrients are taken up across
the cell membrane by permeation, active transport, or
endocytosis (pinocytosis or phagocytosis), partly in
specialised regions of the cell (e.g. flagellar pocket of
trypanosomes, micropores of Apicomplexa, cytostome
of ciliates, peripheral vesicles in Giardia). Energy is
mostly generated by anaerobic glycolysis with excretion
of incompletely oxidised products (e.g. acetate, pyruvate,
succinate), but in some cases also by complete aerobic
oxidation of carbohydrates to CO2 and water.
Systematics. Genetic analyses allow new insights
into relationships between various groups of Protozoa,
resulting in significant modifications of systematics and
taxonomy. Traditionally, the Protozoa were allocated as
regnum or subregnum to the super-regnum Eukaryota,
but nowadays the term 'Protozoa' is regarded as a
collective name without phylogenetic or taxonomic
significance. Taking into account their heterogeneity,
the former 'Protozoa' are now assigned to several
eukaryotic supergroups: Amoebozoa, Excavata, and
SAR (Stramenopiles, Alveolata, Rhizaria) ( ► Table 2.1 ).
Microsporida, originally regarded as Protozoa, are now
thought to be related to fungi and are assigned to the
supergroup Opisthokonta. They are discussed in this
book in the context of Protozoa as a separate phylum.
 Protozoa

-�;.
Table 2.1. Simplified and selective classification of parasitic Protozoa 1 and Microsporidia (also ► Table 1.1, p. 17).
C
\
·'"'·••, ' j; .
C
.....;' '\.

1,0rdet2 FamRy ·Ge,n,s3 0

.. ·-�l.,.,,

1'Ptfjlum: Metamohada, Claat: h�monadll (Supergfdup Exc:allata)

,, - 'Jii' (.)

--
t;::
"iii
(/)
Dlplomonadida - Hexamitidae
-
(0
'!_e�'!'ifa, Gill�!a,_ Oc_f (!_mitus, _5_p!ronu_cl!31JS
Enteromonadlda Enteromonadldae
-- - -· -
Enteromonas ---- - - - - - ---
�etortamonadida Retortamonadldae
·-

Chilomaslix, Retortamonas

J
Phylum: Parabaaala, c,a..: Trlchomonadea (Supergroup Excavata)

Trichomonadida Monocercomonadl Dien/amoeba, Hlstomonas. Monocercomonas, Parahlstomonas

TrichomooacJldaa Penl•""'"'"'°""'· Te1,aMchomonas, T,k,hom/lu;, Trlchomonas,
Trltrlchomonas
_ _LCocl1iosomatidae Coch/osoma ·-

Phylum: Euglenozoa (Supergroup Excavata), Subphylum: Klnetoplasta, Class: Klnetoplastea

_.-o- �� l'l& ._ �.

..,.
-
Trypanosomatida --1
..

\ Tryp��oso�atida; . T;;,pa��s��;. Lei�h,;,a�ia- - .. - •.. -· - . -· -

Bodonida I Bodonidae · Cryptobia, lchth;obod�. Trypano�l�sma -
11Phylum: Percolozoa, Class: Heterolobosea (Supergroup Excavata)
----- - -- -
Schizopyrenida I Vahlkampfiidae I Naegleria, Tetramitus, Vahlkampfia

Phylum: Alveolata (Supergroup SAR) 4, Subphylum: Apicomplexa (syn. Sporozoa), Class: Coccldea

Adelaida Haemogregarinidae Haemogregarina

Karyolysidae Karyolysus
Hepatozoidae Hepatozoon
Klossiellidae Klossiella
Eimeriida Eimeriidae Caryospora, Cyclospora, ElmerlaGoussia, /sospora, Tyzzeria, Wenyonella
Sarcocyslidae Besno/tla, Cysto/sospora, Hammond/a, Neospora, Sarcocystls,
Toxop/asma
Cryptosporida Cryptosporidiidae Cryptosporldlum

!class: Haematozoea (Supergroup SAR) 4

,. . ' ,. '· ' ,S
Haemosporida Plasmodiidae Hepatocr_stl�_!!!�s___fT)odlum
Haemoproteldae Haemoproteus
Leucocytozoidae Leucocytozoon
Piroplasmida Babesiidae Babes/a
Theileriidae Cytauxzoon, Theiler/a
.. -· .
,�ubphylum: Ciliophora, Classes: Litostomatea, Ollgohymenophorea .(Supergroup SAR)4.
.,,,._,.,._. ' i,.. ..
. . ·-"
-·
Vestibuliferida Balantidiidae Balantidium
Pycnotrichidae Buxtonella
lsotrichidae Dasytricha, /sotricha
Entodiniomorphida Buetschliidae Buetschlia
Ophryoscolecidae Diplodinium, Entodinium
Chlamydodontida Chilodonellidae Chilodonel/a
Hymenostomatida lchthyophthiriidae lchthyophthirius
Sessilida Epistylidae Epistylis, Apiosoma, Ambiphrya
Mobilida Trichodinidae Trichodina, Trichodinella, Tripartiel/a
 Part II. Parasites and parasitoses: protozoa

Table 2.1. Continued.

PhY!um: Amoebozoa, Clas�es: Entamoebidae, Lobosea (S�pergrouJ,> Amoebozoa)·

Entamoebida Entamoebidae Endolimax, l:ntamoeba, todamoeba, Matpighamoeba

Euamoebida Hartmannellidae Hartmannella
Thecamoebidae Thecamoeba
Leptomyxiidae Batamuthia
Centramoebida Acanthamoebidae Acanthamoeba
Phylum: Microsporidia5 , Class: Mlcrosporea (Supergroup Oplsthokonta)

Microsporida Nosematidae Anncallia, Encephafitozoon, Enterocytozoon, Nosema, Thelohania,

Vittaforma
Pleistophoridae Gtugea, Loma, Pleistophora, Trachipleistophora
1 Collective name without phylogenetic or taxonomic significance.
2 Latin names of categories, ► Table 1.2, p. 18.
3 In bold: genera with particular relevance to veterinary medicine, as zoonolic agents or as typical examples of the family; alphabetic order
of the genera.
4
SAR: Stramenopiles, Alveolata, Rhizaria.
5 Microsporida now regarded as belonging to the fungal lineage {► p. 155).

I t· Selected references

Adi SM, Simpson AGB, Lane CE, Luke§ J, Bass D, Bowser

SS, Brown MW, Burki F, Dunthorn M, Hampl V, Heiss A,
Hoppenrath M, Lara E, Le Gall L, Lynn DH, McManus
H, Mitchell EA, Mozley-Stanrldge SE, Parfrey LW,
Pawlowski J, Rueckert S, Shadwick RS, Schoch CL,
Smirnov A, Spiegel FW (2012) The revised classif1cation of
Eukaryotes. J Eukary ot Mlcrobiol 59: 429-492.
Leedale GF, Bradbury P (eds.) (2005) Illustrated guide to the
Protozoa. 2°4 revised ed. Lawrence, KS, USA: Allen Press.
ISBN 1-891276-23-9.
Mehlhorn H (ed.) (2008) Encyclopedia of parasitology . 3rd ad,
Berlin, German y: Sp ring er. ISBN: 978-3-640•48 894·8.
Perkins SL (2014 ) Malaria's man y mat.as: past, p resent, and
future of the systematics of tile order Haemos porida. J
Parasltol 100: 1 1-15.
Walker G, Dorrell RG, Schlecht A, Dack• JB (2011)
Eukaryotic systematics: a user's guide for cell biologists
and parasltolog ist.s. Parasitology 138: 1638-1663.
2. Phylum Metamonada

Metamonada are free-living, symbiotic or parasitic

flagellates, adapted to microaerobic or anaerobic •
• Clinical signs. Infections are often asymptomatic, but
co
-0
environments, without mitochondria, but they may '6
can cause disease, especially in young dogs, cats and co
contain non-aerobic alternatives (e.g. mitosomes and ruminants, with acute or chronic, usually intermittent
C
0
hydrogenosomes) and Golgi analogues ( ► Glossary, E
diarrhoea and often malabsorption. 0
p. 620). Metamonada include major human and animal • Diagnosis. Coproscopic detection of cysts (flotation Q_

parasites, for example the genera Giardia, Trichomonas techniques) or cysts and trophozoites ($AFC technique).
0
and Tritriclwmonas. Further options: detection of copro-antigen or copro­
DNA by PCR.
• Treatment and control. Fenbendazole: calves: 10-20
2.1 Class Trepomonadea mg/kg b.w., p.o. for 3 days; dogs and cats: 50 mg/kg
b.w., p.o. for 3-5 days. Alternative for dogs: ronidazole
(off-label-use). Reinfections occur usually after a short
2.1.1 Order Diplomonadida
time In a contaminated environment.
• Zoonotlc Importance. Certain G. duodena/is sub­
Family Hexamitidae groups occur both In animals and humans.

This family contains so-called diplozooic species with

two nuclei and eight flagella. The significance and Agent. In the direct life cycle of Giardia only two stages
function of the double nuclei are still unclear. In Giardia, are involved, the trophozoite as replicative and the cysts
each of the nuclei contains a complete diploid genome. as infective stages. Trophozoites inhabiting the small
intestine have a bilateral and symmetric structure and
Genus Giardia resemble half a pear with a convex dorsal and a flat
ventral side, which carries a large adhesion disk in its
anterior part ( ► Figure 2.1). The cell contains two nuclei
Disease: Giardiosis. at its apical end, 4 pairs of flagella, and characteristic
tubulin-based crescent median bodies. The oval or
roundish cysts, which are excreted by the host to the
Giard, Alfred (1846-1908), French zoologist. environment, contain a parasite cell with 4 nuclei,
fragments of median bodies and flagella. G. duodenalis:
Summary trophozoites: 9-2lx5-12 µm, cysts: 8-15x7-10 µm.
• Agent and o wide
On the basis of morphological criteria, Giardia organisms
distributed I lrds,
reptiles, amp lcal can be assigned to six species or species complexes
features, se Iara/a (hosts in parenthesis): G. duodena/is complex (syn. G.
duoden -,,,,.,-•:iv--_""...., lcrotl intestinalis, G. lamblia) (humans or mammals), G. muris
(roden c:IG. and G. microti (rodents), G. ardeae (birds: herons), and
a fll stlc G. psittaci (birds: parrots), and G. agilis (amphibians). G.
varani, recently isolated from a water monitor (Varanus

Q)
Nucleus
·o
C
A and 8) Adhesion disc
classified 'i'rr-- Median body
'6
Q)

co
Flagellum C
·;::
Q)

C
Posterior pair of flagella >,
0)
0
0
Figure 2.1. Giardia duodena/is. Trophozoite {length
approximately 12 µm) (Graphics: IPZ, M. Mathys). co
0..
Part II. Parasites and parasitoses: protozoa
salvator), has binucleated cysts, but its species status has
not yet been confirmed.
Giardia spp. infect a wide spectrum of hosts, including
mammals (humans and animals), birds, reptiles,
amphibians, and fish. Infections of domestic animals,
wildlife and humans are caused by representatives of
the G. duodena/is group. This is a morphologically
uniform complex with high genetic diversity and
differences in host preferences. Studies of DNA
and protein polymorphisms have revealed that G.
duodena/is consists of several major genetic groups,
described as assemblages A - H (currently available
genome sequences support the view that assemblages
A, B and E are distinct species). Furthermore, sub­
assemblages (clusters of closely related isolates) have
been identified within these genetic variants (which are
called 'genotypes' in a recent publication). It has been
proposed to denote assemblages, sub-assemblages and
variants with capital letters and numbers, e.g. A I - 1 or A
II - 5. In the following simplified overview the currently
known assemblages and hosts are listed (proposed new
species names in parentheses):
• Assemblage A (G. duodena/is): humans, other
primates, cattle and other livestock, dogs, cats, wild
mammals;
• Assemblage B (G. enterica): humans, other primates,
dogs, cats, wild mammals, birds;
• Assemblage CID (G. canis): dogs, other canids, seals;
• Assemblage E (G. bovis): cattle, other ungulates
(sheep, goats, pigs);
• Assemblage F (G. cati): cats;
• Assemblage G (G. simondi): rodents;
• Assemblage H (no proposal): marine mammals
(pinnipeds).
Infections with assemblages A and B occur in a wide
range of hosts, including humans. The human A isolates
belong to A I and A III. Domestic ruminants and pigs
are predominantly infected w1th assemblage E, but
cattle, sheep and pigs are also hosts for assemblage A,
induding A I, which is common In humans. Dogs, often
identified as carriers of the host-specific assemblages C
and D, can also be infected with assemblages A and B,
including A I. A study in the USA revealed that 28 and
41 % of household dogs were infected with assemblages
A and 8, respectively, whereas 15 and 16% harboured
assembl.ages C and D. Cats are hosts of the cat-specific
assemblage F, but may also harbour sub-assemblages A I
and A II[, which also occur in humans. These examples
indicate that some of the assemblages appear to be non­
zoonotic and host specific (e.g. F for cats), while other
assemblages, sub-assemblages and variants occur in
several host species and are therefore considered to be
zoonotic. There is evidence that human infections can
be acquired zoonotically (e.g. cattle -+ humans; dogs
-+ humans). However, a complete understanding of the
extent and significance of zoonotic transmissions under
natural conditions is still limited.
Life cycle (► Figure 2.2). In the direct life cycle of
Giardia, trophozoites colonise the mucosal surface and
lumen of the duodenum and proximal jejunum, more
rarely the distal jejunum and colon or gallbladder. In
these sites trophozoites multiply by longitudinal fission
and may reach high population densities. Mainly in
the distal jejunum, trophozoites encyst by forming
a cyst wall of fibrillar proteins and carbohydrates
(N-acetylgalactosamine). During encystment, the
adhesion disc and the flagella are broken up into
fragments, the nuclei divide, resulting in cysts with 4
nuclei, which are excreted to the environment. After
uptake of the cyst by a susceptible host, the trophozoite is
released - under the influence of low pH in the stomach
and bile in the duodenum. The free trophozoite divides
resulting in 2 trophozoites from each cyst; the adhesion
disc and the flagella are reconstructed. The prepatent
period is usually short (dog, cat: 4-16 days, calf: 4-7 days,
lamb: 10-21 days), the patent period, however, may last
weeks to months.
Epidemiology and occurrence. Cysts excreted in
host faeces are responsible for spreading of the infection.
The number of excreted cysts is usually very large (e.g.
3xl0 5 cysts per g of faeces in calves; equivalent to
150 million cysts in a daily faecal mass of about 500
g/animal). The excretion of cysts often lasts for several
weeks and months; it can vary greatly in intensity
and cease temporarily. Cysts remain infective for up
lo approx.imatdy 3 months in a humid environment
and 3 weeks in cool water, while trophozoites die off
rapidly outside a host. Infection occurs by uptake of
cysts with contaminated drinking water or food, or
by faecal-oral transmission, e.g. in animals by licking
faeces-contaminated parts of the skin. An important
epidemiological parameter is the minimum infective
dose in humans and laboratory animals of only 10-100
cysts.
Worldwide, domestic animals, including ruminants,
swine and carnivores are often infected with Giardia.
In Europe, the average prevalence of G. duodena/is
Infections in calves and lambs is approximately 30%,
and in dogs and cats 3 to > 15%. However, prevalences
are often much higher (S70%) in young animals. In
Germany, the following distribution of assemblages was
identified in 55 Giardia isolates from dogs: A - 60%;
A/C - 27%; non-zoonotic genotypes C and D - 9%
and 4%, respectively. Another recent European study
involving 120 isolates from dogs reported 76% non­
zoonotic genotypes C and/or D. Wild animals can also
be Giardia carriers, as seen in e.g. 1.7% of red deer and
15.5% of roe deer in Norway.
Immunology. Giardia infections in immunocompetent
hosts usually induce immune responses, which can
partially or completely eliminate the parasite population
from the host's intestine and confer some degree of
protection against reinfection. This is reflected, for
 2. Phylum Metamonada

Domestic animals as hosts of

Giardia duodena/is

co
"O
'6
co
C
0
E
0
Q.
0

Trophozoite on
microvillus layer of
Trophozoite small intestine

Oral infection with

cysts

Occasional transmission of certain

Giardia strains to humans

Figure 2.2. Life cycle of Giard/a duodena/is (Graphics: IPZ, S. Ehrat).

example, in decreasing Giardia prevalences in dog of protective immunity T-cell-dependent mechanisms

populations with increasing age or the cessation of
cyst excretion by calves 16 weeks after experimental
infection. G. duodenalis in the gut is capable of expressing
variant-specific proteins (VSPs) against which the host
produces specific IgA and IgG, as shown in various
hosts (humans, mice and cattle). The variability of
the VSPs allows for part of the Giardia population to
escape the immune defence, at least in the early phase of
infection. The appearance of antibodies shortly before
cyst counts start to decline is an indication for their
may also play a role but this needs further clarification.
Pathogenesis. The mechanisms of pathogenicity
are not well understood. Massive infections with
trophozoites can be tolerated by the intestinal mucosa
without apparent disorders or may lead to changes, such
as epithelial damage, increased turnover of enterocytes,
villus atrophy, inflammation of the mucosa, increased
epithelial permeability, disturbance of the absorptive co
C
and digestive functions ( e.g. reduced disaccharase and ·;::

involvement in protective immunity. In infected mice protease activities), enteric loss of fluid and electrolytes,
and humans antibodies (IgG and IgA) increase as soon and effects on the composition of the bacterial flora. .s
as 2 weeks after infection whereas in calves specific >.
OJ
serum antibodies are detectable only 11 weeks p.i. This Clinical signs. In domestic animals, Giardia infections 0
might explain that the elimination of the parasite frnm ofteri remain inapparent. Disease occurs mainly in young
·u5
mice and humans occurs earlier after infection than in animals and manifests as acute, frequently chronic,
cattle. Several studies suggest that in the development catarrhal and intermittent diarrhoea. The incubation co
0..
 Part II. Parasites and parasitoses: protozoa

period usually lasts > 10 days. Clinical signs in dogs cause catarrhal enteritis of medium to high severity in
and cats are soft to watery faeces, presenting increased young mice.
amounts of mucus and fat (steatorrhoea) but rarely
blood, and occasionally vomiting. Symptoms in calves Genus Spironucleus
and lambs include inappetence, loose and watery faeces
for several days or weeks, with reduced weight gain in Spira (L): turn, torsion; nucleus (L): nucleus. Reference
the longer term. Only a few cases of giardiosis have been to shape of nuclei.
described in horses suffering from chronic diarrhoea,
apathy and anorexia. Interestingly, G. duodenalis Spironucleus meleagridis (formerly Hexamita
infections are very common in chinchillas. meleagridis)

Diagnosis. In large animals, Giardia cysts can be

I
� - ' • -·,. -- ..,, .• i:"1

detected with the flotation technique, using ZnCl2
or ZnSO 4 (specific gravity 1.3) as flotation solution
( ► p. 526). The cysts become deformed, but remain
recognisable. In small animals, the SAFC technique
(► p. 530) has proven to be effective, detecting both
trophozoites and cysts (sensitivity of a single sample
examination is approximately 70%). Because of the
intermittent shedding of cysts in faeces, examinations
over 3-5 days may be needed to achieve a higher
sensitivity of detection, reaching up to 94%. Alternatives
are commercial copro-antigen ELISAs (sensitivity >95%)
or rapid tests, based on the detection of cyst wall proteins
using monoclonal antibodies (sensitivity about 80%).
The identification of Giardia species and variants can
be achieved by genetic analyses.
; Disease: Spironucleosis (syn. Hexamitosis) in tl,Jrkey�·
and other bird species.
Agent. Motile trophozoites and non-motile cysts
alternate in the life cycle of Spironucleus meleagridis.
Trophozoites are typically spindle-shaped, 6-12 µm
long, containing two nuclei described as comma- or
S-shaped which may appear in stained smears as a
horseshoe-shaped complex. Six flagella arise anteriorly
from the cell and two caudally. The latter pass from the
anterior end of the cell through tube-like canals to the
posterior end, where they emerge from cytostomes as
free flagella ( ► Figure 2.3). Cysts are ovoid to roundish
(4-5x6-7 µm).

Therapy and control. Fenbendazole in calves and
lambs (l x daily 10-20 mg/kg b.w., p.o. for 3 consecutive
days) and dogs and cats (lx daily 50 mg/kg b.w. for
3-5 days) proved to be effective (clinical improvement,
significant decrease in cyst shedding). Ronidazole in
dogs (2x daily 30-50 mg/kg b.w., p.o. for 7 days) (off­
label-use) has shown high efficacy. However, recurrences
and reinfections in a contaminated environment are
common, therefore, hygiene measures are important.
Cysts a.re killed rapidly by drought or temperatures
>60 °C. Trials with vaccines against Giardia infection in
cats, dogs and calves have so far not shown convincing
protection ( ► p. 570).
Zoonotic importance. The prevalences of Giardia
infections in humans range between 0.4-7% in
temperate regions and 8-30% in tropical areas with
poor living conditions. In Asia, Africa and Latin America
Q}
approximately 200,000 new symptomatic cases are
·u
C
Life cycle and epidemiology. In susceptible hosts
(turkeys}, the flagellates inhabit the entire intestinal tract
during the acute stage of the infection, and later in a
chronic, inapparent phase mainly the caeca. Animals that
survive infections may become asymptomatic carriers
shedding cysts in their faeces. Cysts in faecal material
can survive at room temperature for approximately
1 week, at +4 °C up to 6 weeks. The infection of new
hosts with cysts is favoured by dirty stables, high
population density, and mixing of various age groups.
Chickens and other birds, e.g. young pheasants and
partridges, are susceptible to S. meleagridis and may
act as reservoir hosts and acquire clinically relevant
infections. S. columbae has been described as a causative
agent of intestinal disease in pigeons.

'O recorded each year, but the true incidence is probably

Q} underestimated. As described above, certain genetic
:E
� variants of G. duodena/is are common both to humans
<1J and animal hosts, thus exhibiting zoonoti.c potential.
C
-.::: However, little knowledge exists on the extent and
significance of zoonotic transmission.
_!;
>,
0)
Giardia muris infections in laboratory rodents. G.
0 muris infections frequently go unnoticed in laboratory
0
·1n colonies of mice and hamsters and are often associated
with Spironucleus muris (see below). Most of the Figure 2.3. Trophozoite of Spironucleus sp. (6-12x2-5 µm)
<1J
a.. infections are asymptomatic, but virulent strains can (Graphics: IPZ, A. Seeger; after Roettger 2001).
 2. Phylum Metamonada

Clinical signs. In turkeys, clinical signs may occur
following an incubation of about 1 week. S. meleagridis
infections affect almost exclusively young animals up to
the 10th week of age; the mortality rates can be very high
(up to 80%). Diseased animals have a rough plumage,
are dehydrated and excrete watery-frothy faeces; despite
good food intake they lose weight. After a short duration
of the illness, death may occur or animals survive but
remain often underdeveloped.
Diagnosis. Trophozoites and cysts of S. meleagridis
can be detected microscopically in native and stained
(Heidenhain iron hematoxylin staining) smears of
intestinal fluid or mucus. Necropsy reveals a catarrhal
inflammation of the small intestine with fluid and frothy
content.
Therapy and control. Since nitroimidazole derivatives
are no longer permitted in the EU and in Switzerland,
a satisfactory drug therapy is currently not available,
except in pigeons ( ► Table 17.5, p. 562). Components of
prevention and control include separated maintenance
of young animals, strict hygiene, and no contact with
other gallinaceous birds.
Spironucleus muris
'j
Disease: Spironucleosis in laboratory rodents.
Spironucleus muris (syn. Hexamita muris) occurs globally
in wild and laboratory rodents. Prevalences of 50-80%
have been reported in conventionally maintained mouse
colonies; the parasite can also occur in SPF breeding
colonies. S. muris is pathogenic for young laboratory
mice, occasionally also for young golden hamsters and
rats and can cause catarrhal enteritis (25-50% mortality).
A highly specific and sensitive PCR has been described
for detecting the parasite in faecal samples.
Further genera and species of
Diplomonadida
Various species of the genera Spironucleus or Hexamita
live in the intestine of monkeys (Hexamita pitheci) or in
the intestine and urinary apparatus of amphibians, and
"";:"1 Selected references
Ankarklev J, Jerlstrom-Hultqvist J, Ringqvist E, Troell K,
Svard SG (201O) Behind the smile: cell biology and disease
mechanisms of Giardia species. Nat Rev Microbiol 8: 413-
422.
co
D
Faso C, Hehl AB (2011) Membrane trafficking and organelle D
co
biogenesis in Giardia lamblia: use it or lose it. Int J Parasitol C
0
41, 4 71-480. E
0
Fiechter R, Deplazes P, Schnyder M (2012) Control of Giardia Q.
infections with ronidazole and intensive hygiene management 0
in a dog kennel. Vet Parasltol 187: 93-98.
Geurden T, Vandenhoute E, Pohle H, Casaert S, De Wilde
N, Vercruysse J, Claerebout E (2010) The effect of a
fenbendazole treatment on cyst excretion and weight gain
in calves experimentally infected with Giard/a duodena/is.
Vet Parasitol 169: 18-23.
Geurden T, Olson M (2011) Giard/a in pets and farm animals,
and their zoonotic potential. In: Lujan HD, Svard S (eds.)
Giard/a: a model organism. Wien, Austria: Springer, pp. 71-
85. ISBN 978-3-7091-0197-1.
Grit GH, Van Coppernolle S, Devrlendt B, Geurden T,
Dreesen L, Hope J, Vercruysse J, Cox E, Geldhof P,
Claerebout E (2014) Evaluation of cellular and humoral
systemic immune response against Giard/a duodena/is
infection in cattle. Vet Parasitol 202: 145-155.
Leonhard S, Pfister K, Beelltz P, Wiellnga C, Thompson RCA
(2007) The molecular characterisation of Glardia from dogs
in southern Germany. Vet Parasitol 150: 33-38.
Muller N, von Allman N (2005) Recent insights into the mucosal
reactions associated with Giardia lamblia infections. Int J
Parasitol 35: 1339-1347.
Ryan U, Caccio SM (2013) Zoonotic potential of Giardia. Int J
Parasitol 43: 943-956.
Singer SM (2011) Immunology of Giardia. In: Lujan HD, Svard
S (eds.) Giard/a: a model organism. Wien, Austria: Springer,
pp. 319-328. ISBN 978-3-7091-0197-1.
Thompson RCA (2011) Giardia infections. In: Palmer SR, Lord
Souisby, Torgerson P, Brown DWG (eds.) Oxford textbook
of zoonoses. 2nd ed., Oxford, UK: Oxford University Press,
pp. 522-535. ISBN 978-0-19-857002-8.
Thompson RC, Ash A (2015) Molecular epidemiology of Giard/a
and Cryptosporidium infections. Infect Genet Evol pii: S1567-
1348(15)00404-9.
(!)
C

are also found in humans. S. barkhanus causes systemic

·o
'6
(!)
infections in farmed salmons (high morbidity and 2
mortality). Hexamita spp. are reported to cause enteritis
in trouts and rarely in carps, while Spironucleus spp. co
C
·;::
affect aquarium fish. Species of the genus Chilomastix,
such as C. mesnili in humans and C. gallinarum in
quails and geese have been described as intestinal C

pathogens. In human intestinal infections species of >,

OJ
0
Enteromonas and Retortamonas need to be considered in
differential diagnosis. Octomitus species are commensals ·u;
co
in amphibians and rodents. co
Q_
 3. Phylum Parabasala

Para (G): next, near; basis (lat.): basis. Reference to a in caeca and liver. Outbreaks in turkey flocks are often
parabasal body. associated with high morbidity and mortality. Fatal
histomonosis can also occur in chickens.

3.1 Class Trichomonadea

3.1.1 Order Trichomonadida
Thrix, (G): hair; monas (G): individual being.

The order Trichomonadida (phylum Parabasala)

( ► Table 2.1) is of interest because it contains parasites
of the genital and digestive tract of vertebrates. Main
features of the uninucleated, usually oval-shaped cells
(about 5-25 µm long) are an axostyl composed of
thousands of microtubules, a parabasal body (i.e. an
aggregate of huge dictyosomes), and mostly 4-6 flagella
in certain stages. Reproduction occurs asexually by
longitudinal fission; cyst-like stages (pseudocysts) are
formed only in some species (Tritrichomonas muris, T.
foetus). Since a cytostome is missing, bacteria and other
particles are taken up across the entire cell surface by l<ene.
pinocytosis. ogineala, ollnlcal algns. Turkeys are mostly
nloalfY affected, Hlstomonades Invade the lntestlr:ial
Trichomonadida are microaerophilic/anaerobic �ogenouely to the llver and other orgahs,
organisms; they do not have peroxisomes and present multlply lntercellularly and cause profound necrosis �nd
hydrogenosomes in place of proper mitochondria. Inflammation. In young turkeys, the infection often takes
an acute course, and In older animals a more chronic
These organelles are bounded by a double membrane,
one. Cllnlcel signs Include apathy, weakness, sulphur�
contain no DNA, metabolise pyruvate and produce ATP. /
yellow faecf.tS and occaslonally cyanosls of comb and .,;
Acetate, CO2 and molecular hydrogen are metabolic wattles on the head ('blackhead').
end products. • Dlagnosle. Histological detection of pathogens 11:1.
orgatia, culture, various POR techniques. · ,1,1.
Family Monocercomonadidae • Therapy and control. Currently, there ls"no specific:: .·
antlhlatornonal drug •approved for chemoprophylaxls; "
Monas (G): individual being; kerkos (G): tail. the antibiotic' paromornycln ,11 a potential alternative;
Strateglee for the control. Include hygienic measures,
Typical representatives of this family are characterised aeparate maintenance of turkeys and ,chickens, and
by 3-5 anterior flagella and one traiJing flagellum, but systematic I f H terak/s l11fectlon1.
lack an undulating membrane and costa (compare with
Trichomonas, ► Figure 3.3). The genus Histomonas is
of special veterinary interest. Agent. Histomonas meleagridis ( ► Figure 3.1) involves
several stages in its life cycle: (a) stages inhabiting caecal
Q.)
Genus Histomonas lumina of birds, usually 8-12 µm, are variable in shape
·u
C

'6 and have one, rarely two, flagella. In contrast, tissue­

Q.) invasive stages (b) (caecal wall, liver, etc.) are spheroid,
�
� OisetlSe: HistemonQsii:J in ffl)J.Jlt,yt gl�ead 8-17 µm in size, without flagella, but with pseudopodia,
co
C
dlseaSe. which make active amoeboid movements possible.
·c Spheroid resting stages (c) in Heterakis eggs are smaller
Q.)
than other stages (~3 µm).
-� Histos (G): tissue; monas (G): individual being.
>- Life cycle and epidemiology. H. meleagridis can be
0)
0 Histomonosis, also known as blackhead disease, transmitted indirectly and directly. Indirect transmission
0
infectious enterohepatitis or typhlohepatitis, is caused involves the nematode, Heterakis gallinarum, as a
"ii:i
co by Histomonas meleagridis. The infection affects paratenic host. Female nematodes, parasitising the caeca
co gallinaceous birds, especially turkeys, inducing lesions of gallinaceous birds ( ► p. 341), take up histomonads
0...

a
Figure 3.1. Histomonas meleagrldls: (a) amoeboid form (8·17 µm) In culture (granules in the cells: starch grains). (Photo: M.
Hess); (b) scheme of flagellated form (8· 12 µm) (Graphics: IPZ, M. Mathys).
which multiply in their intestine and subsequently pass
via ovary and oocytes to the eggs of the nematode.
Gallinaceous birds and other susceptible birds become
infected by ingesting Heterakis eggs, containing a
nematode larva infected with Histomonas stages. When
the larva hatches and moults, histomonads are released
and invade the caecal mucosa and are carried in the
bloodstream to the liver and other organs.
Histomonads can survive in Heterakis eggs >2 years
under favourable conditions (moist soil). Long survival
is also possible in earthworms that ingest Heterakis eggs
from which histomonads are released, thereby persisting
in the worm's body cavity. Histomonads voided in faeces
survive only a few hours in the environment (at 22 °C
up to 9 h in faeces and water, 6 h in straw, 3 h on egg­
tray cartons). However, direct transmission is possible
when Histomonas-infected Heterakis-free birds are
commingled with uninfected birds (e.g. turkeys) or when
uninfected birds are exposed to contaminated cages
shortly (1 h) after infected birds have been removed. The
mode of transmission under these conditions is unclear,
but fresh faeces or contaminated water could play a role.
(It is speculated that recently described cyst-like stages
may favour direct transmission, but this has not been
subslantiated). Evidence exists for a direct mode of
transmission by 'cloaca! drinking': when animals sit on
freshly excreted faeces contaminated with histomonads,
reverse peristalsis of the cloaca may allow pathogens to
migrate into the bursa and caeca.
Besides turkey and domestic chicken, further
gallinaceous birds (peacock, guinea fowl, pheasant, quail,
grouse, etc.) and other birds (ostrich, rhea, bustard,
marabou, etc.) are susceptible to H. meleagridis. Chicken
with Heterakis infections are the main reservoir hosts
3. Phylum Parabasala
Flagellum
co
--0
co
C
0
E
0
..c
0
�
Vacuole
of the parasite. The infection risk for turkeys is greatest
in free-range, especially where chickens are also kept.
Occurrence. H. meleagridis has a world-wide
distribution. Outbreaks in turkey flocks are often
associated with high morbidity and mortality, but fatal
histomonosis can also occur in chickens. Since the
ban on the last antihistomonal drug in 2003, disease
outbreaks have increased in Europe and the USA.
Pathogenesis and immunology. From the caecal
lumen, histomonads penetrate into the caecal wall
where they multiply extracellularly, causing lesions in
the mucosa ( ► Figure 3.2). Large parts of the thickened
mucosa become necrotic, and an exudate is produced
that can solidify into hard, cheesy plugs, which adhere to
the mucosa. From the intestinal wall, histomonads can
pass haematogenously to the liver, where they cause a
variety of lesions. Often, these are roundish, usually 3-10
mm wide, yellowish-white necrotic foci with reddish
edges that can merge and reach deep into the liver tissue.
Figure 3.2. Histomonosis in a turkey: lesions in liver and caeca
(Photo: IPB).
Part II. Parasites and parasitoses: protozoa
The pathogen can also colonise the kidney, lung, spleen,
brain, bursa of Fabricius and other organs without
causing noticeable anatomical changes. Gnotobiotic
turkeys were not affected by experimental infection with
H. meleagridis, but typical clinical signs developed when
histomonads were inoculated into the cloaca, together
with Escherichia coli, Clostridium perfringens, Bacillus
subtilis, or the conventional bacterial flora of the caeca.
Immunological studies with chicken experimentally
infected with Heterakis eggs containing infective
Histomonas stages, have shown that a Th2-dominated
immune reaction, induced by Heterakis, shifted to a Thi­
dominated response stimulated by Histomonas. Recent
vaccination trials in chicken with in vitro-attenuated H.
meleagridis present promising results.
Clinical signs. The incubation lasts about 2-3 weeks.
Clinical signs in turkeys include apathy, weakness,
sulphur-yellow faeces and occasionally cyanosis of comb
and wattles on head, which led to the name 'blackhead'.
The degree of illness and mortality depends on age:
young animals, 3-12 weeks old, are very susceptible; the
disease takes an acute course and leads to death in 15-
100% of the animals. In contrast, older turkeys usually
recover after a more chronic course of disease. Chickens
are more resistant than turkeys and may remain
asymptomatically infected with parasites confined to
the caeca. However, they can be severely affected as
a result of liver infection, enhanced by simultaneous
infection of the caeca with Eimeria tenella. Animals that
survive hi.c;tomonosis are partially immune.
Diagnosis. Post-mortem findings must be confirmed
by histological examination (Grocott staining or
PAS reaction), which allows a differential diagnosis
between H. me/eagridis, Candida alb/cans and other
pathogens. PCR techniques for specilk identiflcolion of
H. meleagridis are available. Detection of hlstomonads
in cultures is also possible.
Control. Currently, there ore no speciflc antlhi tomon.iJ
drugs authorised for chemoprophylactic use In Europe.
An alternative is the antibiotic paromomycln which
confers a high degree of protection against H. 111ele11gridis
Infection if applied In feed ot a con entralion of 400
ppm (permitted substan e according 10 EU Regulation
37/2010). The following rneas. ure are recommended
for control: (a) turkeys should be kept separate from
domestic chicken; (b) hygienic maintenance of the
animals In stables with disinfectable floors, metal grids
under automatic feeders and drinkers, litter mu t be kept
dry at all times; (c) before restocking, floors should be
cleaned and disinfected and litter renewed; (d) systematic
control of Heternkis infections ( ► p. 341 ); (t') prevention
of coccldiosis ( ► p. 82). Despite the application of the e
measures, o high infection ri k remains.
Further genera of the family
Monocercomonadidae
Dientamoeba fragilis (usually with 2 nuclei, previously
regarded as amoeba) inhabits the caecum and colon of
humans and some monkey species, rarely of sheep. The
species is considered facultatively pathogenic (irritation
of mucosa). Species of the genus Monocercomonas (3
anterior flagella and I posterior nucleus close to the
anterior end, costa tip extends from the posterior part
of the cell) live in the digestive tract of mammals,
birds, reptiles, amphibians, fish and arthropods.
Monocercomonas ruminantium (syn. Tritrichomonas
ruminantium) occurs in rumen of cattle, rarely of
sheep; non-pathogenic (important: differentiation from
Tritrichomonas foetus, see below). Monocercomonas
cuniculi is found in caecum of rabbits; non-pathogenic.
Family Trichomonadidae
Thrix (G): hair; monas (G): individual being.
Members of this famiJy are usually pyriform, uninucleated
organisms with 2-5 anterior flagella and one posterior
flagellum which passes along an undulating membrane.
Some further cell structures are schematically shown
in ► Figure 3.3 and described below. They contain
hydrogenosomes and Golgi dictyosomes. Several
genera can be distinguished by the number of anterior
flagella: Tritrichomonas (3 ), Trichomonas ( 4 ), and
Pentatrichomonas (5). The genera Tritrichomonas and
Trichomonas are of particular veterinary significance.
Anterior flagella
Parabasal body
Nucleus
Costa
Recurrent
flagellum with
undulating membrane
Flg1.n 3.3. Scheme of a trophoz01te of Trltrichomonas foetus
(length: 10-25 µm) (Graphics: IPZ, M. Mathys).

Genus Tritrichomonas
Tritrichomonas foetus B (bovine strain)
Disease: Bovine tritrichomonosis.
Summary
• Agent Tritrlchomonas foetus: pear- to spindle-shaped
cell bodies (10-25x3-15 µm), 3 anterior flagella, one
flagellum extending backwards, with undulating
membrane and thick axostyl, which projects beyond the
posterior end. T. foetus originating from cattle (bovine
strain "' T. foetus B) is morphologically Identical to T.
foetus orlginatln_g from cats (.. T. foetus C), but thera
are genetic differences (► p. 56).
• Life cycle, epldemlology, occWTtnce. T. foetus B 11 a
sexually tranemitted parasite of the reproductive tract of
cattle. The direct life cycle involve, moblle trophozoltN
which replicate by binary fission. Previous reports that
Immobile 'pseudocysts' may be formed are supported
by recent observation,. Bovine trltrlchomonosls hu a
worldwide distribution, but has been largely eradicated
In central and western Europe.
• Pathogenesis, cllnlcal signs. In bulls uymptomatlc,
persistent infection, predominantly of the preputlal
cavity. In females, ascending Infection to uterus and
oviducts with short persistence of the pathogens for 2-4
months, rartlY longer. Symptoms: early abortions In the
2nd.4th month of gestation, fetal death, endometritls,
reproductive disorders after recovery from Infection.
Repeated Infections are possible, but Immunity
develops in most cases.
• Diagnosis. Parasites are detected mlcroscoplcally, by
culture or by PCR in vaginal mucus, preputlal washings
from bulls or In aborted bovine fetuses.
• Treatment qnd 011trol. Bovine trltrlchomonosls Is
an Ol�llsted noti lable Infection. Control Is based
on anlcnal disease leglslatlon. In cows symptomatic
treatr:l'}ent and sexual rest Is prescribed for three months.
Chemoth�r..a}l)y In bu Is Is not recommended because
of uncertain efficacy. effective control Is possible by
art)flcl�I lpsemihatlon with semen from uninfected
don . In some areas, an Inactivated vaccine against T.
foet s ls t.:JS&d In cattle, but the benefits of this practice
are not well decumented.
Agent and life cycle. I foetus B is pear- to spindle­
shaped, 10-25x3-15 µm in size, has 3 anterior flagella and
1 posteriorly directed which is attached to the cell surface
thus forming an undulating membrane extending almost
over the entire cell body. The posterior flagellum ends in
a free part approximately as long as the anterior flagella
(► Figure 3.3). The axostyl is hyaline and thick, its
pointed posterior end significantly extends the posterior
part of the cell. In the direct life cycle of T. foetus mobile
trophozoites are involved, which multiply by binary
fission. Previous reports that immobile 'pseudocysts'
may be formed are supported by recent observations.
These forms were found in fresh preputial secretions and
3. Phylum Parabasala
described (by light and electron microscopy) as rounded
cells of approximately 8 µm in diameter, without free
flagellum, but with internal flagellar movements. The
rounded forms contain two or more nuclei; they are
capable of dividing by budding, and release pear-shaped
C1:l
trophozoites from the pseudocyst wall. Their potential TI
role in transmission remains to be elucidated. TI
C1:l
C
0
The bovine and cat strain of T. foetus are genetically E
0
.c
closely related to each other and to Tritrichomonas suis. 0
�
Epidemiology and occurrence. T. foetus B has
a worldwide distribution, and is especially important
in certain areas with extensive cattle farming using
natural service. In such regions economic losses can
be significant. Asymptomatic, infected bulls can remain
lifelong carriers of 7: foetus and are the primary source of
infection. Further reservoirs are infected cattle, but the
infection only persists for 2-4 months and not longer than
7 months. Parasite transmission with previously frozen
semen by artificial insemination (AI) is possible, but very
rare, because Al bulls and semen are under regular and
strict control. Other reservoir hosts are not known to
occur. Although 7: foetus B is transmissible to cats (see
below) and T. foetus C to cattle, there is no evidence for
cats representing a source of infection for cattle.
In many countries of central and western Europe, the
wide use of AI has led to the eradication of bovine
tritrichomonosis. As recently shown in Switzerland,
naturally mating bulls are also free of T. foetus.
Pathogenesis and clinical signs. After infection
of female animals during mating, the trichomonads
initially multiply on the vaginal mucosa. Approximately
14-18 days p.i. many parasites are usually detectable
in vaginal mucus. Thereafter, the flagellates migrate
through the cervix into the uterus and may reach
the oviducts. From the vagina, they may disappear
completely or remain and cause a mild catarrhal
inflammation. Early abortions are characteristic of
bovine tritrichomonosis - usually within 2-4 months
after mating - as a result of the parasite's colonisation
of the uterus. If fetus, placenta and fetal membranes are
completely discharged, spontaneous recovery is the rule.
Sometimes abortion does not occur, and the fetus is
macerated in the uterus. Chronic catarrhal inflammation Q)
·u
C
of the mucosa of the genital tract, purulent endometritis, TI
complicated parturition, disorders of reproduction and Q)
sterility may be further episodes of the infection. The
pathogenesis of early abortion is still unclear and may be
ccu
C
linked to the observation that T. foetus cultured in vitro ·c
Q)
produces a protein that is cytotoxic for mammalian cells.
.S
In bulls, T. foetus mainly colonises the preputial cavity, >.
0)
and sometimes the urethra, testicles, epididymides 0
0
and seminal vesicles. Visible lesions do not occur in ·u5
infected bulls and potency and semen quality are not
compromised. cu
Q_
 Part II. Parasites and parasitoses: protozoa
Immunology. In bulls, T.foetus is hardly immunogenic
as the infection usually persists for life. Infected female
cattle are partially immune, but reinfections are possible.
Infected cows produce circulating and local antibodies
(IgG, IgA) against specific antigens of the parasite
(surface polysaccharides, proteins). In some areas, an
inactivated vaccine (TrichGuard•) against T. foetus is
used in cattle, but the benefits of this practice are not
well documented(► p. 569).
Diagnosis. Parasite detection by culture using
a commercial culture system (e.g. InPouch•) with
confirmation by microscopy and DNA analyses has
proved very effective. Sampling under sterile precautions
is essential in order to avoid contamination with
flagellates from the digestive tract (Cercomonas sp.,
Monocercomonas sp.) or the environment. Samples
from bulls: preputial washing fluid or secrete; from
female animals: vaginal or cervical swabs. A bull is
only considered not infected if trichomonads a.re not
found in at least 3 samples, and mating of at least 5
virgin cattle did not lead to an infection(isotest). After
abortion, amniotic fluid, feta.I membranes and the fetus
should be examined. Often trichomonads are found in
the stomach of the fetus.
Therapy and control. Since the infection in cows is
self-limiting, symptomatic treatment is only indicated
if clinical signs exist. After the ban on nitroimidazoles,
there are no registered drugs for systemic treatment of
infected bulls. Local treatments of prepuce and penis have
uncertain outcome and are not recommended. Artificial
insemination with semen from trichomonad-free bulls
is the best method of preventing and eradicating this
infection. 'Bovine tritrichomonosis' is an OEI-listed
notifiable disease.
Tritrichomonas foetus C (cat strain)
Agent, occurrence and epidemiology. Information
on the bovine and cat strains of T. foetus can be found
in the previous section(► p. 55). T. foetus C colonises
Q)
C the intestine of cats and can cause chronic diarrhoea.
·c3
In contrast to T. foetus B in cattle, T. foetus C usually
Q)
does not infect the genital tract in cats. The parasite
�
has a wide geographic range, including numerous
cu
-
C European countries, USA, Australia, Japan, etc. Average
·.::: prevalences in cat populations are high, e.g. 15.7% of
Q)
230 purebred cats in Germany or 14.3% of 140 cats in
-� France. Most of the cats are latent carriers.
-0
0
·u5
cu
Recent studies suggest that transmission via the faecal­
oral route may be more important than direct contact
between infected and non-infected cats. This view is
supported by findings that T. foetus C remains viable in
cat urine and cat food 2:3 h, and can even survive passage
through the alimentary tract of slugs (Limax spp.).
Clinical signs. Colitis and chronic diarrhoea as a
result of the infection of ileum, colon and caecum with
T. foetus C are well documented. Cats younger than 12
months are most frequently affected.
Diagnosis. Parasite detection in culture (InPouch•):
0.5-1 ml native fresh faeces are transferred into the
culture system and incubated for 18-24 h at 37 °C. The
cultures are examined for trichomonads over 5 days.
Other flagellates have to be considered in differential
diagnosis. A PCR has been described allowing the
identification of the bovine and feline strains of T. foetus
to distinguish them from other trichomonads.
Therapy. Ronidazole (off-label-use, ► p. 562) (30
mg/kg b.w., p.o. every 12 h for 2 weeks) is effective in
cats and sometimes leads to complete disruption of
T. foetus shedding. The drug should only be applied
under supervision in small animal clinics because of
occasional side effects.
Trichomonas gallinae
Disease: Avian trlchomonosis.
Summary
• Avian trlchomonosis, ca1Jsed by Trlchomonas gallinae,
is primarily an infection of the upper digestive tract In
pigeons and other birds and can secondarily spread
to other organs (liver, heart, etc.).
Agent. T. gallinae is roughly pear-shaped (6- l 8x2-9
µm), has 4 anterior flagella, a thin axostyl with a short
free tip protruding from the cell, and an undulating
membrane, which does not reach the posterior end of
the cell.
Life cycle, occurrence and epidemiology. T.
gallinae occurs worldwide in domestic pigeons, but is
also found in many other species of birds(gallinaceous
birds, birds of prey, parrots, etc.). In pigeons, the
infection is very common (up to 80% of old birds are
asymptomaticaUy infected); it is also frequent in turkeys,
but rare in domestic chickens. Infected adult pigeons
transmit trichomonads with the so-called crop milk to
the offspring. In contrast, old birds, parrots, turkeys and
chickens acquire the infection through drinking water
that has been contaminated with trichomonads from the
beak cavity of infected pigeons. Birds of prey become
infected by ingestion of captured birds.

Pathogenesis, clinical signs and immunology.
Avian trichomonosis is mainly a disease of young
pigeons in which the infection can lead to a mild or
an acute, fatal disease. Typical lesions occur in beak
cavity, in infraorbital sinuses, pharynx, oesophagus,
crop, and even in the glandular stomach. In addition,
liver, heart, and navel, rarely other organs. The lesions
consist of circumscribed, sometimes disc-shaped,
yellowish, caseous necrotic foci, like 'yellow buttons: In
turkeys and chickens, the lesions usually occur in crop,
oesophagus and pharynx, but only rarely in the beak
cavity or the liver. Since the infection leads to partial
immunity, recovered pigeons remain asymptomatic and
become parasite reservoirs. Avian trichomonosis can
also be important in parrots and birds of prey.
Diagnosis. In living animals samples are taken by crop
swabs and used for microscopic examination of wet or
stained smears or for culture (lnPouch• technique). Post
mortem smears can be made from the boundary layer
between normal and affected tissues or from exudate
of body cavities.
Therapy and control. Nitroimidazole compounds,
effective against trichomonads, are only authorized for
treatment of birds that are not used for food production,
e.g. for carrier pigeons. For this indication several
compounds are registered in various countries, such as
dimetridazole (Chevi-col• 12.5 mg, DE) and ronidazole
(Ridzol•, DE). It should be noted that nitroimidazole­
resistant strains of T. gallinae exist. Prophylactic options
are limited (sanitation, prevention of contact between
pigeons and other domestic or wild birds).
Further species of Trichomonadida
A few species of this group exhibit mild or facultative
pathogenicity (Tetratrichomonas spp., Cochlosoma
spp.), but many are apathogenic, e.g. Tritrichomonas
enteris in caecum and colon of cattle, Tritrichomonas
equi in the large intestine of horses, Tritrichomonas
muris in caecum of rodents (mouse, rat, golden
hamster, Meriones, etc.) or Trichomonas equibuccalis
in oral cavity of horse and donkey. Potential causes of
enteritis are Tetratrichomonas spp. in chickens, turkeys,
geese and ducks and Cochlosoma anatis in ducks and
turkeys. Trichomonas vaginalis is a pathogenic, sexually
transmitted species, causing genital infections in humans
(vaginitis in women, rarely urethritis in men) with
worldwide distribution.
3. Phylum Parabasala
- Selected references
Armstrong PL, McDougald LR (2011) The infection of turkey
poults with Histomonas meleagridis by contact with infected
birds or contaminated cages. Avian Dis 55: 48-50.
Ctl
Baltzell P, Newton H, O'Connor AM (2013) A critical review -0
u
and meta-analysis of the efficacy of whole-cell killed Ctl
C
Tritrichomonas foetus vaccines in beef cattle. J Vet Intern 0
E
Med 27: 760-770. 0
..c
Bernasconi CH, Bodmer M, Doherr MG, Janett F, Thomann (.)
A, Spycher C, lten C, Hentrich B, Gottstein B, Muller
N, Frey CF (2014) Tritrichomonas foetus: prevalence study
in naturally mating bulls in Switzerland. Vet Parasitol 200:
289-294.
Frey CF, Schild M, Hemphill A, Stunzi P, Muller N, Gottstein
B, Burgener IA (2009) Intestinal Tritrichomonas foetus
Infection In cats in Switzerland detected by in vitro cultivation
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Hess M, Grabensteiner E, Liebhart D (2006) Rapid transmission
of the protozon parasite Histomonas meleagridis in turkeys
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Kuehner KA, Marks SL, Kass PH, Sauter-Louis C, Grahn
RA, Barutzki D, Hartmann K (2011) Tritrichomonas foetus
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signs and the role of co-infection with other enteroparasites.
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Liebhart D, Sulejmanovic T, Grafl B, Tichy A, Hess M (2013)
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production in layers following challenge. Avian Pathol 42:
79-84.
Lotti AR, Abdelwhab EM, Hafez HM (2012) Persistence of
Histomonas meteagridis in or on materials used in poultry
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McDougald LR (2005) Blackhead disease (Histomoniasis) in
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Pereira-Neves A, Campero CM, Martinez A, Benchimol M
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Profizi C, Cian A, Meloni D, Hugonnard M, Lambert V, Groud
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Q)
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OJ
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'uj
cu
Cl
Part II. Parasites and parasitoses: protozoa

Schwarz A, Gauly M, Abel H, Dao G, Humburg J, Weiss

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4. Phylum Euglenozoa
Euglenozoa (G): eu: well, good; glene (G): eyeball; zoon
(G): living being, animal. Reference to the eyespot or
stigma of free-living Euglenoida.
- Subphylum Kinetoplasta
4.1 Class Kinetoplastea
Kinein (G): move; plastos (G): formed.
Kinetoplasta are free-living or parasitic protozoa with
1-2 flagella and one or several kinetoplasts, a unique
from of mitochondrial DNA ( ► Figure 4.1). Parasitic
Kinetoplasta occur in all classes of vertebrates and include
pathogens of outstanding importance. For example,
Trypanosoma spp. cause African trypanosomosis in
domestic animals (nagana) and humans (sleeping
sickness or human African trypanosomosis [HAT]), and
Leisl11nania spp. are causative agents of various forms
of leishmaniosis, affecting both humans and animals in
large areas of the world.
Undulating
membrane
Endoplasmatic
reticulum ���;J_.,u____ Golgi apparatus
-'It+--
Autophagosome
Transport vesicle
Basal body and ___.........,.,_,_
flagellar pocket
Figure 4.1. Diagram of a trypomastigote form of Trypanosoma sp. (Graphics: IPZ, M. Mathys).
4.1.1 Order Trypanosomatida ro
'"O
Family Trypanosomatidae E
0
(/)
Trypanon (G): drill; soma (G): body. 0
C
ro
t
Q.
While most species of the Trypanosomatidae pass
through indirect life-cycles, including vertebrates and
vectors (mostly insects), some species are transmitted
directly. In mammalian hosts, trypanosomatids live
freely in blood or body fluids and some of them infect
cells. Development of certain species in vertebrate
and insect hosts is associated with an alternation of
morphological forms that differ in physiology and
function and represent an adaption to diverse living
conditions in hosts and vectors. Spindle-shaped forms
with one flagellum (trypomastigote, epimastigote,
promastigote stages) and a rounded form without a
free flagellum (amastigote stage) are major forms that
can be differentiated morphologically ( ► Figure 4.2).
Trypomastigote forms of the genus Trypanosoma,
occurring in the blood of vertebrates, are spindle­
shaped cells, covered by a cell membrane with a layer
of subpellicular microtubules conferring stability of the
cell. A large nucleus is located centrally, and a single,
large mitochondrion extends through the cell body,
containing in its posterior part a kinetoplast ( ► Figure
4.1). The latter is composed of a network of circular
Cytoskeleton
Mitochondrion
 Part IL Parasites and parasltoses: protozoa
0 0
g
I.
a b C d
Figure 4.2. Forms of Trypanosomatldae: (a) amastlgote form;
(b) promastlgote form; (c) eplmastlgote form; (cl) trypomastlgote
form (Graphics: IPZ, M. Mathys).
DNA molecules with about 50 maxicirdes (23-36 kb)
and several thousand minicirclcs (0.5-2.5 kb) (the
former coding for enzymes of the respiratory chain
and ribosomal RNA, the latter for guide RNA). Close
to the kinetoplast, but outside the mitochondrion, a
flagellum emanates from a basal body located in the
flagellar pocket, a specialised invagination ofthe plasma
membrane with endocylic and secretory functions.
The basal body is linked to the kinetoplast by a special
attachment complex. The flagellum is a 9 + 2 axoneme,
composed of nine outer doublet rnicrotubules and a
central pair of singlet microtubules. As the flagellum
emerges from the flagcllar pocket it is entirely allached to
the cell body except for the tip which might project over
the anterior cell boundary as a free flagellum. Junctionnl
protein complexes hold lhc membrnnes oft he flagellum
and the cell in tight contact, so that during movement nn
undulating membrane is folded out; thl phenomenon
is visible under a light microscope. The flagellar waves
cause forward movements (flagellum lip leading) of
the cell and simultaneously rotations around ils axis,
comparable to a drill (see name: trypm1011 = drill). In
addition to cell propulsion, the flagellum plays a role in
(I)
other functions, such as morphogenesis and parasite­
·o
C
'6 host Interactions (e.g. attachment of r co11golense to
(I)
endothelial cells in blood vessels of the vertebrate host).
The cell surface(except flagellar pocket) of blood stages
ofcertain species ('I: brucei-group, T. co11gole11se and r
<1l
C
·c
(I) vivnx) is covered with a 15 nm thick surface coat, almost
exclusively consisting of variable gl)1coproteins (VSG)
.!: (► p. 36). Under the light microscope the following
>,
structures can be seen in Giemsa-stained thin blood
0)
0 smears: nucleus (possibly nucleolus), kinetoplast,
0
'iii flagellum, undulating membrane, a few cytoplasmatic
ro granules and basal body(► Figure 4.3 and 4.6).
ro
a..
Genus Trypanosoma
Members of the genus Trypanosoma are grouped
into two categories: the pathogenic Salivaria and the
mostly apathogenic Stercoraria, the latter including
the pathogenic species Trypanosoma cruzi. Salivarian
trypanosomes develop in the anterior digestive tract of
insect vectors, stercorarian species in the posterior part
(►Table 4.1 and 4.2).
Trypanosomes of the Salivaria group
Saliva (L): saliva. Reference to transmission of pathogens
in saliva of vectors.
Summary
• Agentl and ooowrwnce. Sallvartan trypanosomes are
aplndle-1haped, flagellated, extra-cellular parasites
containing a klnetoplut. Pathogenic species usually
have a blunt posterior end, with the klnetoplast In
terminal or 1Ubtermlnal position; a free flagellum tip
at the anterior end may be present ( ► Figure 4.3).
»ypano,oma congo/enM, T. vlvax, T. brucel brucel
caUN animal African bypanolomOsls (nagana), and T.
bruc»I gernb/ense and T. b. rhodes/ense human African
trypanoeomoels (sleeping slckneu). Surra, caused by T.
brucel evansl, Is distributed In large areas of Africa, Asia
and Latin America and affects many animal species,
predominantly camels, equlds and dogs. Oourine Is
a widely distributed sexually transmitted Infection of
horses and other equlds, caused by T,ypanosoma
brucei equlperdum. Most parts of Europe are cunently
surra- and dourlne-free, but ■ risk of spreading the
Infection from endemic to non-endemic areas exlats.
Both dlseues are OIE-llsted notifiable dlHaw
• Life cycle. Trypanoaornea of the T. brucel group, T.
vlvax and T. congo/ense are cycllcally transmitted
through ullva of blood-sucking tHtN flies, within
which the paruitn pan through a developmental
cycle. 'hnlmlulon of T. ..,_ (partially allO of T. VMlt)
happtnl non-cyclically via contaminated mouthparta
of tabanld1 or other haematophagou1 ftlN. T. b.
� II tranlmltted chctly during mating.
• lnvnunoloD, Antibody-mediated rnechanlarnl can
ltrangly oontrol perulte 1'9productlon, hc>Mwr, long·
llltlflg pnlatenoe of lnf9ctlonl In vertebrate ham la
IOOOfflPlllhld by hqua,t and complete rwplacernent
"'uflce lntlglna (antigenic variation). thul avoiding
Immune lllninatlon.
• Cllnlcll ...... Ginni cllnical llgl,a of the dlNaNa
ITW1tiallld lboYe n limlllr and not pathognomonic.
Thay Include lntlnnlttant few,(cauMd by rwapelng,
Immunological paratte ellmlnatlon), progrualve
....., lnfllmmalian and-. necroail, cachexla.
CNS dilofdera, and death. In dourine of horHa,
ll1lclrill aim, -- and oedema of genital organs
and lower body pll1S may be partlcularty striking, but
limfllr ligns can lllo occur In other trypanosome
•
lnfectianl(e.g. lUITI).
 4. Phylum Euglenozoa

Table 4.1. Trypanosoma species (selection) of the Salivaria group.

Trypanosoma species1 and Name of disease, vertebrate host! and host-related Vec1ors and mode of �
disbibution (D) pathogenicity of causative ag1tft!i2 transmission

Trypanosoma vivaxD I Animal African Trypanosomosis (AAT) or Nagana tsetse flies (Glossina spp.): cu
-0
D: Sub-Saharan Africa(within and Bovinae •·•, Equidae, Camelidae.. , Caprinae·, antelopes, cyclic; haematophagous
outside the 'tsetse belt') giraffe n flies: non-cyclic �
E0
Trypanosoma vivaxD inapparent infection haematophagous flies: (/)
D: Central and South America domestic ruminants n, Equidae· non-cyclic 0
C
Trypanosoma congo/enseN
cu
Nagana tsetse flies: cyclic 0.
D: Sub-Saharan Africa Bovinae··. Equidae, Camelidae, Caprinae, Suidae, >,
Carnivora· I antelopes, giraffe n �
Trypanosoma simiae N
Nagana tsetse flies: cyclic
D: Sub-Saharan Africa Suidae, Camelidae ... , Equidae, Bovinae, Caprinae,
Carnivora (")
Trypanosoma suisP Nagana tsetse flies: cyclic
D: Sub-Saharan Africa Suidae·r♦
Trypanosoma brucef brucefT Nagana tsetse flies: cyclic
D: Sub-Saharan Africa Equldae, Carnelldae ... , Carnivore..
Bovinae, Suldae•, Caprinae, antilopes(')
Trypanosoma brucef rhodesfenseT Human African trypanosomosls(HAT) or Sleeping sickness tsetse flies: cyclic
D: Sub-Saharan Africa(eastern and humans· 0, bushbuck, duiker, Impala, reedbuck, warthog,
southern) zebra, giraffe, lion, hyena, etc. (')
Trypanosoma brucef gambfenseT Human African trypanosomosis(HAT) or Sleeping sickness tsetse flies: cyclic
D: Sub-Saharan Africa (western and humans···, (pig, cattle, sheep, dog, antelopes) (')3
central)
Trypanosoma brucei evansiT Surra tabanids, other flies and
D: Africa, Middle East, Eurasia, Latin Equidae, Camelidae..·, Carnivora*.., Bovinae, elephants'/*' vampire bats: non-cyclic;
America carnivores: peroral
transmission
Trypanosoma brucei equiperdumT Dourine coitus: non-cyclic, direct
D: Asia, Africa, eastern Europe, Latin Equidae•· transmission
America
1 Subgenera: 0 = Duttonel/a, N =Nannomonas, P = Pycnomonas, T = Trypanozoon.
2 Asterics refer to the preceding names and indicate approximate degrees of pathogenicity: ... high, •• medium, • low, (") usually inapparent

infection.
3 Animals of low, if any, epidemiological significance.

Table 4.2. Trypanosoma species (selection) of the section Stercorarla.

:.��:�r'.1(,.--.i ;:1,,�11:rr; .1:,rJ)t,11d1j) 1 :�c ..1 (,u:11, •1 1 ·.

l�' p1 l I H·.,�' �l •
(!!:O I
1/·•�; ;�), i,,_-)1,"�;� \<_ 1a!�\-�1.£.'.J��,,·1tt1'":l
II''r I: 1t.L.., <) ·_,l',;'..l
\¥{�c-j\�l[� �;°11,·tfGg: .�i'
\:� 1,CF�01t!Y,\
Trypanosoma cruz/S Chagas disease (American Try�lnosc;>mos1s) Reauviida.e (kissing buQJs):
D: Central and South America, USA humans•••, dog, cat •r-,
guinea pig, oposswms, armadillos, cyclic
many species of other mammals (*)
i 't,ypanosoma theileriM apathogenlc or facultatlve pathogenic Talbanidae: cyclic;
I D: worldwicle cattle(*, rarely *") lxG€iidae: cyclic3

I T,ypanosoma melophagium apathogernlc Melo/;ihagus ovinus(sheep

M

D: worldwide sheep(*) ked): cyclic

I Trypanosoma cew,-M4 apathoQJenic Tabal'lidae: cyclic
D: Eurasia, No11th America red deer(*) ..,
Tr;ypanosoma lewisi H5 apatmogenie fleas: cy,clic
D�olldwLde
1
Subgenera: H = Herpetosoma, M = Megatrypanum s = Schizotrypanum.
2 Asterics refer to the preceding names and indicate approximate degrees of pathogenicity: ••• high, •• medium, • low, (") usually inapparent

infection.
3 Developmental stages of T. theileri, detected in salivary glands and haemolymph of ticks (lxodes, Hyalomma, etc.) are indicative of cyclic

transmission but it is not proven.

4 Further species in roe deer and other cervids (vectors: always tabanids).
5 Further species in many rodents (vectors: always fleas).
 Part II. Parasites and parasitoses: protozoa

•
• Diagnosis. Because cllnlcal signs are not characterlatlc,
Trypanosoma vivax,
species
T. congolense and other

aetlologlcal confirmation Is required by parasite
detection In wet or stained smears of blood, lymph node
or other materials �ow sensitivity) or by concentration
techniques (haematocrlt centrifugation technique)
(higher sensitivity). Highly sensitive PCR strategies are
preferentlally used for the Identification of Ttypanosoma
species. Techniques for detecting specific humoral
antibodies (eUSA, etc.) are mainly employed for surveys
and monitoring of animal populatlone, eometlmu u
diagnostic aids In Individual cases. OFT 11 the official
test for dourlne preacrlbed by OIE.
• Therapy and control. ll'eatment of trypanoeome
Infections In domestic animals rellea on eeveral
drugs, such as leometamldlum chorlde, melaraomlne,
and dlmlnazlne. Control measures against African
trypanosomoaea In cattle Include monitoring and
treatment of herds, teetee control, and uee of
trypanotolerant breeds. Surra and dourlne .,. OIE•
listed notifiable dll88181; epeclal regulatlone muet be
observed In International animal export and Import.
• Zoonotlc Importance. Sleeping alckneu, caused by
T. b. rhodeslense, 11 a zoonottc Infection with wild and
domestic animals II reaervolr hoet. In contrast, the T. b.
gamblense form of the dlaease Is predominantly a non­
zoonotlc Infection with human to human transmission
of the pathogen, but animals may be locally Involved
In the cycle.
J•
Disease: African animal trypanosomosis (AAn
(Nagana).
_ j
Sir D. Bruce (1855-1931) detected Trypanosoma brucei
in J 894; nagana (Zulu): powerless, weak.
Agents. All species of domestic mammals are
susceptible to one or more species of African animal
trypanosomes ( ► Table 4. J ). The species most
pathogenic for cattle are T. vivax and T. congolense, for
pigs T. simiae, and for horses T. b. brucei. Within these
species, strains of different virulence (nosodemes) occur
in various regions. Wild mammals (including warthog,
antelope species, etc.) act as reservoir hosts, but are
usually asymptomatic despite prolonged parasitaemia.
Blood stages of the various species vary in length from
about 12 to 40 µm ( ► Figure 4.3). In T. congolense and
T. vivax these stages are uniform (monomorphic), but
in the 1: brucei group they occur as longer slim and
shorter 'stumpy' forms (pleomorphic); the latter are no
longer capable of multiplication in the mammalian host.
Life cycle. ► Figure 4.4. In the vertebrate host,
trypanosomes live freely in blood; they multiply as
trypomastigote forms by longitudinal fission, and can
be taken up by tsetse flies with a blood meal. Only
the stumpy forms of the T. brucei group (see above)
are infectious to the vector. In the fly, the pathogens

Salivaria Stercorarla

T>C
(l)

'6

ro T. b. brucei T. congolense T. vivax T. b. equiperdum T. cruzi T. theileri

C
·;:: 12-26 µm· 12-15 µm 20-27 µm 15-30 µm 16-22 µm 60/70-120 µm
(l)
30-40 µm··
.£ • Stumpy forms. " Slender forms
>-
0)
0 Figure 4.3. Trypanosoma species. Salivaria: blunt posterior end; Stercoraria: pointy posterior end (pleomorphy only in T. b.
0
·enro brucet) (Graphics: IPZ, A. Seeger; after Levine 1985).

ro
0..
 4. Phylum Euglenozoa

Cattle, equids, camelids, and other

host animals

co
"O
�
E
0
(,/)
............ 0

'\
C
co
0.
>,
/
I
I -� \
I .,
Trans1t1on to
stumpy form
- -----...
.
f.
1-'\'.:'..
I
I
.,.,..,;_
Trypomastigote form
(slender form)
:---..._�,
Stumpy form I
'( Development in blood plasma

Tsetse fly

Trypomastigote metacy­
clic form

Trypomastigote
form

Epimastigote
dividing form

Epimastigote form

Figure 4.4. Life cycle of Trypanosoma b. brucei (Graphics: IPZ, S. Ehrat).

transform into epimastigote forms and multiply only
in mouthparts (proboscis) (T. vivax), in proboscis and
midgut (T. congolense) or in midgut and salivary glands
(T. b. brucei). Finally, infective metacyclic stages are
formed, morphologically very similar to trypomastigote
stages, which are transmitted in saliva of a blood-feeding
tsetse fly to a new host. The development in the tsetse
fly takes about 1-3 weeks depending on environmental
temperature. Once infected, tsetse flies are capable of
transmitting metacyclic stages throughout their life
(up to 6 months). In addition to cyclical transmission,
non-cyclical (mechanical) transmission may happen
through other biting flies (mainly Tabanidae, also
Stomoxynae) which can transfer infective stages with
their contaminated mouthparts when they interrupt
a blood meal on an infected host and bite a new host
shortly thereafter. This represents an epidemiologically
important mode of transmission for T. vivax.
Part II. Parasites and parasitoses: protozoa
After vector-mediated inoculation of infective stages
into the mammalian skin, the parasites multiply by
binary fission in tissue fluid at the bite site. After 4-8
days they pass into lymph and blood, where further
multiplication occurs. In this phase they are especially
numerous in lymph nodes. Whereas T. vivax and T.
congolense live almost exclusively in blood plasma, T.
b. brucei passes also into tissue fluids. At some stage,
trypanosomes can invade the liquor cerebrospinalis
and multiply there as well as in intercellular spaces in
the brain. Trypomastigote forms are first detectable in
blood about 1-2 weeks p.i.; the duration of parasitaemia
is variable and may last many months.
Occurrence and epidemiology. The geographic
range of nagana is largely identical to that of the tsetse
flies (Glossina spp.), which occur in Sub-Saharan Africa
in an area of about 10 million km2 between 14 °N and
29 °S. Because T. vivax is also transmitted non-cyclically
by biting flies other than tsetse flies, it can exist in Africa
outside the tsetse belt. This species has spread from
Africa to Mauritius and Latin America where T. vivax is
commonly in enzootic equilibrium, but outbreaks with
clinical signs in cattle are known to occur. Isolates from
South America are genetically closely related to isolates
of West African origin, but both are widely separated
from east African isolates.
Trypanosomes in Africa occur in heterogeneously
distributed endemic foci and in cycles between tsetse
flies and wild mammals, in which the infection is almost
exclusively inapparent (see below). Nagana becomes a
problem when humans with their domestic animals
expand to habitats or even displace them. In this
situation, tsetse flies use domestic mammals as blood
donors and can transmit trypanosomes to them. Many
Glossina species are vectors of African tr ypanosomes,
Figure 4.5. Clinical signs of trypanosomoses: (a) chronic nagana in cattle with extreme emaciation (Photo: IPZ, R. Eugster); (b)
horse, infected with Trypanosoma b. brucei showing distinct oedema at anterior chest and abdomen (Photo: W.O. Neitz; A. Latif).
belonging to two main groups living in different habitats:
G. morsitans group (savannas) and G. palpalis group
(wetlands)(► p. 481).
Clinical signs. T. congolense can cause peracute to
chronic disease in cattle, sheep, horses and camels. T.
vivax comprises strains differing widely in virulence;
cattle, sheep and goats are at most risk, while this
species is less pathogenic for horses. T. b. brucei causes
severe disease in horses, camels, dogs and cats. In other
domestic animals the infection is asymptomatic or
associated with rather mild clinical signs. T. vivax and
T. congolense are considered 'haematic' trypanosomes
because they do not usually leave blood and lymph
vessels, while T. b. brucei may also reside in extravascular
tissue spaces.
The first sign of an infection with any of the nagana
trypanosomes is an inflammatory focus at the
inoculation site in response to local multiplication
of trypanosomes in the skin. Usually, this reaction
remains unnoticed. After migration of trypanosomes
to the bloodstream and incubation periods of 4 days
to 5 weeks (T. congolense, T. vivax) or 1-2 weeks (T. b.
brucei), intermittent episodes of fever occur, associated
with weakness, apathy, nasal discharge, lacrinial and
salivary flow (► Figure 4.Sa). However, the cardinal
sign of infection is progressive anaemia, which may
begin in the second week p.i. Within 2-3 months the
haematocrit values can decline by half, accompanied
by leukopenia and thrombocytopenia. In T. b. brucei
infections, inflammation and necrosis in various
tissues play an important role in the extravascular
immunological elimination of parasites. Often animals
show extensive oedema in the anterior chest area, lower
abdomen, male genitalia and on limbs(► Figure 4.Sb).
Furthermore, locomotory and CNS disorders may

occur. In the late phases of infection, depending on
host and trypanosome species/strain, the disease leads
to emaciation, ascites and jaundice within weeks or
months, and finally to death.
Immunology and pathogenesis. Specific antibodies
directed against the parasites' surface may directly or
by antibody-mediated cellular mechanisms damage
or kill the parasites. Immunological processes play a
significant role in the pathogenesis of nagana. Antigenic
variation of trypanosomes (► p. 36) leads to alternating
waves of parasitaemia and irregular fevers. High levels
of antibodies (particularly lgM as a result of polyclonal
B-cell activation) and antigens of trypanosomes result
in the formation of circulating immune complexes
causing organ damage (endarteritis, glomerulonephritis,
etc.). Additional changes in T. brucei infections include
inflammatory and degenerative processes in organ
parenchyma, even in the CNS. In infections with
haematic trypanosomes (see above), central nervous
changes due to formation of microthrombi and
resulting hypoxemia play an important role. One of
the decisive factors in the pathogenesis of nagana is
immunosuppression, which generally reduces resistance
of the infected animals and paves the way to secondary
infections. An important role is also played by anaemia
which is aetiologically complex. Hypoglycaemia,
regularly occurring in highly parasitaemic animals,
has a negative effect on the stability of the erythrocyte
membrane. Trypanosomes can release phospholipases
which damage the erythrocyte membrane resulting in
haemolysis. Another mechanism is binding of circulating
trypanosome antigens to the surface of erythrocytes,
resulting in immune elimination of these cells. Finally,
infected animals develop dyserythropoiesis after initially
increased erythropoiesis. Resistance of humans and
some primates to several African animal pathogenic
trypanosomes ( T. b. brucei, T. b. evansi) is attributed to
a lipoprotein (apolipoprotein LI) which occurs in serum
and kills the parasites.
Pathology. At necropsy, the animal body in typical
chronic cases is highly emaciated and anaemic; other
findings include swelling of the liver, spleen and lymph
nodes, gastroenteritis and in acute cases bleeding
in mucous and serous membranes. Histologically,
the depletion of lymphoid cells and inflammatory­
degenerative processes are detectable.
Oiagnosis. The aetiological diagnosis is based on
microscopic detection of trypanosomes in blood or
aspirated lymph node material (wet mount, Giemsa­
stained thin or thick smears) (► Figure 4.3 and 4.6).
Thin smears allow the morphological identification of
certain Trypanosoma species. However, the sensitivity
of this technique is low, especially in chronic infections
with low parasitaemia. Higher sensitivities can be
achieved with concentration techniques, such as
haematocrit centrifugation technique (HCT). In a
4. Phylum Euglenozoa
0
··�
-
C'Cl
0 el")
-0
�
co
•
,.,... 1 E
0
(/)
;
0
C
co
>-
i=
�
A
Figure 4.6. Thin blood smear with Trypanosoma b. brucei
(length: 30-40 µm) (Photo: IPZ).
recent comparative field study, 12% of 411 cattle scored
positive for trypanosomes in HCT, and 18 or 30% in
two different PCRs, respectively. PCRs play a special
role in the species identification of trypanosomes; a
procedure for discrimination of several species (T.
vivax, T. congolense, T. b. brucei) in mixed infections of
cattle has been described. Serological methods (ELISAs)
for detecting specific antibodies are suitable for herd
surveillance, but they do not allow a species-specific
diagnosis.
Therapy. Chemotherapy of AAT in cattle, sheep
and goats relies on several drugs, such as diminazene
aceturate and isometamidium; the latter is also used in
prophylaxis. However, drug resistance is a considerable
problem. Diminazene is toxic to camels, equids and dogs.
These animals can be safely treated with melarsomine
(► p. 67).
Control. Several options exist for controlling AAT in
cattle, sheep and goats, either as single or combined
measures: (a) chemotherapy/chemoprophylaxis
and monitoring, (b) tsetse control and (c) livestock
husbandry with trypanotolerant breeds. A vaccine
against nagana is currently not available. AAT in cattle
('tsetse-transmitted') is an OIE-listed notifiable infection.
• Chemotherapy/chemoprophy laxis. Regular
treatment of cattle with trypanocidal drugs in certain
intervals is indicated if animals are permanently
exposed to the infection (at low exposure only
treatment of diseased individuals, at high exposure
treatment of all animals in a herd). Isometamidium
is preferred for cattle, sheep and goats because of
its long-lasting efficacy (2-6 months). Cattle from
tsetse-free areas should be treated during transport
through endemic areas; as should potentially infected
animals if imported into tsetse-free areas.
• Tsetse control. See Glossinidae ► p. 481.
• Livestock husbandry with trypanotolerant breeds.
Certain African cattle breeds (e.g. N'Dama, Muturu,
Baoule) and some sheep and goat breeds have a higher
 Part II. Parasites and parasitoses: protozoa
resistance to trypanosomes (limited multiplication of
the parasites) and exhibit milder clinical signs after
infection (lower degree of anaemia) than European
or zebu breeds. Therefore, at high exposure, resistant
local breeds can be economically superior to
imported breeds.
Zoonotic importance. Sleeping sickness or Human
African Trypanosomosis (HAT ) is caused by T. brucei
gambiense or T. brucei rhodesiense and is transmitted by
tsetse flies (Glossina spp.). HAT is known as an important
disease in Sub-Saharan Africa since the end of the 19th
century ( ► Table 4.1). Currently, HAT occurs in around
360 foci in 36 Sub-Saharan countries, mainly located in
rural and remote areas. In recent years, the prevalence
of HAT has decreased to approximately 6,300 new cases
reported in 2013 with 99% caused by 1: l,. gambiense.
Although gambiense HAT takes a more chronic course
than rhodesiense HAT, both diseases are considered
to have a fatality rate of 100% in untreated patients.
Currently, approximately 70 million people in Africa
live at different levels of risk for HAT. For travellers, the
infection risk during short stays in Africa is low, as long
as recommended precautions are observed. As indicated
in ► Table 4.1 rhodesiense HAT is a zoonosis with
many vertebrate animals playing an epidemiological
role as reservoir hosts. In contrast, T. b. gambiense is
predominantly transmitted between humans by tsetse
flies. However, there is some evidence that animals (e.g.
pigs) may be involved in the transmission cycle in some
foci. Occasionally, animal-specific Trypanosoma species
(T. b. brucei, T. congolense, T. vivax, T. b. evansi, T. lewisi)
have caused mostly transient infections in humans (19
cases between 1974 and 2010).
Trypanosoma brucei evansi (syn. Trypanosoma
evansi)
Surra (Hindi): rotten. G.H. Evans (1835-1935), British
veterinary officer, detected the causative agent of surra
in equines and dromedaries in India in 1880.
Q)
Agent and life cycle. Trypanosoma brucei evansi, the
·u
C
'6 causative agent of surra, has a wide host range, which
Q)
� includes, amongst others, camels, horses, cattle, buffaloes,
cco pigs, dogs and many species of wildlife ( ► Table 4.1 ).
C The pathogen is transmitted non-cyclically by tabanids,
·c
Q) other haematophagous flies or (in Latin America) by
vampire bats. Carnivores may acquire the infection by
C ingestion of fresh blood or meat of infected hosts with
>, subsequent transition of trypanosomes into the body via
0)
0 the oral mucosa. In susceptible mammalian hosts, T. b.
0
·u5 evansi multiplies by binary fission in the trypomastigote
co form which lives in blood and extravascularly in tissue
co
0.. fluids, including the CNS. These stages resemble slender
forms of T. b. brucei ( ► Figure 4.3) and are covered with
a layer of variable surface glycoprotein (VSG, ► p. 36).
It is believed that T. brucei evansi has evolved from T.
brucei brucei through the complete loss of maxicircles in
kinetoplast DNA (kDNA), associated with the inability
to undergo cyclic development in an insect vector. Thus,
T. b. evansi is restricted to trypomastigote forms, which
are mechanically transmitted by insects or other vectors.
Isolates of T. b. evansi may have minicircles or can be
devoid of both maxi- and minicircles. Such isolates are
more frequent in Latin America compared to T. b. evansi
isolates from the Old World. T. equinum, previously
described as a distinct species, has been synonymised
with T. b. evansi or 1: b. equiperdum and will not
be further considered herein. T. b. evansi and T. b.
equiperdum are closely related, but they differ regarding
transmission routes, diseases caused and kDNA content.
Whereas in the former species maxicircles are missing,
the latter contains at least fragments of them.
Occurrence and epidemiology. T. b. evansi origi­
nated in Africa and currently has a wide geographic
range, including Africa (north of the tsetse belt, but also
within this zone in arid regions of Sudan and northern
Kenya), the Arabian Peninsula, Middle East, and Eurasia
(Turkey, from southern Russia to central, southern and
south-eastern Asia). In the 15th century the parasite was
introduced with Arabian horses to Latin America and is
now endemic in regions from Argentina to Panama. In
the 20th century the parasite was introduced to Canada
and Australia, but was subsequently eradicated. In
Europe, T. b. evansi was known to occur in the Canary
Islands/Spain since 1997, when the first case was
diagnosed in a dromedary imported from Mauretania.
Further outbreaks were observed in France in 2006
and in mainland Spain in 2008, both associated with
the importation of camels from Canary Islands. Strict
control measures have prevented spreading and resulted
in eradication.
T. b. evansi is predominantly a parasite of Camelidae and
Equidae, but it also infects domestic ruminants, pigs,
dogs, cats, elephants and a vast number of wild mammals.
In some local outbreaks prevalences may be high, e.g.
around 70-80% in horses in South America. In various
regions the significance of the infection for certain hosts
varies. For example, cattle are more susceptible to T.
b. evansi in Asia than in Africa or Latin America. The
list of wild animals described as hosts of T. b. evansi
is long and includes, among others, many species of
ruminants, pigs, rabbits, rodents, carnivores, and also
marsupials, vampire bats, and primates (the latter two
in Latin America). However, the epidemiological role
is known only for some of them. Furthermore, different
vectors are involved, predominantly several species of
Tabanidae and Stomoxys with vampire bats as additional
vectors in regions of Latin America. Non-vectorial
modes include iatrogenic and peroral transmission (the

latter in carnivores). Large numbers of mammalian
hosts, 'silent' parasite carriers, non-cyclic means of
vectorial transmission, climate change and international
dislocations of animals (trade, travelling) are specific
risk factors for disease spreading.
Clinical signs. Clinical entities caused by T. b. evansi
were described under many different names, including
Surra (India), Mal de Caderas (Latin America) and
El Debab (North Africa). Infections of various hosts
with T. b. evansi may remain inapparent and persist for
many years or lead to acute and chronic disease with
fatal outcome, depending on the host species and other
factors. Camelids, equids and dogs are highly susceptible
and are often severely affected. As an example, the
clinical course in horses is outlined here. Clinical signs
appear after incubation periods of 1-4 (up to 8) weeks,
such as intermittent fever, associated with parasitaemia,
progressive anaemia, weakness and weight loss,
urticaria! skin plaques, oedema predominantly in lower
parts of the body (abdomen, genital organs, etc.), and
sometimes petechial haemorrhages (conjunctiva, vaginal
mucosa, etc.). Disturbed locomotion, central nervous
disorders (paralysis, paresis) and immunosuppression
are signs of advanced phases of the disease. In na'ive
horse populations mortality can be high (>50%), but
in endemic areas horses and donkeys may exhibit mild
clinical signs, or they may remain infected as latent
parasite carriers. In dogs the infection can take a rapid
acute course leading to death within a week or month.
Diagnosis. In the acute phase of the infection with
high parasite densities, trypanosomes can be detected
microscopically in wet or stained smears of blood
or lymph node material. Lower parasite densities in
the chronic phase require concentration techniques
(e.g. haematocrit centrifugation technique, HCT). A
PCR protocol has been described which allows the
differentiation between T. b. brucei/T. b. evansi and T.
b. equiperdum. Several serological tests are available
for specific antibody detection, including ELISAs and
a card agglutination test (CCT/T. evansi); the latter has
a sensitivity of around 85% in horses or camels (with
lower sensitivity in cattle) and is suitable for field use.
Therapy and control. T. b. evansi infections can be
eliminated from camels by treatment with melarsomine
(Cymelarsan•) (0.5 mg/kg b.w., i.m.) twice with an
interval of one month. The following doses (mg/kg b.w.)
are recommended in the literature for other animals:
horses 0.25-0.5, cattle 0.5, buffalo 0.75 and dogs 1.0-2.0.
Surra is listed by OIE as a notifiable infection. Sporadic
outbreaks can be controlled by chemotherapy of
infected or suspected animals and sanitary measures
(quarantine, long-term monitoring of animals using
sensitive diagnostic methods, insect control). In view
of favourable conditions for spreading of the infection
(see above), strict preventive regulations for animals
4. Phylum Euglenozoa
imported from endemic to non-endemic areas are of
great importance.
Zoonotic importance. Due to the trypanolytic serum
factor apolipoprotein L-1 (APOL-1) ( ► p. 65) humans co
are usually resistant to infections with T. b. evansi. In -0
2005, a case of T. b. evansi infection was detected in India E
in a patient with a mutation in both APOL-1 alleles and 0
en
0
a consequent lack of APO-LI activity in serum. There C
ro
are no reports on other cases. Q.
>,
Trypanosoma brucei equiperdum (syn.
Trypanosoma equiperdum)
Disease: Dourine in equids.
Dourine (Arabic): dirt.
Summary
• Agent and occurrence. r. b. equlperdum Is the
causative agent of a venereal disease In horses and
donkeys. Previously of worldwlde distribution, it rs now
confined to parts of Asia, Africa, Latin America, and
eastern Europe; central and western Europe are free
of this disease.
• Life cycle and cllnlcal signs. Transmission during
mating. Disease occurs usually In three phases: (a)
local inflammation of genital organs; (b) transition of
parasites to blood and formation of transient urtlcarlal
skin plaques weeks after infection: (c) trypanosomes
pass to the cerebrosplnal fluid resulting in locomotory
disorders, paralysis and finally death If highly virulent
parasite strains are involved.
• Diagnosis and control. Detection of specific antibodies
(CFT in many countries mandatory). Dourlne Is notifiable
to OIE and to national authorities in many countries.
Outbreaks in non-endemic areas have been controlled
by quarantine measures and ellminatlon of infected
equines (stamping-out). Melarsomine (CymelarsanGD)
(0.25-0.5 mg/kg b.w. i.m.) has proven highly effective
against T. b. equlperdum In horses, but chemotherapy
Is rarely Indicated.
Parasite and life cy cle. Dourine is a mostly chronic
venereal disease of horses and other equines, caused by
T. b. equiperdum and transmitted directly during mating.
The pathogen is morphologically indistinguishable from
T. b. evansi ( ► Figure 4.3), but differs in several features
( ► p. 66). Natural infections have been found only in
equids; other mammals (e.g. mouse, rat, rabbit) can
experimentally be infected, although they are rather
resistant. T. b. equiperdum is primarily an extracellular
tissue parasite and is rarely detected in blood.
Occurrence and epidemiology. Dourine occurs in
parts of Africa (including Ethiopia, Namibia, Botswana,
South Africa), in the Middle East, Asia (e.g. Pakistan),
 Part II. Parasites and parasitoses: protozoa
South America and eastern Europe (e.g. Russia). In other
parts of Europe, dourine has been observed in recent
decades only in Italy, where the last outbreak occurred
in 2011. However, uncertainties exist regarding the
reliability of official animal disease reports from certain
countries. In some areas, it is unclear whether infections
in horses are due to T. b. evansi or T. b. equiperdum.
Spreading of the disease is possible during the latent
phase of the infection. £quids are the only natural
reservoir hosts for this pathogen. Aside from mating,
T. b. equiperdum can be transmitted via semen and,
rarely, via milk from mares to their foals.
Pathogenesis and clinical signs. After trans­
mission from stallion to mare or mare to stallion,
parasites are initially found free on the mucosa! surface
or between epithelial cells. Subsequently, they pass into
tissues, inducing oedematous patches in the genital
tract, and into the bloodstream which carries them to
various parts of the body. Once they reach tissues, the
parasites can persist extracellularly for months or years,
and occasionally pass to the cerebrospinal fluid. In some
horses and more often in donkeys and mules, which are
more resistant, the infection can remain unapparent.
In horses, the infection may be acute, but it is typically
chronic with an incubation period of 2-12 weeks and a
duration of ½-2 years. Frequently the following three
phases of the disease can be distinguished:
• Phase 1. Mucoid vaginal discharge, formation of
nodules, blisters and ulcers in the mucosa of vagina,
penis and prepuce, local oedema in lower body
parts (chest, abdomen, genitalia, mammary gland),
sometimes accompanied by low-grade intermittent
fever or subfebrile temperatures.
• Phase 2. Usually 4-9 weeks p.i. occurrence of typical,
transient urticaria!, non-itching plaques in skin,
particularly over the ribs and lateral abdominal
wall, consisting of elevated lesions, up to 5-8 cm in
diameter and I cm thick. They persist a few hours
or days and can appear repeatedly.
• Phase 3. Either chronic, almost inapparent infection
(only mild anaemia) or progressive deterioration
of the general condition with anaemia as a result
from bone marrow damage and general metabolic
disturbances. Clinical signs: Muscle atrophy,
locomotory incoordination, progressive paresis
Q)
C and paralysis of muscles of the nostrils and neck,
·c3
i5 hindquarters and eventually the entire body. Highly
Q)
� viruJent strains of T. b. equiperdum usually lead to
c
co
fataJ disease while less virulent lead to low-grade
C disease or unapparent infections.
·.:
Q)
Diagnosis. Clinical signs, especially urticaria! patches,
C are indicative for dourine, but not pathognomonic.
>­ Therefore, diagnosis has to be confirmed by laboratory
CJ)
tests, usually by detection of specific serum antibodies.
·en
co
In many states, CFT is used which is prescribed by OIE
co
Cl.
for testing of equids in international trade. T his test
cross-reacts with T. b. evansi and T. b. brucei, it has a
low sensitivity and could be replaced by better methods
(e.g. ELISA). Differential diagnosis between infections
with T. b. brucei, T. b. evansi and T. b. equiperdum is
possible by DNA analysis. The microscopic detection
of T. b. equiperdum in liquid from plaques or swabs in
the genital mucosa is rarely successful.
Therapy and control. Dourine is a notifiable disease
to OIE and to national authorities in many countries.
Most European countries are dourine-free. Prevention
of disease importation to non-endemic areas by infected
equines is subject to specific OIE and national rules whid.
include mandatory examination by CFT. Quaranti1
measures and elimination of infected equines (stampir
out) have proven successful in controlling of outbrea:
Melarsomine (Cymelarsan•) (0.25-0.5 mg/kg b.w., i.r
has proven highly effective against T. b. equiperdu,· .i
horses, but chemotherapy is rarely indicated.
r.'.'l' Selected references ·
Cauchard J, Soldan A, Madeline A, Johnson P, Buscher
P, Petry S (2014) Inter-laboratory ring trials to evaluate
serological methods for dourine diagnosis. Vet Parasitol
205: 70-76.
Desquesnes M, Holzmuller P, Lai DH, Dargantes A, Lun
ZR, Jittaplapong S (2013) Trypanosoma evansi and surra:
a review and perspectives on origin , history, distribution.
taxonomy, morphology, hosts. and pathogenic effects.
Biomed Res Int 2013: 194176.
Desquesnes M, Dargantes A, Lai DH, Lun ZR, Holzmuller
P, Jittapalapong 5 (2013) Trypanosoma evansi and surra:
a review and perspectives on transmission , epidemiology
and control. impact, and zoonotic aspects. Biomed Res Int
2013: 321237.
Franco JR, Slmarro PP, Diarra A, Jannin JG (2014)
Epidemiology of human African trypanosomiasis. Clin
Epldemiol 6: 257-275.
Gutierrez C, Tamarlt A, Gonzalez-Martin M, Tejedor-Junco
MT (2014) Control and eventual eradication of Trypanosoma
evansi Infection in dromedary camels after an episodic
outbreak in mainland Spain: an example in a non-endemic
area. Vet Parasitol 204: 153-157.
Hablla N, lnuwa MH, Aimola IA, Udeh MU, Haruna E (2012)
Pathogenic mechanisms of Trypanosoma evansi infections.
Res Vet Sci 93: 13-17.
Motl Y, Fikru R, Buscher P, Van Den Abbeele J, Duchateau
L, Delespaux V. (2014) Detection of African animal
trypanosomes: the haematocrit centrifugation technique
compared to PCR with samples stored on filter paper or in
DNA protecting buffer. Vet Parasitol 203: 253-258.

Tran T, Napier G, Rowan T, Cordel C, Labuschagne M,
Delespaux V, Van Reet N, Erasmus H, Joubert A,
Buscher P (2014) Development and evaluation of an ITS1
'Touchdown' PCR for assessment of drug efficacy against
animal African trypanosomosis. Vet Parasitol 202: 164-170.
True P, Buscher P, Cuny G, Gonzatti Ml, Jannin J, Joshi P,
Juyal P, Lun ZR, Mattioli R, Pays E, Simarro PP, Teixeira
MM, Touratler L, Vincendeau P, Desquesnes M (2013)
Atypical human infections by animal trypanosomes. PLoS
Negl Trop Dis 7(9): e2256.
■ Trypanosomes of the section Stercoraria
Stacus (L): manure, faeces. Reference to transmission
of the pathogen in faeces of vectors.
Summary
Stercorarla trypanosomes are usually non-pathogenic
(!)r faeultatlve pathogenic. Characteristics of blood
forms are: free flagellum always present, posterior end
pointed, large klnetoplast In subtermlnal position. The
i1Y.1Panasomes are cyclically transmitted by Insects
wlnleh excrete metacycllc forms In their faeces.
• tl:le pathogenic species Ttypsnosoms cruzl Is the
causative agent of Chagas disease In humans, an
Important zoonotlc disease, occumlng In Central and
South America. Vectors are blood-sucking bugs.
(a) Pathogenic species
Trypanosoma cruzi
Carlos Chagas, bacteriologist, Rio de Janeiro, 1879-
1934, discoverer of T. cruzi. Oswaldo Cruz, Brazilian
physician (1872-1917).
Agent. In vertebrates, T. cruzi multiplies intracellularly
in the amastigote form (0 1.5-4.0 µm) and appears
in the blood plasma in the trypomastigote form (16-
22 �Lm long), which is characterised by an unusually
large kinetoplast in subterminal position, and a pointed
posterior end ( ► Figure 4.3). Several strains exist,
referred to as T. cruzi I and II a-e, adapted to different
host species.
U',- • �de. Vectors are bugs (Reduviidae, Triatominae),
including species of the genera Triatoma, Rhodnius,
Panstrongylus and others. During blood-sucking on
an infected host, bugs ingest trypomastigote forms
of T. cruzi, which transform in the digestive tract to
intermediary stages and epimastigotes which multiply
by binary fission. Finally, epimastigotes give rise to
trypomastigote, metacyclic stages which are excreted
4. Phylum Euglenozoa
in faeces. This cycle takes about one to two weeks
( ► Figure 4.7). If infected bugs have deposited faeces
during blood-feeding on a new host, metacyclic forms
can pass into the body through small skin lesions or
mucous membranes (eyes, mouth). Animals may acquire ro
-0
the infection by ingestion and crushing infected vectors
�
or by eating an infected host. E
0
(/)
0
In vertebrate hosts, the trypomastigotes infect cells where C
ro
they transform into amastigotes that multiply by binary
t
Q.
fission free in the cytoplasm (without parasitophorous
vacuole). This leads to the formation of parasite 'nests'
in host tissues comprising hundreds of amastigote
stages called 'pseudocysts', because parasites are only
bounded by the cell membrane and not by a cyst wall.
Eventually, intracellular amastigotes differentiate into
trypomastigotes that burst out of the cell and enter
the blood stream, whereupon the cell infection cycle is
repeated. Trypomastigotes do not multiply in the blood
stream, but resume replication either in a new cell or in
the vector. Pseudocysts may be found in various tissues,
including cardiac and skeletal muscles, smooth muscles
and neuroglia.
Occurrence and epidemiology. r cruzi with its
different strains occurs in wild and domestic animals in
a wide range, extending from southern Argentina and
Chile to the southern United States (up to California and
Virginia). Approximately, 150 species of mammals are
susceptible, including humans, whereas birds, reptiles
and amphibians are refractory. Important reservoir hosts
are rodents, opossums, armadillos, and dogs. Numerous
species of Triatominae are capable of transmitting
the pathogen. Many of them are epidemiologically
insignificant as they live in sylvatic habitats. The most
important vector species from an epidemiological
perspective are the ones which have adapted to life in
simple human dwellings and animal stables, profiting
from protection and food sources.
Pathogenesis and clinical signs. In dogs up
to the first year of age, the infection is often acute
with sudden heart failure, due to direct, parasite­
induced cell damage. Deaths from heart failure are
not uncommon at this stage. In surviving animals
hepatomegaly and splenomegaly, anaemia, oedema and
ascites, cachexia, fever, respiratory symptoms and heart
failure dominate the clinical picture. The acute phase is
followed by a transitional period of 8-36 months with
minor clinical signs. Thereafter, progressive chronic
myocardia develops, characterised by heart dilatation
(megacor) with poor prognosis. Pathogenesis includes
immunologically induced destruction of ganglia cells
of the autonomic nervous system and inflammatory
processes, especially in myocardial tissues. Cats are
also susceptible to T. cruzi infections, but little is known
about the corresponding clinical picture.
 Part II. Parasites and parasitoses: protozoa

Human as accidental host

Reservoir hosts

Multiplication in an Transition into

amastigote form trypomastigote forms

Reduvild bug

....
:r::;":.r:::,s� ""'-'
Excretion of �
Uptake of trypomast1gote stages
t r 1 /
; durlng blood-feeding

Intestine of \
(
( reduviid bug �

j
Q)
C
·c3 Epimastigote and
'6
Q) / other forms
�
� "'-----
al
C
·c
Q) Figure 4.7. Life cycle of Trypanosoma cruzi (Graphics: IPZ, S. Ehrat).

j
.£
>, Diagnosis. Trypanosomes are only detectable in serological detection of specific antibodies (ELISA,
-
0)
0 the blood shortly before or during the acute phase of IFAT cross-reactions in dogs with leishmaniosis!) or
0
""ialn the disease. Chronic infections can be diagnosed by by molecular detection of the pathogen (PCR).
....
a..
al

�herapy and control. Chemotherapy in dogs is
difficult. In acute cases, treatment with benznidazole
5-7 mg/kg b.w. daily for about 2 months may mitigate
the clinical course, but does not prevent subsequent
chronic cardiac disease. Vector control with insecticides
and prevention of disease transmission through blood
transfusions or by ingestion of potential reservoir hosts
are recommended.
Zoonotic importance. In humans, Chagas disease is
largely inapparent during the acute phase. However, after
an incubation period of 10-20 years, serious pathological
changes can occur. They are due to the damage to tissue
cells and ganglia of the autonomic nervous system and
are characterised by marked dilatations, so-called
mega formations, of internal organs, e.g. megacor,
megaoesophagus, megacolon and by neurological
disorders. Chagas disease is endemic in Latin America;
the number of infected people is currently estimated
to be around 7 million with approximately 50,000 new
cases each year. In Europe, cases of Chagas disease are
diagnosed occasionally in people from Latin America.
(b) Apathogenic or facultative pathogenic
species
Stercorarian trypanosomes, occurring in domestic and
wild animals, have previously attracted little attention
because of low or apparently lacking pathogenicity. So
far, the pathogenic potential of only a few species is
known, and respective knowledge on many other species
is lacking. Therefore, more research is needed to evaluate
the impact of these parasites, especially for wild animals.
In recent years molecular techniques have significantly
improved the possibilities for such studies.
Trypanosoma (Megatrypanum) theileri
Sir Arnold Theiler (1867-1936), veterinarian of Swiss
origin, scientist and pioneer of South African veterinary
services.
Agent. Trypanosomes of the subgenus Megatrypanum
are large flagellates with a pointed posterior end and a
kinetoplast not in terminal position(► Figure 4.3). T.
theileri is 60-70 µm long with variations between 25
and 120 µm. Species of the subgenus Megatrypanum
are restricted to domestic or wild ruminants. Recent
molecular analyses revealed several lineages and
genotypes within the subgenus, including T. theileri.
For example, cattle and buffaloes are infected by different
genotypes of this species.
L1t · ;ycle and epidemiology. T. theileri is transmitted
cyclically by tabanid flies (Tabanus spp., Haematopota
spp., etc.). It is assumed that cattle become infected
during defence against fly attacks when they accidentally
capture flies with the tongue and crush them, so that the
pathogens are released. Subsequently, the trypanosomes
4. Phylum Euglenozoa
can penetrate the oral mucosa and pass into the lymph
and blood vascular system and tissues. Multiplication
occurs in the epimastigote form by binary fission. In
blood, lymph and liquor cerebrospinalis (LCS) both
trypomastigote and epimastigote stages can be found. co
-0
There are indications that ixodid ticks may be capable
�
of transmitting T. theileri trypanosomes, but this has E
not been cohfirmed. Vertical transmission from cows 0
(/)
0
to offspring has been reported. C
co
0.
T. theilerihas a worldwide distribution with variable
prevalences(up to 80%) in cattle. For example, according
to a recent report (2013) 35% of cattle in the USA are
infected. T. theileri also occurs in European game
animals, for example in roe deer and European elk in
Sweden.
Clinical signs and diagnosis. Infections with T.
theilerl in cattle are almost always inapparent. Massive
T. theileri infections in calves and adult cattle have been
associated with clinical signs (e.g. anaemia, abortion,
CNS disorders), but the causal relationship remains
unclear. The parasite can easily be detected in blood,
lymph node aspirates or LCS in cultures(using different
media) or by PCR.
Other species of vertebrates
Examples of further species of this group are
Trypanosoma melophagium specific to sheep (vector:
sheep ked, Melophagus ovinus), T. nabiasi (rabbit,
vector: flea, Spilopsyllus) belonging to the subgenus
Megatrypanum, and T. lewisi (rats, vector: rat flea,
Nosopsyllus) from the subgenus Herpetosoma.
■ Trypanosomes in birds and fish
Hundreds of bird species (chickens, pigeons, ducks,
finches, crows, birds of prey, etc.) have been identified
as hosts of trypanosomes allocated to the Trypanosoma
avium complex which includes three genetic clades
named after the principle species: T. avium, T. corvi
and T. bennetti.
It appears that these avian trypanosomes have a
certain degree of host and vector specificity. Blackflies,
hippoboscid flies and mosquitoes have been described
as vectors that transmit the trypanosomes cyclically
through their faeces. The T. avium complex is distributed
worldwide and can occasionally cause disease, for
example in captive falcons; these cases were successfully
treated with melarsomine(Cyrnelarsan•).
An example of trypanosomes occurring in fish is
Trypanosoma danilewskyi. This species infects freshwater
fish (carp, tench, perch, eel, pike and others), lives in
blood plasma and extravascularly in kidney, spleen
and other organs, and can cause high parasitaemia
with clinical signs(listlessness and emaciation). Blood
 Part II. Parasites and parasitoses: protozoa
stages are about 20 µm long, slender and very mobile.
The parasite is transmitted by fish leeches (Piscicola,
Hemiclepsis).
11111 Selected references:,,;;;,-""
Fisher AC , Schuster G, Cobb WJ, James AM, Cooper
SM, Perez de Leon AA, Holm an PJ (2013) Molecular
characterization of Trypanosoma (Megatrypanum) spp.
infecting cattle (Bos taurus), white-tailed deer (Odocoileus
virginianus), and elk (Cervus elaphus canadensis) in the United
States. Vet Parasitol 197: 29-42.
Hughes AL , Piontkivsk a H (2003) Phylogeny of Trypano­
somatidae and Bodonidae (Kinetoplastlda) based on 18S
rRNA: evidence for paraphyly of Trypanosoma and six other
genera. Mol Biol Evol 20: 644-652.
Kir chhoff LV (2011) Epidemiology of American trypanosomiasis
(Chagas disease). Adv Parasitol 75: 1-18.
Martinkovi c F, Mat anovic K, Rodrigues AC, Garcia HA,
Teixeir a MM (2012) Trypanosoma (Megatrypanum)
melophagium in the sheep ked Melophagus ovlnus from
organic farms in Croatia: phylogenetic inferences support
restriction to sheep and sheep keds and close relationship
with trypanosomes from other ruminant species. J Eukaryot
Microbiol 59: 134-144.
Neumuller M, NIisson K, P ahlson C (2012) Trypanosoma
spp. in Swedish game animals. Parasitol Res 110: 135-139.
Schofield CJ (2011) American trypanosomosis (Chagas disease).
In: Palmer SR, Lord Soulsby, Torgerson PR, Brown DW (eds.)
Oxford textbook of zoonoses. 2nd ed. Oxford, UK: Oxford
University Press, pp. 498-508. ISBN 978-0-19-857002-8.
Tarallo W (2005) Trypanosoma avium incidence, pathogenicity
and response to melarsomine in falcons from Kuwait. Parasite
12: 85-87.
Thompson CK, Godfrey SS, Thompson RC (2014)
Trypanosomes of Australian mammals: a review. Int J
Pa,asitol Parasites Wild! 3: 57-66.
Votypka J, Obomlk M, Volf P, Svobodova M, Lukes J (2002)
Trypa.nosoma av/um of raptors (Falconiformes): phylogeny
and identification of vectors. Parasitology 125: 253-263.
Genus Leishmania
Species of the genus LeishmaniQ (subgenera Leishmania
and Viannia) are parasites of mammals, causing disease
(lei.shmaniosis) in humans and animals, including
carnivores, ruminants and horses. Some species occur
in reptiles, e.g. Leishmania adleri in lizards, geckos and
chameleons. The parasites pass through an indirect
life cycle and are transmitted cyclically by sand flies
(Phlebotominae). In the mammalian host, the parasite
C exists in an amastigote form in cells of the mononuclear
phagocytic system (MPS) {macrophages, monocytes,
Langerhans cells, etc.), and in a promastigote form
extracellularly in the intestine of the insect vector.
Leishmanioses are widespread in tropical. subtropical
and temperate regions, including southern parts of
Europe.
Various Leishmania species and strains are morpho­
logically indistinguishable and are often referred to
as 'species complexes'. Their differentiation is based
on biological criteria (clinical picture, hosts, vectors)
and molecular characteristics. In humans, Leishmania
species cause different forms of disease, which can be
roughly classified into three main groups (the list of
species is not complete):
a. Visceral leishmanioses. Old World: Leishmania
donovani complex and L. infantum complex; vectors:
Phlebotomus species. New World: L. infantum
complex, vectors: Lutzomyia species.
b. Cutaneous leishmanioses. Old World: L. tropica,
L. major and L. aethiopica, vectors: Phlebotomus
species.
c. Mucocutaneous leishmanioses. New World: L.
mexicana complex, L. braziliensis complex, vectors:
Lutzomyia species.
Of the species listed above the Leishmania braziliensis
complex belongs to the subgenus Viannia, all others
are members of the subgenus Leishmania. Among the
15 Leishmania species known to infect humans, 13 are
zoonotic.
t..eishmania infantum
· Disease: Leishmaniosis in animals and humans. ti
Sir W.B. Leishman ( 1865-1926), Scottish pathologist and
British Army Medical Officer, detected the causative
agent of leishmaniosis in 190 l; infans (L): small child.
Leishmaniosis in dogs
Summary
• Agent and IHe cycle. L. lnf,ntum, the causative agent
of oanlne lef1hmanlosla, 11 transmitted cycllcally by
bltN of tend nre. (PhlebQ�om1nae). In the verte.bra.t e
hOet th• parulte muttlplltt In cells of the mol'lOnuclear
phagooytle l}'lltttm (MPS).
• Oooufflno., tPldtmloJ0ty. The geographloal range
of b lntantum tncludn the Mediterranean region
(t,rt,lfl(fing nQfthwMta to th• AIPI), IQUth·WMtem
an<t tQuth-,i&Jt•n t;yrope, Middle E,qt, areaa In
fOUtflem ��trill� l.Att1n Americtt anc! North
� S,,,oprevalencq in dgpo r&J1go from <,1 �
VP to 'lbout �% in endemic M4'diterranean regions.
f. � are #le ma!Jl r�o,r hotM; tox�. rarely cats,
wtld rlbbitf, hares, and r1t1 can be parasite carriers,
� art CQf'IJl'(terecf epldem1ologlcally less lmportaht.
LMhmln/f:.'tnfeeted dogs fromendemic areas are often
�ed to non�mle regions, tor example to
Ctnvol or northem European countries or to the UK 1
t "

•
• Immunology and pathogenesis. Dominant cell-
mediated immunity (Th1 activation, coa + cytotoxic T
cells) is usually associated with inapparent or subcllnlcal
infection, but dominance of Th2 cell activities and
polyclonal 8-cell activation Is associated with pathology.
Humoral antibodies directed against Leishman/a
antigens are not protective. lmmunopathologlcal
processes (granuloma formation, Immune complexes)
play an important role In pathogenesis.
• Cllnlcal signs. Incubation period 1-3 months to
several years. Chronic disease includes signs such as
generalised iymphadenopathy, skin lesions (usually
starting In the head region), weight 1018, fever, apathy,
anorexia, spleen and liver enlargement (hepato• and
splenomegaly), anaemia, hypergammaglobullnaemla.
hypoalbumlnaemla, renal fallure with protelnur1a.
• Dlagnoala. Dlagnoatlc procedul'88 comprfae anamnaatlc
reports (e.g. stay of the dog In an endemic arN), clinical
signs, detection of specific serum antibodies or parulte
Identification In lymph node or bone marrow uplratea
by PCR, atalnlng procedures or In vitro cultivation.
• Therapy. Chemotherapy with mlltefoaln, allopurlnol,
glucantime (mono• or combined therapy) or with other
drugs (details ► p. 76).
• Prophy laxis. Prophylaxis is predominantly based
on protection of dogs against phlebotome bites by
Insecticides (collar, spot-on). Experiences with a
► vaccine are stlll llmlted.
' • Zoonotlc Importance. In the endemic areas dogs
are main reservoir hosts for vector-borne L. lnfantum
� Infections of humans.
Agent. In endemic areas of the Old World(see below)
canine leishmaniosis is caused by L. infantum and
transmitted by sand flies of the genus Phlebotomus.
Dogs are rarely infected with L. tropica. In Central
and South America sand flies of the genus Lutzomyia
function as vectors for L. infantum (syn. L. chagasi).
In the vertebrate host, L. infantum infects cells of the
mononuclear phagocytic system(MPS), in which they
multiply as amastigotes. These stages are round to
oval, 2-4 µm in diameter, containing a large nucleus
and a small kinetoplast. Electron microscopy reveals
a flagellar pocket and short flagellum which does not
project beyond the cell border ( ► Figure 4.8). In the
intestine of the insect vector, amastigotes transform to
----�promastigotes which can also arise from amastigotes
during in vitro cultivation.
Life cycle. Along with blood-feeding on an infected host,
female phlebotomes acquire Leishmania amastigotes,
located in skin macrophages or blood monocytes
(► Figure 4.9). In the midgut of the vector, amastigotes
transform into promastigotes, which multiply intensively
by binary fission. A portion of these stages attaches to
intestinal epithelia, while others remain freely motile and
colonise the anterior digestive tract. The latter include
non-dividing promastigotes (metacyclic forms) which
are transmitted during a further blood meal of the insect
4. Phylum Euglenozoa
Cil
"O
�
Kineto­ E
0
plast Cl)
0
C
Cil
0.
Short
flagellum
Figure 4.8. Leishman/a sp.: amastigote form (0 2-4 microns)
in a cell. TEM image (Photo: H. Mehlhorn).
to a new mammalian host. The development in the
vector can be completed already in 5-8 days. It has been
observed under experimental conditions that infected
phlebotomes probe the skin at a higher rate compared
to non-infected ones. This behaviour may increase
the chances of transmission. The infectious dose for a
vertebrate host is estimated at 10-100 metacyclic stages.
In the skin, the promastigote stage binds to its surface
host opsonins(complement proteins, immunoglobulins)
which aid binding to receptors of MPS cells. Thereafter,
parasites are phagocytised and enclosed in phagosomes,
which convert into phagolysosomes(Phi) by fusion with
lysosomes. Meanwhile, the promastigotes transform to
amastigotes that multiply by binary fission. Since the Phi
also divides, each leishmanial daughter cell is enclosed
in a compartment( ► Figure 4.9). Due to protection of
their cell surface by glycolipids and lipophosphoglycans,
the amastigotes withstand the acidic environment and
enzymatic activities in the Phi. These substances can
also prevent macrophage activation and downregulate
antigen presentation. Thus, the amastigotes can survive
in a cellular environment that is deadly for many
other microorganisms. The intracellular location
of the parasites also provides protection from host
immune responses. After the multiplication phase
the cells disintegrate, the amastigotes are released and
can then infect new cells and may be distributed to
various internal organs. The cycle is completed when
amastigotes are taken up by a competent insect vector.
Occurrence and epidemiology. L. infantum is
distributed in large areas of the Mediterranean region,
the Middle East, southern Russia, central Asia, Latin
America and North America. The Mediterranean
endemic area of L. infantum includes the North African
coast and in Europe a broad zone stretching from the
Iberian Peninsula, through southern France, Italy,
coastal areas of the Balkan region to Turkey and Cyprus.
With a few exceptions, the endemic area does not extend
beyond the 46 °N (approximately B ordeaux - South
 Part II. Parasites and parasitoses: protozoa

Dog as main
host Human as
accidental host

- --
----- ..
/
/ ;y '
Multiplication as
amastigote form
'
'\
I
I - I
I
L
I
I Development in macrophages of dogs

Sand fly

Promastigote form
Promastigote,
metacyclic form

.....,
..
Promastigote,
multiplicating form

Figure 4.9. Life cycle of Leishman/a infantum (Graphics: IPZ, S. Ehrat).

Q)
Tyrol - Belgrade). In recent years, the endemic area of to the Mediterranean (from the NL approximately 58,000
·u
C

'O canine leishmaniosis in Italy has shifted north to the dogs a year) are exposed to an infection risk of about
Q)
� Alpine area. 1 :430. It is known that individual dogs or groups of
cco dogs are imported from endemic into non-endemic
C ln coastal areas of the Mediterranean, Leishmania countries without precautions being taken to prevent
·;:: clinical outbreaks and spreading of the infection. In
seroprevalences in dogs vary from < 1 % to about
50%. However, the sensitivity of the serological tests is non-endemic areas, cases of leishmaniosis were rarely
C reduced in asymptomatic dogs. A PCR study in southern diagnosed in hosts (humans, dogs, horses) that had
>,
CJ)
France revealed higher prevalences, reaching> 75%. In allegedly not been in an endemic area. In such cases
0 non-endemic areas (e.g. central and northern Europe) uncertainties of case histories and alternative modes
0
'in leishmaniosis is occasionally diagnosed in dogs that of transmission have to be considered (e.g. iatrogenic
co have returned from an endemic area. Dogs from non­ infection, blood transfusion, prenatal or venereal
co
a. endemic areas, travelling with their owners on vacation infection in dogs).

In European endemic areas, L. infantum is usually
transmitted by sand flies from dog to dog, but rarely
other animals may be involved as reservoir hosts (e.g.
foxes, rabbits, hares, rats, cats). Occasionally the infection
is transmitted to humans. Dogs are convenient infection
sources for the vectors because their skin macrophages
are far more frequently Leishmania infected than human
cells.
In the Mediterranean endemic area, synanthropic
Phlebotomus species act as vectors, among others
Phlebotomus perniciosus, P. papatasi, P. ariasi, and P.
perfiliewi, with outdoor activity at dawn and during
the night. They are inactive during the day, resting in
burrows of rodents, tree holes, etc., but they also fly into
buildings to suck blood on available hosts (including
dogs, sheep, horses, humans, birds)( ► p. 463 ). In Latin
America Leishmania spp. are transmitted by Lutzomyia
phlebotome species.
Suspected non-cyclical transmission by direct contacts
between dogs(bites and wounds) or by insects have been
reported, but are not convincingly proven. However, in
dogs transmission through blood transfusion, prenatal
and venereal infections are well documented.
Immunology. Immunological processes start with the
bite of an infected sand fly. Salivary components of the
vector can inhibit local cellular mechanisms and thus
create a Th2-friendly microenvironment in which the
promastigotes can easily find their host cells. However,
if dogs have already previously been sensitised with
saliva antigens, they react with a strong Th I-mediated
response to new bites, restricting the establishment of
the infection. A breed-specific resistance of dogs to the
Leishmania infection was observed in endemic areas.
The clinical course of the Leishmania infection is
determined by the polarisation of the T-cell response
and depends, in principle(simplified) on whether a Th2-
or a Th I-immune response dominates ( ► Figure 1.3,
► p. 29). In symptomatic dogs, Th2-mediated immune
reactions dominate. The dogs develop high levels of
specific antibodies (IgGl, IgG2, IgM, IgA, IgE), which
have no protective effect, and a polyclonal(not parasite
related) B-cell activation leads to hyperglobulinaemia.
Furthermore, symptomatic dogs have a suppressed T cell
proliferation against Leishmania antigen. In contrast, in
infected dogs without clinical signs over years and dogs
with successful chemotherapy (which still carry the
parasite), a Th I -response(delayed-type hypersensitivity)
predominates. Such animals usually show lower levels
of parasite specific antibodies.
Pathogenesis. After inoculation of promastigotes
by a sand fly, a primary reaction occurs (nodule
formation, inflammation) in the skin, but remains
usually unnoticed in animal hosts. Macrophages that
4. Phylum Euglenozoa
are recruited in the area of the primary lesion become
infected and can disseminate parasites to other organs
(lymph nodes, spleen, liver, bone marrow, lung, intestine,
skin, etc.)( ► Figure 4.10). At the same time plasma cells
proliferate. Disseminated granulomatous inflammation ro
causes multiple organ damage. Due to specific and 'O
'-§
polyclonal B cell activation high levels of circulating E
immune complexes and a variety of auto-antibodies 0
Cl)
0
lead to endothelial damage, glomerulonephritis C
cu
and amyloidosis contributing to the outcome of the
t
Q.
visceral and cutaneous canine leishmaniosis. Overall,
the pathogenesis of leishmaniosis in dogs is extremely
complex and poorly understood in many details.
Clinical signs. In endemic areas >50% of dogs may
be infected without presenting clinical signs. Clinical
canine leishmaniosis starts as a visceral form of disease,
but in advanced cases approximately 90% of the dogs
present also cutaneous lesions.
• Visceral form. Incubation periods may last 1-3
months, but often much longer(up to several years).
Clinical signs develop gradually during a chronic
course, ranging from low-grade lymphadenopathy
without constitutional disturbances to severe visceral
disease. The main signs are manifold and include
apathy, inappetence, generalised lymphadenopathy,
spleno- and hepatomegaly, fever, renal insufficiency,
proteinuria, diarrhoea, polymyositis, muscle atrophy,
lameness(quadriplegia), osteolysis (carpus, tarsus)
and weight loss. Furthermore, keratoconjunctivitis,
uveitis, and panophthalmia can be associated with
canine leishmaniosis. Blood parameters exhibit
often changes, such as anaemia (mild to moderate,
normochromic), hypergammaglobulinaemia,
hypoalbuminaemia and acetonaemia.
• Cutaneous signs. Initial signs are alopecia and bran­
like desquamation, followed by nodules, pustules,
and excessive growth of claws( ► Figure 4.11). Skin
lesions manifest at the ears, around the eyes, the
nose, later on the back, legs and tail.
Figure 4.10. Leishmania infantum: amastigote forms (0 2-4
microns) (arrow) in a macrophage (Photo: IPZ, P. Deplazes).
Part II. Parasites and parasitoses: protozoa
Figure 4.11. Dog with lesions caused by Leishman/a infantum
(Photo: IPZ).
Diagnosis. An anamnestic report on the dog's stay in
an endemic area (implying a potentia.lly long incubation
period!), clinical symptoms and laboratory parameters
(hyperglobulinaemia, etc.) allow a presumptive
diagnosis that must be confirmed by adequate diagnostic
procedures. Serological detection of specific antibodies
(ELISA, IFAT, WB, etc.) is very sensitive (up to 99%)
in symptomatic cases, but it drops to about 60-80%
in inapparent infections ( caution: possible cross­
reactions with Trypanosoma spp. in dogs, e.g. from
Africa or South America). Seroconversion may occur
within a few months, i.e. within the incubation period.
DNA detection by PCR (conventional or quantitative
methods) is very reliable; several studies revealed a
sensitivity of 80-90%. However, the sensitivity of PCR
is significantly influenced by the diagnostic sample and
the severity of the disease (before or during treatment).
Invasive biopsy specimens taken from popliteal lymph
nodes or bone marrow and skin biopsies are more
suitable as test material than less-invasively collected
specimens such as blood samples or conjunctiva! swabs.
For detecting asymptomatic infections in dogs, PCR with
biopsy material from lymph nodes or bone marrow is to
be preferred to serology. Diagnostic in vitro cultivation
of promastigote stages from aseptically-collected biopsy
material is performed in specialised laboratories and
allows a zymodeme characterisation of the isolate.
In differential diagnosis several diseases have to be
considered, such as trypanosomosis, ehrlichiosis,
hepatozoonosis, babesiosis, demodicosis or chronic
septicaemic and immunological diseases.
Therapy. Chemotherapy may lead to an improvement
of the clinical condition, but will not eliminate the
infection. In some European countries (CH, CY, ES,
GR, IT, PT, SL) miltefosine (hexadecyl-phosphocholin)
is registered as Milteforan• and is approved for treatment
of canine leishmaniosis at a dose of 2 mg/kg b.w.
p.o. daily for 4 weeks. A well validated alternative is
treatment with allopurinol (purine analogue; off-label-
use) at a daily dose of 2x 10 mg/kg b.w. p.o. for several
months to years. Clinical cure can be expected after a
treatment period of 2-6 months in about 90% of dogs.
However, recurrences are possible even after 2 years
of treatment. After discontinuation of therapy due
to clinical improvement and normalisation of blood
parameters, dogs should be monitored clinically and
in case of relapses (beginning hyperglobulinaemia) re­
treated. Around 75% of treated dogs have a chance to
survive for more than 6 years. Therapy with Glucantime•
(antimony compound) which is registered only in a few
European countries is indicated in special cases. This
therapy is not recommended for dogs with hepatic or
renal impairment because of risks of severe side effects.
Combination therapies with Glucantime• and miltefosin
or with allopurinol have been used in recent studies,
in which lower recurrence rates were observed. Such
combination therapy may be suitable in cases where
recurrences occur after therapy with a single drug.
Prophylaxis and control. Prophylaxis is predomi­
nantly based on protection of dogs against phlebotome
bites during their seasonal activity. This is achieved
through the use of a deltamethrin-impregnated
collar or spot-on treatment either with permethrin
or imidacloprid/permethrin ( ► p. 602). A vaccine
(CaniLeish•) against leishmaniosis in dogs has recently
been authorised in Europe by EMA, but experiences
with the vaccine are still limited. Serological and clinical
monitoring of dogs after return from endemic areas may
be indicated for early diagnosis. Control of phlebotomes
► p. 463.
Zoonotic importance. In the endemic regions,
dogs are the main reservoir hosts of L. infantum (syn.
L. chagasi), causing leishmaniosis in humans which
occurs as visceral, rarely as cutaneous form. Children
and adults are affected. especially persons with impaired
immune defence (e.g. AIDS patients). In addition to
vector-borne transmission, Leishmania parasites can be
transmitted prenatally, through blood transfusion and
contaminated instruments (e.g. syringes). An infection
of humans through contact with infected dogs has never
been documented.
Leishmaniosis in cats, equines, bovines and
macropods
In recent years, cases of leishmaniosis in cats have been
observed in Europe (endemic areas of L. infantum), Asia
and Latin America (endemic areas of L. mexicana, L.
venezuelensis, L. amazonensis). Diseased cats exhibited
skin lesions on the head (nodules on lips, nose, eyelids
and ears) or generalised dermatitis. In a study in the
Lisbon region, Leishmania DNA was detected by PCR
in peripheral blood of 20% of 138 cats and 35% of 152
dogs, but specific antibodies were only rarely detected.
It is still unclear whether cats play a role as reservoir
hosts for L. infantum.

Indigenous cases of cutaneous leishmaniosis in horses,
caused by L. infantum, have been reported in several
European countries (CH, DE, ES, PT). Rare cases in
Germany and Switzerland exhibited clinical signs
consisting of singular or multiple nodules or lesions
(1-3 cm diameter), most of them with self-healing
tendency. Molecular analyses of the ITS sequence
identified these pathogens as phylogenetically closely
related to L. siamensis isolated from a human patient
with visceral leishmaniosis in Asia. In Latin America,
cutaneous leishmaniosis, caused by L. braziliensis is
quite common in horses, donkeys, and mules. In Brazil,
a mixed infection with L. infantum and L. braziliensis
was diagnosed in a horse. Little information exists on
Leishmania infections in ruminants, for example for
L. donovani in goats. In some cattle in Switzerland,
large skin lesions (1-10 cm) with self-healing tendency
were observed, caused by Leishmania pathogens,
corresponding to those identified in horses (see above).
In Australia, the first cases of indigenous cutaneous
leishmaniosis in macropods (kangaroos) were observed
in 2004. The causative agent could be clearly assigned
to the genus Leishmania, but species allocation was not
possible. Evidence for Phlebotomes as vectors could not
be found, but midges (Ceratopogonidae) are suspected.
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Bongiorno G, Paparcone R, Foglia Manzlllo V, Oliva G,
Cuisinier AM, Gradoni L (2013) Vaccination with LiESP/
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4. Phylum Euglenozoa
Deplazes P, Staebler S, Gottstein B (2006) Reisemedizin
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Spain? Vet Parasitol 202: 296-300.
Lobsiger L, MOiier N, Schweizer T, Frey CF, Wiederkehr D,
Zumkehr B, Gottsteln B (2010) An autochthonous case of
cutaneous bovine leishmaniasis in Switzerland. Vet Parasitol
169: 408-414.
Maia C, Gomes J, Crist6vio J, Nunes M, Martins A, Reb61o
E, Campino L (201 O) Feline Leishman/a infection in a canine
lelshmanlasis endemic region, Portugal. Vet Parasitol 174:
336-340.
Martin-Sanchez J, Acedo C, Mui'los-Perez M, Pesson
B, Marchal 0, Morlllas-Marquez F (2007) Infection by
Leishmania fnfantum in cats: epidemiological study in Spain.
Vet Parasitol 145: 267-273.
Mettler M, Grimm F, Capelli G, Camp H, Deplazes P (2005)
Evaluation of enzyme-linked immunosorbent assays, an
immunofluorescent-antibody test, and two rapid tests
(immunochromatographic-dipstick and gel tests) for
serological diagnosis of symptomatic and asymptomatic
Leishman/a infections in dogs. J Clin Microbial 43: 5515-
5519.
Molina R, Jimenez Ml, Cruz I, lriso A, Martin-Martin I,
Sevillano 0, Melero S, Bernal J (2012) The hare (Lepus
granatensis) as potential sylvatic reservoir of Leishman/a
infantum In Span. Vet Parasitol 190: 268-271.
Millier N, Welle M, Lobsiger L, Stoffel MH, Boghenbor KK,
Hllbe M, Gottstein B, Frey CF, Geyer C, von Bomhard
W (2009) Occurrence of Leishmania sp. in cutaneous lesions
of horses in Central Europe. Vet Parasitol 166: 346-351.
Pennisi M, Cardoso L, Baneth G, Bourdeau P, Koutinas
A, Miro G, Oliva G, Solano-Gallego L (2015) LeishVet
update and recommendations on feline leishmaniosis. Parasit
Vectors 8: 302.
Reis AB, Giunchetti RC, Carrillo E, Martins-Filho OA,
Moreno J (2010) Immunity to Leishman/a and the rational
search for vaccines against canine leishmaniasis. Trends
Parasite/ 26: 341-349.
Soares IR, Silva SO, Moreira FM, Prado LG, Fantini P,
Maranhao Ade P, da SilvaFilho JM, Melo MN, Palhares
MS (2013) First evidence of autochthonous cases of
Leishmania (Leishmania) infantum in horse (Equus cabal/us)
in the Americas and mixed infection of Leishmania infantum
and Leishmania (Viannia) braziliensis. Vet. Parasite/ 197:
665-669.
Solano-Gallego L, Miro G, Koutinas A, Cardoso L, Pennisi
MG, Ferrer L, Bourdeau P, Oliva G, Baneth G, T he
LeishVet Group (2011) LeishVet guidelines for the practical
management of canine leishmaniosis. Parasit Vectors 4: 86.
Part 11. Parasites and parasitoses: protozoa

4.1.2 Order Bodonida

Family Bodonidae

The following species of this family are mentioned

here as examples: Ichthyobodo necator (syn. Costia
necatrix), a worldwide distributed causative agent of
a dreaded skin disease (ichthyobodosis) of freshwater
fish. Trypanoplasma borreli is a common blood parasite,
especially in carp and tench, which is transmitted by fish
leeches of the genera Piscicola and Hemiclepsis. Clinical
signs include anaemia, ascites, focal necrosis in liver and
kidneys and hyperplasia of vascular endothelia.

Selected reference

Roberts RJ (ed.) (2012) Fish pathology, 4th ed. Ames, IA, USA:
Wiley-Blackwell. ISBN 978-1-4443-3282-7.
 5. Phylum Alveolata

Alveolus (L): trough. Refers to the common characteristic Micronemes Polar ring
of the phylum (see below). Pellicula Preconoidal

The phylum Alveolata, including its subphyla Rhoptri

Apicomplexa, Dinoflagellata and Ciliophora, was Microp
introduced in 1992 as a new taxon. The common
characteristic of these groups is a system of alveoles
(alveolar system) in the pellicula that is differentially
shaped in the various subphyla. The subphylum
Apicomplexa is of particular parasitological interest.
Golgi apparatus

- Subphylum Apicomplexa
Nucleus with nucleolus
Apex (L): point; complexio (L): accumulation, refers to
the apical complex.

Apicomplexa (previously Sporozoa) are common

intracellular parasites of invertebrates (annelids,
arthropods, molluscs and others) and vertebrates. The
subphylum contains monoxenous and heteroxenous
groups. Most of the stages of the various species
reside within a parasitophorous vacuole that separates
them from the host cell cytoplasm. Members of the
Sarcocystidae are characterised by the formation of
cysts in intermediate host tissue containing stages
(cystozoites) that are infectious for definitive hosts.
\"11----Amylopectin
a -------Posterior polar ring
Figure 5.1. Merozoite of Apicomplexa (class Coccidea):
schematic diagram based on TEM studies (dense granules
are not shown for the sake of clarity) (Graphics: IPZ, A. Seeger;
after Mehlhorn and Ruthmann 1992).

The life cycle of the Apicomplexa follows a basic but
variable scheme including alternating generations with
asexual multiplication (merogony, ► Glossary, p. 620),
sexual reproduction (gamogony and zygote formation),
and asexual formation of infective stages (sporogony).
Merogony and gamogony are intracellular processes
within a host, sporogony usually occurs extracellularly
in the environment or within a host. Most developmental
stages are haploid, only zygotes are diploid. In some
groups (e.g. Eimeria, Toxoplasma, Sarcocystis) encysted
stages (oocysts) are released by the definitive host
to the environment. Species of the classes Coccidea
and Haematozoea are causative agents of important
parasitoses of domestic animals and humans, such as
coccidiosis, toxoplasmosis, babesiosis, and malaria.
,- : Selected references
Cowper B, Matthews S, Tomley F (2012) The molecular basis
for the distinct host and distinct tissue tropism of coccidian
parasites. Mol Blochem Parasitol 186: 1-10.
Mehlhorn H (ed.) (2008) Encyclopedia of parasitology. Third
Edition. Berlin, Germany: Springer. ISBN: 978-3-540-48994-8.
Weiss LM, Kim K (eds.) (2014) Toxop/asma gondii. The model
Aplcomplexan. Perspectives and methods. Second edition.
London, UK: Academic Press. eBook ISBN 9780123965363.
Print book ISBN 9780123964816.
5.1 Class Coccidea
Q)
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C

Kokkos (G): berry, round fruit; eidos (G): shape. Refers '5
Some stages of the Apicomplexa that are motile and to the shape of oocysts (see below). Q)
�
capable of invading cells (e.g. sporozoites, merozoites)
are characterised by special cellular structures which Characteristics of the class Coccidea are the formation co
C
are schematically presented in ► Figure 5.1 and of resistant oocysts and a distinct anisogamy: merozoites ·;::
Q)
described below in some detail ( ► Box 5.1 and ► Figure develop directly to macrogamonts (hologamy),
1.2, p. 24). whereas microgamonts develop by multiple divisions C
of microgametes (few in the case of Adeleida, many >,
Ol
flagellated stages in the case ofEimeriidae). Members of 0
0
this class are agents of coccidioses. The term 'coccidiosis' 'ii)
is also used in a narrower sense to name infections that
co
are caused by members of the family Eimeriidae. Q_
 Part II. Parasites and parasitoses: protozoa
Box 5.1. Cellular structures of a merozoite.
Merozoites are usually spindle- or banana-shaped
and commonly <10 µm long. They are enclosed by
a pellicula, consisting of one outer and two closely­
spaced inner membranes and subpellicular microtubules
(with the two inner membranes representing the
alveolar system). Micropores are small cytostomes
for endocytosis. Besides the common structures and
organelles of eukaryotic cells, the motile stages of
Apicomplexa possess an apical complex at the front
end (apex). It consists of several structures, including
the conoid, polar ring and subpellicular microtubules
as well as secretory organelles such as micronemes,
rhoptries and dense granules. Most apicomplexan
genera also possess an apicoplast ( ► Glossary, p.
620).
The apical complex, its organelles and the molecules
exocytosed by the organelles play an important role
in identification and infection of suitable host cells
and formation of the parasitophorous vacuole within
the cell (► Figure 1.2, p. 24). Tl1e conoid is a hollow,
cone-shaped stump that consists of a species-specific
number of spirally arranged microtubules. It is connected
with preconoldal rings and the polar ring and anchors
the subpellicular microtubules. The micronemes,
rhoptries and dense granules release their proteins in a
temporal sequence by exocytosis. The various proteins
participate in the recognition of suitable host cells. the
movement ('gliding') of the parasites. the infection
of host cells, the formation and modification ot the
membrane of the parasitophorous vacuole, metal,olic
transport and host cell modulation.
Micronemes are cylindrical, small (length 0.05 µm)
organelles that cluster in the apical portion of the cell
(► Figure 5.1). Their number varies with the parasite
genera. Exocytosis of micronemes is Ca2+-dependent
and represents the initial response to contact between
parasite and host cell membrane. Almost all mlcroneme
proteins (MIC) contain sequences with homology to
adhesive proteins from higher eukaryotes, such as
thrombospondin type I-like repeats, lectln domains,
epidermal growth factor (EGF)-like domains and
Q)
others. These interact with carbohydrates on host cell
·u
C
surfaces or with other (parasite) proteins. Thus, MIGs
'6
Q) may be the major regulators of host and tissue tropism
of apicomplexans. Interestingly, MIGs of Toxoplasma
co gondii, a parasite with low host and cell type specificity,
C
·c seem to recognise a wider range of epitopes than MIGs
Q)
of Bmeria tenella, a parasite limited to the caecum of
C
chickens. MIGs play a crucial role in parasite locomotion
>- (gliding mobility) and its infection machinery. They
0)
0 constitute the link between the host cell surface and
0 the actin-myosin motor system of the parasite. MIGs
"in
co
co
a..
become part of the moving junction as a complex of
MIGs and rhoptry neck proteins (RONs; see rhoptries
below), by which the invading parasite slides into the
host cell taking the cell membrane inside as part of
the parasitophorous vacuole membrane. The host cell
invasion process is depicted in ► Figure 1.2, p. 24.
Rhoptries are pairwise secretory, club-shaped
organelles (numbers vary with species and parasite
stages), that open to the apical pole of the sporozoites
or merozoites. They consist of an anterior duct-like
neck portion and a posterior bulb portion ( ► Figure
1.2 and 5.1). Both portions contain and secrete distinct
Ga2+-independent proteins (so-called RONs) and ROPs
(rhoptry proteins), respectively. Rhoptry proteins are
highly versatile. For instance, 12 RON proteins and 48
ROP proteins are hitherto described in Toxoplasma
gondii, probably the best studied parasite in this regard.
RON protein exocytosis starts after final orientation of
the parasite with its apical end to the host cell surface
and continues during the invasion process. This
process takes 15-20 s to complete and is distinctly
faster than phagocytosis. A subset of RON proteins is
essential for genesis and function of the moving junction
between parasite and host membranes. ROP proteins
are secreted later, into the nascent parasitophorous
vacuole and into the host cell; the majority are kinases
and pseudokinases. They play a role in modifying the
parasite environment in the parasitophorous vacuole
and its membrane. Some of those released into the host
cell cytoplasm are considered key determinants in host
parasite interactions by influencing host cell signalling
pathways (e.g. TgROP16, TgROP18).
Dense granules are small (0.02 µm), globular,
membrane-enclosed vesicles that are distributed
throughout the parasite cytoplasm (not shown in
► Figure 5.1 for the sake of clarity of the figure). They
release their contents rather late, i.e. 10-30 min after
cell invasion, into the parasitophorous vacuole in a
Ga2+ -independent manner. Approximately twenty dense
granule protein (GRA) family members are known in T.
gondii tachyzoites. The various GRA proteins of 20-
75 kDa are subsequently found in structures within
the parasitophorous vacuole and in the membrane
of the vacuole and persist until the parasite's egress
from the cell. At least one dense granule protein of
T. gondii (TgGRA3) seems to become associated
with the host cell nucleus suggesting it is involved in
reprogramming the host cell. The expression of GRA
proteins is maintained at the bradyzoite stage and GRAs
can also be detected later in the cyst wall. Thus, they
are probably essential for the cyst wall biogenesis.

5.1.1 Order Adeleida
Family Hepatozoidae
Genus Hepatozoon
Disease: Hepatozoonosis in dogs and cats.
Hepar (G): liver; zoon (G): animal.
Summary
• Agents and llfe cycle. Hepatozoon canls Is a common
parasite in dogs and other canlds (red fox, Jackal, hyena)
In the Mediterranean area and other warm climate
regions. H. amerlcanum occurs In North and South
America. Hepatozoonosls In Central Europe Is a rare,
Imported disease. H. canls Is cyclically transmitted by
Ingestion of Infected Rhlplcephalus sangulneus s.l. After
Infection of a susceptible host two meront generations
occur In lymph nodes, liver, spleen, muscles and other
organs; subsequently brick-shaped gamonts are formed
In neutrophils and monocytes.
• Cllnlcal signs, diagnosis, therapy. In dogs fever and
other non-specific symptoms. Microscopic detection
of gamonts In Glemsa-stalned blood smears. Treatment
with lmidocarb is not always successful.
Agents and occurrence. Hepatozoon canis infects
dogs, red foxes, jackals, other canids, and hyenas. Also
cats and other felids are described as hosts. The infection
occurs worldwide in areas of warm climates, particularly
in southern Europe, Africa and Asia. Prevalences of
>30% are reported in dogs in Spain. Unlike other tick­
borne infections, these parasites are transmitted by
ingestion of infected Rhipicephalus sanguineus s.l. Some
other tick species are also considered as vectors. Cases
of H. canis infections diagnosed in Central Europe are
a 0
Figure 5.2. Hepatozoon canis, Giemsa-staining: (a) brick-shaped gamont (10x5 µm in a neutrophil granulocyte; (b) meront
(diameter ~50 µm) in skeletal muscle (Photos: IPZ, J. Eckert, P. Deplazes).
5. Phylum Alveolata
usually due to the import of either infected dogs or
ticks harbouring the parasite. However, recently, H.
canis infections of wild canids were observed in eastern
countries of Central Europe (SK, PL, AT, HU) in areas
previously considered non-endemic due to the absence
of R. sanguineus s.l. H. americanum occurs frequently
in the southern states of the USA but is also found in
Central and South America. Mixed infections have been
reported in the USA with H. canis and H. americanum.
H. felis is a rare cat parasite.
Life cycle. After ingestion of an infected tick by a
susceptible host sporozoites are released; they invade
the intestinal wall and are haematogenously spread to
various organs (lymph nodes, liver, spleen, bone marrow,
striated muscles), where macromeronts develop. After a
second meront generation (micromeronts), merozoites
transform to brick-shaped gamonts (approximately
IOxS µm) in neutrophils and monocytes in the blood
( ► Figure 5.2a). Nymphal tick stages ingest the gamonts
in leukocytes with the blood meal. Ookinetes are
formed after union of male and female gametes in the
tick intestine and invade the haemocoel. Large oocysts
(ca. 100 µm) with 30-50 sporocysts, each containing
16 sporozoites, develop after moulting in the adult
stages. Ticks taken up by a dog are broken with the
teeth and ingested. H. canis is also transmitted via the
transplacental route.
Clinical signs. Infection may be asymptomatic but
severe clinical disease due to H. canis is also observed.
The meronts of the first generation are the pathogenic
stages inducing inflammatory responses in infected
organs and causing manifold symptoms, such as
irregular fever, anorexia, anaemia, muscular pain and
emaciation. H. americanum infections usually lead to
more severe, sometimes fatal disease with involvement
of the skeletal muscles (granulomatous myositis and
periostitis).
Q)
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 Part II. Parasites and parasitoses: protozoa
Diagnosis. Gamonts are first found 28 days after
experimental infection and may be detected in leukocytes
in stained blood smears (parasitaemia levels of 1-5%).
PCR is an effective diagnostic tool to detect in H. canis
infections. Since clinical symptoms usually precede the
appearance of blood stages, serology may be employed
(ELISA, IFAT).
Therapy and control. Two injections of imidocarb
diproprionate (5.0-6.0 mg/kg. b.w. s.c.; off-label use)
applied 14 days apart can be regarded as basic therapy
of canine hepatozoonosis. Clinical improvement may
be achieved in a high percentage of the cases; if not,
treatment should be extended to 6 weeks. However,
the elimination of the parasite will be achieved only
in a small percentage of the animals. Tick control is
strongly recommended.
Further families of the order Adeleida
• Hepatozoidae: Hepatozoon muris in Rattus norve­
I
I
gicus and R. rattus; oral transmission with Laelaps
spp. (mites); Hepatozoon spp. in snakes and saurians,
oral transmission by ingestion of infected Diptera.
• Haemogregarinidae: Haemogregarina spp. in
turtles; transmission by leeches with saliva.
• Karyolysidae: Karyolysus spp. in saurians, oral
transmission by ingestion of infected mites.
• Klossiellidae: Klossiella equi in equids. Meronts in
endothelial cells of Bowman's capsule, gamogony in
epithelial cells of the Loop of Henle in the kidney.
Sporocysts ( l 6x10 µm, with eight sporozoites each)
are shed in the urine. The parasite is usually detected
incidentally during histopathological investigations.
Approximately 15 further species in the renal tract
of mammals (e.g. K. muris in mice, K. cobayae in
guinea pigs). One species (K. boae) in the intestine
and kidney of snakes (Boa constrictor).
Selected references ; -
Baneth G (2011) Perspectives on canine and feline hepato­
zoonosis. Vet Parasitol 181: 3-11.
Baneth G, Sheiner A, Eyal 0, Hahn S, Beaufills JP, Anug
Y, Talml-Frank D (2013) Redescription of Hepatozoon
felis (Apicomplexa: Hepatozoidae) based on phylogenetic
analysis, tissue and bloodform morphology, and possible
transplacental transmission. Parasit Vectors 6: 102.
De Tomasi AS, Giannelli A, de Caprarils D, Ramos RA,
Di Paola G, Crescenzo G, Dantas-Torres F, Baneth
G, Otranto D (2014) Failure of imidocarb diproprionate
and toltrazuril/emodepside plus clindamycin in treating
Hepatozoon canis infection. Vet Parasitol 200: 242-245.
Farkas R, Solymosi N, Takacs N, Hornyak A, Hornak S,
Nachum-Biala Y, Baneth G (2014) First molecular evidence
of Hepatozoon canis infection in red foxes and golden jackals
from Hungary. Parasit Vectors 7: 303. doi: 10.1186/1756-
3305-7-303.
5.1.2 Order Eimeriida
Family Eimeriidae
Theodor G.H. Eimer (1843-1891), Swiss born zoologist
and physician.
Genus Eimeria
■ Eimeria species of domestic chicken
Disease: Eimeriosis {coccidiosis) in domestic
chickens.
Globally, various forms of coccidiosis, caused by several
Eimeria species, belong to the most common diseases
of chickens. The economic losses caused by them and
expenditure for control are considerable.
Summary
• Agents. Globally chickens are hosts of seven Eimeria
spp., each with a special precfllection site in the intestine.
The species cause different forms of coccidiosis.
• Life cycle. Chickens acquire the infection by ingestion of
sporulated oocysta. Endogenous development includes
2-4 merogonies and the gamogony. Sporogony occurs
In the environment (sporulated oocysts contain four
sporocysts with two sporozoites each). In all species,
short prepatency periods of 4-6 days. Endogenous
cycles expire without reinfection since the number of
merogonies is genetically limited in the various species.
• Epldemlology, occumtnce. All species are distributed
worldwide. Coccidlosis Is Important in all poultry
management systems.
• Cllnlcal signs. Elmerla spp. Infect chickens regardless
of their age, sometimes causing diseases of high
morbidity and mortality, more frequently occurring
as subcllnical Infections, associated with reduced
weight gains and egg yields, and poor feed utilisation.
E. tenella (causing haemorrhagic coccldlal typhlltls)
and E. necatrlx (haemorrhagic coccldlosls of the small
Intestine) are highly pathogenic species; E. brunettl
(necrotlslng enteritis) le ellghtly less pathogenic. Other
speclet cauae mild to severe catarrhallc enteritis (E.
maxima, E. acervu/lna) or exhibit little pathogenlclty
(J:. mltla, E. p,aecox).
• Dlagnoeltl. Necropsy findings (localisation, types of
lesions) and microscopical demonstration of typical
developmental stages In mucoaal Impression smears,
facilitate a species diagnosis. Shapes and sizes of
oocyata are not species-specific (except E. maxima).
Species and particular strains can be Identified by
molecular techniques.
• T herapy. Diseased chickens cannot be cured.
Nevertheless, a flock with diseased animals should
be treated to protect yet uninfected animals or those
•
In an early stage of Infection.
 5. Phylum Alveolata

Life cycle. The monoxenous cycle of Eimeria species

A
, Control. Hygiene measures are Important, but not
usually sufficient In chickens kept on litter or In
case of free-range husbandry. Chemoprophylaxls is
performed by application of licensed antlcoccldlals In
feed or drinking water. Broilers kept under conditions
of Intensive floor husbandry are usually treated with
medicated feed throughout the whole fattening
period until premarketlng withdrawal. Laying hens are
treated until the start of egg laying to avoid residues
of antlcoccldlals In the eggs. The emergence of
drug-resistant strains Is a eertous problem In chicken
husbandry and concema all antlcocoldlala and all
Elmerla species In chickens. Several vaccines are
Hcenaed: the most common types contain aporulated
oocyats of attenuated Elmerla lines.
Agents. Seven Eimeria species occur in chickens:
E. tenel/a; E. necatrix; E. acervulina; E. maxima; E.
brunetti; E. mitis; and E. praecox ( ► Table 5.1 ). Species
identification is based on various criteria, including
genomic characteristics ( ► diagnosis, below p. 88). The
nuclear genome of all seven species has been sequenced
recently. An important biological feature of Eimeria
species in general and those of chickens is their narrow
host spectrum.
in chickens and other animals includes three distinct
phases: asexual proliferation (merogony) and sexual
reproduction (gamogony) in the host and sporogony in
the environment ( ► Glossary, p. 620). As an example,
the life cycle of E. tenet/a is presented in ► Figure 5.3
and described below. Cll
:g
·c
Q)
Life cycle of E. tenella E
w
• Infection and merogony. The infection of chickens
occurs by ingestion of sporulated oocysts ( ► Figure
5.5) in feed or drinking water. It is of epidemiological
significance that even small oocyst numbers can trigger
an infection (e.g. a single oocyst is sufficient to infect
an immunologically na'ive chick). In the host's intestine
sporozoltes are activated by CO2, bile, trypsin and the
body temperature and induced to 'hatch' from the
oocyst. Single sporozoites infect a host cell, mostly a
caecal enterocyte, and develop inside a parasitophorous
vacuole into a rounded and growing cell, the meront
( ► Figure 5.3 ). Thereafter, merogony is initiated by
multiple divisions of the parasite's nucleus without
division of the cytoplasm. Ultimately, the meront
measures approximately 50 µm and contains hundreds
of nuclei. Subsequently, division of the cytoplasm starts

Table 5.1. Eimeria species of domestic chickens(► Figure 5.7).

. I
1Prepa.� ,MalrW,affected
1,Etmeda Mafn site of development; type Location animal group; :M orbid�
s�cles of disease and lesions ·and max.. ·te"!CY clinical signs (f,48)1,
,, size of
meronta
, ,(days)
i--
. iM
mor.fal!W
llJ
C' {'_ "'-' :. '
E. tenel/a caeca meronts II 6 4•8 weeks old animals(also chicks MB:+++
Haemorrhagic typhlltls: swollen subeplthelial of 1 ·2 weeks); acute disease, MT:+++
mucosa, erosions, bloody, later 54µm faintness, anorexia, initially pulpy,
caseous content, thickened caecal later on watery and bloody
walls, enlarged caeca diarrhoea
E. necatrix middle part of jejunum(caeca) meronts II 6 5·7 weeks old animals; progressing MB:+++
Haemorrhagic enteritis: bloated subepithelial enteritis, reddish faeces, partially MT:+++
intestine, petechiae, bloody 66µm bloody, seriously affected general
exudate condition
E. brunetti ileum, caecum, rectum meronts II 5 chickens of all ages; seriously MB:++ '
Necrotising enteritis: hyperaemic, subeplthelial affected general condition, pink MT:++
swollen mucosa, necroses 30µm faeces, often bloody
E. acervulina duodenum, proximal jejunum epithelial 4 young hens; reduced egg yields, MB:+++
Catarrhalic enteritis: whitish 10µm weight loss, temporary diarrhoea MT:+ Q)
C
transverse striations, later confluent with watery, slimy faeces ·u
foci, rarely bloody '6
Q)
E. maxima middle part of jejunum epithelial 5 mainly 5-6 months old laying hens; MB:+++ 2
Catarrhalic enteritis: thickened 9µm mostly mild infection with temporary MT:+
mucosa, petechiae, mucous diarrhoea, reduced egg yields C1:l
C
exudate ·c
Q)

E. mitis distal jejunum, ileum epithelial 4 rarely sickness, possibly reduced MB:+
Catarrhalic enteritis: mucous 15 µm eggs yields MT:- .£
exudate, no distinct lesions >­
0
CJ)
E.praecox duodenum, proximal jejunum epithelial 4 only in heavy infections enteritis, MB:+
Catarrhalic enteritis: mucous 20µm particularly in fledglings, pasty MT:- 0
exudate, no lesions faeces ·u5
1 Degree of MB and MT: +++ = high, ++ = moderate, + = low, - = none. Cll
Q_
 Part II. Parasites and parasitoses: protozoa

--�-----­--
Gamogony
Merogony I � ... "",,
�
\

Figure 5.3. Life cycle of Bmeris tene/ls (Graphics: IPZ, S. Ehrat).

Q)
resulting in the formation of numerous mononuclear, In addition to enterocytes, intraepithelial lymphocytes
spindle-shaped, motile daughter cells, the merozoites. are infected and seem to be responsible for spreading of
·u
C

'5 During this process, the host cell size increases to several the parasites in the intestinal wall and the stimulation
Q)
� times the normal ( ► Figure 5.3 and 5.4). The merozoites of specific immune responses.
cro are set free from the host cell, invade new cells and
C initiate a further merogony. Since the merozoites • Gamogony. Most merozoites develop into a single,
-;::
frequently infect neighbouring cells, groups of 50-100 large, mononuclear, spheroid cell, the macrogamete
meronts of the second generation virtually form 'nests' ( ► Figure 5.6). Developing macrogametes are
C that may extend to deeper tissue layers down to the characterised by eosinophilic granules - arranged as
>,
CJ)
lamina muscularis. Meronts of the second generation an outer layer containing glycoproteins and an inner
0 contain 200-350 merozoites of an approximate length proteinaceous layer - called wall-forming bodies. A
0

"cii of 16 µm ( ► Figure 5.4). While most merozoites invade few merozoites develop into large, polynucleated eel.ls
new host cells and start sexual development (gamogony) (mkrogamonts) that form many spindle-shaped cells
n:)
a.. some may develop into a third generation of meronts. with two (sometimes three) flagella, the micro gametes.
- 5. Phylum Alveolata

ro
:g
·;:::
E
Q)

Figure 5.4. Eimeria tenella (Photos: IPH, K.F.): (a) meront II, native (0 = 50 µm); (b) meronts (HE staining).

Mlcropyle cap

Oocyst wall
(2 layers)

Small retractile
globule
\lA,+-�--
+H--'H--+tt-- large retractile
globule

yst residuum

Sporocyst residuum

Figure 5.5. Sporulated Eimeria oocyst, schematic (Graphics: IPZ).

The microgametes are set free and fertilise macrogametes

thus forming zygotes( ► Figure 5.3). The eosinophilic
granules converge and form a resistant cyst wall
surrounding the zygote which decreases in size and
is referred to as sporont. The construct resembles an
egg and is, therefore, called an oocyst. The oocysts are
released from ruptured host cells and are excreted in
the faeces.

The prepatency periods of chicken Eimeria spp. last 4-6

days, followed by a short patency of several days. It is
especially noteworthy that without reinfection oocyst
shedding expires after some time, since the number of
Figure 5.6. Eimeria maxima: macrogametes, HE staining
merogonies is species-specifically limited, in case of E.
(Photo: IPH, K.F.).
tenella to 2-3 (maximum 4) generations.

• Sporogony. At the time of shedding from the host

oocysts contain a diploid sporont which develops further
 Part II. Parasites and parasitoses: protozoa
by meiosis. In a first step, four haploid sporonts are
simultaneously generated and enclosed by a shell, thus
becoming sporocysts. In each of the sporocysts two
sporozoites are formed, the stages infectious for the host
( ► Figure 5.5). This process of sporulation requires
suitable environmental conditions, including sufficient
oxygen and moisture as well as favourable temperatures.
Optimum temperatures range between 25 °C and 30 °C;
higher temperatures of >35 °C damage the oocysts.
Sporogony is suspended at temperatures <10 °C. Under
favourable conditions, sporulation takes about 2 days.
Life cycle of other Eimeria species. The
development of other Eimeria species in chickens in
principle corresponds to the scheme described above
( ► Figure 5.6). Differences between the species exist
with regard to their predilection sites in different parts
of the intestine and the intestinal tissue ( ► Table 5.1).
For instance, the developmental stages of some species
are localised only in the epithelium, while those of others
occur in subepithelial layers. Furthermore, differences
exist in the number of merogonies (2-4, rarely more), the
prepatent periods (<4-6 days) and also in times required
for sporulation under defined conditions.
Occurrence and epidemiology. The Eimeria
species of domestic chickens are distributed worldwide
and are ubiquitous wherever chickens are maintained.
Due to their distinct host specificity, only chickens can
be sources of infection and reservoirs. Under practical
conditions, it is impossible to prevent Eimeria infections
in chickens since oocysts are passively drifted on strong
air currents and can be displaced, adhering to people,
animals, tools, etc.
The epidemiological course of chicken coccidiosis
is determined by several key factors, including the
involved Eimeria species, the contamination of the
environment with oocysts, the husbandry system, as
well as the age structure and immune status of the flock.
Although chickens can become infe<,:ted by any of the
seven Eimeria species, experience shows that the major
problems in chicken raising and fattening are due to £.
ttnella and£. necatrix, whereas coccidiosis in laying hens
is predominantly caused by E. acervulina, E. maxima
Q)
C and£. brunetti. Disease outbreaks are mostly observed
·u in broilers, beginning at an age of 3 weeks, and in hens
'6
Q)
� when they are adapted lo the egg laying conditions at
an age of 14-20 weeks by suspending chemoprophylaxis
co with anticoccidiaJs (see below).
C
·c
Q.)
j The degree of environmental contamination with
-� oocysts is most notably a question of the husbandry
>-
0)
system. The contamination may be very low in
0 extensive free-range systems resulting in weak,
0
·u; asymptomatic infections of the chickens, associated
with the stimulation of species-specific immunity
co
CL which protects from disease. Nevertheless, heavy
environmental contamination with oocysts may provoke
disease before sufficient immunity has developed under
such conditions. Battery cage husbandry - in many
parts of the world still used for laying hens - usually
protects animals from disease as it largely reduces oocyst
transmission. However, this system was banned 1992
in Switzerland and 2012 in the EU for animal welfare
reasons. Hens are now increasingly maintained under
welfare oriented husbandry conditions, e.g. in aviary
systems or free-range.
Intensive floor husbandry may expose susceptible
animals to a high risk of infection, in particular
broilers in the course of the short fattening period
of 5-6 weeks. Sporulated oocysts are long-lived
(under suitable conditions >l year) and resistant to
chemical disinfectants ( ► p. 571). If stables are cleaned
insufficiently before new stocking, residual amounts
of oocysts may induce initial infections in chicks,
followed by high oocyst excretion. Oocysts sporulate
and accumulate in the litter, resulting in a subsequent
high infection pressure.
Immunology. Innate and adaptive immune responses
regulate the course of coccidial infections. Many types of
cells are involved in innate responses (e.g. macrophages,
dendritic cells, NK cells, mast cells, eosinophils) with
IFN-y as a key cytokine in immunoregulation. More
recently, the stimulating effect of Eimeria profilin
(profilin is a potential ligand of Toll-like receptors TLR,
► p. 28) on chicken splenocytes has provided evidence
for a role of TLR-mediated responses in innate immunity.
Furthermore, it was shown that in an early response to
some avian Eimeria species, a particular T helper cell
subset (Th 17) is involved, which releases a diversified
spectrum of I L-17 molecules upon stimulation; IL-17
shows strong prointlammatory capacities. Level and
duration of oocyst excretion after primary infection are
regulated by Th 1-associated mechanisms.
Protective immunity to challenges after primary
infection is generally species-specific, sometimes even
strain-specific, although some cross-immunity seems to
exist between E. tenella and£. necatrix. lmmunogenicity
varies between the species. E. maxima induces the
strongest, E. acervu/ina the weakest effects. Immunity
is maintained and boosted under field conditions by
permanent reinfections. Immune protection is usually
not complete but at least prevents disease. The second
generation meronts are regarded as the principle
immunising stages whereas the first generation meronts
are considered the main targets of protective immune
reactions. Protective immunity under field conditions
with continuous reinfections is built up until the 3 rd to
4 th week of age.
Immunity to avian coccidia is predominately mediated
by cellular mechanisms, involving CD4 + and cos+
cells. However, humoral IgY (corresponding to IgG in

mammals) produced by the hen are transferred in egg
yolk to the hatchlings. In recent studies it has been shown
that immunisation of hens with large doses of E. maxima
oocysts is followed by a significant maternal antibody
transfer to hatchlings. If hatchlings were challenged with
a homologous infection, oocyst shedding was reduced
by 90 and 68% when they originated from eggs laid
by the hen 3-4 weeks or 8 weeks after immunisation,
respectively. Maternal antibodies against E. maxima are
not species-specific and confer partial protection (up to
about 60%) to E. tenella.
Although the immune mechanisms in chicken
coccidiosis are not completely understood, vaccines
have been developed which are successfully used in
practice (see below).
Pathogenesis and clinical signs. The various
Eimeria species cause specific pathological changes,
resulting in several forms of coccidiosis which are listed
(a) Eimeria tenella
(b) Eimeria brunetti
(c) Eimeria maxima
Figure 5.7. Typical alterations in chicken intestine caused by single Eimeria species (Photo: P. Hllbrich; Kuhn).
5. Phylum Alveolata
in ► Table 5.1 and shown in ► Figure 5.7. Since natural
infections are usually caused by several species, the
pathological changes and clinical signs are determined
by the dominating species or mixture of species.
The damage and loss of enterocytes and other intestinal
cells are associated with intestinal dysfunctions, such co
:g
as malabsorption of essential amino acids, glucose, ·53
vitamins, calcium, phosphorus, trace minerals, and E
leakage of proteins and fluid into the intestinal lumen, i.D
followed by hypoproteinaemia. In addition, E. tenella
and E. necatrixcause bleeding, with subsequent anaemia,
due to the location of their meronts deep in the mucosa
and immunosuppressive effects/activity. Some of the
many surface antigens of sporozoites may suppress cell­
mediated immunity and contribute to proinflammatory
reactions. In the course of immune reactions to the
parasites, TN F, free oxygen radicals and nitric oxide
are generated which induce supplementary mucosa)
damage.
(d) Eimeria necatrix
(e) Eimeria acervulina
(t) Eimer/a mitis
Part II. Parasites and parasitoses: protozoa
Coccidia may be trailblazers of other diseases by inducing
damage to the intestine or by immunosuppression. Thus,
intestinal damage by concurrent Eimeria infections may
play a role in necrotic enteritis in chickens, an important
disease by toxin-producing strains of Clostridium
perfringens.
Diagnosis. Symptoms of avian coccidiosis are often
non-specific. Diagnosis is based on necropsy findings and
microscopic detection of typical developmental stages in
native impression preparations of the intestinal mucosa.
Localisation and the type of lesions, in combination
with site and size of the meronts and gamonts, often
allow a tentative species diagnosis ( ► Table 5.1; ►
Figure 5.7). Sporulated oocysts of the Eimeria species of
chickens exhibit the general features of the genus with
4 sporocysts, each with 2 sporozoites. However, shape,
size and other morphological features of the oocysts
are not species-specific, except for the large oocysts
of E. maxima (30x21 µm; oocysts of the other species
measure 16-25xl4-19 µm). Attempts have been made
to differentiate Eimeria oocysts (e.g. from chicken, pigs,
cattle) using computerised imaging systems based on
various features (dimensions, structure, colour, etc.).
COCCI MORPH is a system which uses morphological
characteristics, obtained by shape analysis algorithms.
It is online available and provides support for quick
identification of oocysts (www.coccidia.icb.usp.br./
coccimorph). Molecular techniques are well suited for
species-specific and strain-related diagnoses.
Therapy. The treatment of diseased chickens is
usually unsuccessful. Nevertheless, flocks in which
first cases of disease are observed should be treated
with anticoccidials to prevent disease outbreaks in
yet uninfected animals or those in an early stage of
infection. In this indication toltrazuril (7 mg/kg b.w.
on 2-3 successive days in drinking water; not for laying
hens!) and sulfonamides may be used.
Control. Hygiene, chemoprophylaxis and vaccination
are established control measures.
• Hygiene and good animal husbandry
practices. The contamination of stables with oocysts
can be reduced by thorough cleaning (using steam jet
cleaners) and chemical disinfection before re-stocking
with chickens. For disinfection, products must be used
with proven efficacy against oocysts ( ► p. 571). In
the stables the litter should be kept dry to constrain
sporulation of oocysts and to impair their survival.
Hygiene is generally indispensable but as a sole measure
usually not sufficient to prevent outbreaks of coccidioses.
Good animal husbandry practices are also important,
such as adequate stocking rate, climate management in
chicken houses, adequate feeding and drinking devices,
careful supervision, etc.
• Chemoprophylaxis. Worldwide, anticoccidial
agents ( ► p. 89) are used in chemoprophylaxis of
coccidioses. They are administered over a sustained
period in feed, more rarely in drinking water, and
generally prevent disease and loss in performance.
Anticoccidials are registered in the 'European Union
Register of Feed Additives pursuant to Regulation
(EC) No. 1831/2003' (released 15.06.2015) and in
corresponding national lists ( ► Table 5.2).
Broilers kept on litter (intensive floor husbandry) have
to be protected throughout the whole period of growth
and fattening (5-6 weeks) by anticoccidial additives.
Application Is discontinued shortly before slaughtering
according to the prescribed withdrawal periods ( ► Table
5.2). Efficient control of coccidiosis in broilers is also
possible by treatment with toltrazuril (7 mg/kg b.w. in
drinking water) on days 10 and 14 after hatching. Pullets
reared for laying may only be treated with anticoccidials
until a maximum age (i.e. before the laying period) to
prevent drug residues in eggs ( ► Table 5.2).
During the rearing phase of layer pullets, attempts are
made to induce protective immunity by the application
of only partially effective drugs or employing special
regimens of drug administration. However, the creation
of a balance between protection by anticoccidials and
development of immunity is difficult under practical
conditions. Laying hens are at a particular risk of
infection after withdrawal of the anticoccidials, which
must be compensated for with hygiene and husbandry
measures. An alternative is vaccination of layer pullets
(see below).
Drug resistance. All anticoccidials registered hitherto
have induced the selection of drug-resistant Eimeria
strains (including side resistance and multiple
resistances; ► Chapter 17.3, p. 563). Thus, almost in
a race against the emergence of drug resistance, new
anticoccidials with alternative modes of action have
been developed to counteract the resistance problem.
Shuttle and rotation programmes have been developed
to slow down the development of resistance. For example,
in the first option (shuttle), an anticoccidial is given for
a maximum of two cycles, followed by a drug with a
different mode of action for an equal period of time.
In the second option, the anticoccidial is replaced by a
second compound after about 2/3 of a single production
cycle. It is believed that such programmes have helped
extend the time of efficacy of certain anticoccidials.
Another option is an alternation between cycles of
vaccination (see below) and chemoprophylaxis. It has
been shown that the sensitivity of Eimeria populations,
resistant to monensin or diclazuril, could be increased
following vaccination of broiler chicken.
 5. Phylum Alveolata

Table 5.2. Anticoccidials listed in the European Register of Feed Additives .1

- ---- j
Chemical group and active Target animals !use until Concentration in complete Withdrawai
compound . max. age feed: mg/kg period (daysJ
��e=- -
min. -/max.
---- Cu
Polyether ionophorous antibiot� __ ___ _ _ :g
_ _ ___ _
Monensin broiler__ _ j --- --l.100_ __ 125 _
·.::
E
�ullets 2
_ _ J 16 __I 100
____ _gs__ ·-+-------1 jjJ
1---- ------- ---_....,_tu _rk ey
� ,______ ! !6_______60-'-----+-_OO _____ t--- --- -1
l 1

Lasalocid broiler - 125 5

_ __ -=-----+---=-=----+--- ---f
75
-- -------+ ____ ,
P�!e!s2 16 75 _1_ 2_5___-+-------1
turkey 5___ :-1=-
16:____ - .........:..7::.. 25 --- 5- ___
i + t --j
-
=----
Salino mycin broiler - 50 70 1
-------4- -- --- - --------
________
pullets2
rabbit
12
, - --
50-- - ---· 50
- 20 25 5 -
Maduram icin broiler 5 6 3
f--- -- ------- ____
tu_rk�y ___ 16 5 5 . ---- - 5
------i
e
t-_S_ m d ura ici n b r o l '------l--- ----1-- 0_ _____,__ .:.5____ __
le
_ _ _ _ _ m_ _ _ ________ 1_ .c...:.....: r 2 2 5____--i
1
Narasin broiler - 80 100 53
Guanidines
Robenidine broiler 30 36 5
turkey 30 36 5
----- --
rabbit 50 66 5 -
Quinolines and quinazolinones
Decoquinate (quinoline) broiler 20 40 3
Halofuginone (quinazolinone) broiler 2 3 5
pullet2 16 2 3 -
turkey 1 2 2 3 5
Triazine derivatives
Diclazuril broiler 1 03
turkey 12 1 03
rabbit 1 1
1 Anticoccidials listed in 'European Register of Feed Additives pursuant to Regulation (EC) No. 1831/2003', (released 15.06.2015), European
Union. Source of detailed data: Swiss list of anticoccldlals (10. 06. 2015) (www.agroscope.ch, search term 'Kokzidiostatika').
2 Pullets reared for laying.
3 According to product label.

• Vaccination. Various types of vaccines for oral vaccine (Livacox• T), containing oocysts of E. tenella, E.
application have been developed against chicken acervulina and E. maxina, is recommended for broiler
coccidiosis (details ► p. 86, p.569). In European chicken, whereas a vaccine containing an additional
countries several live vaccines, containing sporulated species (E. necatrix) (Livacox• Q) is designed for chicken
Q)
oocysts of attenuated (non-pathogenic) Eimeria species raised for laying or breeding. c::
or strains are registered (Paracox•, Livacox•, Hipracox•).
·u
'6
These vaccines are applied to newly-hatched chicks • Other measures. Coccidiosis, particularly E. Q)

2
(less than 10 days old) in drinking water or they are maxima infections, causes considerable dysbacteriosis.
sprayed on food. Another application form is spraying Special diets with essential amino acids or ionophores co
c::
·;::
the chicks with the vaccine in the hatchery. Following (monensin, etc.) may stabilise the normal gut microflora.
ingestion of oocysts, immunity develops two weeks Probiotic and prebiotic supplements in feed preparations
after vaccination, which is continuously re-stimulated have been shown to lessen depressive effects on growth c::
by oocyst uptake from the environment, providing long­ in coccidian-infected broilers. Genetically-based >,
0
0)

lasting protection against disease. Depending on the resistance to clinical coccidiosis in chickens has been
composition of the vaccines with regard to the Eimeria demonstrated and could be correlated to quantitative ·u5
species and their numbers they contain, the vaccines are trait loci (QTL). However, practical advantages are yet co
co
used for different target groups. For example, a trivalent to be derived from these findings. Q_
 Part II. Parasites and parasitoses: protozoa
■ Eimeria species and coccidiosis in turkeys
As in fowl, the development of Eimeria species takes
place in various parts of the intestine: E. meleagrimitis
(predominantly small intestine), E. innocua and E.
subrotunda (exclusively small intestine), E. dispersa
(small intestine and rectum), E. adenoides and E.
gallopavonis (small intestine, rectum and caeca). All
species are host-specific, except E. dispersa; strains of
this species could be transmitted to quails and pheasants.
These species may cause conditions ranging from mild
enteritis to severe necrotic and haemorrhagic lesions.
The most pathogenic species are E. adenoides, E.
gallopavonis and E. meleagrimitis. Clinical signs are
usually less pronounced than in chicken coccidiosis.
Diseases are generally limited to young animals, which
also must be protected by anticoccidials ( ► Table 5.2).
Alternatively, a vaccine is available in some countries
(Immucox• T, ► p. 569).
■ Eimeria species and other coccidia in ducks
Ducks are parasitised by coccidia of the genera Tyzzeria
(8 sporozoites in the oocyst without sporocysts),
Wenyonella (4 sporozoites in each of 4 four sporocysts
in the oocyst), and Eimeria. A total of 13 species have
been described although the validity is not clear in every
case. In ducks in France, two Tyzzeria spp. ('f. pellerdyi,
T. perniciosa) and four Eimeria spp. (E. danailovi, E.
nyroca, E. aythyae, E. mulardi) were reported. Tyzzeria
species are the most common. T. perniciosa is pathogenic
in ducklings, causing haemorrhagic enteritis. CNS
symptoms are observed in cases of heavy intestinal
infections with E. danailovi. E. mulardi infects the nuclei
of enterocytes of jejunum and ileum, and it may cause
haemorrhagic enteritis. As a whole, coccidiosis seems
to be relatively rare in ducks and related deaths have
only been observed in ducklings after heavy exposure.
Chemoprophylaxis is, therefore, usually not required.
Toltrazuril is recommended for chemotherapy. Caution:
some anticoccidials are toxic to ducks!
■ Eimeria species and other coccidia in geese
At least 15 Eimeriidae are found in Anserinae, 6 of
them in the domestic goose. Except for one Tyzzeria
(IJ
species, all belong to the genus Eimeria. T. parvula
·o
C
'6 shows little pathogenicity and infects epithelial cell of
(IJ
�
the smaJl intestine. Of the Eimeria species, E. anseri
and E. nocens cause coccidiosis of the small intestine.
co E. kotlani infects epithelial rectum cells and may cause
C
·;;::
moderate alterations. E. truncata is an exception in that
it infects epithelial cells of the renal tubules. In infected
-� animals kidneys and the renal tubuli are enlarged, and
>- the kidney parenchyma is interspersed with many small,
0)
0 yellow-whitish foci, frequently in striated arrangement.
0
·w The infection causes necroses of the tubules and reactive
co interstitial nephritis. E. truncata is highly pathogenic in
co
0... goslings (sometimes whole flocks die within a few days).
Successful treatment can be achieved with monensin and
toltrazuril (halofuginone is toxic to geese!).
■ Eimeria species in other birds (pigeons,
pheasants, guinea fowls, quails)
In Europe, two Eimeria species, E. labbeana and E.
columbarum, are found coexisting in pigeons. They
cause mild catarrhalic, usually asymptomatic enteritis,
which, however, may impair the performance of carrier
pigeons. Chemotherapy is possible using toltrazuril,
clazuril and other anticoccidials. Caution is necessary
since most of the drugs may cause damage to the feathers
if applied during moulting. Hygiene measures (regular
cleaning and disinfection of the pigeon loft and of
feeding and drinking facilities, drying of the loft, use
of drinking vessels with narrow openings) are necessary.
Pheasants, guinea fowls, quails and other bird species,
which are maintained as pet birds or in intensive
husbandry, each have their own, usually specific coccidia
of varying pathogenicity; e.g. seven Eimeria species are
found in pheasants. Coccidiosis may become a serious
disease problem with high mortality particularly in
young birds, for instance in rearing establishments.
Control is based on hygienic rules, as mentioned above.
Anticoccidials may be used as for domestic chickens.
Selected references
Chapman HD (2014) Milestones in avian coccidiosis research:
a review. Poult Sci 93: 501-511.
Chapman HD, Barta JR, Blake D, Gruber A, Jenkins M,
Smith NC, Suo X, Tomley FM (2013) A selective review of
advances in coccldiosls research. Adv Parasitol 83: 93-171.
Kim ES, Hong YH, Min W, Llllehoj HS (2006) Fine mapping
of coccldla resistant quantitative trait loci in chickens. Poult
Sci 85: 2028-2030.
Krautwald-Junghanna ME, Zeblsch R, Schmidt V (2009)
Prelevance and treatment of coccidiosis in domestic pigeons
(Columba I/via forma domestica) with particular emphasis on
toltrazuril. J Avian Med Surg 23: 1-5.
Min W, Kim WH, Llllehoj EP, Lillehoj HS (2013) Recent
progress in host immunity to avian coccidiosis: IL-17 family
cytokines as sentinels of the Intestinal mucosa. Develop
Comp lmmunol 41: 418-428.
Peek HW, Landman WJ (2011) Coccidlosis In poultry:
anticoccidial products, vaccines and other prevention
strategies. Vet Q 31: 143-161.
Reid AJ, Blake DP, Ansari HR, Billington K, Browne HP,
Bryant J, Dunn M, Hung SS, Kawahara F, Miranda­
Saavedra D, Malas TB, Mourier T, Naghra H, Nair M,
Otto T D, Rawlings ND, Rlvailler P, Sanchez-Flores
A. Sanders M, Subramaniam C, Tay YL, Woo Y, Wu
X, Barrell B, Dear PH, Doerig C, Gruber A. Ivens AC,
Parkinson J, Rajandream MA. Shir1ey MW, Wan KL,

Berrlman M, Tomley FM, Pain A (2014) Genomic analysis
of the causative agents of coccidiosis in domestic chickens.
Genome Res 24: 1676-1685.
Witcombe OM, Smith NC (2014) Strategies for anti-coccidial
prophylaxis. Parasitology 141: 1379-1389.
Zhang L, Liu R, Ma L, Wang Y, Pan B, Cai J, Wang M (2012)
Bmeria tenella: expression profiling of toll-like receptors and
associated cytokines in the caecum of infected day-old and
three week old SPF chickens. Exp Parasitol 130: 442-228.
■ Eimeria species and eimerlosis (coccidiosis)
of cattle
Summary
• Agenta. A broad diversity of Elmerla specln occurs in
cattle worldwide. Thirteen species are found In Europe.
The moat important species are E. bovls, E. zuemll and
E. alabamensls.
• Life cycle. Infection occurs by ingestion of sporulated
oocysts. Endogenous development In the small
Intestine or in the small and large intestines (E. bovls,
E. zueml�. In E. bovls, E. zuern/1, E. auburnensls there
seem to be two meront generations with formation
of macromeronts (0 200-300 µm) as first generation
meronts in the distal small Intestine. Prepatency Is
dependent on the species, ranging from 6 to 24 days.
• Occurrence, epidemiology. High prevalences (>80%)
worldwide. Most common species are E. bovls, E.
zuemll, E. ellipsoldalls and E. auburnensls. Sporulated
oocysts survive In stables and In soil for months.
Disease is found predominantly in young animals up to
an age of 1½ years. However, mostly endemic stability
develops due to an early development of Immunity. E.
a/abamens/s coccidlosls occurs approximately 2 weeks
after turnout to graze In the first season.
• Pathogenesis, clinical slgna. E. bovls and E. zuemll
may cause severe haemorrhagic typhlitls and colitis,
and E. alabamensls Induces profound catarrhalic
enteritis.
• Diagnosis. Symptomatic diagnosis la supported by
detection of usually numerous oocysts In the faecn
(flotation techniques). Size and shape of oocysts allow
species Identification.
• Therapy, control. Treatment of exposed animals with
toltrazurll (1>< 15-20 mg/kg b.w., p.o. or 2>< 10 mg/kg
b.w., p.o. on consecutive days) or dlclazurll (1 mg/kg
b.w., p.o.). Palllatlve treatment (electrolytes, etc.).
Hygiene measures In stables; particular measures In
case of E. a/abamensls.
Agents. In European cattle at least 13 Eimeria
species are known to occur which can be identified by
morphological features of sporulated oocysts ( ► Table
5.3; ► Figure 16.9, p. 540). These species are principally
host-specific but some are also found in other bovines
(e.g. buffalo, bison). E. zuernii and E. bovis can be highly
pathogenic.
Life cycle. The life cycle of bovine coccidia corre­
sponds with the general development scheme of other
5. Phylum Alveolata
Eimeria species ( ► Figure 5.3) but has been investigated
in detail only for E. bovis, E. zuernii, E. alabamensis
and E. auburnensis ( ► Table 5.3). After ingestion of
sporulated oocysts, sporozoites are released into the
intestine and infect, in a species-dependent manner,
cells of the jejunum or the ileum. The subsequent
development follows two different strategies: E. bovis, ni
D
E. zuernii and E. aubumensis form large macromeronts ·;::
Q)
(meronts I) of a size of 200-300 µm within a period of E
approximately 2 weeks; other species, e.g. E. alabamensis w
create small (0 10 µm) meronts I within a few days.
Macromeronts are macroscopically detectable and
contain, ultimately, > I 00,000 merozoites, whereas the
small meronts I contain only ~30 merozoites. The 2 nd
merogony and the subsequent gamogony proceed in all
species relatively quickly in cntcrocytes or in cells of the
lamina propria of more distal sections of the intestine.
The differences in meront I development are reflected
by diverging prepatencics of >2 weeks in the first case
and 6-10 days in the latter.
Further species-specific distinctions concern the
localisation of the meronts I; for instance, the meronts
I of E. bovis establish in endothelial cells of the central
lymph capillaries of the intestinal villi whereas meronts
I of E. alabamensis develop in nuclei of epithelial cells
of the small intestine. In both cases, the use of these
peculiar locations is interpreted as an evasion into an
immunologically privileged niche.
Provided there are no re-infections, the patent periods
are usually relatively short and last a few days up to
2 weeks. The maximum oocyst excretion is generally
observed a few days after the commencement of oocyst
shedding. Sporogony of oocysts in the environment is
completed within 2-3 days under conditions of suitable
temperature and moisture.
Occurrence and epidemiology. E. bovis, E. zuernii,
E. auburne11sis and E. alabamensis are frequently found
worldwide. The occurrence of the other species varies
regionally. In most cases, mixed infections with several
species are observed. Prevalences fluctuate considerably
with seasons and geographical regions and may reach
90%. Generally, prevalence and intensity of oocyst
excretion are higher in 3-18 months old animals than
Q)
in older cattle, although oocyst excretion of cows may
·o
C
markedly increase around calving. Calves are often '6
Q)
infected within the first days of life and shed oocysts at 2
an age of 2 weeks. Maximum prevalences and oocyst c
co
excretion in housed calves are usually observed at C
·;::
an age of 9-10 weeks. Husbandry systems that allow
intense contact between individual calves are regarded as
predisposing factors for infection. Oocysts are spread by -�
contamination of boxes, outside pens, pastures, feed and >,
CJ)
the coat of the animals; they are ingested with feed and 0
0
water and by licking. Moisture and warm temperatures ·u5
favour sporulation. In moist and shady places on pasture �
&
 Part II. Parasites and parasitoses: protozoa

Table 5.3. Eimeria species (selection) of cattle (oocyst morphology, ► Figure 16.9, p. 540).
" .. - "'
Elmerla spe_ cies Main lo�alisatien of develo�mental stages and disease Pathogenlcity1 .Prepaten:y (da)'s)J
_
E. bovis ileum (endothelial cells of central lymph capillaries of villi): large +++ 18-21
meronts I (0 >200 µm); epithelial cells of caecum and colon: small
meronts II and gamonts
--- - Haemorrhagic typhlltis and colitis
E. zuernii ileum (lamina propria): large meronts I (0 >200 µm); epithelial cells +++ 15-17
of caecum and colon: small meronts II and gamonts
Haemorrhagic typhlltls and colitis --
E. alabamensis jejunum and especially ileum (in nuclei of epithelial cells): meronts ++ 6-8
1-11 and gamonts: rarely gamonts in colon and caecum
- --Catarrhallc enteritis
- --- - - - --- - -·
E. auburnensls jejunum, Ileum (epithelium): large meronts I (up to 240 µm) and ++ �16
1T1eronts II; gamont in lamina proprla
-·- Catarrhallc enteritis - -- -- -- . --·
E. ellipsolda/1s jejunum. especially Ileum (epithelium): meronts HI and gamonts + 8-10
i------- Catarrhalic enteritis - - --
- ·
E. wyomingensis
p,,,--.-. - --
�istal small lntest�e (no furthe_r d�la _!lva�ble) - �13
Endogenous development unknown: E. bukidnonensis, E. subspherica, E. cylindrical, E. canadensis, E. brasiliensis
1 Degree of pathogenicity: +++=high:++ =moderate:+= low; - = none.

sporulated oocysts may survive for many months and
may overwinter.
In most cases, Eimeria infections in calves remain
asymptomatic. Those affected by disease are usually
animals at an age of½- l ½ years, rarely younger and
older ones (special situation in E. alabamensis, see
below). Change of housing and rearrangement of groups
of young animals (integration of individual animals into
groups or merging small groups into large ones) are
often followed by an increasing intensity and duration
of oocyst excretion. Outbreaks due to E. bovls and E.
zuernii in Central Europe are mostly observed during
the grazing season in early summer to autumn, but they
may also occur independent of season in housed animals
with or without access to outside pens.
E. alabamensis infections are typically seen in animals
on pasture. The species causes severe catarrhalic enteritis
in animals in the course of the first grazing season up to
an age of 15 months. Such outbreaks have been observed
in northern DE, DK and SE 2 weeks after turnout to
grazing. Oocysts of E. alabamensis are exceptionally
Q)
persistent (>2 years on pasture) and resistant to dryness.
·u
C
macromeronts I. Neutrophils seem to be important
effector cells in innate reactions, e.g. by forming
NETs (neutrophil extracellular traps, ► p. 27) and by
phagocytosis. Under experimental conditions, protective
immunity develops after single massive infection as
well as after repeated low-dose infections. In primary
and challenge infections, CD4 + and cos + T cells,
respectively, accumulate in infected mucosal areas, and
it appears that cytotoxic T cells are effector cells in the
latter case.
Pathogenesis. E. bovis and E. zuernii are the most
pathogenic species. The large meronts I are not important
in this respect but the release of meronts II and gamonts
is associated with distinct lesions in the large intestine.
Depending on the intensity of the infection, focal up to
extended losses of epithelial cells and necroses of the
mucosa, dilation of blood and lymph vessels, cellular
infiltrations and oedemas develop in the tissue. Due
to the lesions, fluids, minerals, proteins (particularly
albumin) and blood are lost into the intestine. The
contents of the caecum and colon liquefy, and the watery
faeces contain blood, fibrin and mucosa! shreds.

'6 Hay stored for 8 months still contained enough oocysts In the case of E. alabamensis, the release of meronts II
Q)
to provoke coccidiosis in calves and heifers. is associated with profound catarrhalic enteritis with
desquamation of the mucosa and thickening of the
co
C
Immunology. Cattle acquire species-specific immunity intestinal wall. Bleeding is usually not observed. Other
·c which protects them from disease after repeated natural species settling in the small intestine (i.e. E. ellipsoidalis)
Q)
infections but immunity does not completely suppress may cause catarrhalic enteritis but, for most species, the
C oocyst excretion. Experimental data on immunological pathogenic impact is not known.
>, responses refer mainly to E. bovis infections. Meronts
CJ)
0 I of this species grow up in endothelial cells and Clinical signs. In Europe, diseases caused by E. bovis,
0
suppress all important inflammation parameters, by E. zuernii and E. alabamensis are of special importance.
·u5
this means securing the long-lasting maturation of the
co
a..

• E. bovis and E. zuernii. In benign cases, the
animals excrete pasty or liquid faeces. They do not
feed but are thirsty; these animals usually recover
quickly. Severely diseased calves are febrile and suffer
considerable pain (tenesmus, rectal prolapse), excrete
liquid, bloody faeces with mucus and mucosa! shreds
(► Figure 5.8). Occasionally, CNS symptoms may arise.
Mortality is high in these cases. Animals are dehydrated
and anaemic and often in a febrile state. Surviving calves
and heifers recover slowly (after weeks) but they rarely
catch up with the status of age-matched uninfected
animals. The economic effects of subclinical infections
should not be underestimated. Weight losses of clinically
and subclinically diseased calves can amount to 6 kg and
2 kg, respectively, within 3 weeks.
• E. alabamensis. Diseased animals excrete foamy,
liquid faeces for some days; they are apathetic , anorexic
but thirsty and lose approximately 10-15% of weight in
the course of the initial 2 weeks on pasture. Often, >80%
of the calves in a herd suffer from diarrhoea. Deaths are
rare. Recovery takes approximately 4 weeks.
Diagnosis. The diagnosis of the disease is based on
clinical signs and the coproscopic detection of large
numbers of oocysts (opg > 10,000 up to several millions)
by flotation techniques. The involved Eimeria species
should be determined by oocyst morphology ( ► Figure
16.9, p. 540} or molecular tools. Oocysts shedding may
be absent at the beginning of the disease, or may be very
Figure 5.8. Eimeriosis in cattle: heifer with bloody diarrhoea
(Photo: IPZ, G.S. Willi).
5. Phylum Alveolata
minimal in the late phase of patency. In severe E. bovis and
E. zuernii infections, gamonts may be demonstrated in
rectally taken mucosa( samples. Animals kept on pasture
frequently show mixed infections with gastrointestinal
nematodes. Differential diagnosis in cases of bloody
faeces should consider Salmonella infections.
ell
-0
Therapy and control. Calves should be treated ·.:
Q)
immediately after first signs of coccidiosis with E
toltrazuril (15 mg/kg b.w., p.o.) or diclazuril (I mg/kg w
b.w., p.o.) (withdrawal period for toltrazuril: 63 days;
diclazuril: none). Best efficacy is seen in animals that
are treated during prepatency. PaJliative treatment
of sick animals is often essential. Sulfonamides
(sulfaquinoxaline, sulfadimidine) show little effect
against Eimeria spp. but may be helpful for treating
concurrent bacterial infections. Treatment with
toltrazuril does not interfere with the development of
immunity to challenge infections. In E. alabamensis
endemic areas, metaphylactic application of toltrazuril
at turnout to grazing has prevented clinical outbreaks
and resulted in significant weight gain when compared
to placebo-treated controls.
Hygiene measures (pasture hygiene, clean drinking
water, dry litter, cleaning and disinfection of calf boxes,
good stable climate) contribute to reducing the risk of
infection. As prophylaxis against E. alabamensis it is
recommended that calves in their first grazing season
are not put on pastures that have been grazed during
the previous season by young animals. Hay from
contaminated grassland should not be fed to calves.
■ Eimeria species and eimeriosis in sheep and
goats
Summary
Sheep and goats are hosts of several pathogenic
Eimeria species which may cause catarrhalic enteritis
or haemorrhagic inflammation of the large intestine,
particularly in lambs. Therapy with toltrazuril or diclazuril.
Agents. Sheep are hosts of 11-15 Eimeria species with
E. ovinoidalis and E. crandallis as the most pathogenic
species ( ► Table 5.4). At least nine Eimeria species occur Q)
in goats, including E. ninakohlyakimovae, E. arloingi, C
E. alijevi, E. caprina, E. christenseni, E. caprovina, and
·u
'6
Q)
E. hirci. The three first mentioned species are regarded
as pathogenic.
ell
C
·.:
Occurrence and life cycle. The Eimeria parasites Q)
of small ruminants are cosmopolitan. E. ovinoidalis,
E. bakuensis, E. weybridgensis and E. crandallis are the C
>,
most frequent species in sheep. E. ninakohlyakimovae, O'l
0
E. arloingi and E. alijevi are common in goats.
·u5
Some data on the development of coccidia in sheep ell
are presented in ► Table 5.4. Some species form Q..
 Part II. Parasites and parasitoses: protozoa

Table 5.4. Eimeria species in sheep.

t:tmeria species
� ;;,., -
Main localisations of developmental stages and. disease Pathogeniclty1
-
Prepatency (days)
.
. ' - ' . ' .

E. ovinoidalis distal small intestine (epithelium): large meronts I, caecum, colon +++ 10-15
(epithelium): meronts II and gamonts
haemorrhagic typhlitis and colitis
E. crandallis small intestine: large meronts I (250 µm) in lamina propria; distal ++ 16-20
small intestine, caecum (epithelium): meronts II and gamonts
focal desquamation of epitheli�m
I
E. bakuensis small intestine: large meronts I in endothelial cells of central lymph + 19
vessels of villi; meronts II and gamonts in epithelial cells
focal lesions of the mucosa, formation of 'polyps'
I
E. ahsata small intestine (epithelium): all stages (large meronts I, 185 µm) ++ 18-20
--
catarrhalic enteritis I

I
E. faurei small intestine: all stages + 14
----�-·
catarrhalic enteritis ----- -
E. weybridgensis jejunum: (no further data available) :2:23

-
disease: no data
E. intricata distal small intestine: meronts I and II; caecum: gamonts :2:20
I disease:
--- data ----·----
no -----·--
I :2:11
I.
E. parva small Intestine (predominantly epithelium): large meronts I; ?
caecum, colon: gamonts

l
disease: no data ------ ·----
Endogenous development unknown: E. gilruthi, E. granulosa, E. marsica, E. pa/Iida

t
I 1 Degree of pathogenicity: +++ = high; ++ = moderate: + = low; - = none.

macromeronts in cells of the gastrointestinal tract. For
instance, E. bakuensis in sheep and E. ninakohlyakimovae
in goats infect endothelial cells of the lymph capillaries
of the intestinal villi in which the macromeronts develop
(like E. bovis). Meronts I of other species establish
in cells of the lamina propria or in epithelial cells of
the small intestine. Special features are known for E.
bakuensis and E. crandallis; gamonts in an early stage,
so-called pro-gamonts, divide synchronously with the
host cell, so that the host daughter cells are also infected.
This proliferation of the pro-gamonts results in the
formation of mature gametes. Finally, accumulations
of pro-gamonts, gametes and oocysts are found in
polyp -shaped, circumscribed areas of 1-2 mm in size
in the distal small intestine (£. bakuensis) or diffusely
distributed in the hyperplastic mucosa of small intestine
and caecum (E. crandallis).
E. gilruthi (syn. G/obidium gilruthi) takes an exceptional
position. This species is found in the abomasum of
sheep and goats as large macromeronts (up to 900 µm).
Further stages and the life cycle are unknown. It is not
clear whether this species comprises a larger spectrum of
miscellaneous agents. E. gilruthi seems to be apathogenic
and usually represents an incidental finding.
Epidemiology, immunology and clinical signs.
Eimeria species of sheep and goats are common
and cosmopolitan. They are usually found as mixed
infections. Mostly, lambs fall sick at an age of 4-8 weeks
(partly before weaning) either in the stable or at the start
of the grazing season in Central Europe (May to June) on
densely stocked pastures. Lambs excrete many oocysts
(opg up to 10 million) and heavily contaminate their
environment. Subsequently, in general, immunity to
challenge infections develops. Stress (e.g. from transport,
weather, faulty feeding, dense stocking, other infections)
may interfere with immunity. Insufficient exposure
to coccidia in the first 4 weeks of life may derogate
immunity. Fattening lambs are often clinically affected
(diarrhoea, loss of weight) due to an infection with E.
ovinoidalis within the first 6 weeks of housing.
Goat kids are particularly at risk of infection with Eimeria
shortly after weaning. Even subclinical infections can
affect performance.
Diagnosis. Diagnosis is performed as for cattle
coccidiosis, i.e. by demonstration of oocysts in the
faeces. Many of the Eimeria species of sheep and goats
can be differentiated by morphological features of the
sporulated oocysts.
Treatment and control. Chemotherapy uses
toltrazuril (20 mg/kg b.w., p.o) or diclazuril (1 mg/kg
b.w., p.o.). Treatment should be started immediately
after first detection of clinical signs in a herd or
metaphylactically 7 days after turning out to pasture.
Hygiene measures are the same as those described for
cattle coccidiosis.
■ Eimeria species in pigs
► p.98.

- Selected references ,-..,,,.....-:"""'.:==-=�:-:J.
Daugschies A, Agneessens J, Goossens L, Mengel H, Veys
P (2007) The effect of metaphylactic treatment with diclazuril
(Vecoxan) on the oocyst excretion and growth performance
of calves exposed to natural Eimeria infection. Vet Parasitol
149: 199-206.
Enemark HL, Dahl J, Enemark JM (2013) Eimeriosis in Danish
dairy calves: correlation between species, oocyst excretion
and diarrhoea. Parasitol Res 112 Suppl 1 : 169-176.
Faber JE, Kollmann D, Heise A, Bauer C, Falling K, BOrger
HJ, Zahner H (2002) Eimeria infections In cows in the
periparturient phase and their calves: oocyst excretions
and levels of specific serum and colostrum antibodies. Vet
Parasitol 104: 1-17.
Hermosilla C, Ruiz A, Taubert A (2012) Elmer/a bovls: an
update on parasite-host cell interactions. Int J Med Mlcrobiol
302: 210-215.
Hermosilla C, Zahner H, Taubert A (2006) Eimeris bovls
modulates adhesion molecule gene transcription in and
PMN adhesion to infected bovine endothelial cells. Int J
Parasitol 36: 423-431.
Jager M, Gauly M, Bauer C, Failing K, Erhardt G, Zahner
H (2005) Endoparasites in calves of beef cattle herds:
management dependent and genetic influences. Vet Parasitol
131: 173-191.
Lassen B, Lepik T, Bangoura B (2013) Persistence of Eimeria
bovis in soil. Parasitol Res 112: 2481-2486.
Reeg KJ; Gauly M, Bauer C, Mertens C, Erhardt G, Zahner H.
(2005) Coccidial infections in housed lambs: oocyst excretion,
antibody levels and genetic influences on the infection. Vet
Parasitol; 127: 209-219.
Ruiz A, Guedes AC, Munoz MC, Molina JM, Hermosilla C,
Martin S, Hernandez YI, Hernandez A, Perez D, Matos
L, Lopez AM, Taubert A (2012) Control strategies using
diclazuril against coccidiosis in goat kids. Parasltol Res 110:
2131-2136.
Ruiz A, Matos L, Munoz MC, Hermosilla C, Molina JM,
Andrada M, Rodriguez F, Perez D, Lopez A, Guedes
A, Taubert A (2013) Isolation of Eimeria ninakohlyakimovae
field strain (Canary Islands) and analysis of its infection
characteristics in goat kids. Res Vet Sci 94: 277-284.
Saratsis A, Karagiannis I, Brozos C, Kiossis E, Tzanadakis
N, Joachim A, Sotiraki S (2013) Lamb eimeriosis: applied
treatment protocols in dairy sheep production systems. Vet
Parasitol 196: 56-63.
■ Eimeria in equids
Eimeria /euckarti
Only a single Eimeria species, E. leuckarti, is found
worldwide in horses and donkeys. It forms large
(85x55 µm), dark-brown, pear-shaped oocysts with a
distinct micropyle at the acute pole (► Figure 16.13,
p. 545). The thick (~8 µm) oocyst wall consists of two
layers that occasionally separate into the outer brown
and inner transparent layer. Besides a generation of
5. Phylum Alveolata
meronts in epithelial cells of the small intestine, large
(~200 µm) microgamonts and smaller macrogamonts
accumulate in the lamina propria of jejunum and
ileum. After a prepatency of 4-5 weeks, foals and, very
rarely, older equines shed oocysts sporadically for 2-4
months. Infections are generally asymptomatic and
clinically irrelevant. Due to the high specific gravity of
the oocysts, their detection in faecal samples requires
either a sedimentation technique or a flotation method
using a flotation solution of high specific gravity(>1.3).
■ Eimeria species and eimeriosis (coccidiosis)
in rabbits
Summary
Agents and llfe cycle. Rabbits are hosts of 11 Eimer/a
species Infecting particular parts of the small and large
intestine. A further species, E. st/eds/, infects the bile
duct epithelium.
• Occurrence, epidemiology. Prevalence and
importance of coccidiosis in rabbits depend on �
husbandry systems.
• Cllnical signs. Similar symptoms of intestinal and bile
duct coccidiosis: diarrhoea or obstipation; bloated
abdomen; anorexia; exhaustion; in bile duct coccidiosis,
also icterus.
Diagnosis. Demonstration of oocysts in the faeces,
necropsy.
Therapy and control. Therapy with toltrazuril (25 ppm
in drinking water for 2 days). Tentatively, repetition of ·l
drug application after 5 days and palliative treatment. �
Chemoprophylaxls with salinomycin, robenidine or
diclazuril (► Table 5.2). Hygiene measures are important.
.i.
Agents and occurrence. Worldwide, many Eimeria
species have been described in domestic rabbits, of
which 11 belong to the common species. One species, E.
stiedai, infects epithelial cells of the bile duct (bile duct
or liver coccidiosis), the other species infect cells of the
intestine (intestinal coccidiosis). E. intestinalis (small
intestine) and E. flavescens (colon, caecum) are highly
pathogenic; E. irresidua, E. magna, E. media (small
intestine) and E. piriformis (colon) are of moderate
pathogenicity; the other species (E. coecicola, E. exigua,
E. perforans, E. vejdovskyi) show little pathogenicity.
Q)
Life cycle. After ingestion of sporulated oocysts of
·u
C
intestinal species, the sporozoites settle in various parts '6
Q)
of the small and large intestine and develop mostly in
enterocytes, though some species also develop deep in
the mucosa. For instance, E. irresidua infects epithelial cu
C
·;::
cells of the crypts (merogony I), subsequently the Q)
lamina propria (merogony II) and, finally, epithelia of
the villi of the small intestine (merogonies III and IV -�
and gamogony). The various developmental steps may >,
Ol
take place in different sections of the intestine, e.g. in the 0
0
case of E. flavescens, in the small intestine(merogony I) ·cn
and in the caecum(merogonies II-V). Sporozoites may
cu
Q_
 Part II. Parasites and parasitoses: protozoa

also take an extraintestinal route to migrate and reach

lymph nodes and the spleen (E. coecicola). The asexual
development of the various species occurs in 2-5
merogonies and ends, in some species, with mono- or
binuclear stages that are regarded as preliminary male or
female forms. Such stages have, so far, not been detected
in any other host species of Eimeria. Prepatency of the
intestinal species lasts 5-10 days.

E. stiedai infects epithelial cells of the bile ducts. The

sporozoites invade the intestinal mucosa and probably
reach their destination via blood vessels. E. stiedai passes
up to 6 merogonies before developing into gamonts. In
the course of these multiplications E. stiedai induces a
papillomatous proliferation of the bile duct mucosa,
which increases the number of potential host cells. The
bile ducts dilate, and the liver exhibits a knobbly surface.
Prepatency takes 14-18 days.

Epidemiology. Mixed infections of several species are

usually found. Clinical coccidiosis occurs predominantly
in young animals after weaning at an age of 5-7 weeks.
I Caecotrophy is not an important source of infection
since freshly shed oocysts are not yet sporulated. The
I
floor of the cages, the litter and polluted drinking and
l, feeding troughs are often heavily contaminated with
sporulated oocysts. The epidemiological situation differs
with husbandry systems; coccidiosis is not usually
observed in individually housed animals but common
in animals kept in groups on the floor. Figure 5.9. Eimeria stiedai: (a) liver (fixed) of a rabbit with knob­
like alterations (Photo: IPZ); (b) histological section through a
Immunology, pathogenesis and clinical signs. bile duct with papillomatous proliferations of the mucosa and
Animals that survive infection develop a species-specific, numerous developmental stages of E. stiedai (Photo: IPH, K.F.).
sometimes strain-specific, predominantly cell-mediated
immunity.
depends on necropsy and additional parasitological,
Intestinal coccidiosis is characterised by catarrhalic bacteriological and virological investigations. Some
enteritis with diarrhoea or obstipation, tympany, rabbit Eimeria species can be differentiated by means
anorexia and exhaustion. Haemorrhagic alterations of of sporulated oocysts; molecular techniques allow the
the intestine are generally absent. Intestinal diseases diagnosis of all Eimeria species of rabbits.
of rabbits are frequently multifactorial disorders
(enteritis complex in rabbits), complicated by pathogenic Therapy and control. Individual treatment is
Escherichia coli strains, Clostridium spp., Bacillus Indicated in valuable breeding animals and pets and
piliformis and rotavirus infections. Faulty husbandry and should always consider bacterial infections as well
feeding mistakes represent additional negative factors. as husbandry and feeding errors. The drug of choice
is toltrazuril (25 ppm in drinking water for 2 days,
(l)
Bile duct coccidiosis (liver coccidiosis) shows similar eventually repeated after 5 days), supported by palliative
·u
C

'6 clinical signs, partly associated with icterus. The treatment. Sulfadimethoxine (40 mg/kg b.w., p.o. daily
(l)
�
extremely dilated bile ducts are congested by detritus for 5-7 days) has also proved its worth, particularly in
� and oocysts. The mucosa is folded and the epithelial concurrent bacterial infections.
<tl
C cells are infected by meronts, gamonts and oocysts. The • Hygiene measures. Daily removal of faeces and
·.:: neighbouring damaged liver parenchyma is replaced regular cleaning and disinfection of troughs and
(l)

� by connective tissue. The liver may be enlarged and gratings with hot water/steam (steam jet cleaner)
C the dilated bile ducts emerge as pea- or hazelnut-sized, or, when needed, by suitable disinfectants to reduce
>, greyish-white knobs ( ► Figure 5.9). contamination. Water supply by nozzle drinkers,

-
0)
0 avoidance of feeding errors and attention to stall
0
·en Diagnosis. Clinical signs and coproscopical findings climate are helpful.
• Chemoprophylaxis. Several anticoccidials are
<tl can be ambiguous since oocyst excretion and symptoms
<tl
a.. often d o not correlate. Aetiological clarification licensed for chemoprophylaxis against rabbit

coccidiosis ( ► Table 5.2). Resistance to particular
drugs (e.g. robenidine) is not uncommon in
commercial rabbit production. Vaccines are under
development; several strains of precocious lines
of rabbit coccidia are available and have been
successfully tested in vaccination studies.
■ Eimeria species in hares
Hares carry a manifold spectrum of intestinal Eimeria
spp. different from that of rabbits. The most frequently
occurring species in Europe are E. tow11se11di and E.
leporis. Prepatencies of the various species last 5-14
days. According to a study in the Czech Republic E.
townsendi was found in 70%, E. leporis in -40%, and E.
balmtica, E. europaea, E. robertsoni in approximately 30%
of brown European hares. Clinical intestinal coccidiosis
in wild hares is rare, but it may occur in wet seasons,
particularly in young hares.
■ Eimeria species in laboratory rodents
Various host-specific Eimeria species infect laboratory
rodents. The species show little pathogenicity. E.
falciformis, E. vermiformis, E. papillata and other species
infect mice (Mus musculus). E. separata, E. nieschulzi, and
others are parasites of rats (Rattus rattus, R. norvegicus).
Guinea pigs are hosts for E. caviae. Because of high
hygienic standards in keeping laboratory animals,
coccidial infections are rare in this group of animals.
Caution is necessary with all immunosuppressed rodent
strains where all coccidia display pathogenicity.
■ Eimeria and other coccidia in fishes
A large diversity of coccidial genera and species are
described in fishes, e.g. E. (syn. Goussia) carpelli and£.
(syn. Goussia) subepithelialis that may cause enteritis.
For details the reader is referred to the special literature
on coccidia and fish diseases.
Selected references
Akpo Y, Kpodeon MT, DJago Y, Llcois D, Youssao IA (2012)
Vaccination of rabbits against coccidiosls using precocious
lines of Eimeria magna and Eimeria media In Benin. Vet
Parasitol 184: 73-76.
Bauer C (1988) Prevalence of Eimeria feuckarti (Flesch, 1883)
and intensity of faecal oocyst output in a herd of horses
during a summer grazing season. Vet Parasitol 30: 11-15.
Coudert P, Licois D, Drout-Viard F (1995) Eimeria species and
strains of rabbits. In: Eckert J, Brown R, Shirley MW, Coudert
P (eds.) Guidelines on techniques in Coccidiosis research.
COST 89/820. Luxembourg, Luxembourg: European
Commission. ISBN 92-827-4970-3.
Davies AJ, Ball SJ {1993) The biology of fish coccidia. Adv
Parasitol 32: 293-366.
5. Phylum Alveolata
Dykova I, Lom J (1981) Fish coccidia: critical notes on life cycles.
classification and pathogenicity. J Fish Dis 4: 487-505.
Levine ND, Ivens V (1990) The coccidian parasites of rodents.
Boca Raton. FL. USA: CRC Press. ISBN 0-8493-4898-6.
Oliveira UC, Fraga JS, Licois D, Pakandl M, Gruber A (2011)
Development of molecular assays for the identrfication of
11 Eimeria species in the domestic rabbit (Oryctolagus co
:Q
cunicufus). Vet Parasitol 176: 275-280. ·;::
Q)
Pakandl M (1990) Some remarks on the prevalence and species E
composition of hare coccidia. Folia Parasitol 37: 35-42.
i.iJ
Pakandl M (2009) Coccidia of rabbit: a review. Folia Parasitol
56: 153-166.
Pellerdy LP (1974) Coccldia and coccidiosis. 2nd ed. Berlin.
Germany: Paray. ISBN 3-489-73317 -7.
Genus /sospora
Some time ago it was shown that lsospora species infecting
mammals and birds are not closely related, as indicated
by morphological, biological and genetic differences.
Therefore, it was proposed to separate the previously
uniform genus lsospora into the genera Isospora
infecting birds and Cystoisospora infecting mammals.
Based on genetic features the genus Cystoisospora was
classified with the cyst-forming coccidia in the family
Sarcocystidae. In spite of some taxonomic uncertainties
we apply this concept in this book, but mention previous
genus names as synonyms.
■ lsospora and Eimeria species in wild or
captive birds
Disease: Visceral coccidioses in birds.
Agents and diseases. Many Isospora and Eimeria
species have been identified as parasites of wild or
captive birds and reptiles. Here, only some species of
birds are mentioned as agents of visceral coccidiosis.
• lsospora serini. This species causes visceral
coccidiosis (VC) predominantly in passerine birds;
canaries, other finches and some exotic bird species
are predominantly affected. After ingestion of sporulated
oocysts, five successive merogonies have been observed
Q)
in mononuclear phagocytes, followed by two further C
·c3
merogonies and gamogony in intestinal epithelial cells. '6
The prepatency period lasts 9-10 days. Presumably, there Q)
2
are further continuous extraintestinal proliferation steps
as oocysts can be shed by infected canaries for >200 days
cco
C
after experimental infection. ·;::
Q)
j
Mainly fledglings are affected by the disease, whereas .S
adult birds may be latent carriers. Pathological alterations, >,
CJ)
corresponding with the long lasting extraintestinal 0
0
proliferation, include multifocal inflammation and ·u5
necrosis in spleen, liver and other organs associated with ro
ro
hepato- and splenomegaly. The enlarged dark organs CL
 Part II. Parasites and parasitoses: protozoa
may be visible through the skin, leading to the name
'black spot' disease. The animals suffer from diarrhoea,
emaciation, often resulting in death. Toltrazuril can
be used to treat the infection. If treated in time, the
therapy may temporarily improve the clinical condition
but cannot eradicate the infection in an aviary. Control
requires strict hygiene measures. It is recommended to
stop breeding for a year to allow immunity to develop
in the birds.
• Eimeria species. Eimeria ssp. are also known
as causative agents of VC, for example E. reichenowi
and E. gruis in cranes. In cranes Eimeria spp. stages
are found in the digestive tract, in lymphocytes and
many extraintestinal tissues (liver, spleen, lung, muscle,
etc.). Oocysts are not only formed in the intestine, but
remarkably also in the respiratory tract.
.. Selected references r --�-�-
i'
I Berto BP, Flausino W, McIntosh D, Telxeira-Filho WL, Lopes
CW (2011) Coccidia of New World passerine birds (Aves:
'.
L
Passeriformes): a review of Eimeria Schneider, 1815 and
lsospora Schneider, 1881 (Apicomplexa: Eimeriidae). Syst
Parasitol 80: 159-204.
Hafeez MA, Stasiak I, Delnatte P, El-Sherry S, Smith DA,
Barta JR (2014) Description of 2 new lsospora species
causing visceral coccidiosis in captive superb glossy starlings,
Lamprotornis superbus (Aves: Sturmidae). Parasitol Res
113: 3287-3297.
Novllla MN, Carpenter JW (2004) Pathology and pathogenesis
of visceral coccidiosis in cranes. Avian Pathol 35: 275-280.
Family Sarcocystidae
Sarx, gen. sarcos (G): meat muscle; kystis (G): bladder.
The family Sarcocystid.ae includes the genera
Cystoisospora, Sarcocystis, Toxoplasma, Hammondia,
Neospora and Besnoitia. Toxoplasma and Sarcocystis, as
wonotic agents, and Neospora, as an agent of abortion
in cattle, are of particular interest. The species of this
family are h.eteroxenous but monoxenous transmission
is also possible. The development i.n final hosts consists
of merogonies (with the exception of Sarcocystis spp.,
► p. 116) and ga.mogony in the intestine whereas in
intermediate hosts only asexual proliferation occurs in
various extra.intestinal tissues.
Genus Cystoisospora
Cystoisospora (syn. Jsospora) suis
Kytos (G): bladder; iso- (G): prefix: equal; sporos (G):
semen, germ.
lo�;as:��ystois�;porosis (c�idio;i�) in p;gs. --,
l--�- - - - --� - - _: -� - --------...
Cystoisospora suis is the only species of the genus
Cystoisospora infecting pigs and a common and
important cause of clinical coccidiosis in piglets. The
sporulated oocysts of this species contain 2 sporocysts
with 4 sporozoites each (Jsospora-type). Older pigs are
often infected with several Eimeria species of which the
following are most common: Eimeria scabra, E.
perminuta, E. spinosa (with a rough oocyst surface) and
E. debliecki, E. neodebliecki, E. porci, E. suis (with a
smooth oocyst surface). Apart from the surface structure,
other features of the unsporulated and sporulated
oocysts allow a species diagnosis. Although intestinal
infections of pigs with Eimeria spp. are quite frequent,
cases of disease with diarrhoea are rare.
Summary
• Agent, life cycle and occurrence. Cystoisospora suis
la an Important agent 'J! lr.testlnal coccldlosis in piglets,
which beoome Infected upon ingestion of sporulated
oocysts. The endogenous cycle is short with a patency
of 4-7 days. Sporulated oocysts contain two sporocysts
with four sporozoltes each. The parasite Is common
worldwide: regionally a high percentage of litters may
be Infected.
• Cllnloal llgnL They occur almost exclusively in 5-15
day old IUCkllng piglet, with catanhallc to necrotic
tntlrltl1, high morbidity, and usually low mortality.
• DlllflNII. Cop1"0100plc detection of oocysts, and
necropey findings.
• Therapy, oontrol. Tr9atment of diseased piglets Is often
untUOCIUful. Metaphylactlo treatment of 3-6 days old
plglett with toltruurU (20 mg/kg b.w., p.o.). Hygiene
ffllllUl'II n Important.
Agent. Cystoisospora suis is the only relevant species
of the genus inhabiting pigs. As mentioned above,
sporulated oocysts are of the lsospora type; they are
spheroid, colourless with a smooth surface and measure
21xl8 µm.
Life cycle. After ingestion of sporulated oocysts, several
types of meront generations develop in enterocytes of
the jejunum and ileum, occasionally also in the colon.
After gamogony and a prepatent period of 5-7 days,
oocysts are excreted during a short patency of 4-6, rarely
up to 16, days. Extraintestinal stages have been found
in lymph nodes, liver and spleen, but their importance
is not known.

Occurrence and epidemiology. C. su,s is a
cosmopolitan parasite. It is found frequently in piglet
rearing farms. regardless of the type of husbandry
( in Central Europe high percentages of litters may be
infected regionally). The prevalence of oocyst excretion
is strong!}' age dependent. Typically it increases in piglets
up to an age of 2-3 weeks and declines in the course
of the following weeks to very low le,·els. In contrast.
older pigs shed Eimeria oocysts in variable frequencies
and intensities. Concordant reports from DE and the
USA hold C. suis responsible for 20-30% of diarrhoea
in suckling piglets.
Oocyst.s of C. s11is sporuJate at 25 °C within 12-18 h. These
oocysts are less resistant than previously suggested, and
particularly sensitive to higher temperatures ( �30 °C) In
combination with low humidity. Oocysts surviving in
insufficiently sanitised farrowing pens are probably the
main source of infection for piglets. Sows, also those in
piglet-producing farms at risk, do not generally excrete
large numbers of C. suis oocysts. But only a few oocysts
are normally necessary for the initial infection of a litter
and, after a few days, a considerable oocyst excretion and
accumulation in the environment may result.
Immunology. It is unclear whether the increased
resistance of older piglets to C. suis infection is based
on adaptive immunity or, rather, on age-related
mechanisms. Data published so far are conflicting,
but some cellular and molecular factors potentially
involved in early responses against C. suis have been
identified recently. Superinfections of sows with C. suis
before farrowing leads to a milder course of disease in
nursing piglets, and these protective effects correlate
with increased levels of specific antibodies in colostnun
and milk.
Pathogenesis and clinical signs. C. suis causes
catarrhalic up to necrotising enteritis, associated with
atrophy and fusion of intestinal villi. Predominantly 5-15
day old piglets are affected by disease, independent of
the season. Infections of older piglets usually remain
asymptomatic, even after ingestion of large numbers
of oocysts. Diseased piglets excrete semi-fluid and
later on liquid, malodorous, yellowish, sometimes grey
faeces without blood. Diarrhoea persists for 5-7 days.
Piglets are apathetic but continue to suck milk; weaning
weights may be significantly reduced. Morbidity is high,
mortality usually low. Concurrent bacterial or viral
infections may worsen the pathogenic implications and
lead to higher mortality.
Diagnosis. Case history of diarrhoea in 5-15 days
old piglets and coproscopic detection of C. suis oocysts
allowing a diagnosis (because of the high fat content of
faeces salt-sugar flotation ( ► p. 116) is recommended;
oocysts show blue autofluorescence under UV light).
Faecal samples should be taken from three to five
animals per litter 2-3 days after the beginning of
diarrhoea. Necropsy (necrotising enteritis of jejunum
5. Phylum Alveolata
and ileum) and the detection of small meronts and
pairs of merozoites in mucosa! impression smears
(Giemsa staining) or H&E stained thin sections confirm
the diagnosis. Differential diagnosis should consider
bacterial and viral infections.
Therapy and control. A single appl.ication of
toltrazuril (20 mg/kg b.w., p.o.) is highly effective against
C. suis in piglets if the disease has not adva.nced too
much. Litters should. therefore, be treated immediately
after the first appearance of diarrhoea. In stocks at risk,
a single metaphylaclic treatment of piglets at the age
of 3-6 days is recommended. This treatment usually
prevents deaths and reduces losses. Hygiene measures
are of particular importance: deaning of farrowing pens
with a steam jet cleaner; chemical disinfection; drying
of the pen ; and prevention of oocyst introduction into
stables. However, outbreaks of cystoisosporosis may
occur even in well-managed farms.
, Selected references
Koudela B, Kucerova S (1999) Role of acquired immunity and
natural age resistance in the course of Cystoisospora suis
coccidiosis in nursing piglets. Vet Parasitol 82: 93-99.
Mengel H, Kruger M, Kruger MU, Westphal B, Swidsinski
A, Schwarz S, Mundt HC, Dittmar K, Oaugschles A
(2012) Necrotic enteritis due to simultaneous infection with
Cystoisospora suis and clostridia in newborn piglets and its
prevention by earty treatment with toltrazl.Jfil. Parasitol Res
110: 1347-1355.
Mundt HC, Mundt-W0stenberg S, Oaugschies A, Joachim A
(2007) Efficacy of various anticoccidials against experimental
porcine neonatal isosporosis. Parasitol Res 100: 401-411.
Schwarz L, Worllczek HL, Winkler M, Joachim A (2014)
Superinlections of sows with Cystoisospora suis ante partum
leads to a milder course of cystoisosporosis in suckling
piglets. Vet Parasitol 204: 158-168.
Skampardonis V, Sotiraki S, Kostoulas P, Leontides L (2012)
Factors associated with the occurrence and level of /sospora
suis oocysts excretion in nursing piglets of Greek farrow-to­
finish 11erds. BMC Vet Res 8: 228.
Sotlraki S, Roepstorff A, Nielsen JP, Maddox-Hyttel C,
Enoe C, Boes J, Murrell KD, Thamsborg SM (2008)
Population-dynamics and intra-litter transmission patterns of
lsospora suis in suckling piglets under on-farm conditions.
Parasitology 135: 395-405.
Straberg E, Oaugschies A (2007) Control of piglet coccidiosis
by chemical disinfection with a cresol-based product
(Neopredisan 135-1). Parasitol Res 101: 599-604.
Wieler LH, llieff A, Herbst W, Bauer C, Vieler E, Bauerfeind R,
Failing K, Klos H, Wengert D, Baljer G, Zahner H (2001)
Prevalence of enteropathogens in suckling and weaned
piglets with diarrhoea in southern Gennany. J Vet Med 8
Infect Dis Vet Public Health 48: 151-159.
Worliczek HL, Buggelsheim M, Saalmuller A, Joachim
A (2007) Porcine isosporosis: infection dynamics.
patl1ophysiology and immunology of experimental infections.
Wien Klin Wochenschr 119: 33-39.
 Part II. Parasites and parasitoses: protozoa
Cystoisospora species in carnivores
I Disease: Cystoisosporosls in carnivores.
• Menta, Several Cystolsospora species (syn. /sospora)
are fntestlnal parasites of dogs and cats. These species
develop In a direct cycle or, facultatlvely, in an Indirect
cyc)e Involving paratenlc hosts in which tissue stages
1dormozoltes) develop rn extralntestinal organs. Oocysta
aporulate lnithe environment, forming two sporocyata
With four aporozoltea each.
Occurrence and cllnloal algne. :rhe parultea are
common worldwide and usually cauae unapparent
loteatlnal infection•: catarrhallo enteritis occura almost
excluaJvely In young dogs and cata.
• Diagnosis and therapy. Coproacopic detection of
unaporutatect oocyata. Therapy of dogs and cats with
toltrazurll.
Agents. Dogs are hosts of four and cats of two
Cystoisospora species, all having been regarded as host
specific ( ► Table 5.5; ► Figure 16.17. p. 550). However,
recent studies revealed that Cystoisospora isolates from
dogs and raccoon dogs in Japan are genetically identical.
There are no Eimeria species infecting dogs and cats.
Eimeria oocysts may occasionally be found in faeces
of these animals due to coprophagy with ingestion of
oocysts from other hosts.
Life cycle. Cystoisospora species of dogs and cats may
develop in a direct cycle and in a facultative indirect
cycle ( ► Table 5.5). In cases of direct development,
infection occuis by ingestion of sporulated oocysts.
The subsequent intestinal development resembles that
Table 5.5. Cystolsospora species of dogs and cats (oocysts ► Figure 16.17, p. 550).
- - -
I
11
°-GI
c.� dlltal enwl illld'W,
ca«un;llminlp,ap,11
c.ohlt»na' -- i!Mlli18, CIIICl.m �pig.�
C. burrowll
- 0111 �.011
dlllalernalirUllnt, IOd91la.blM>
..
CMQ.ln,00Dt
I ,i.rnMPia
c.,.,.
cat
I!I C.rlvolta
lrnll1Ulli19;.
lmlll11f811i111,caaa,n.
OOlon; ..
'PathOgenaoty IOI· young animals;..-.::. rnooerate. +"'low
2 A SIITldaf species ,s C. t"lflOnVO/la toocysts 1 1 • 13 IM11' wnct, de"leiops preoomnanlly ., eels ol tne lalT1ina pmpna of the postenor half of
the small 1111esune.
of Eimeria spp. though the intracellular multiplication
occurs by endodyogeny or endopolygeny (see
Toxoplasma). The prepatent periods and patencies are
listed in ► Table 5.5.
The facultative indirect cycle includes paratenic hosts
( ► Table 5.5). After ingestion of sporulated oocysts
by paratenic hosts, the sporozoites infect cells of the
Peyer's patches in the intestine or the extraintestinal
tissues, such as lymph nodes, liver, spleen, lungs, and
skeletal muscles, where they persist intracellularly in a
parasitophorous vacuole without dividing. These stages
are called dormozoites (dormire [L]: sleep) or monozoic
tissue cysts (as they contain a single infectious stage).
Dormozoites may remain infectious for at least 2 years
and continue their development only after being ingested
by a definitive host as prey or undercooked meat. The
subsequent development is similar to that after infection
by sporulated oocysts, although the prepatency may
be shortened. Dormozoites are not infectious for other
paratenic hosts (compare with Toxoplasma).
Occurrence and epidemiology. Cystoisospora
species are distributed globally. r n a recent study
including nine European countries an average of 9.7%
of owned cats of various age groups (n=1519) were
shedding Cystoisospora oocysts. In a stray cat population
(n= 162) in Portugal 14% excreted oocysts of C.felis and
46% of C. rivolta. Young dogs are frequent excretors
of Cystoisospora oocysts ( 12-23% in Central Europe)
whereas older dogs (>6 months) are more rarely (1-
6%) infected. Some studies have revealed Cystoisospora
oocyst shedding in >90% of whelps.
The major infection source for dogs and cats are
sporulated oocysts which can survive for months in moist
conditions. Unsanitary environments and crowding of
I
rodlratr,Qa,tlll, 30-32 8-10112·28 ++
..,..,,plg.tulllo,
Cllfflll. CII
2'11120 &'12·19 ♦
2h18 8-914-12
♦
4 43 1&-8113-30
: 5
llldlns. cal1l8, nap, ♦
2 S-7/13-30
5
QWT&,rabbil +
1 1123
I

animals (e.g. in kennels or pet shops) promote oocyst
transmission. A second infection source is the ingestion
of fresh meat or entrails.
Clinical signs and immunology. Weak to moderate
infections are generally asymptomatic, also in young
dogs. Heavy infections, especially with C. canis, cause
clinical disease in whelps, particularly at an age of 3-4
weeks, with diarrhoea, vomiting, anorexia, apathy,
impaired growth, sometimes fever, and watery (rarely
bloody) faeces. Diarrhoea in C. canis infected dogs starts
2-3 days before the onset of oocyst excretion. Animals
usually recover within I week; deaths are very rare. C.
rivolta and C. felis show a weak pathogenicity in cats after
experimental infections. Older cats are hardly affected
by Cystoisospora species. Primary infections induce
immunity to homologous challenges, characterised by
the absence of oocyst excretion.
Diagnosis. Demonstration of oocysts in faeces
by flotation techniques. Cystoisospora oocysts are
unsporulated when released in fresh faeces, but can
sporulate quickly at favourable temperatures. They are
ovoid or spherical in shape, colourless with smooth
surfaces without micropyle. In dogs, only C. canis
oocysts can be differentiated by their large size from
oocysts of the other species, which are in routine
diagnostics often grouped together and termed C.
ohioensis-like oocysts. Differential diagnosis has to
consider the smaller oocysts of Hammondia heydorni
(IO-l 5x9- l 3 µm) and Neospora caninum (10-I3x l 0-11
µm) as well as stages of Sarcocystls spp. (the latter are
shed in a sporulated state) ( ► Figure 16.17, p. 550). In
cat faeces, the large oocysts of I. felis can be differentiated
by their size from other oocysts/sporocysts.
Treatment and control. The drug of choice against
Cystoisospora in dogs is toltrazuril (9 mg/kg b.w., p.o.).
In cases of particular risk (e.g. kennels), metaphylactic
treatment with toltrazuril (dogs: single doses at weeks
of age 3, 5 and 7) is recommended. In cats, a single
dose treatment with 18 mg/kg b.w. of toltrazuril reduces
oocyst excretion by 97-100%. Control measures arc
good hygiene, protection from rodents and no feeding
of uncooked meat or entrails.
Selected references
Barutzki D, Schaper R (2011) Results of parosltologlcal
examinations of faecal samples of cats and dogs in Germany
between 2003 and 2010. Parasltol Res 109: S45-S60.
Beugnet F, Bourdeau P, Chalvet-Monfray K, Cozmo V,
Farkas R, Guillot J, et al. (2014) Parasites of domestic
owned cals In Europe: co-lnfestallons and risk factors. Paroslt
Vectors 7: 291.
5. Phylum Alveolata
Buel IE, Prosl H, Mundt HG, Tichy AC, Joachim A (2006)
Canine isosporosis - epidemiology of field and experimental
infections. J Vet Med Series B 53: 482-487.
Lappin MR (2010) Update on the diagnosis and management of
lsospora spp. infections in dogs and cats. Top Comp Anim
Med 25: 133-135.
Litster AL, Nichols J, Hall K, Camp J, Mohamed S (2014) ro
:g
Use of ponazuril paste to treat coccidiosis in shelter-housed ·;::
cats and dogs. Vet Parasitol 202: 319-325. E
uJ
Mitchell SM, Zajac AM, Charles S, Duncan RB, Lindsay DS
(2007) Cystoisospora canis Nemeseri, 1959 (syn. /sospora
canis) infections in dogs: clinical signs. pathogenesis, and
reproducible clinical disease in beagle dogs fed oocysts. J
Parasitol 93: 345-352.
Waap H, Gomes J, Nunes T (2014) Parasite communities in
stray cat populations from Lisbon, Portugal. J Helminthol
88: 389-395.
Genus Toxoplasma
Toxoplasma gondii
Disease: Toxoplasmosls. II
Toxo11 (G): bow; plasma {G): organic entity, body; gundi:
African rodent in which the parasite was detected,
Morocco 1908.
Summary
• Agent. Toxoplasma gondll, the only speclea of the
genus, ls a cyst-forming coccidial parasite of worldwlde
distribution, with a facultatlve heteroxenous llfecycte.
Final hosts are the domestic cat and other fellda.
Numerous species of warm-blooded vertebrate apectee
are susceptible, and many of them can serve u natural
Intermediate hoatl carrying tluue cysts. Endogenous
development la llmlted to nucleated cells. Humana are
frequently Infected u aben'ant hoata.
• Development In the definitive hoat. Cata acqulr9 the
Infection by oral lngeatlon of bradyzoltll (In tlaaue cysts
In lnt.-rnedlate hoata) or by aporozoltea On aporulated
oocyata). lnftctJon with brldyzoltN la followed by an
tnteroeplthtllal phue with merogonlee, gamogony
and oocyat formation. Excretion of unaporulated
oocyata In the fHOII occura after a pi.patency of
3-10 daya. Staid• that. an txtralntatlnal eprud
and p,ollfntton with formation of t111ue cyata may
occur u In Intermediate hoeta (111 below). Infection
with 1porulated oocyata 11 followed by extralnteatlnal,
uexual tachyzoltt prollftratlon and eubuquent
bl'ldyzoltt formation In cyate. Some extralntutlnal
pnalte atag• may Ntum to tht lnteatlne and conclude
the development by mtrogonl11 and gamogony and
oocyat formation. After Infection with aporozoltes,
prepattncy 11 extended to 18-38 days. Patency lasts
few ctaya up to 3 Wllkl.
'f
Part II. Parasites and parasitoses: protozoa

between strains happens under natural conditions in

cats in the course of sexual reproduction and may alter
• ve o men n • env ronmen nsp<>ru a
the virulence.
ooc a n ve os o e environm ent
I
Sporu a o con n os ur
rocys In the life cycle of the parasite there are several infectious
zoltes eac h and ma survive In moist soll for stages that are relevant for parasite transmission
( ► Figure 5.10):
g
r by • Oocysts. Oocysts, released by final hosts are round
I nal (► Figure 5.10), 10-12 µm in size, colourless, without
yog Idly micropyle. Sporulated oocysts contain two sporocysts
rollfwatlng �ea). The n11 with four sporozoites each. Sporulated oocysts are
associated with etage co o ea, I.e. infectious for final and intermediate hosts.
dMdlrig zoltte In n
aaues. 0yste with brad ozo a
• Tachyzoites. Tachyzoites (endozoites) are slightly
,pee
llnlcal bent, crescent-shaped cells (4-7x2-4 µm) with cellular
ly In young or structures shown in ► Figure 5.1, p. 79. They are
ta may show generated within nucleated host cells in a parasitophorous
eum lmmou, vacuole by rapid endodyogeny, containing up to 16-32
, nep , 1, and tachyzoites. Tachyzoites are covered with stadium­
, goata, ploa, ti w.11 •m bwnanl, specific, highly immunogenic surface antigens (SAG
tranlplaoental tranlmllllon of the paraltt (ueually after and SAG-related antigens) which play a role in the
1to attachment to host cells during the infection process
(► p. 23). These stages possess a predominantly aerobic

....••
metabolism and are pathogenic due to their rapid
proliferation and the associated destruction of host cells.
oril)i They are infectious for other nucleated cells in various
tissues and may rarely penetrate mucous membranes of
the upper intestinal tract after ingestion by a host thus
inducing an infection.

• • Bradyzoites. Bradyzoites (cystozoites) are trans­

formed from tachyzoites. They modify the membrane
of the parasitophorous vacuole to a cyst wall and change
boxel their metabolism. For instance, they lack enzymes of
flOift",:,fgltll,lte the citric acid cycle and of the respiratory chain, and
roclelMlllrwquhd.
their antigenic rnake-up (surface and other antigens)
vmrwtoprevem
differs markedly from that of tachyzoites. Brndyzoites
parultlc multiply relatively slowly by cndodyogcny within the
nUIUllly lntroccllulnrly growing cyst. Initially, cysts arc small

-••i•-----"� �--
nflotton during (-5 �1111) whereas older cysts may reach large sizes (in
prllll'III I Nk mu cle cell > 100 �1m In length), containing hundreds
dlmlgl to lhe
..
or thousand of bradyzoites which differ only slightly

,,.. ..
� In size and structure from tachywhes ( ► Figure 5.11 ).
ffllnllf,OCIAlr Cyst may be formed in many visceral organs, but they
are most prevalent in musculature and neural tissues;
--llffl-lllll)'NVIIIII), fflDIIIV bV
they can persist In a host for years without doing any
.....,,...,..., whlat'I ,._, eecalata tD
, harm. After ingestion of tissue cysts by a definitive or
intermediate host the bradyzoltes are released which
withstand the acid environment of the stomach and
Agent. Toxopltmna gondii is currently the onl)1 species induce an infection.
of the genus. h shows a clonal population structure with
different genotypes worldwide. Three clonal strains (type Triggers responsible for the conversion of tachyzoites
1-111) dominate in Europe, North America, Africa and into bradrzoites and vice versa (stage conversion)
Asia. Strains in South America are more differentiated. are only partially understood. Type ll and Ill strains
Though genetic variations between the strains are of T. gondii tend to more readily form cysts than do
generaJly small ( ~ l %), they differ in growth rates, type l strains. Particular organs/host cell types (brain
virulence in mice (pronounced virulence only in type !neurons, astrocytesl, skeletal muscle, eye, heart) seem
I) and the tendency to form tissue cysts. Cross-breeding to be especially appropriate for cyst formation, but
 5. Phylum Alveolata

Cat as definitive host

co
:Q
·c
(I)
E
i.D
Infection of cat with
oocysts or cysts

Development In cat Intestine

•�action with
Infection

R
with cysts _ � sporulated
In meat �- · od'cysts

Bradyzoltes
in cyst ,
Y/1.

,A Dlntermedl�te
),
evelopm.,ent in ,:t$J Sporozoite
• hos
j ·.
\_.., j't -�,,
a,,__ ·· · Tachyzoites
�
Tacnyzote

Figure 5.10. Life cycle of Toxoplasma gond/1 (Graphics: IPZ, S. Ehrat, modified by S. Amrein).

conversion can also be induced in vitro in a variety of

other cell types. Conversion to the bradyzoite stage in
vitro can be best provoked by various forms ofexogenous
stress (acidic or .ilkaline pH, heat and others). Factors
involved i11 vivo may be those of immune responses,
particularly I FN-y release by N K cells or Th I cells,
resulting, e.g. in NO generation and tryptophan starving
of the intracellular parasites (see immunology below).
Q)
C

The switch to anaerobic metabolism in bradyzoites may

·13

be interpreted as an evasion strategy. The conversion

'5
Q)

of the bradyzoite to the tachyzoite stage, as seems to

�
c
occur continuously in the course oflatent toxoplasmosis,
co

can be easily induced in vitro by withdrawal of stress

C
·;::
Q)

factors. In vivo, extensive reversion is the central event in

reactivation oflatent T. gondii infections in humans who
�
Figure 5.11. Cysts in the CNS of (a) Toxoplasma gondii (thin .£

suffer immunosuppression (see below) and may reflect

wall, 0 up to 100 µm) and (b) Neospora canlnum (thick wall, 0 >.

the relaxation of immune pressure in such patients.

Ol
30-100 µm (Photos: J.P. Dubey). 0
0
.-t=
Cl)
�
co
Cl..
 Part II. Parasites and parasitoses: protozoa
Life cycle. The complex life cycle of T. gondii( ► Figure
5.10) includes phases in definitive and intermediate hosts
(endogenous development) and in the environment
(exogenous development). Endogenous development
can take place in all nucleated cells(i.e. in birds also in
erythrocytes).
• Development in definitive hosts. The domestic
cat is the most important definitive host of T. gondii.
Wild felids are epidemiologically negligible in Europe,
but of significance e.g. in North America. Cats may
acquire the infection by ingestion of intermediate host
tissue containing cysts with bradyzoites or tachyzoites
or by sporozoites in sporulated oocysts. Nearly all(non­
immune) cats shed oocysts after ingesting tissue cysts,
whereas the proportion is much lower after ingestion
of tachyzoites or sporozoites. The duration of the
prepatency period depends on the infectious stage
(see below) and is short (3-10 days) after ingestion of
bradyzoites, and longer(18 days or more) after infection
with tachyzoites or sporozoites.
Infection by bradyzoites. After ingestion of tissue
cysts, the cyst wall is dissolved and the bradyzoites
are released. They infect enterocytes in the small
intestine and reproduce asexually in several
generations using various modes of multiplication
(endodyogeny, endopolygeny, merogony ► Glossary,
p. 620). Subsequently, the sexual cycle takes place
with gamogony and oocyst formation. After a
prepatency of 3-10 days oocysts are excreted into
the environment. Besides the development in the
intestine, parasites may spread to other tissues,
where they may proliferate as tachyzoites, convert
to bradyzoites and form tissue cysts.
Infection by sporozoites and tachyzoites. Sporo­
wites invade the intestinal wall, settle in cells of the
lamina propria, divide by endopolygeny, transform
to tachyzoites; these are released by rupture of the
host cell and spread throughout the body via the
blood. The majority of extraintestinal stages probably
convert to bradywites, as in intermediate host.s, and
multiply in tissue cysts. Prepatency after Infection
with sporowites may last I 8-36 days, but only a small
fraction of cats infected by this mode will e)(crete
oocysts. Infection with tachyzoites see below.
(])
• Development in the environment. Oocysts
·o
C
:a excreted in the faeces of cats and other felids(see below)
(])
sporulate within 1-5 days at suitable temperatures(> 10-
�
2:- 30 °C) and with sufficient moisture.
ro
C
·;:: • Development in intermediate and accidental
hosts. ► Figure 5.10. Numerous species of warm­
C blooded vertebrates, including birds, may serve as
>,
CJ)
natural intermediate hosts. Humans are also susceptible
0 and are classified as accidental hosts ( ► Glossary, p.
0
·u5 620). Both sporozoites and bradywites are infectious
ro
.... for these hosts.
ro
CL
After ingestion of sporulated oocysts or tissue cysts,
the released sporozoites or bradyzoites penetrate into
the intestinal wall and infect cells. In the host cell they
induce the formation of a parasitophorous vacuole;
they transform into tachyzoites and proliferate by
endodyogeny. Tachyzoites released from host cells
spread lympho-haematogenously to various organs,
including the CNS. They continue to proliferate as
tachyzoites until stage conversion to bradyzoites and
cyst formation takes place (see above).
Modes of infection. In addition to the infection modes
described above, some others should also be considered.
Cats as well as other hosts may be occasionally infected
by tachyzoites, for instance after preying on intermediate
hosts in which tachyzoite multiplication is actively
proceeding; humans have been infected with tachyzoites
in goat milk. Tachyzoites probably enter the host via the
mucosa of the upper intestinal tract. Prenatal infections
after transplacental transmission are known in a variety
of intermediate host species(sheep, goats, pigs, rodents),
as well as in humans and in cats. Prenatal infections
usually take place after primary infection of female
hosts shortly before conception or during pregnancy.
Occurrence and epidemiology. T. gondii is a
cosmopolitan zoonotic parasite infecting not only many
species of vertebrate animals, but also a considerable
part of the human population( ► zoonotic importance,
p. I 07). Important factors in the epidemiology of
toxoplasmosis are the excretion patterns of oocysts
by cats, the distribution and survival of oocysts in
the environment, the infection of a broad spectrum
of intermediate hosts and the long persistence of
bradyzoites in some of them, the modes of transmission
to final and intermediate hosts and the immune status
of the hosts.
• Cats and oocyst shedding. It is generally
estimated that less than I% of the entire cat population
In any geographic region Is likely to shed Toxoplasma
oocysts. Of 24, I 06 cats from Germany and other
European countries examined In 2004-2006, only
0.11% were shedding 'foxoplasma oocysts (confirmed
by DNA analysis). Such low figures have to be related
to the large cat populations (estimates: ~40 million in
Europe, ~80-90 million in USA) and the high numbers
of oocysts shed by a single cat during its life (up to
810 million). In a French study the number of oocysts
contaminating the environment was calculated at ~ 30 to
3,350/m 2 • In Poland, 18% of 10 I soil samples collected
from sandboxes, playgrounds, parks, etc., contained
Toxoplasma oocysts (confirmed by DNA analysis).
• Oocyst survival. Regarding the risk of transmission
to other hosts(including humans), it has to be considered
that Toxoplasma oocysts may survive for long periods
in the environment (in moist soil for 1-1.5 years, in
cool freshwater for 4.5 years), and that a few sporulated

oocysts are sufficient to i_nfect a non-immune host.
Cats frequently bury their faeces in gardens, thereby
contaminating the soil and earthy plants. Drinking water
may also become contaminated, and wastewater often
contains T. go11dii oocysts.
• Seroprevalence rates in animals (intermediate
and definitive hosts). Given the ubiquitous and wide­
ranged infection risks with Toxoplasma oocyst.s, it is not
surprising that many animal species and large parts of
the human population are infected, as indicated by the
seroprevalence rateJI.
For example, in the 1970s, I 0-50% of sJaughtered pigs
in Central Europe howcd antibodic.5 lo 7: gomlii but
the prevalence in fattening pigs has since decreased,
e.g. in Germany and Au lria lo <0.1%. However, 20%
of sows in small holder farms In Germany were 7:
go11dii seropositive in 2000, and new trends in animal
husbandry may increase the risks again. Thus, J:
go11dii seroprevalcncc in organic free-range pigs in the
Netherlands was 15-fold higher when compared to pigs
from intensive management farms. The scroprevalcnce
In European cattle amounts to approximately 10%
according to most studies. Seroprevalences in small
ruminants arc often quite high, e.g. 48.6% in sheep
and 30.7% in goats in Greece (2012). In a Swiss survey
(2011) seroprevalence rates were 23.3% in pigs, 45.6% in
cattle and 6 J .6% in sheep. Seroprevalences in European
equids (horse, mules, donkeys} were low in Greece
and Sweden (0.5-2%) and higher in Spain (25-30%). T.
gondii infections of poultry are often disregarded, and
prevalences are low in intensive poultry husbandry.
However, in free-ranged flocks 30-50% of chickens and
approximately 20% of turkeys showed antibodies to 'J:
gondii. In Germany 5.7% of ducks and 25.2% of geese
had antibodies against 7: gondii. Wild mammals are also
frequently infected as indicated by high seroprcvalences
(wild boars 15-33%, roe and red deer I 3%, >74% of foxes,
hares 2.6%). The same holds true for marine mammals.
Sea otters, sea lions, walruses and various dolphin species
(prevalence at the Japanese coast I 0%} and orcas have
been shown to be infected. The prevalence of 7'. gondii in
house mice is usually low (I%) but often higher in ruts,
voles, other rodents and in small birds (up to 27%).
Populations of adult cats, especially stray cats in
rural areas can have high anti-'Joxopltmna antibody
prevalences; cats kept strictly indoors are often
seronegalive.
• Seroprevalence in humans and infection
sources.(► p. 107)
• Transmission routes. Cats are infected with
T. gondii by ingestion of meat or other tissues of
intermediate hosts (e.g. mice, birds) containing T. gondii
cysts, resulting after primary infections mostly in patent
infections, or by ingestion of oocysts mostly resulting
5. Phylum Alveolata
in extraintestinal, rarely in patent infections. Primary
infected kittens may excrete> I million oocysts/g faeces
and contaminate the environment with several hu.ndred
million oocysts in the course of patency. Rarely, old
and immune cats may re-shed oocysts at low intensity
without re-infections. The mechanisms and reasons
for such 're-shedding' are unknown (temporary ('O
:g
immunodepression could theoreticalJy be a factor). '-
Q)
Grazing animals acquire lhe infection by ingestion of E
w
sporulated oocysts spread wilh food or drinking water.
Prenat.aJ infections play a role in various host species
and have been demonstrated in sheep. goats, pigs, dogs,
cats and rodents. however, this method of transmission
is negligible in cattle. Transplacental infections in sheep
ecm to be limited to primary infections in the course
of pregnancy whereas goats may abort repeatedly
wll.hout re-lnfcclion. A similar situation is reported
for mice. Transmission of 7: gondii through sexual
intercourse in sheep and goats has been suggested but
the epidemiological significance is unclear.
Immunology. In the course of natural infections.
cats often develop a solid immunity, which is
probably maintained by supcrinfections with cysts
from intermediate hosts. Immunity, in general,
controls efficiently challenge infections and prevents,
in approximately 90% of cats, oocyst excretion after
re-infection. Nevertheless, in some cases renewed
oocyst excretion may occur after months without re­
infection. The cause for these recurrences (re-shedding)
is unknown ( ► risk assessment in cats, p. 107).
Possibly, an impaired cellular immunity could favour
tachyzoite multiplication and dispersion, initiating a new
intestinal phase. However, cats infected with the feline
immunodeficiency virus (FIV} rarely develop clinical
toxoplasmosis with re-shedding of oocysts.
In intermediate hosts 7: gondii usually stimulates a long­
lasting concomitant immunity which does not eliminate
infection but can protect from disease and detrimental
effects. However, there a.re differences between hosts
and the involved 'foxoplasma strains. For example, in
cattle, which are less susceptible to T. gondii than sheep,
the infection is only rarely associated with abortion. In
contrast, in highly susceptible sheep 1: gondii induces
abortions quite frequently, particularly if infected in
early pregnancy. 1: gondii also contributes to abortions
in goats. Furthermore, the parasite may even cause
repeated abortions in chronically infected goats and
sheep. Regarding other hosts, see specialised literature.
T. gondii is amongst the best studied of parasites from an
immunological point of view. The clinical consequences
of 1: gondii infections are determined by innate and
adaptive immune responses of the host. lL-12 and IFN-y
are the key molecules in innate responses to the parasite.
IL-12 synthesis is initiated in a variety of cell types
(neutrophils, dendritic cells, macrophages) by TLRs
Part II. Parasites and parasitoses: protozoa
(Toll like receptors) reacting with PAMPs (pathogen
associated molecular patterns; ► p. 25). One of these
ligands is profilin, a molecule obviously conserved in
parasitic protozoa ( ► also p. 26). IL-12 activates Thl cells
and NK cells to synthesise IFN-y, which in turn initiates
effector cell reactions (macrophages, neutrophils and
others). These reaction chains are essential to control
T. gondii; mice deficient in one or more of these factors
acquire massively increased numbers of cysts or even
die of acute toxoplasmosis.
Adaptive immune responses control the subsequent
phases of toxoplasmosis. Mice deficient in B cells, CD4+
(T helper cells) and cos+ T cells overcome the early
phase of infection but fail to adequately control the
chronic phase of cyst formation, resulting in dramatically
increased numbers of cysts, particularly in the brain, or
deaths. Also, a lack of antibodies in T. gondii infected
mice is, e.g. associated with death 3-4 weeks p.i. and can
be overcome by passive transfer of antibodies.
Effector mechanisms that damage or eliminate T. gondii
are multifaceted. Humoral antibodies may act against
extracellular stages by opsonisation , blocking of cell
invasion and complement-mediated lysis. Meanwhile,
IFN-y released by Thl and other cells may, e.g. enhance
the synthesis of inducible nitric oxide synthase (iNOS),
providing increased levels of NO in several cell types,
where it inhibits the parasite's replication. IFN-y may
also damage the parasites by indirectly enhancing the
degradation of tryptophan in infected cells since T.
gondii is a tryptophan-auxotrophic organism. cos+ cells
may participate in immune elimination of T. gondii by
cytokine release and cytolysis via perforin.
Apart from their protective effects, immunological
reactions to T. gondii contribute substantially to
pathological and clinical consequences of the infection.
This applies to parasite-induced intestinal reactions
(ileitis) as well as, e.g. sometimes to severe pathology
in the CNS and in infected eyes. These pathological
reactions are particul.arly mediated by co4+ T cells. In
a double-edged way, T helper cells are involved in long­
term control of T. gondii and in immunopathological
impacts of the disease by the release of pro-inflammatory
cytokines (e.g. IL-2, IL-12, IL-17). A potent regulator,
providing protection from hyper-inflammatory effects,
seems to be IL-10, another T-cell-derived cytokine.
Thus, T. gondii initiates a complicated network that
regulates the coexistence of parasite and host.
Pathogenesis and clinical signs. The patho­
genesis of toxoplasmosis is characterised by focal
necro ses due to cell damage in the course of parasite
proliferation, associated with adjacent inflammatory
and immunopathological lesions. Such lesions may
develop in many organs. Most of the natural infections
are asymptomatic, both in definitive and other hosts.
Clinical signs are determined by various factors,
including the virulence of the Toxoplasma strain, the
infection dose, the species, age and immune status of the
host, the affected organ(s), and the extent of the lesions.
• Toxoplasmosis in cats. The intestinal infection
is usually unapparent or a self-limiting diarrhoea of a few
days duration with fever, especially in heavily infected
kittens. Although disease caused by extraintestinal
infection is generally rare, it may occur, in particular in
kittens, exhibiting distinct symptoms, such as anorexia,
apathy, pneumonia, fever, diarrhoea, encephalitis,
hepatitis, and myositis. Uveitis is a relatively frequent
sign in kittens. Prenatal infections may cause abortion
or acute disease in the offspring. Occasionally, acute
toxoplasmosis develops after immunosuppressive
treatment and in cases of intercurrent infections
(rickettsiae, viruses) (for FIV infections see immunology
above). Necropsy findings include necrotic foci,
inflammatory reactions and perivascular infiltrations
in various organs (liver, spleen lungs, etc.), ulcerative
enteritis with swelling of mesenteric lymph nodes,
degenerative alterations in the brain, sometimes with
involvement of the spinal cord, the nervus opticus
and the retina (chorioretinitis), chronic interstitional
nephritis, pancreatitis, etc.
• Toxoplasmosis in dogs. Although dogs are
frequently infected with T. go11dii as documented by high
seroprevalences, clinical cases are very rare. Primary
infections in pregnant bitches may cause abortion and
generalised central nervous symptoms in puppies.
Differential diagnosis has to consider neosporosis ( ► p.
110). T. gondii never produces oocysts in the intestine of
dogs, however, oocysts have been exceptionally detected
in dog faeces as contaminants after coprophagy.
• Toxoplasmosis in sheep and goats. Small
ruminants are highly susceptible to T. gondii and are
frequently infected with tissue cysts as indicated by
high seroprevalences (20-100%). Often whole flocks
are infected, living in endemic stability without clinical
signs ( ► Glossary, p. 620). Only lambs/kids may show
transient patterns of acute disease (fever, respiratory
signs, diarrhoea). However, infections of naive, pregnant
sheep or goats may have severe consequences. Infections
in the early phase of pregnancy cause abortions or
death of the fetus with its subsequent resorption or
mummification. Infections during later gestation phases
are followed by abortion, stillbirth or perinatal death
of the new-born. However, after infections during late
gestation infected lambs/kids may be born without
any signs of toxoplasmosis. Chronically infected sheep
and goats may repeatedly abort. Necropsy findings: in
about 50% of T. gondii-induced abortions, characteristic,
whitish necrotic lesions of up to 3 mm in size are
macroscopically detectable in the cotyledons. These
lesions are often interspersed with microscopically
detectable tachyzoites. Histopathology of aborted fetuses
shows multiple necrotic and inflammatory lesions,

perivascular lymphoid inftltrations and, occasionally,
parasites in the CNS and other organs.
• Toxoplasmosis in pigs. Pigs Ingest Infectious
Toxoplasma stages in form of sporulatcd oocysts with
food and earth (outside pen, free-range) or as cysts
with rodents, carcasses or slaughter offal. Housed pigs
in farms with high hygiene standards arc Toxoplamsa­
free or seroprevalences are very low (<I%). In contrast,
prevalences are usually higher in 'animal-friendly'
husbandries or free-range pig farms.
T. go11dii infections in pigs usually remain asymptomatic,
but infected piglets may be affected showing apathy,
anorexia, fever, dyspnoea, cyanosis, atony or paralysis
of the hind limbs. Primary infection in pregnant sows
may cause abortion, stillbirth or weakness of new­
borns. Necropsy findings: desquamantive, interstitial
pneumonia, non-purulent meningo-encephalitis,
necrotic foci in liver and lymphatic organs, multifocal
necrotising myocarditis, and enteritis are lesions
associated with toxoplasmosis in pigs.
• Toxoplasmosis in other animals. Cattle and
horses are susceptible to T. gondii but there are no
reports on clinical cases. Sporadic outbreaks have been
reported in many animal groups, such as rabbits, minks,
marsupials (kangaroos, etc.), New World monkeys in
zoos, poultry, and wild birds.
Diagnosis. Patent infections in cats are diagnosed by
detection of oocysts in faeces by flotation techniques.
Toxoplasma oocysts cannot be morphologically
differentiated from those of Hammondia hammondi.
Various test procedures (ELISA, IFAT and others) are
available to demonstrate specific antibodies in sera
of cats and intermediate hosts. 1\vo serum samples
should be investigated at 2-4 weeks intervals to
determine acute infections. If possible, isotype specific
antibodies (IgM and IgG) should be determined. High
or rising IgM antibody levels or rising IgG antibody
levels and low antibody avidity usually indicate recent
infections. Occurrence of specific antibodies in body
cavities of aborted sheep or goat fetuses as well as in sera
taken from new-borns before colostrum uptake prove
intrauterine T. gondii infections (maternal antibodies
are not transmitted to the fetuses i n ruminants).
Antibodies in fetuses may not be expected before
the middle of pregnancy (when fetuses have become
immunocompetent). Tissue stages (tachyzoites in cells or
bradyzoites in unseptated tissue cysts) may be detected
histologically, by means of immunohistology or DNA
analyses in tissue samples taken post mortem (brain,
muscle, fetal tissue). Highly sensitive magnetic capture
DNA isolation followed by PCR has been developed for
the detection of T. gondii in meat.
5. Phylum Alveolata
• Diagnostic risk assessment in cats. A question
frequently asked in the veterinary practice is whether a
particular cat may represent a risk of infection for the
family or especially for pregnant women. This can be
answered based on the resuIts of the above-mentioned
coproscopic and serological investigations. Por risk
(1j
assessment it is recommended to perform a serological :g
test and subsequently 4 faecal examinations at weekly ·.:::
E
(1)
Intervals. Cats shedding oocysts are hazardous. Animals
not shedding oocysts and showing specific antibodies
w
are most likely immune (exception re-shedding, see
above) and, with a high degree of probability, may not
be a source of infection In future. On the other hand,
cats free of specific antibodies are susceptible; they can
be subjected to preventive measures, e.g. supervision,
indoor maintenance, feeding with safe food (see below).
Therapy. Treatment of domestic carnivores is only
recommended in case of acute systemic toxoplasmosis.
Tissue cysts cannot be eliminated by chemotherapy.
Cats are treated with clindamycin (12.5-25 mg/kg
b.w., p.o. every 12 hours for 2-4 weeks or, alternatively,
with sulfadiazine plus trimethoprim (sometimes
intolerance!). In cases of uveitis, glucocorticoids should
be administered additionally to prevent secondary
luxation of the lens and glaucoma.
Control. Control options are limited. Measures
applicable to cats are described elsewhere ( ► p. 604).
1oxoplasma infections in housed pigs can be reduced
or prevented by keeping cats away from stables and feed
storage facilities. Any carry-over of oocysts by persons,
vehicles, tools must be precluded. Rodent populations
have to be controlled. In some areas such measures
have resulted in a significant reduction of prevalences.
Free-range husbandry increases the infection risk. Sheep
may be protected against T. gondii-induced abortions by
a live vaccine (Ovilis Toxovac•). The vaccine contains
tachyzoites of an in vitro attenuated strain (S48) that
proliferate in sheep but do not transform to brady1wites,
so that the infection becomes extinguished. Vaccination
has to be performed at least 3 weeks before mating.
Zoonotic importance. T. gondii is the most
frequent agent of parasitic zoonoses worldwide. It
infects approximately 1/3 of the human population,
but seropositivity rates between countries vary from
less than 10% to over 90%. In a Swiss study (1995)
comprising 4,300 persons 21% were seropositive in
the age group 1-19 years, and 68% in the group 40-70
years. However, the overall seroprevalence appears to
have decreased in recent decades as indicated by the
prevalences determined in women of child-bearing age:
Switzerland 1996: 39%, 2006: 23%; France 1960: 84%,
2003: 44%; the Netherlands: 1995/96: 35.2%, 2006/07:
18.5%; Norway 1998: 11%, 2015: 9%.
 Part II. Parasites and parasitoses: protozoa
T. gondii infections of immunocompetent persons
are often asymptomatic but in 10-20% of the cases
mild symptoms (low fever, lymphadenopathy) are
observed, which cease within a few weeks. Patients with
impaired immune responses (AIDS patients, patients
with organ transplants), however, may develop severe
disease patterns. In >90% of cases, they are a matter of
reactivation of latent T. gondii infections. The major
clinical consequence is encephalitis. The most serious
complications by T. gondii arise when women acquire a
primary Toxoplasma infection during pregnancy and the
parasites infect the fetus. The implications for the fetus
depend on the stage of pregnancy at infection and vary
from abortion, severe fetopathy to late sequelae in new­
born and adolescents(chorioretinitis, blindness, mental
retardation, hearing disorders, etc.). With reference to
the number of all children born alive, the risk of prenatal
toxoplasmosis in Central Europe amounts to 0.0 l-0.03%.
It should be noted that a prenatal infection of the fetus
is unlikely in women who have serum antibodies to T.
gondii prior to pregnancy.
Humans may become infected with T. gondii by ingestion
of sporulated oocysts, of cysts in animal tissues and by
I. transplacental parasite transmission mentioned above.
The relative importance of infections with oocysts or
with cysts is still unclear. Retrospective analyses of
infections in pregnant women in Europe suggest that
30-63% had been caused by eating undercooked or
c ured, contaminated food.
Infections with oocysts. Humans may be exposed to
sporulated oocysts, e.g. by contaminated vegetables,
by hands polluted with contaminated garden soil or by
unhygienic handling of cat faeces.
Infection with meat and other food products of animal
origin. A major infection source is raw or undercooked
meat of domestic or wild animals containing tissue
cysts. There is agreement that pigs, sheep, goats
and various game (e.g. wild boar) arc cyst carriers,
representing infection sources. For instance, in 2005,
0.38% of 2094 pork samples from retail meat stores in the
USA contained viable stages of 7'. gondll as determined
by bioassays in cats and mice, but samples of beef or
chicken were negative. It is documented that cattle are
(l)
susceptible to T. gondil but they usually eliminate the
·u
C
'6 parasite within 8 weeks p.i., and cysts are only rarely
�
(l)
formed. In contrast, cysts in sheep and goats may persist
c
a,
fur life. Therefore, beef was not regarded as an important
source of human infections. Yet, in a more recent study
C
·c from the Netherlands, based on quantitative detection
(l)
of T. gondii DNA in beef, it.s epidemiological role as
.£ a source of infeci-ion was estimated to be significant.
>- However, there are no data avaiJable on relations between
0)
0 the occurrence of T. gondii DNA and infectious I:
0
·u5 gondii stages. The infection risk associated with the
ctl
a,
consumption of chick.en meat is regarded as low, because
0... Toxoplasma prevalences in commercial chicken farms
are mostly low, and poultry meat is usually eaten well
cooked. There may be a higher risk with meat from
free-range chickens(► p. 105). T. gondii has hitherto
not been found in eggs. Infective T. gondii stages can
be excreted in goat's milk and survive in fresh cheese
produced by cold-enzyme treatment.
When estimating the infection risk not only the
incidence of Toxoplasma stages is to be considered in
meat and other products, but also the eating habits of
the people and the quantities of food products consumed
per capita. To date there are no legal regulations in the
EU with regard to screening slaughtered animals for
T. gondii.
Personal protection measures are particularly important
for seronegative, i.e. susceptible pregnant women, and
immunosuppressed persons. Infections can be prevented
by avoiding raw or undercooked meat or other products
which might contain infective Toxoplasma stages. When
preparing raw meat special hygienic precautions should
be taken (e.g. washing of dishes or plates with hot water,
protection against contamination of hands, eyes, mouth).
T. gondii cysts remain infectious for 3 weeks in cooled
meat; heating (>67 °C for some minutes) and freezing
(-18 °C for 3 or more days) kills bradyzoites. Curing and
salting, according to most investigations, inactivates T.
gondii within a few days. However, short-time smoking
and fresh, raw sausages are risky. Protection against
contamination with oocysts - apart from rules for
handling cats (see above) - may be accomplished by
thorough washing and heating of vegetables and washing
of hands after working in gardens or fields.
, Selected references.
Basso W, Handke M, Sydler T, Borel N, Grimm F, Sidler
X, Deplazes P (2014) Involvement of Toxoplasma gondii
In reproductive disorders In Swiss pig farms. Parasitol Int
64: 157-160,
Bokken GC, Potengen L, Cornellssen JP, Bergwerff AA,
van Knapen F (2015) Bayesian estimation of diagnostic
accuracy or a new bead based antibody detection test to
reveal Toxoplasma gond// Infections in pig populations. Vet
Parasltol 207: 1-6.
Butler NS, Harris TH, Blader IJ (2013) Regulation of
immunogenesls during Plasmodium and Toxoplasma
infections: more parallels than distinction. Trends Parasitol
29: 593-602.
Damriyaaa IM, Bauer C, Edelhofer R, Failing K, Lind P,
Petersen E, Schares G, Tenter AM, Volmer R, Zahner H
(2004) Cross-sectional survey in pig breeding farms in Hesse,
Germany: seroprevalence and risk factors of infections with
Toxoplasma gondii, Sarcocystis spp. and Neospora caninum
in sows. Vet Parasitol 126: 271-286 .

Dubey JP (2010) Toxoplasma gondii infections in dlickens (Galus
domesticus): prevalences, clinical disease, diagnosis and
public health significance. Zoonoses Public Health 57: 60-73.
Dubey JP, Hill DE, Jones JL, Hightower AW, Kirkland E,
Roberts JM, Marcet PL, Lehmann T, Vianna MC, Miska
K, Sreekumar C, Kwok OC, Shen SK, Gamble HR (2005)
Prevalence of viable Toxoplasma gondii in beef, chicken
and pork from retail meat stores in the United States: risk
assessment to consumers. J Parasitol 91: 1082-1093.
Dupont CD, Christian DA, Hunter CA (2012) Immune response
and immunopathology during toxoplasmosis. Semin
lmmunopathot 34: 793-813.
English ED, Adomako-Ankomah Y, Boyle JP (2015)
Secreted effectors in Toxoplasma gondii and related species:
detenninants of host range and pathogenesis? Parasite
lmmunol 37: 127-140.
Fritz HM, Conrad PA (2015) Role of cats In Toxoplasma
transmission and disease. In: Beugnet F, Halos L (eds.)
Parasitoses & Vector Borne Diseases of Cats. Lyon, France:
Merial S.A.S., pp, 351-362. ISBN 978-2-9550805·0-4.
Hehl AB, Basso WU, Llppuner C, Ramakrlshnan C,
Okoniewski M, Walker RA, Grigg ME, Smith NC,
Deplazes P (2015) Asexual expansion of Toxoplasma gondii
merozoites is distinct from tachyzoites and entails expression
of non-overlapping gene families to attach, invade, and
replicate within feline enterocytes. BMC Gonomics 16: 66.
Innes EA, Bartley PM, Buxton D, Katzer F (2009i Ovine
toxoplasmosis. Parasitology 136: 1887 -1894.
Lopes WD, Rodriguez JD, Souza FA, dos Santos T R, dos
Santos RS, Rosanese WM, Lopes WR, Sakamoto CA,
da Costa AJ (2013) Sexual transmission of Toxoplasma
gondii in sheep. Vet Parasitol 195: 47-56.
Maenz M, Schluter D, Liesenfeld 0, Schares G, Gross U,
Pleyer U (2014) Ocular toxoplasmosis, past, present and
new aspects of an old disease. Prog Retin Eye Res 39:
77-106.
Opsteegh M, Kortbeek T M, Havelaar AH, van der Giessen
JW (2015) Intervention strategies to reduce Toxop/asma
gondli disease burden. Clin Infect Dis 60: 101-107.
Opsteegh M, Prickaerts S, Frankena K, Evers EG (2011)
A quantitative microbial risk assessment for meatborne
Toxoplasma gondii infection in The Netherlands. Int J Food
Microbiol 150: 103-114.
Opsteegh M, Langelaar M, Sprong H, den Hartog L, De
Craeye S, Bokken G, Ajzenberg D, Kijlstra A, van
der Giessen J (2010) Direct detection and genotyping of
Toxoplasma gondii in meat samples using magnetic capture
and PCR. Int J Food Microbiol 139: 193-201.
Schares G, Vrhovec MG, Pantchev N, Herrmann DC,
Conraths FJ (2008) Occurrence of Toxoplasma gondii and
Hammondia hammondi oocysts in the faeces of cats from
Germany and other European countries. Vet Parasitol 152:
34-45.
Skariah S, McIntyre MK, Mordue DG (2010) Toxoplasma
gondii: determinants of tachyzoite to bradyzoite conversion.
Parasitol Res 107: 253-260.
Tenter AM, Heckerot AR, Weiss LM (2000) Toxoplasma gondii:
from animals to humans. Int J Parasitol 30: 1217-1258.
5. Phylum Alveolata
Torgerson PR, Masttroiacovo P (2013) The global burden of
congenital toxoplamosis: a systematic review. Bull World
Health Org 91: 501-508.
Torrey EF, Yolken RH (2013) Toxoplasma oocysts as a public
health problem. Trends Parasitol 29: 380-384.
Genus Hammondia
·;:::
E
i.iJ
Datus M. Hammond, protozoologist, USA (1911-1974).
Agents. Hammond/a hammondi is a worldwide parasite
of domestic cats; H. parda/is infects wild felids in Central
America and north-western Mexico. Dogs are hosts
of H. heydorni. There are close relaUonships between
the genera Hammondia, Toxoplasma and Neospora.
Hammond/a spp. form oocysts of the Cystoisospora type.
Life cycle, occurrence and epidemiology.
Hammondia species are obligate heteroxenous parasites.
• H. hammondi. Definitive hosts are domestic cats
which release oocysts in faeces. The oocysts sporulate in
the environment and are ingested by intermediate hosts
(rodents, rabbits, sheep, goats, pigs, roe deer and others).
Sporozoites proliferate by endodyogeny in cells of the
intestinal wall, Peyer's patches and mesenterial lymph
nodes. Merozoites arising from this process disseminate
to various organs and multiply further. Approximately
11 days p.i., the formation of thin-walled, unseptated
cysts starts in skeletal and heart muscles and in the brain.
Cats get infected by ingestion of tissue cysts. Cystozoites
infect the epithelium of the small intestine in which
merogonies and gamogony occur. Unsporulated oocysts
are shed beginning 5-13 days p.i. for 1-4 weeks, but
some cats may excrete oocysts temporarily for 3 months.
Sporulated oocysts are infectious only for intermediate
hosts, not for cats. Unlike T. gondii, H. hammondi
appears not to infect extraintestinal tissues in the cat.
Of 24,106 faecal samples from cats collected in 2004-
2006 in Central Europe 0.09% contained oocysts of
Q)
H. hammondi as determined by coproscopy and DNA C
·5
analysis.
• H. heydorni (syn. Isospora bigemina). Definitive
hosts are dogs and fox species. Infection occurs by co
C
·;:::
ingestion of cysts in tissues of infected intermediate Q)
hosts (ruminants including cervids, camels, horses,
rabbits, guinea pigs and dogs). In epithelial cells of the C
small intestine cystozoites develop to meronts, gamonts >,
CJ)
and finally to oocysts which are shed unsporulated after 0
0
a prepatency of 7-17 days. There are no extraintestinal :t::
(/)
stages in dogs after infection by cysts although dogs
co
develop tissue cysts in muscles and in brain after 0.
Part II. Parasites and parasitoses: protozoa
infection with sporulated oocysts (without oocyst
shedding in faeces). In intermediate hosts, proliferation
occurs by endodyogeny and cyst formation in muscles,
brain and other organs.
Hammondia spp. are distributed worldwide in cats, dogs
and foxes. Oocysts are found in 1- 7.5% of cats and dogs
but cannot be distinguished morphologically from those
of T. gondii and N. caninum, respectively.
Pathogenesis and clinical signs. Hammondia
spp. induce hardly any clinical effects. Occasionally,
diarrhoea and anorexia is observed in puppies infected
with H. heydorni.
Diagnosis. Oocysts of H. heydorni measure
approximately llxl2 µm, those of H. hammondi
l l.4x 10.6 µm. Differentiation from Neospora and
Toxoplasma oocysts, respectively, can be performed by
DNA analysis.
Dubey JP (2009) The evolution of knowledge of cat and dog
coccidia. Parasitology 136: 1469-1475.
Dubey JP, Ferguson DJ (2014) Life cycle of Hammondia
hammondi (Apicomplexa: Sarcocystidae) in the cat. J
Eukaryot Microbiol: doi: 10.1111/jeu.12188.
Monteiro RM, Pena HF, Gennari SM, de Souza SO,
Rlchtzenhain W, Soares RM (2008) Differential diagnosis
of oocysts of Hammondia-like organisms in dogs and cats
by PCR-RFLP analysis of 70 kilodalton heat shock protein
(HSP70) gene. Parasitol Res 103: 235-238.
Schares G, Vrhovec MG, Pantchev N, Herrmann DC,
Conraths FJ (2008) Occurrence of Toxoplasma gondii and
Hammond/a hammondl oocysts In the faeces of cats from
Germany and other European countries. Vet Parasitol 152:
34-45.
Genus Neospora
Disease: Neosporosis in cattle, dogs and other
animals.
Neas (G): young, new; spora (G): germ, semen.
Summary
• Agents. Genus with two species: Neospora can/num
and N. hughesl. Dogs, coyotes and wolves are definitive
hosts of N. can/num. Cattle and many other animal
species, Including carnivores, may act as lntennedlate
hosts. The horse Is an lntennedlate host of N. hughesl,
lta final host Is unknown. N. canlnum Is one of the most
Important causea of abortion In cattle. It also Induces
neuromuscular disease In doge.
• Life cycle. Dogs are Infected with N. canlnum by
Ingestion of cyats In tl11Ues of lntennedlate hosts. The
detalled endogenous development In dogs Is not yet
known. Prapatenc:y lasts 5 days. Sporulatlon of oocysts
needs 1 ·3 days. Sporulated oocysts are Ingested by
lntennedlate hosts In which, after endodyogeny, cysts
develop predominantly In the CNS and muscle cells.
• OccurNnce, epidemiology. N. canlnum Is widespread
worldwide with variable seroprevalences in dogs
and lntennedlate hosts. Vertical transmission by
transplacental Infections (cattle, sheep, goats, wild
ruminants, dogs, rodents), horizontal transmission by
sporulated oocysts and cysts.
• Pathogenesle, cllnlcal elgne. Abortions or stillbirths
can be induced by N. canlnum In pregnant cattle
after primary Infection and after reactivation of latent
Infections; placental retention and fertility disorders a,e
also observed. New-borns a,e mostly asymptomatic or
rarely show weakness and die by encephalomyelitis.
Transplacentally infected dog puppies may suffer
from a polyradlculitls syndrome (ascending paralysis,
amyosthenla and other signs); older whelps and dogs
may develop encephalitis, encephalomyelltls, partly
aaoc:tated with myopathlee•
• Dlagnolll.
- Cattle: Intra vttam dlagnoals by detection of apecific
Mtlboclill and pnalt• (hiltology, lmmunohlltology,
DNA analylN) In brain and musclee of aborted
ftluHI.
- Dog: ooproecoplc demonltnltlon of oocyats (flotation
techniquel); dlffnntlatlon from Harnmondla he-ydom
oocysta by DNA analysee: detection of 1peclflc
antl>odlee end parultN u In lnt.-medlate holts.
• 1hlrlpr. oontrol. CUnwntly no therapeutic meuurN
In cattle. Aborted fetUHI and afterbirth• have to
be NCUnld away from doQ9 and other camtvora
Avaldance of wet. and fodder contamination with
dog ..... TlfltatlvetrNtnWtt of dlNued doga wtth
clindlmycln combined with potentlated IUlfonamldel.
Two species of the genus are known. N. caninum
(first description 1988) causes abortions in cattle
and neuromuscular disorders in dogs. The species
 5. Phylum Alveolata

differs morphologically, biologically and genetically
from the closely related 1: gondii and H. heydorni
(► p. 116). In 1998, N. hughesi was separated from
N. caninum as a distinct species by ultrastructural,
antigenetic and molecular differences. It causes
myeloencephalitis similar to Sarcocystis neurona in
horses in North America.
Neospora caninum
Agent and life cycle. N. caninum produces oocysts
(IO- l 3x I 0-11 µm) of the Isospora type and tachyzoites
and tissue cysts with bradyzoiles. The parasite has a
heteroxenous life cycle, involving dogs and other canids
as definitive hosts and cattle and a wide range of other
animals as natural or potential intermediate hosts.
Alternatively, the parasite can be directly transmitted
( ► Figure 5.12).
• Development in definitive hosts. Dogs (domestic
dogs and Australian dingos). coyotes and wolves have so
far been identified as defmitive hosts of N. caninum. The
role of red foxes (Vulpes vulpes) is unclear (identification
of oocysts found in foxes in Canada by a specific PCR, but
foxes experimentally infected in Europe with tissue cysts
failed to excrete oocysts). Dogs infected with bradyzoites cu
"O
in tissue cysts shed unsporulated oocysts beginning 5 ·c
Q)
days p.i. for 2-3 weeks, in some animals intermittently E
for months. Oocysts sporulate within 1-3 days and form
w
two sporocysts with four sporozoites each. The tenacity
in the environment is not yet known, however, might
correspond with that of Toxoplasma oocysts.
Dogs acquire the infection by oral ingestion of tissue
cysts and by transplacental transmission. probably also
by lactogcnic transmission. After a primary infection
of the bitch transplacental infections of the fetuses may
occur repeatedly in the course of subsequent pregnancies.

Prenatal infection
of puppies

Development in dog Intestine

- - - - - - -�-�ated

•
/ Q)
oocysts ·u
C

'6
Q)
Intermediate hosts
with tissue cysts
cu
C
Prenatal ·;::
Q)

C
>-
0)
0
0
·u5
cu
Figure 5.12. Life cycle of Neospora caninum (Graphics: IPZ, S. Ehrat). 0....
 Part II. Parasites and parasitoses: protozoa
Sources of infection of dogs may be afterbirths of cattle,
as well as tissues of other intermediate hosts ( other
ruminants, rabbits, rodents, etc.). It is not known
whether dogs and other definitive hosts can be infected
under natural conditions by sporulated oocysts.
• Development in intermediate hosts. In a
domestic environment intermediate hosts of N. caninum
are predominantly cattle. They become infected by
ingestion of sporulated oocysts and by transplacental
parasite transmission. After ingestion of oocysts, the
released sporozoites invade the intestinal wall, transform
to tachyzoites, which reach various organs where
they infect nucleated cells (nerve cells, macrophages,
fibroblasts, endothelial cells, muscle cells). Tachyzoites
(6x2 µm) proliferate by endodyogeny. One host cell
may be inhabited by hundreds of tachyzoites. After
apprmdmately 20 divisions (about 3 weeks after
infection), cyst formation starts. Mature cysts are round­
oval, measure 30-100 �1m, are unseptated, show a mostly
thick wall (up to 4 µm in old cysts) ( ► Figure 5. l l)
and contain numerous slender bradyzoites (7-8x2 µm).
Cysts are mostly found in neuronal tissues (brain, spinal
cord, spinal nerves, retina) and in muscles. A similar
development is assumed for other intermediate hosts.
In addition to cattle other domestic animals (e.g. sheep,
goats, horses, dogs, chicken) and many wild animals
(free-living or in captivity) have been found infected,
mostly by detecting specific antibodies and/or DNA.
The long list includes inter alia Artiodactyla (red deer,
roe deer, chamois, ibex, mouflon, bison, buffalo, etc.),
zebra, rhinoceros, elephant, rodents (rats, voles, etc.),
lagomorphs, marsupials (wallaby, kangaroo), carnivores
(wolf, jackal, fox, bear, etc.) and even marine mammals
(seals, dolphins, etc.). Little is known about the potential
epidemiological role of these potential intermediate
hosts. In North America high seroprevalcnces in cervids
(>40%) and detection of oocysts or copro-ONA in faeces
of coyotes and wolves suggest a wild animal cycle in this
geographic region.
• Transmission. In catt.le stocks N. cat1i1111m is
predominantly vertically transmitted by transplacental
infections, but horizontal transmission by ingestion of
sporulated oocysts also plays a role. Transmission of N.
<l)
C caninum from cattle to cattl.e by ingestion of afterbirth,
·c3 colostrum or miJ.k, or sexually via semen is insignificant.
'6
(l)
�
N. caninum infections in female cattle may lead 10
�
C
abortions that can occur endemically or epidemically.
·c Most endemic (sporadic) abortions are attributed to the
(l)
reactivation of chronic (latent) infections of the dams in
j
-� the course of pregnancy and subsequem transplacental
transmission of the agent. Most abortions happen during
.>
CJ)
0 the mid-gestation period, 100-1SO days after fertilisation,
0
Earlier infections of the fetus may result in it resorption
if)
cc or mummification. Later infections do not necessarily
a.. cause abortions; instead seemingly healthy but infected
calves may be born which, later on, may themselves
suffer abortions. Endemic abortions may occur in a herd
at a low level over several years. From an epidemiological
point of view, vertical transmission is the most important
route by which the infection may persist in a herd over
several breeding generations. However, mathematical
models suggest that a certain level of transmission
by ingestion of oocysts is required to perpetuate the
infection in a cattle herd.
In contrast, a primary infection of a herd by sporulated
oocysts on pastures may cause a more dramatic,
epidemic situation. In its worst form an 'abortion storm'
may be created, resulting in abortions of 10% or more of
the pregnant cows within a period of 4-8 weeks.
Occurrence and epidemiology. N. caninum
is found worldwide. It is one of the most important
agents of abortions in cattle. For instance, the parasite
was detected in l0-42% of aborted bovine fetuses in
Europe. The total worldwide losses in cattle husbandry
are estimated at US$ 1.3 billion per annum.
The frequency of oocyst excretion by dogs is not
well known. Just 0.1 % of 24,089 dogs investigated in
Germany in 2001-2004 excreted Neospora oocysts.
Seroprevalences in dogs vary greatly, depending on
the geographical region and type of husbandry (0.5-
46% in Europe). Dogs in rural areas are more often
antibody positive to N. caninum than urban dogs (e.g.
CH: 20%/7%, NL: 24%/5%, UK: 17%/6%, Argentina:
48%/26%). Neospora seroprevalences in cattle are
highly variable. Up to 94% of dairy cow herds and 2-44%
of individual dairy cows showed specific antibodies in
various European countries (DE, DK, CH, FR, UK, SE,
ES). Similar prevalences are found in beef cattle.
The wide distribution of Neospora infections in wildlife
is mentioned above.
Immunology. Cellul.lr nnd humoral immune responses
to N. ca11ir1t1m develop within 2-4 weeks after primary
infection of na'ive cattle. Corresponding with other
coccldlal infections, the key cytokine is IFN-y. which
causes inhibition of para. ite proliferation, mediates
immune elimination of tachyzoites and is involved in
stage conversion from tachyzoites to bradyzoites (see
T gondii, ► p. 102). This kind of immunity seems to
protect cattle from exogenous infections with sporulated
oocysts but is only partially effective at protecting fetuses
against the parasite. There is also some protection against
transplacental infection as only about 4'¾> of infected
cows suffer repeated abortions by recrudescence of
a previously established parasite population whereas
primary infections in the course of pregnancy cause
distinctly higher abortion rates (e.g. see above reference
to 'abortion storm'). Since transplacental transmission
is not prevented in surviving animals during their later
pregnacy, the infection can persist in a herd.

Abortion or at least prenatal infection of the calf
is commonly seen in connection with maternal
immunomodulation in favour of the survival of the
fetus. This seems to allow the reactivation of bradyzoites
and the invasion of placenta and fetus by tachyzoites.
The current view assumes that the fate of the fetus
of an infected dam is finally decided by its age and
immunocompetence at the time of transplacental
infection by N. caninum. Having reached the last
trimester of pregnancy, the fetus may survive and be
born as a clinically asymptomatic calf but with a high
probability (80-90%) of being a prenatally-infected
carrier of N. caninum.
The immunology of N. caninum infections in dogs,
particularly concerning neurological alterations (see
below), needs to be clarified.
Pathogenesis and clinical signs. In several animal
species and age groups Neospora infections may cause
a variety of clinical syndromes.
• Neosporosis in cattle. Infections in adult cattle
are usually unapparent, and most infected cows deliver
clinically asymptomatic calves. On the other hand, the
infection can induce abortion, stillbirth and rarely
the birth of impaired calves. Abortions occur most
frequently in heifers or cows after a primary infection,
independent of age, breed and season. The risk of
abortion in infected (seropositive) cows is estimated
to be 7.4 times higher compared to non-infected
(seronegative) heifers. Abortions may occur from the 3rd
month of gestation, but they are most frequent between
months 4-6 of gestation. Cows may repeatedly abort
without reinfection but the risk decreases with time and
age by a factor of 2-3. Abortions in the early gestation
phase may be overlooked due to resorption of the fetus.
Necrosis and inflammatory reactions, caused directly
or by immunopathological processes in the placenta or
in the fetus, are regarded as major causes of abortion.
In most cases aborted fetuses appear physically
unaffected. Histology reveals multifocal degeneration
and inflammation, especially in the brain and spinal
cord. Corresponding lesions in other tissues may result,
e.g. in myocarditis, myositis, hepatitis or nephritis.
Surviving, prenatally infected calves seem healthy in
most cases (>95%); a few may show neuromuscular
symptoms with ataxia, hyperinflexion or hyperextension
of the extremities, encephalomyelitis and other signs.
• Neosporosis in other ruminants. The clinical
and epidemiological significance of neosporosis in
sheep and goats is unknown. In Europe, seroprevalences
in sheep vary between 0.5 and 17%. Occasionally, N.
caninum DNA has been found in aborted fetuses of
sheep and goats. In a few cases, focal encephalitis and
5. Phylum Alveolata
CNS symptoms have been observed in sheep and were
associated with N. caninum infections.
• Neosporosis in wild animals. Many species of
wild mammals are susceptible to N. caninum (see above).
Several reports indicate that clinical cases of neosporosis
may occur in wildlife species, e.g. in pine martens and ccs
:cQ)
"O
foxes (wild), wild ruminants (captive/wild), rhinoceros
(captive) and wallaby (captive). E
iii
• Neosporosis in dogs. Neosporosis is observed
in new-born and young dogs, occasionally also in adult
dogs. Concerning the latter, it is not clear whether or
not disease is caused by newly acquired infections or as
a result of activated, latent infections. Abortions after
transplacental infections have so far not been observed
in dogs.
Prenatal Infections become manifest in whelps and
young dogs up to an age of approximately 1 year. First
symptoms are mostly detected after weaning. Usually
only part of a litter is affected. Typically, the animals
develop a polyradiculoneuritis-myositis syndrome
with focal necroses predominantly in brain, spinal
cord and spinal nerves. Clinical signs include muscular
atrophy, ataxia, paresis, ascending paralysis, spastical
hyperextension (mainly of the hind legs), muscular
pain in the lumbar, pelvic region and quadriceps region,
torticollis, dysphagia and incontinence ( ► Figure 5.13).
Normally, the sensitivity remains intact and dogs may
show good general condition for months. Sometimes
dogs develop a generalised multifaceted clinical picture
including megaoesophagus with dysphagia, muscular
pain, pneumonia, myocarditis, myositis and, especially
in older dogs, ulcerative dermatitis.
Diagnosis. Serology for specific antibody detection is
the basic method for diagnosing the Neospora infection
intra vitam in various animal species. Cross reactions
with antibodies against T. gondii or other protozoa are
of minor relevance. In diseased dogs, the examination
of muscle biopsies and liquor (immunohistology, DNA
analyses) is a further diagnostic option. Oocysts may be
c
ccs
C
·;::
_!;
>,
0)
0
0
Figure 5.13. Neosporosis in a dog: clinical signs of -�
ccs
polyradiculoneuritls-myositis (Photo: IPZ, P. Deplazes). Q..
 Part II. Parasites and parasitoses: protozoa
demonstrated (low density) in dog faeces during patency
by flotation techniques. They measure 10-13x 10-11 µm
and strongly resemble oocysts of Hammondia heydorni.
Differentiation is possible by DNA analysis.
Post mortem diagnosis in aborted cattle fetuses
is performed by histology, immunohistology and,
primarily, by DNA analysis. Suitable tissues are brain,
heart, liver, and placenta. Mature cysts measure up to
110 µm, are not septated, contain many bradyzoites (6-
8x 1-1.8 µm) and differ from those of T. gondii by thick
walls (up to 4 µm in old cysts) (► Figure 5.11 ). In dogs,
necrotic foci in brain and liver, and subtle yellow-whitish
striations in muscles (atrophy and fibrous replacement)
provide diagnostic hints.
Therapy and control. Abortions cannot be prevented
by antiparasitic treatment. There is currently no
protective commercial vaccine available. To reduce the
risk of horizontal parasite transmission to cattle, dogs
should be kept away from aborted fetuses, afterbirths
and dead calves. Dogs should not be fed with raw meat
or organs. Contamination of water, fodder and pastures
by dog faeces must be avoided. In low prevalence
herds, culling of seropositive cows and their offspring
is sometimes practised. In high prevalence herds,
infection rates could be reduced over a 2-3 year period
by excluding seropositive female calves from breeding.
For treatment of systemic infections in dogs clindamycin
or pyrimethamine in combination with sulfonamides
has been used (► Table 19.13, p. 599). The prospect of
success is lower in acutely diseased dogs with rapidly
developing paresis than in animals with a more chronic
course of disease. Relapses generalJy respond welJ to
repeated treatments. Cysts cannot be eliminated by
chemotherapy.
Neospora hughesi infections in horses
N. hughesi was detected in the CNS of an adult horse
in California/USA and distinguished from N. caninum
by morphological, antigenic and molecular features.
Meanwhile, the parasite was also found outside the
USA, in Canada, Mexico and Brazil. Definitive host(s)
and potential intermediate hosts besides equines are
Q)
C unknown. The seroprevalences in horses vary depending
·c3
'5 on the geographical location. In a recent study
Q)
investigating horse serum samples from 49 US states,
�
1.2% of horses in 21 states showed specific antibodies.
co An annual rate of exposure of 1.7% was calculated for
C
·.: California. N. hughesi is vertically transmitted to foals
Q)
( ~4% of presuckle foals born from seropositive mares
-� show antibodies to N. hughesi) but associations with
>,
Ol
abortions in horses are not yet clear. However, N. hugl,esi
0 infections have to be considered in the differential
0
.if)
diagnosis of'equine protozoal myeloencephalitis' (EPM),
co which seems to be caused, primarily, by Sarcocystis
co
Q. neurona (► p. 121).
Selected references
Canton GJ, Katzer F, Maley SW, Bartley PM, Benavides-
Silvan J, Palarea-Albaladejo J, Pang Y, Smith SH, Rocchi
MS, Buxton D, Innes EA, Chianini F (2014) Inflammatory
infiltration into placentas of Neospora caninum challenged
cattle correlates with clinical outcome of pregnancy. Vet
Res 45: 11.
Cavalcante GT, Soares RM, Nishi SM, Hagen SC, Vannucchi
Cl, Maiorka PC, Paixao AS, Gennari SM (2012)
Experimental infection with Neospora caninum in pregnant
bitches. Rev Bras Parasitol Vet 21: 232-236.
Dubey JP, Schares G (2011) Neosporosis in animals - the last
five years. Vet Parasitol 180: 90-108.
Goodswen SJ, Kennedy PJ, Ellis JT (2013) A review on the
Infection. genetics. and evolution of Neospora caninum: from
the past to the present. Infect Genetics Evolut; 13: 133-150.
Maley SW, Buxton D, Rae AG, Wright SE, Schock A, Bartley
PM, Esteban-Redondo I, Swales C, Hamilton CM, Sales
J, Innes EA (2003) The pathogenesis of neosporosis in
pregnant cattle: inoculation at midgestation. J Comp Pathol
129: 189-195.
Marsh AE, Barr BC, Packham AE, Conrad PA (1998)
Description of a new Neospora species (Protozoa:
Apicomplexa: Sarcocystidae). J Parasitol 84: 983-991.
Monney T, Hemphill A (2014) Vaccines against neosporosis:
what can we learn from the past studies? Exp Parasitol
140: 152-170.
Pusterla N, Tamez-Trevino E, White A, Vangeene J, Packham
A, Conrad PA, Kass P (2014) Comparison of prevalence
factors in horses with and without seropositivity to Neospora
hughesi and/or Sarcocystis neurona. Vet J 200: 332-334.
Regidor-Cerillo J, Arranz-Solis D, Benavides J, Gomez­
Bautista M, Castro-Hermida JA, Mezo M, Perez V,
Ortega-Mora LM, Gonzalez-War1eta M (2014) Neospora
caninum infection during early pregnancy in cattle: how the
isolate influences infection dynamics, clinical outcome and
peripheral and local immune responses. Vet Res 45: 10.
Reichel MP, McAllister MM, Pomroy WE, Campero C,
Ortega-Mora LM, Ellis JT (2014) Control options for
Neospora caninum - is there anything new or are we going
backwards? Parasitology 141: 1455-14 70.
Sager H, Moret CS, Muller N, Staubll D, Esposito M, Schares
G, Hassig M, Stirk K, Gottstein B (2006) Incidence of
Neospora caninum and other intestinal protozoan parasites
m populations of Swiss dogs. Vet Parasitol 139: 84-92.
Schares G, Pantchev N, Barutzki D, Heydorn HO, Bauer
C, Conraths FJ (2005) Oocysts of Neospora caninum,
Hammondia heydomi, Toxoplasma gondii, and Hammondia
hammondi in faeces collected from dogs in Germany. Int J
Parasitol; 35: 1525-1537.

Genus Besnoitia
C. Besnoit, former professor at the �cole Veterinaire de
Toulouse, France.
Members of the genus have heteroxenous life cycles,
which are only partly known in detail. Ten species are
described; final and intermediate hosts are known for
four species: B. wallacei: cat/rat; B. darlingi: cat/opossum;
B. oryctofelisi: cat/rabbit; B. neotomofelis: cat/pack rat
(southern plains woodrat). Oocysts of Besnoitia spp.
have not been found so far in cat faeces in Europe.
Oocysts can only be differentiated from Hammondia
and Toxoplasma oocysts by DNA analysis. Intermediate
hosts of other Besnoitia species are domestic and wild
ruminants, equids, rodents, reptiles and others. The most
important species is B. besnoiti which may cause severe
disease in cattle. Other species are B. caprae (goat), B.
tarandi (reindeer), B. benetti (donkey), B. jellisoni, B.
akodoni (rodents).
Besnoitia besnoiti
Disease: Bovine besnoitiosis.
Agent and life cycle. The only known stages in the
life cycle of B. besnoiti are tachyzoites (5-9x2-5 µm)
and bradyzoites (8x2 µm). Tachyzoites develop in
endothelial cells of blood vessels, in macrophages and
fibroblasts, whereas bradyzoites proliferate in thick­
walled, unseptated cysts (0 up to 600 µm), located in
skin, mucous membranes and many organs (see below).
A definitive host of B. besnoiti has not yet been identified.
Experimental infections of dogs and cats with cysts from
naturally infected European cattle did not lead to oocyst
shedding, and serological surveys in wild carnivores did
not provide any indication for a potential role of these
animals. It is also unknown whether animals other than
bovines could be involved in the cycle as intermediate
hosts, e.g. rodents or wild ruminants. Specific antibodies
to B. besnoiti have been sporadically found in red and
roe deer in Spain, and voles (Microtus arvalis) proved
susceptible to a European isolate of B. besnoiti in
experimental studies. Parasite DNA was detectable for
at least 5 months p.i. in lungs, heart, skin, kidneys and
skeletal musculature of the voles.
Transmission of B. besnoiti in cattle populations under
natural conditions is assumed to occur by blood-sucking
insects (Stomoxys calcitrans, tabanids) in a non-cyclic
(mechanical) manner ( ► Glossary, p. 620). Also,
iatrogenic transmission by re-used injection needles
may occur. Sexual transmission seems unlikely.
5. Phylum Alveolata
iO::clJIITIRK:r Iagl�� OitiOSlS ar
■
:.
own from countries in Africa, Asia and southe
urope (Le. Spain, Portugal. southern France, Italy).
rnalenca at the Cum level can be very high, e.g
2-1009' in Iraly, 87'6 in Spain (Spanish Pyrenees)
. banold bu ,pread. in the put few years, througij
ranee to the MaaifCentnl and the eastern Alps up to
e Swil8 bard«.Cua olborine banoitiosb were also
ntly diapoMd in Swtberland, Germany, Hun
dCroatia.
and cllnlcal etgna. Jn endemk areas
nottioau la reapon,lble for considerable economi"
oaset in cattle hu,bandry because of high morbidi�
nclm rtalttr lup to 1096,- fertiJicy dis.order ,-reduced
performance and skin damage. In France, most clinical
cases have been observed in 2-4 year-old cattle, but
younger animals (>6 months) may also be affected.
Disease is mostly detected during spring to autumn.
Severe clinical symptoms are observed in 10-20% of the
seropositive cases; some show only scleral-conjunctival
cysts but the majority of animals with specific antibodies
to Besnoitia are free of clinical symptoms.
Usually, three phases of disease are observed. In the
course of an acute, parasitaemic phase, 1-3 weeks after
infection, tachyzoites proliferate in endothelial cells,
fibroblasts and macrophages. This phase is associated
with fever (41-42 °C), inappetence, tachycardia,
tachypnoea, nose and eye discharge. After a temporary,
almost asymptomatic phase, the final chronic stage
starts approximately 2 months p.i. with swelling of
lymph nodes and subcutaneous oedemas at head and
cervical areas, presternal and underbelly regions and
the extremities. The animals move stiffly and slowly
because of severe pain. Bulls may develop orchitis with
temporary or permanent infertility, and abortions
may occur in pregnant cows. As infection proceeds,
characteristic thick-walled cysts develop in the cutis
and subcutis, at the mucosa! sites of the respiratory
and genital tract, in muscle fasciae and tendons, and in
the walls of blood and lymph vessels in various organs.
The cysts (0.2-0. 6 mm) are macroscopically visible on
the mucosa! surface of the conjunctivae, nose, vulva
and vagina. The thickened, indurated skin becomes
wrinkled and hairless (sclerodermia, hyperkeratosis,
alopecia). Alterations are usually most distinct in the
head and neck region, at the perineum and the forelegs
('elephant skin')(► Figure 5.14).
Diagnosis. A tentative diagnosis from clinical signs can
be confirmed by serology and histological and molecular
investigation of skin biopsy specimens. Serology was
recently partly validated by an inter-laboratory trial
in Europe. ELISA or IFAT, with confirmatory Western
blotting, is recommended.
Therapy, control. There is currently no effective
chemotherapy available. Infected animals represent a
Part II. Parasites and parasitoses: protozoa
Figure 5.14. Besnoitiosis in cattle (Photos: H.C.E. Cortes) (a) skin alteration; (b) histological section: skin with multiple cysts.
lifelong source of infection. To prevent importation of
infected cattle, animals intended for acquisition should
be serologically investigated. An attenuated live vaccine
is available in some countries (Israel, South Africa).
Control of tabanids and other blood-sucking insects
is recommended.
Selected references
Alvarez-Garcia G, Frey CF, Mora LM, Schares G (2013)
A century of bovine besnoitiosis: an unknown disease re-
emerging in Europe. Trends Parasitoi 29: 407-415.
Basso W, Schares G, Gollnick NS, Rutten M, Deplazes
P (2011) Exploring the life cycle of Besnoitia besnoiti -
experimental infection of putative definitive and intermediate
host species. Vet Parasitol 178: 223-234.
Basso W, Lesser M, Grimm F, Hllbe M, Sydler T, Trosch L,
Ochs H, Braun U, Deplazes P (2013) Bovine besnoitiosis
in Switzerland: Imported cases and local transmission. Vet
Parasltol 198: 265-273.
Cortes H, Leitio A. Gottsteln B, Hemphill A (2014) A review
on bovine besnottiosis: a disease wi th economic impact
in herd health management. caused by Besnoitia beSnoiti
(Franco and Borges, 1916). Parasitology 141: 1406-1417.
Frey CF, Gutierrez-Exposlto D, Ortega-Mora LM, Benavides
J, Marcen JM, Castillo JA, Casasua I, Sanz A. Garcia­
Lunar P, Esteban-GU A. Alvarez-Garc{a G (2013) Ovonic
bovine besnoitlOSIS: 1ntra-organ paras,te distroution, parasile
loads and parasite-associated lesions 1n subel:nical cases.
Vet Parasitol 197: 95-103.
Garcia-Lunar P, Ortega-Mora LM, Schares G, Gollnick NS,
Jacquiet P, Grisez C, Prevot F, Frey CF, Gottstein B,
Alvarez-Garcia G (2013) An interlaborato,y comparatrve
study of serological tools employed in the ct.agnoS1s of
BesnoitJa oesnoitJ infecoons 111 oovnes. Transbound Emerg
Dis 60: 59-68.
Gazzonis AL, Garcia GA. Zanzani SA, Garippa G, Rossi L,
Maggiora M, Dini V, lnvemizzi A. Luim M, Tranquillo VM,
Mora LO, Manfredi MT �14) Besnottia besnOlri among
cattle in insular and northwestern Italy: enoemc tifecoon 01
endemic outbma.ks. Paras,te Vectors 7: 585.
Langenmayer MC, Gollnick NS, Majzoub-Altweck M,
Scharr JC, Schares G, Herrmanns W (2014) Naturally
acquired bovine besnoitiosls: histological and immunological
findings in acute subacute and chronic disease. Vet Pathol
pii: 0300985814541705.
Llenard E, Salem A, Grisez C, Prevot F, Bergeaud JP,
Franc M, Gottstein B, Alzieu JP, Lagalisse Y, Jacquiet
P (2011) A longitudinal study of Besnoitia besnoiti infections
and seasonal abundance of Stomoxys calcdrans in a dairy
cattle farm of southwest France. Vet Parasitol 177: 20-27.
Genus Sarcocystis
•
Disease: Sarcocystiosis.
Sarkos (G). flesh; kystis (G): bladder.
Members of the genus Sarcocystis (named also
sarcosporidia) are obligatory heteroxenous parasites.
Gnmogony and sporogony occur in the intestine of
definitive hosts (carnivores. humans, birds, reptiles};
mcrogonies and cyst formation take place in intermediate
ho ts (mammals, including humans, marsupials, birds
and poikilothermic animals). Cysts ( = sarcocysts) are in
mo t cases septated, have thin or thick walls and develop
in striated muscles, rarely in the CNS.
Summary
• ..... Approxinately 200 SMx>eystis apectes 11'8
known. They .,. obligatoly heteroxenous parasites
al CllfflMJIOUI and omnlvaroul mammals, birds and
...... definitive hoata. In Intermediate hosts (prey),
� OJ8 (Mi111hr tubal) dewlop predominantly
In striated nuclla.

A and l0-12x7-8 µm in cats, depending on the species.
• Life cycle. Definitive ho8ta acquire the Infection by
Ingesting cysts In musculature of Intermediate hosta.
Gamogony and formation of aporulated oocysts occur
In enterocytes of the small Intestine (no merogony
In final hosts!). Excretion of sporocysta and (few)
oocysts Qsospora type) In the faeces after short (days)
prepatency. Patency laats for weeks to months. In
lntennedlate hoata (herbivores and omnivores) after
Ingestion of sporoeysts/oocysts, two merogonles In
endothelial cells of capillaries; cysts are formed In
muscle cells. Development In Intermediate hosts lasts
several months.
Occurrence, epidemiology. The genus occura
worldwide. The various species are relatively host
specific and depend on particular ecological ayatema.
Sporocysts/oocysts of Sarcocyst/s spp. are found
In Europe In 15 and 5% of dog and cat faecu,
respectively. Prevalences In cattle and pigs are low In
closed husbandry systems but high under traditional
conditions.
• Immunology. Definitive hosts develop a partial
Immunity, which reduces sporocyst excretion after
challenge Infections. Immunity In Intermediate hosts
Is boosted by re-Infections. There Is no Immunological
cross-protection between Sarcocysts les.
• Clinical signs. Infections In defi ltlve hosts are usually
asymptomatic. Heavy lnfectlo11,s In Intermediate hosts
cause severe endothelial amage b erogornes with
��·
fever, weakness, CNS elsorcile('S a.nclJa6ortlons. Deaths
may occur. Muscle cysts �&oU$uaJIY.,\barmless.
• Diagnosis. In defi ltlve �osts coliro;.co . al detection
�•,,.',
(flotation technl ues of sporo y� ocysts. Cysts In
Intermediate hosts of som species macroscopically
detectable, in other cases by mlc oscopy. The best
method for species identification Is DNA analysis.
• Therapy, control. Options for chemotherapy do not
exist. Prevention by keeping potential final hosts away
from pastures, stables, food storage facllltles, etc.
• Special Gase PM (Equine Protozoa! Menlngo•
encephalitis): Neurolo!!Jlcal disease In the Americas
In equids caused b� merogonles of Sarcocystls neurons
in the CNS, n '1 _osls are opossums; several mammals
(armadillos, racco0 s, sea otters, skunks, cata) have
been Ide eg its ntermedlate hosts. Hol'8N are
dlate flosts. A similar syndrome la
ra hughesl (► p. 114).
ce. Humans are definitive hosts
p. from cattle and pigs. Prevalence
ns <:1 %. Occasionally, humans are
· late hosts for Sarcocyst/s spp. which
lature with cyst formation.
Agents. The genus Sarcocystis comprises approximately
200 species with mammals, birds and reptiles as definitive
hosts( ► Table 5.6). Oocysts sporulate in the intestine
of definitive hosts, forming two sporocysts with four
sporozoites each (Isospora type). The thin oocyst wall
is closely attached to the sporocysts and often forms a
typical constriction ( ► Figure 5.15). In most cases the
thin oocyst wall ruptures releasing the sporocysts into
5. Phylum Alveolata
the faeces. Sporocysts measure 13-16x8-l l µm in dogs
Sarcocystis spp. form septated cysts(= sarcocysts) in the
striated muscles of intermediate hosts; cysts have been
known as Miescher tubes since 1843. Some Sarcocystis
species are listed in ► Table 5.6.
co
:g
Life cycle. ► Figure 5.15. Sarcocystis species are ·;::
Q)
heteroxenous parasites. They are usually highly host E
i.jJ
specific with regard to the intermediate host (often
strictly limited to one species, e.g. cattle) whereas the
spectrum of definitjve hosts is generally broader and may
include several members of related families. However,
one species(e.g. cattJe) can serve as intermediate host
for several Sarcocystis species.
• Definitive hosts. Definitive hosts are carnivores
and omnivores (including humans), which acquire
the infection by ingesting cysts in muscular tissue of
intermediate hosts. Cystozoites released from cysts into
the intestine infect cells of the lamina propria and develop
into gamonts(there is no merogony in definitive hosts!).
Oocysts sporulate in the lamina propria (endogenous
sporulation) and are continuously released from the
mucosa. Often, the oocyst wall ruptures and sporocysts,
containing four sporozoites each, are shed in the faeces.
Intensity of sporocyst excretion is highest in the second
week p.i., although shedding may last for months.
• Intermediate hosts. Intermediate hosts are
herbivorous and omnivorous animals. They get
infected by ingesting sporocysts with food or water.
Excysted sporozoites jnvade the intestinal wall and
settle in endothelial cells of arterioles and arteries in
the intestine, in lymph nodes, kidneys and other organs.
They develop directly in the cytoplasm of the host cell
without forming a parasitophorous vacuole. After two
merogonies(endopolygenies) in endothelial cells, second
generation merozoites may induce a third merogony
(endodyogeny) in mononuclear blood cells, but most
of them infect cells of the striated muscles and develop
into cysts in a parasitophorous vacuole. Some species
also invade cells of the CNS and Purkinje fibres of the
heart. After infecting host cells the merozoites transform
into rounded forms (metrocytes) which continuously
multiply by endodyogony. Finally, banana-shaped
cystozoites (= bradyzoites) arise, which are infectious
Q)
C
to the final host. In the course of this development ·13
the infected cell forms a cyst wall. Depending on the �
Q)
Sarcocystis species, the cyst wall varies in thickness
(2 - > 10 µm) ( ► Table 5.6) and shows characteristic
c
Cll
C
surface structures and septae( <2 µm), which subdivide -;::
Q)
the cysts into irregular compartments which are filled
with cystozoites or partially with trophe. In some .s
species, the cysts are additionally enclosed by hosts' >,
OJ
connective tissue. Cystozoites continue to proliferate for 0
2-3 months. Mature cysts may finally contain 100,000 .2
·u5
to 1 million cystozoites. The development of mature
Cll
Q_
Part II. Parasites and parasitoses: protozoa

Table 5.6. Domestic animals as intermediate hosts of Sarcocystis species (selection).

Cattle s. cruzj +++ <1 2 dog, fox, raocoon, others

S. hlrsuta + 73 cat
S. hominis + 73 humans, monkeys
S. rommeli 4 ? 0.5 3 ?
Sheep S. tenet/a +++ 0.73 dog, fox, others
S. arleticanis ++ 0.9 dog
S. glgantea 10 3 cat
S. meduslformls 8 cat
Goat S. capracanls +++ 1 8 dog, fox, others
S. hlrcicanls ++ 2.5 dog
S. moulel 7.53 cat
Pigs S. mlescherlana +++ 1.53 dog, fox, raccoon, others
S. sulhomlnls ++ 1.53 humans, monkeys
Horses 8. bertram/ II ? 12 3 dog
s. fayerl <1 2 dog
S. neurons +++ ? opossums6
Chicken S. horvathl ++ 10 ?
1 Pathogenicity for intermediate hosts: +++ high; ++ moderate; + low; ? = unknown.
2 Thin-walled cyst (<5 µm).
3 Thick-walled cysts (>5 µm).
4 New name proposed for S. sinensls.
5 Syn. S. equicanis.
6 Horses are aberrant hosts, Indigenous Infections only In the Americas.

cysts containing infectious cystozoites takes at least 2-3
months(► Figure 5.16 and 5. 17). Cysts in intermediate
hosts usually persist during the life-span of the host; only
a few might degenerate after months or years.
Occurrence and epidemiology. Sarcosporidiae
are found worldwide in mammals(including marine
mammals), birds and reptiles. Prevalences are high
under natural conditions due to undisturbed predator­
prey relationships. The persistence of the cycles and high
preval.ences are favoured by the ability of intermediate
hosts to harbour several Sarcocystis spp. concomitantly,
the relatively broad spectrum of various species of
definitive hosts(► Table 5.6), the long-lasting sporocyst
excretion by final hosts, the intense proliferation in
intermediate hosts and the persistence of tissue cysts.
Sporocysts are immediately infectious, survive for
months and years in the environment(also at winter
temperatures), and they may pass through sewage
treatment plants. They are, however, sensitive to dryness.
Definitive hosts can contaminate pastures, fodder plants,
water, etc. with sporocysts.
Sporocyst excretion is observed in up to 15% of dogs and
5% of cats in Central Europe. Routine faecal examinations
of 24,600 dogs in Germany(2003-2010) revealed 0.3%
as oocyst excretors. In areas with traditional, small­
hold farms, prevalences in dogs and cats may reach
20-80 and 15%, respectively. The local prevalences
in intermediate hosts may be correspondingly high.
Prevalences in domestic animals as intermediate hosts
are often variable. S. cruzi is the most common species
in cattle; S. rommeli, originally described as S. sinenis
in water buffaloes(the final host is unknown), seems
the most prevalent thick-walled Sarcocystis species in
cattle(► Table 5.6). The zoonotic species S. hominis
was recently demonstrated by PCR in 97% of samples
of minced meat from retail meat stores in Belgium. The
prevalence of S. suihominis in pork is estimated to be 5%.
S. miescheriana is more common. The hygienic condition
of piggerics is the crucial factor in the occurrence of
sarcocystiosis in pigs. Sarcocystis infections are common
in wild ruminants. Prevalences reach 100%; however,
most of the species are not adequately described.
Immunology. Cattle, sheep, goats and pigs develop
protective immunity to otherwise lethal challenges after
low-dose primary infections with pathogenic Sarcocystis
species. There is no inter-species cross-protection.
Protection persists, without reinfection, for 3 months in
pigs and for at least 8 months in cattle. Most intermediate
hosts on pastures ingest a few oocysts on a regular
basis and maintain Immunity for a long time(enzootic
stability). Definitive hosts remain susceptible after a
primary infection but sporocyst excretion is reduced and
patency is shortened when compared to naive controls.
 5. Phylum Alveolata

�1
-- -----:11
ij!,f ! ,i�
ctl
-0
·;::
Q)
E
i.Ii

Development in definitive host: gamogony and sporogony

in intestinal wall (no merogony)

Mature septated cyst ' "'-o Sporozoite

with cystozoites Development U
in intermediate\
�
·� Merogony I in endothelium

e/
� host

Young muscle cyst f

UllflllJn
\ �
of blood vessels

�-
Merozoite
with metrocytes \
\ �,
�-�
Merogony in
mononuclear
/
. Merogony II in endothelium
of blood vessels

blood cells

Figure 5.15. Life cycle of Sarcocystis cruzi (Graphics: IPZ, S. Ehrat).

Q)

·o
C

'6
Q)
2
cCil
C
·;::
Q)

j
C

>.
Ol
0
0
·u5
�
► Figure 5.16. Cysts of Sarcocystis gigantea (length: up to 1.5 Figure 5.17. Cysts of Sarcocystis sp. (length: 1.8 mm) in the cu
Cl.
cm) in the oesophagus of a sheep (Photo: IPZ). skeletal muscle of a pig (Photo: IPZ).
 Part II. Parasites and parasitoses: protozoa
Pathogenesis and clinical signs. Infections of dogs
and cats as definitive hosts are usually asymptomatic;
diarrhoea is only rarely observed. The species
transmitted by dogs are generally more pathogenic to
intermediate hosts than those released by cats. However,
since clinical disease is usually prevented by enzootic
stability, Sarcocystis infections in domestic animals are
rarely associated with clinical problems.
• Acute and subacute sarcocystiosis. This form
of disease is very rare and occurs in cattle and pigs only
when naive animals ingest large numbers of sporocysts
(depending on the species, 50,000 up to 3 million). The
meronts I and II are the pathogenic stages. After an
I '
incubation period of2-3 weeks, symptoms may develop
that are similar in all intermediate host species, i.e. fever,
apathy, anorexia, severe normocytic, normochromic
anaemia (low haematocrit values), lymphocytosis,
reduced serum albumin concentrations, coagulation
disorders, dyspnoea, cyanosis, temporarily elevated
serum enzyme levels (LOH, AST, CK), bilirubinaemia,
muscle stiffness, ataxia and weight loss. In addition,
abortions are observed after infections with S. cruzi
(cattle), S. tenella (sheep) and S. mies cheriana (pigs), as
well as in rare cases CNS disorders. Subserosal petechiae
and ecchymosis, petechial bleedings in skeletal and
heart muscles, vasculature damages, interstitial and
perivascular infiltrations and necrotising foci in various
organs are found at necropsy. Degenerating cysts are
demarcated by neutrophils, eosinophils and giant cells.
Lethal cases were reported particularly in cases of CNS
infection. Lower infection doses may induce subacute
forms of the disease.
• Chronic sarcocystiosis. Chronic sarcocystiosis is
generally clinically inconspicuous. Generalised myositis
is only rarely observed in infected animals. Usually
cysts are found in the muscles without detectable host
tissue reactions at slaughter. Degenerating cysts may be
enclosed by granulomas and mononuclear infiltrations.
Diagnosis. Patent infections of definitive hosts are
diagnosed by coproscopic detection of oocysts/sporocysts
in faecal samples (morphological species identification
is not possible). Serological tests for detecting specific
antibodies in definitive and intermediate hosts are used
in research.
Acute sarcocystiosis can be diagnosed post mortem
by necropsy findings and the detection of meronts in
Giemsa stained smear preparations of internal organs
(relatively insensitive). Better results are obtained by
histological examinations and DNA analyses. The
diagnosis of chronic sarcocystiosis is based on the
detection of cysts in muscles. Routine meat inspection
at slaughter will detect sarcocystiosis only when cysts
are macroscopically visible or when mass infections
cause gross muscles lesions (myositis, oedema) which
make the affected organs unfit for human consumption.
Microscopic small cysts will be overlooked. Some species
can be identified by morphological characteristics of
the cysts or by immunohistology, but DNA analysis is
more accurate.
Therapy. There is usually no indication for treating
acute or chronic cases of sarcocystiosis in intermediate
or definitive hosts, and reports on effective drugs are
lacking. An exception is the chemotherapy of EPM in
horses (see below).
Control. Contamination of pastures, stables, etc.
by faeces of carnivores or humans must be avoided.
Furthermore, measures are recommended for restricting
the distribution of oocysts/sporocysts by wastewater
or slurry. Dogs and cats should not be fed with meat
unless it has been cooked or frozen (3 days at -20 °C).
For disinfection the same measures can be applied as
in coccidiosis ( ► p. 571 ). For food regulatory measures
► p. 561.
• Sarcocystis infections in domestic ruminants
and pigs. The Sarcocystis species occurring in these
hosts are listed in ► Table 5.6, and the rare forms of
acute and subacute sarcocystiosis are described above.
In cattle, acute infections with S. cruzi may in rare
cases cause systemic, sometimes lethal disease, abortion
and CNS disorders. The same holds true for S. tenella
infections in sheep. Goats and pigs may also suffer
occasionally from acute sarcocystiosis and perish.
• Sarcocystis infections in wild ruminants. Up
to 100% of cervids (deer, fallow deer, red deer, moose,
reindeer, etc.) may be infected with Sarcocystis cysts.
For example, in Norway, 5 Sarcocystis species have
been identified either in red deer (Cervus elaphus) or
moose (Alces alces), including S. hardangeri, S. ovalis,
S. rangiferi, S. tarandi, and S. hjorti. The latter species
was most prevalent in red deer and was recently held
responsible for severe muscular lesions in hunted deer
in Switzerland. Definitive hosts for S. hjorti are red and
arctic foxes.
• Sarcocystis infections in carnivores. Dogs,
other canids and cats are definitive hosts of numerous
Sarcocystis species (selection in ► Table 5.6). In addition,
they can also be intermediate hosts, e.g. in the USA the
dog for S. canis and the cat for S. felis. S. canis can cause
systemic disease with hepatitis and encephalitis in dogs.
S. neurona is infectious for dogs, cats, raccoons, etc.
and can cause a disease syndrome similar to EPM (see
below).
• Sarcocystis infections in equids. Several named
Sarcocystis species occur in horses, including S. bertrami
(Europe), S.fayeri (USA) and S. neurona (North, Central
and South America). S. neurona is the most important
species as agent of a serious neurological disease of
horses, the Equine Protozoa} Myeloencephalitis (EMP),

and of infections in a variety of other animals. Neospora
hughesi (► p. 114) produces a disease similar to EMP,
but 30-40 times less frequent than S. neurona.
Sarcocystis neurona and EMP
Life cycle. Definitive hosts of S. neurona are the North
American opossum (Didelphis virginiana) and the South
American opossum (D. albiventris) which may excrete
large numbers of sporocysts in faeces. In various regions
of the USA 6-31 % of the opossums have been found
to excrete sporocysts which may be ingested by a wide
spectrum of mammals and birds. Raccoons, skunks,
armadillos, sea otters and cats are experimentally proven
intermediate hosts in which mature sarcocysts develop.
Epidemiological evidence suggests that raccoons are
the most important intermediate hosts. Horses become
infected with S. neurona by ingesting sporocysts.
Clinical signs. Horses are regarded as aberrant
intermediate hosts because the development of the
parasite is restricted to merogonies. Meronts develop
without forming a parasitophorous vacuole in neural
and inflammatory cells of the brain and spinal cord,
causing focal bleeding, necroses and a nonpurulent
myeloencephalitis. Clinical signs include weakness, gait
abnormalities, lameness, head tilt, unilateral facioplegia,
partial paralysis of the tongue, ataxia, spasms, paresis
and recumbency. The course of EPM may vary from
acute to chronic with slow progression.
Epidemiology and occurrence. To date, EMP has
only been observed in horses raised in the Americas,
coinciding with the geographical range of opossums
(one case in a zebra in California). Although the
seroprevalence in horses amounts to approximately
30-50%, the incidence of EMP was estimated at 0.5-
1.0% in the USA. EMP has been diagnosed in horses
exported from the USA to other countries (e.g. Japan,
Europe). Several reports on healthy horses in Spain
and France with antibodies against S. neurona are not
fully explained, but interpreted by specialists as due to
cross-reactivity with other Sarcocystis species.
Many other animal species (to be classified as aberrant
intermediate hosts) are susceptible to S. neurona,
including dog, cat, wild carnivores, mustelids, marine
mammals (sea otter, seals, etc.) and even birds. Clinical
disease has been reported inter alia in dog, cat, lynx,
skunk, raccoon, ferret and some of the marine mammals.
The discovery of S. neurona DNA in neonates of marine
mammals may be an indication of vertical transmission
of the parasite.
Diagnosis and therapy. Clinical signs, detection
of specific antibodies (IFT, Western blotting) in serum
or CSF and parasite detection at necropsy (histology,
immunohistochemistry, DNA analysis) are options for
diagnosing EMP in horses. Several drugs are licensed
5. Phylum Alveolata
in the USA for treatment of EMP, including panazuril
(Marquis•), diclazuril (Protazil•) and sulfadiazine/
pyrimethamine (ReBalance•). For details see literature.
• Sarcocystis infections in birds. Numerous,
including some as yet unnamed, Sarcocystis species are
found in muscles of chickens, ducks, geese, turkeys, Ctl
:Q
pigeons and other birds. The life cycles of the parasites ·;:::
are only partially known. Dogs, cats, skunks, opossums E
and particularly birds of prey have been identified as i.iJ
definitive hosts. The host specificity for intermediate
hosts is often relatively low. For instance, the spectrum
of S.falcatula (final host: opossum) comprises sparrows,
pigeons and several others birds. The species was found
to be pathogenic for parakeets under experimental
conditions; natural infections have been observed in
owls and eagles. Another example is S. calchasi (final
host: hawks), which affects a variety of psittacine birds,
pigeons and others by lesions in the CNS. Intensively
reared poultry is rarely infected by Sarcocystis spp.
Zoonotic importance. Ingestion of pork containing
cysts of S. suihominis by human volunteers has caused
temporary nausea, vomiting, abdominal pain, diarrhoea
and dyspnoea within 24 hours. Sporocysts were shed
11-13 days p.i. S. hominis is less pathogenic for humans,
but may cause similar symptoms. Muscular cysts are
believed to be very rare in humans. The parasite,
incidentally found in approximately 100 cases to date,
was generally named S. lindemanni without anything
being known about it. However, unapparent infections
were suspected in some ethnic groups in South East Asia
based on antibody detection (seroprevalence >20%).
Recently, groups of travellers returned from Malaysia
suffering from severe muscular disorders and seriously
affected general condition. The agent was identified as
S. nesbitti, a species parasitising cobras and pythons as
definitive hosts.
r-==�====-
Selected references
Abubakar S, Teoh BT, Sam SS, Chang LY, Johar! J, Hooi PS,
Lakhbeer-Slngh HK, Italiano CM, Omar SF, Wong KT,
Ramil N, Tan CT (2013) Outbreak of human infection with
Sarcocyst/s, Malaysia, 2012. Emerg Infect Dis 19: 1989-1991.
Blazejewski T, Nursimulu N, Pszenny V, Dangoudoubiyam
S, Namasivayam S, Chiasson MA, Chessman K,
Tonkin M, Swapna LS, Hung SS, Bridgers J, Ricklefs
SM, Boulanger MJ, Dubey JP, Porcella SF, Kissinger
JC, Howe DK, Grigg ME, Parkinson J (2015) System­
based analysis of the Sarcocystis neurona genome identifies
pathways that contribute to a heteroxenous life cycle. MBio
pii: e02445-14.
Damriyasa IM, Edelhofer R, Failing K, Lind P, Petersen E,
Schares G, Tenter AM, Volmer R, Zahner H (2004) Cross­
sectional survey in pig breeding farms in Hesse, Germany:
 Part II. Parasites and parasitoses: protozoa
seroprevalence and risk factors of infections with Toxoplasma
gondii, Sarcocystis spp. and Neospora caninum in sows. Vet
Parasitol 126: 271-286.
Dubey JP, Calero-Bernal R, Rosenthal BM, Speer CA, Fayer
R (2015) Sarcocystosis of animals and humans. Boca Raton,
FL, USA: CRC Press. ISBN 9781498710121.
Dubey JP, Howe DK, Furr M, Saville WJ, Marsh AE, Reed
SM, Grigg ME (2015) An update on Sarcocystis neurona
infections in animals and equine protozoa! myeloencephalitis
(EPM). Vet Parasitol 209: 1-42.
Dubey JP, Sykes JE, Shelton GD, Sharp N, Verma SK,
Calero-Bernal R, Viviano J, Sundar N, Khan A, Grigg
ME (2014) Sarcocystis caninum and Sarcocystis svanai n.
sp. (Apicomplexa: Sarcocystidae) associated with severe
myositis and hepatitis in the domestic dog (Canis familiaris).
J Eukaryot Microbiol 62: 307-317.
Homok S, Mester A, Takacs N, Baska F, Majoros G, Fok
E, Biksi I, Nemet z, Hornyak A, Janosi s, Farkas R
(2015) Sarcocystis infection in cattle In Hungary. Parasite
Vectors 8: 69.
Howe DK, MacKay RJ, Reed SM (2014) Equine protozoa!
myeloencephalitis. Vet Clin North Am Equine Pract 30: 659-
675.
Italiano CM, Wong KT, Abu Bakar S, Lau YL, Ramly N, Syed
Omar SF, Kahar Bador M, Tan CT (2014) Sarcocystis
nesbitti causes acute, relapsing, febrile myosltis with a high
attack rate: description of a large outbreak of muscular
sarcocystosis in Pangkor Island, Malaysia, 2012. P1oS Negl
Trop Dis 8: e2876.
Maier K, Ollas P, Endertein D, Klopffleisch R, Mayr SL,
Gruber AD, Lierz M (2015) Parasite distribution and
early-stage encephalitis In Sarcocystis calchasi infections
in domestic pigeons (Columba livia f. domestics). Avian
Pathol 44: 5-12.
More G, Schares S, Makslmov A, Conraths FJ, Venturini
MC, Schares G. (2013) Development of a multiplex real
PCR to differentiate Sarcocystls spp. affecting cattle. Vet
Parasitol 197: 85-94.
C
>­
Ol
0
0 to tvnlrll. lht two rnanliQnad ll)IGlea and a vartety
·wro
ro
0....
5.1.3 Order Cryptosporida
Family Cryptosporidiidae
Genus Cryptosporidium
r Disease: .Cryptosporidiosis.
----�...........__
Cryptos (G): hidden; sporo (G): semen, germ.
9'f'IUI Cryptosporj_dlum currently includes
�ad apecles that are considered valid
���'40 genotypes, but the taxonomy Is
�- Three subgroups are recognis
baiict n ffil:>lecular differences and oocyst
n,orphotogy. The epeclN/genotypes show different
hNt e'peOlftcltlea (e.g. C. homlnls is found almost
!lf!Ullvlly In humane whlr8as C. parvum has a broad
halt apedrum). Cryptoeportdla cause predominantly
Jnteltlnll lnfectlona In vertebratee. Some species are
zoonotlc agents. Members of the genus are impol'tant
cauaee of diarrhoea In calves, small ruminants and
lmmunooompromlsed humans.
• Life cycle. Direct developmental cycle. lr,ifectioo by
oral Ingestion of sporulated oocysts·,.two merqgonies
and gamogony in enterac di u de th&,:
lumlnal border line �At� 1�e����10 Rll��-Elttc
position): formation of spp I t con alnl
,.
four sporozoites wlilio rs1st r:1
Infections by endogenous a I actions.
• OCCUT'8nce, epidemiology. orl wet dTI ifbutlon.
li'ansmlsalon by means of contaminated feed, drinking
water or objects. Oocysts survive in tiumid envf ent
for months.
• Cllnloal llgne. Often unapparent Infections. In young
calves C. paMJm may cause catarrhallc enteritis with
watay or profuH diarrhoea, fever, exalecolls, acidosl8,
weight lou and, oocuionally, death. In other hosts,
partlcullrty In young anlmall, enterttll may be cauaed
by varloua CtyptoaporidJum apeclel. In birds, alao
lnftellonl of the� eyltem.
• DllgllCIIII. Demoollrat!CM of oocylt8 In faecal amwe
by tplOlal ltalnlng tlohnlqute (e.g. modified Zlehl­
tl11l11n ltllnlng) or mnlng with labelled antlbodlel:
• n.an
dlllutlorlofGOplQll1tlgw.DNAanalylil.
IIMI oantroL Symptomatic trNtment of
diarrhoel and exalooolll. TrNtment of calvea with
hlllofuglncn (lidl lffecla. rwn, w Nfety Index). Hygiene
ffllllltnl (cllenlng, dlllnfectlon), good huabandry '
practice. and coloatnm eupply.,. recommended.
• loono1lo lmportanoe. lnfectlona In humans with
14 C,,,,tarporiclum app. are documented. MOit
lnfectloM worldwide have been attributed to the
,aonadc ..,... 0. ptlMlffl and to C. homlnJa but
thl -- II pr1ldclnlnln� b■••·Hed tn,m IUiW1I
o l � IPldlO f1IIIY C8Ul8 .... enterltill
tn 1mrnunooampnHni patientl with oocaslonal
IK1nllnteetinlllnvofvement.
 5. Phylum Alveolata

Agent. Cryptosporidium spp. predominantly parasitise
the gastrointestinal tract and less frequently other
organs of mammals, birds, amphibia, reptiles and fishes.
Currently around 30 species are considered valid; in
addition >40 genotypes are known. Of the named
species, 18 are found in mammals, three in birds, three
in amphibia, and five in fishes. Based on molecular
differences, oocyst morphology and host specificities,
Oocysts of members of the 'gastric' group are oval and
relatively large (0 -7 µm), those of the 'intestinal' group
are round and generally smaller (0 -4-5 µm).
Cryptosporidia resemble coccidia but are evolutionarily
divergent and show relationships to gregarines, a group co
u
of endoparasites of invertebrates. Considerations ·c
0
Q_
on the taxonomic status of the Cryptosporidia are (/)

three subgroups can be distinguished: (1) a so-called

gastric group, parasitising the stomach of mammals,
birds and reptiles ( C. muris, C. andersoni, C. serpentis, C.
gnlli, C. fi·agile); (2) an intestinal group (including most
of the zoonotic species), parasitising predominantly the
small intestine of various vertebrate species. ( ► Table
5.7); and (3) a group infecting various marine and
freshwater fishes.
0
ongoing and re-evaluations may be necessary in the Q_
future. Compared with Eimeriida, Cryptosporiida �
0
show several peculiarities: (a) The various stages are
localised in epithelial cells in a parasitophorous vacuole
directly under the luminal borderline (intracellular
but extracytoplasmatic localisation) ( ► Figure
5.18}; (b) Cryptosporidia form a multimembranous
attachment layer, a feeder organelle at the base of the
parasitophorous vacuole connecting the parasite with the

Table 5.7. Cryptosporidium spp. (selection).

. I - -- "
Species Natural hosts1 Main locallsatlon
¥
Species in mammals
C. hominis 2 humans (monkeys) small intestine
C. viatorum humans small intestine
C. parvum3.4 cattle5 , other ruminants, humans, small intestine
rodents
C. bovis cattle, sheep small intestine
C. anderson/3 cattle6, other ruminants, camels abomasum
C. suis3•7 pigs small intestine
C. scrofarum 3 domestic and wild pigs small intestine
C. can/s 3 dogs, other canids small intestine
C. fe!is 3 cats, (cattle) small intestine
C. muris 3 mice various mammals, birds small intestine
C. fayer(J marsupials small intestine
C. cuniculus 3 rabbits, other mammals small intestine
C. wrairi guinea pig small intestine
C. ubiquitum 3 mammals small intestine
Species in birds
C. bailey/ chickens and various other birds respiratory tract, intestine, bursa fabricii
C. galli chickens, other birds stomach
C. meleagridis 3 turkeys, other birds intestine, also other organs
Species in amphibia and reptiles
C. fragile amphibia stomach, intestine
C. serpentis -· - snakes, lizards stomach
C. varanii6
-- ·- lizards, snakes intestine
Species in ti, ' -·-
C.moh.=.,; - marine fish stomach
C. cichi·;i_
··- --- freshwater fish stomach
1 Main hosts in i)cld.
2 Previously C. parvum 'human genotype'.
3 Zoonotic species, pathogenic in opportunistic infections.
4 Previously C. parvum 'bovine genotype', Syn: C. pastis.
5 Pathogenic in calves <3 weeks of age.
6 Heifers and older cattle.
7 Previously C. parvum 'porcine genotype'.
8 Syn: C. saurophilum.
 Part II. Parasites and parasitoses: protozoa

host cell cytoplasm, probably facilitating the exchange
of substrates(► Figure 5.18); and (c) Cryptosporidia
produce small oocysts which sporulate already within
the host cell, finally containing 4 'naked' sporozoites
without sporocyst. The oocysts are infectious to a host
at the time of shedding.
Life cycle. After ingestion of oocysts by a host the
released sporozoites infect enterocytes (preferentially at
the basis of the villi), form a parasitophorous vacuole and
develop to type I meronts(diameter 4-5 µm) with eight
merozoites. Merozoites either repeat this replication
step or develop to type II meronts, which contain
four merozoites each(► Figure 5.18 and 5.19). The
latter stages develop to gamonts. Syngamy results in
the formation of oocysts, which sporulate in the host
cell without forming sporocysts, i.e. oocysts contain
four 'naked' sporozoites. Release of sporozoites directly
within the host's intestine is thought to be responsible
for continuous endogenous autoinfections, for instance,
in immunodepressed hosts. Prepatency in calves lasts
3-6 days, and oocysts are usually shed for 1-2 weeks.

Mlcrogamonl

,' \"I '

� Mlcrngamete
/
Maroni II
Maroni I l I \

Sporozolte

Endogenlc cuJtolnfoctlon

Q)

·o
C

'6
Q)

cu
C
·c
Q)

j
_£;
>,
Ol
0
0
·w
cu
0.. Figure 5.18. Life cycle of Cryptosporidium parvum (Graphics: IPZ, S. Ehrat).

Figure 5.19. Cryptosporidium parvum: developmental stages
in the ileum of a calf (REM; Photos: J. Pohlenz).
The endogenous development usually takes place in the
stomach or small intestine. Aside from this, depending
on the parasite and host species and the immune
status of the host, other organs(respiratory tract, large
intestine, bile ducts, conjunctiva) may also be inhabited
by Cryptosporidia.
Occurrence, epidemiology. Cryptosporidia have
a worldwide distribution and are common parasites
of mammals, birds, reptiles, amphibia and fishes.
For instance, they have been demonstrated in > l 70
mammalian species, including humans, and in >70
reptile species. Many Cryptosporidium spp. have a
broad host spectrum and are transmittable, for example,
between mammals and birds, while others are more host
specific( ► Table 5.7). The occurrence of the various
parasite species and genotypes varies geographically.
Cryptosporidia are important causes of diarrhoea in
young calves (C. parvum), lambs and goat kids but
play a lesser role in other domestic animals. They are
common in healthy domestic animals, e.g. 20-80%
of clinically asymptomatic calves in Central Europe
shed Cryptosporidium oocysts at least temporarily.
Cryptosporidium spp. are important pathogens in
immunosuppressed humans. The general prevalence
in healthy persons in Central Europe is ~2-3%, and in
tropical countries~ l0%, but approximately 25% of AIDS
patients shed Cryptosporidium oocysts.
5. Phylum Alveolata
• Epidemiology in cattle. Major agents in cattle are C.
parvum, C. bovis, C. andersoni and a 'deer-like genotype:
Until weaning age, 85% of infections of calves(in the
U SA) are caused by C. parvum; however, C. parvum is
only found in I% of older animals and is replaced by
the other species. Sources of infection for new-born (1j
-0
·;::
calves are usually other calves. Oocyst excretion is most 0
-
Q_
common and most intensive at an age of l-2 weeks, Cf)
0
when up to I07 oocysts per gram faeces may be shed. 0.
Oocyst excretion ceases subsequently; calves older than c
0
3 months rarely shed C. parvum oocysts. Transmission
is facilitated by the fact that oocysts are immediately
infectious when they are excreted and relatively small
infection doses(~ 100 oocysts) are sufficient to induce
clinical disease in calves. Most infections are observed
in housed animals. Infections based on contact with
faeces of patent animals represent an important route
of transmission. Bad housing conditions may enhance
transmission, however, clinical cryptosporidiosis in
calves is sometimes also observed in weJJ managed
husbandry systems. Clinical cryptosporidiosis is rare
in cow-calf herds although high Cryptosporidium
prevalences are often observed in the calves.
Provided suitable moisture, Cryptosporidium oocysts
survive at 15-20 °C for approximately 3 months; they
remain infectious for about l year at 5 °C. Desiccation
and temperatures below -20 °C or above 65 °C are lethal.
Basically, the above-described epidemiological facts
may also hold true for other Cryptosporidium and
host species. In the case of birds, in addition to oral
transmission, aerogenic infections may also play a role.
Immunology. The early observation that human
HIV-patients with significantly reduced CD4 + T cell
levels suffer from severe disease after C ryptosporidium
infection, whereas in immunocompetent persons
the infection may cause at most only miJd, transient
diarrhoea, suggested an effective immunological control
of Cryptosporidium infections. It has been demonstrated
that both innate and adaptive immune responses are
important with IFN-y and a� co4 + T cells playing
crucial roles; cos + T cells are also involved but are of
minor importance in protection.
Attachment and infection of epithelial cells are
succeeded by recognition and induction of antiparasitic
responses(synthesis of iN OS, IFN-y, etc.; ► p. 37) and
triggering of adaptive immune mechanisms(Th 1 type
responses, which are necessary for complete elimination
of Cryptosporidia), and accumulation of immune cells
at the base of the intestinal villi. Humoral antibodies,
particularly maternal antibodies in colostrum, may have
some protective effects in calves, e.g. by shortening
the patency period. Convalescent calves are partiaJJy
protected against new infections, with immunity
maintained by continuous ingestion of oocysts.
 Part II. Parasites and parasitoses: protozoa

Pathogenesis. Cryptosporidiosis in immuno­

competent hosts is usually a self-limiting, unapparent
infection. In very young and old animals and in
immunocompromised humans (e.g. AIDS patients),
however, Cr yptosporidia, in particular those of the
intestinal group, may induce severe, long-lasting
diarrhoea and sometimes death. Proinflammatory
cytokines and chemokines are released early after
infection of enterocytes, resulting in catarrhalic enteritis
with fusion and atrophy of villi and hyp ertrophy of
the cr ypt epithelium. Damage to epithelial cells,
focal necroses, and infiltration of the lamina propria
by inflammatory cells are associated with enhanced
secretion and malabsorption. Concomitant infections
(e.g. in calves by rotavirus, coronavirus, ETEC,
Salmonella spp.) may boost the clinical consequences.

Clinical signs. In calves profuse diarrhoea, often

with light-yellow faeces. is the lead symptom of C.
parvum-induced cryptosporidiosis. In addition, animals
show anorexia, exsiccosis, acidosis, fever, apathy and
weakness. Most calves fall ill in the 1st-3 rd week of life,
suffer from diarrhoea for 4-7 days, and recover within
a few weeks, however, usually without cmnpensation
of developmental losses. Severe cases may be fatal. C.
andersoni infects heifers and adult cattle, predominantly
cows (prevalences up to 10%), which may continuously
shed oocysts. The endogenous stages infe1:t epithelial
cells of the fundic glands in the abomasum. Elevated
plasma pepsinogen levels, reduced milk yields and Figure 5.20. Cryptosporidium parvum: oocysts (5x4.5 µm)
loss of weight in beef cattle are reported as clinical in stained faecal smears of a calf (Photos: IPZ): (a) exclusion
consequences. staining after Heine; (b) modified Ziehl-Neelsen staining.

Clinical manifestations of cryptosporidiosis in other host

species depend on the specific localisation of the agents
( ► Table 5.7). C. baileyi causes respiratory symptoms in
birds and also infects the bursa fnbricii and the cloaca. In
some animal species and in immu.nodeficient humans,
Cryptosporidium spp. that are otherwise localised in
the inte tinal tract may be found in other organs (e.g.
caecum, colon, tomach, gall bladder, bile duct, pancreas,
uterus, trachea, lung , conjunctivae).
Diagnosis. Intra vitam diagnosis relie on the detection
of oocysts in faecal samples by special staining techniques
(e.g. modified staining after Ziehl-Neelsen, exclusion
(1)
C sta.iniog according to Heine) ( ► Figure 5.20) or by
u enzyme or fluorescein-t.agged monoclonal antibodies.
-0
CD Demonstration of coproanrigens has been proven and
�
� successfully tested. Commercial reagents and assays are
CD
C available. Attempts to demonstrate specific antibodies in
.:: plasma or serum are not of practical value. Parasites can
(D
Therapy and control. Treatment of diarrhoea and
exsiccosis takes priority in diseased calves. In endangered
herds, treatment with halofuginone (e.g. Halocur•) may
be considered (0. l mg/kg b.w. orally daily starting l
or 2 days after birth for 7 consecutive days (cave: very
narrow safety index).
To control cryptosporidiosis, calves, lambs and goat
kids should be supplied early and sufficiently with
colostrum. The environmental contamination with
oocysts and the transmission of oocysts must be reduced.
Hygiene measures (clean boxes for calving and calves,
separation of infected animals) may reduce the risk of
heavy infection for new-born animals. Disinfection is
possible by steam jet cleaning and application of selected
chemical disinfectants ( ► p. 571 ). Dryness in stables
supports elimination of oocysts.

j be found post mortem in Giemsa-staioed impression Zoonotic importance. Several Cryptosporidium

C smear (mucosa of the ileum) or HE-stained tissue species ( ► Table 5.7) and a variety of different genotypes
> sections. Species or genotype identification requires have been found in humans, with C. hominis and C.
0)
0 DNA analyses. Viral or bacterial infections need to be parvum being the most common species in Europe,
0
.....
(J')
considered in the differential diagnosis. occurring in similar frequencies. C. hominis generally
co
.... prevails in tropical and subtropical countries, although
co
a.. situations may differ regionally. Human infections by

other species ( C. meleagridis, C. cuniculus and others) are
rare. Dogs and cats are obviously not common sources
of human Cryptosporidium infections. A further species
infecting humans is C. viatorum, which has so far not
been found in animals. Infection rates in humans may
be generally underestimated because diagnosis is not
systematically performed, especially in cases of self­
limiting diarrhoea. Prevalences in healthy Europeans are
<3%. Diarrhoeic immunocompetent persons and AIDS
patients shed Cryptosporidium oocysts to >5% and >25%,
respectively. In contrast to immunocompetent persons
who may show an often mild, self-limiting disease,
although with common relapses, immunocompromised
patients may develop severe chronic, life-threatening
illness. The most important cause of human infection
with zoonotic Cryptosporidium spp. is direct or indirect
contact with infected animals (calves, lambs) and
contaminated drinking water. In a study in the UK,
C. parvum was more common in rural populations,
associated with animal exposure, and peaked in spring,
whereas C. hominis was more urban, associated with
young children (non-zoonotic transmission), and
peaked in late summer and autumn. In Switzerland C.
hominis infections were associated with travel history
in children with diarrhoea.
Selected references tElmL�'"'.:·w.,•..i ��.!" >,., ,1
Abeywardena H, Jex AR, Gasser RB (2015) A perspective
on Cryptosporidium and Giardia, with an emphasis on
bovines and recent epidemiological findings. Adv Parasitol
88: 243-301.
Al Mawley J, Grinberg A, Prattley D, Moffat J, Marshall J,
French N (2015) Risk factors for neonatal calf diarrhoea
and enteropathogen shedding in New Zealand dairy farms.
Vet J 203: 155-160.
Caccio SM, Widmer G (eds.) (2014) Cryptosporidium: parasite
and disease. Heidelberg, Germany: Springer. ISBN 978-3-
7091-1562-6.
Checkley W, White AC Jr, Jaganath D, Arrowood MJ,
Chalmers RM, Chen XM, Fayer R, Griffiths JK, Guerrant
RL, Hedstrom L, Huston CD, Kotloff KL, Kang G, Mead
JR, Miller M, Petri Jr WA, Priest JW, Roos OS, Striepen
B, Thompson RC, Ward HD, Van Voorhis WA, Xiao L,
Zhu G, Houpt ER (2015) A review of the global burden,
novel diagnostics, therapeutics, and vaccine targets for
Cryptosporidium. Lancet Infect Dis 15: 85-94.
Delafosse E, Chartier C, Dupuy MC, Dumoulin M, Poss I,
Paraud C (2015) Cryptosporidium parvum infection and
associated risk factors in dairy calves in western France.
Prev Med Vet pii: SO167-5877(15)00020-3.
Dreelin EA, Ives RL, Molloy S, Rose JB (2014) Cryptosporidium
and Giardia in surface water: a case study from Michigan,
USA to inform management of rural water systems. Int J
Environ Res Public Health 11: 10480-10503.
5. Phylum Alveolata
Glaser C, Grimm F, Mathis A, Weber R, Nadal D, Deplazes
P (2004) Detection and molecular characterization of
Cryptosporidium species isolated from diarrheic children in
Switzerland. J Ped Infect 23: 359-361.
Gormley FJ, Little CL, Chalmers RM, Rawal N, Adak GK
(2011) Zoonotic cryptosporidiosis from petting farms. England m
TI
·.::::
and Wales, 1992-2009. Emerg Inf Dis 17: 151-152. 0
Q.
Meganck V, Hoflack G, Opsomer G (2014) Advances in (/)
0
prevention and therapy of neonatal dairy calf diarrhoea: a E
Q)
systematical review with emphasis on colostrum management m
and fluid therapy. Acta Vet Scand 56: 75.
I
Slapeta J (2013) Cryptosporidiosis and Cryptosporidium species
In animals and humans: a thirty colour rainbow? Int J Parasitol
43; 557-570.
fhompson RC, Ash A (2015) Molecular epidemiology of Giardia
and Cryptosporldium infections. Infect Genet Evol pii: S1567-
1348(15)00404-9.
Young I, Smith BA, Fazll A (2015) A systematic review and
meta-analysis of the effects of extreme weather events and
other weather-related variables on Cryptosporidium and
Giard/a In fresh surface waters. J Weather Health 13: 1-17.
5.2 Class Haematozoea
Haima (G): blood; zoon (G): creature, animal.
The class contains blood parasites (including the agents
of human malaria) and other Haemosporida as well as
Piroplasmida as important animal parasites.
5.2.1 Order Haemosporida
Haemosporida are heteroxenous protozoa that develop
in vertebrates (merogony and gamogony) and in
haematophagous insects (syngamy and sporogony). In
vertebrates, merogony occurs in tissue cells or, in the case
of Plasmodium spp., also in erythrocytes. Intracellular
stages are enclosed by a parasitophorous vacuole. Motile
zygotes (ookinetes) are formed in insects. Haemosporida
and other Haematozoea differ from other Apicomplexa
by possessing a reduced apical complex, i.e. sporozoites
and merozoites lack a conoid ( ► Figure 5.1, p. 79).
Family Plasmodiidae
Genus Plasmodium
Plasma (G): plasm, image; -eides (G): similar.
 Part II. Parasites and parasitoses: protozoa
rocytes. The sexual ce In fem
ultoes, whldh tnmsmlt the agentssto verteb
e most Important disease caused by P.lasmodiu
p Is human)Tialarla, Important animal P.lasmodlu
ections concem fowl-llke birds In the ttoples. M
nlc lq, their aln n t
re dleeasea n terna v
osts. ea enera eucoc n
Haemoproteus, H ce
In
■ Malaria in humans
i Genuine human malaria agents are Plasmodium vivax,
I !
.· ' P. ovale, P. malariae and P. falciparum. P. malariae is
zoonotic, occurring also in various monkeys; the other
I
111
species are specific to humans. Another zoonotic species
I : is P. knowlesi, which is common in natural infections
in humans and monkeys in South East Asia. The major
I
l,;, 1 types of human malaria are (agents in parenthesis):
Malaria tertiana (P. vivax, P. ovale), Malaria quartana (P.
malariae) and Malaria tropica (P.falciparum). Several
other Plasmodium species can infect humans but are of
minor importance. P. falciparum is the most pathogenic
species causing severe disease and deaths, particularly
in children in endemic regions and in persons from
non-endemic areas.
Human malaria is a common disease in tropical Africa,
Asia, Oceania, Central and South America and in the
Caribbean. WHO estimated the annual number of
malaria cases in 2013 at 198 million (range: 124-283
million) and of associated deaths at 584,000 (range:
367,000-755,000). Since 2000, malaria mortality rates
have fallen by 47% globally, and by 54% in the African
Region. Most deaths occur among chi.ldren living in
Africa where every minute a child dies from malaria.
Malaria mortality rates among children in Africa have
decreased by an estimated 58% since 2000.
Q.l
C In natural cycles, malaria is transmitted to humans
·u exclusively by female mosquitoes of the genus Anopheles.
"O
Q.l
�
After inoculation of sporozoites by a mosquito,
the parasites develop to meronts in hepatocytes.
ro Subsequently, the merozoites generated by this process
C
·c: infect erythrocytes and start further merogony cycles
Q.l
+-'
that are associated with fever attacks. Some merozoites
C develop into gamonts, which are taken up by blood­
>,
CJ)
feeding mosquitoes in which syngamy and sporogony
0 take place, leading to the formation of sporozoites.
0
+-'
.iii Sporozoites are transmitted to new hosts in the course of
the insect's subsequent blood meals. Transmission is also
ro
CL possible by blood transfusion. Stays in malaria endemic
areas require preventive measures (chemoprophylaxis,
protection from mosquito bites).
■ Malaria in animals
Numerous Plasmodium species, which are transmitted
by Culicidae, are known to infect reptiles, birds and
monkeys. Approximately 30 Plasmodium species have
been described in ca. 500 bird species but rarely cause
disease in their specific hosts, for instance P. praecox,
which occurs worldwide in passerine birds. In contrast,
a broad spectrum of imported, exotic birds (owls,
penguins and others) fall ill relatively often from P.
praecox infections, e.g. in European zoos. P. gallinaceum
and P. iuxtanucleare are pathogenic parasites in domestic
chickens in tropical regions. Monkeys of the family
Cebidae in Central and South America are frequently
infected with P. brasilianum and P. simium. Old World
monkeys, predominantly macaques, are also often
carriers of plasmodia (P. cynomolgi, P. eylesi, P. inui,
P. knowlesi); P. schwetzi infects chimpanzees in Africa.
Under natural conditions, these infections in monkeys
are generally asymptomatic or, at most, cause mild
symptoms such as fever or loss of appetite. Monkey
malaria serves as a model infection for human malaria;
laboratory infections may occur in exposed personnel.
Genus Leucocytozoon
Leucocytozoon spp. (L. simondi, L. smithi and others)
are parasites of wild birds (finches, corvids, owls, etc.)
but may occasionally also cause illness in domestic
poultry (ducks, geese, pigeons, turkeys). Indigenous
lethal infections have been reported from Europe in
common pet parakeets. Simuliidae are natural vectors
for sporozoites. In birds, small meronts (20 µm in
diameter) develop in hepatocytes. Subsequently, larger
meronts (up to 500 µm), which contain numerous small
( ~ l µm) merozoites, are generated in cells of various
parenchymatous organs. These merozoites enter the
blood stream, infect leucocytes (in some species also
Immature erythrocytes) and develop into gamonts which
are taken up by the blood-sucking Simuliidae, in which
sporozoites develop after syngamy.
Genus Haemoproteus
Birds and reptiles are vertebrate hosts; Hypoboscidae
and biting midges ( Culicoides spp.) function as vectors.
Infections are common in pigeons (Haemoproteus
columbae), ducks and turkeys but are generally
asymptomatic. Merogony occurs in endothelial cells of
blood vessels, gamonts develop in erythrocytes.
Genus Hepatocystis
Species of the genus are mainly parasites of African
monkeys (e.g. Hepatocystis kochi, H. simiae) but also
occur in some other animals, e.g. hippopotami. Vectors

are Ceratopogonidae. Hepatocystis spp. form huge
meronts in hepatocytes (up to 4 mm in diameter);
subsequently (without preceding merogonies), gamonts
develop in erythrocytes.
1 Selected references
Clark NJ, Clegg SM, Lima MR (2014) A review of global diversity
in avian hemosporidians (Plasmodium and Haemoproteus):
new insights from molecular data. Int J Parasitol 44: 329-338.
Cox FE (2011) Babesiosis and malaria. In: Palmer SR, Lord
Soulsby EJL, Torgeson PR, Brown DWG (eds.). Oxford
textbook of zoonoses. 2nd edition, Oxford, UK: Oxford
University Press, pp. 589-595. ISBN 978-0-19-857002-8.
Krone 0, Waldenstrom J, Valkl0nas G, Lessow 0, MOiier
K, lezhova TA, Fickel J, Bensch S (2008) Haemosporidlan
blood parasites in European birds of prey and owls. J Parasitol
94: 709-715.
5.2.2 Order Piroplasmida
Pirum (L): pear. Refers to the pear-shaped merozoites
in erythrocytes.
The families Babesiidae and Theileriidae of the order
Piroplasmida are the most important blood parasites
of domestic mammals. Piroplasmida are transmitted
by Ixodidae (only one species by argasid ticks). In
mammals Babesia spp. replicate by merogony exclusively
in erythrocytes whereas Theileria spp. multiply in
mononuclear leukocytes (predominantly lymphocytes)
and subsequently in erythrocytes. The intracellular
stages develop directly in the cytoplasm of the host cell
without forming a parasitophorous vacuole. Gamogony
and sporogony occur in the ticks. The gametes are
characterised by long processes and are referred to as
ray-bodies.
Family Babesiidae
Genus Babesia
Disease: Babesiosis.
Victor Babes: Romanian veterinarian, detected Babesia
in cattle (1888).
I •
Summary
Agents. Babesia spp. (>100) parasitise erythrocytes
of many mammalian species. Only a few species are
found in birds. They cause diseases in cattle, sheep,
equids, dogs and other animals.
...
5. Phylum Alveolata
vartau1 cell Of the vlOtOr. n,� ttwtovirtei fn
� tlektltUe�lng,__,IN��
lll!Onoftl'll�to the nect ti�
�ldftlttt lnf,ot the l8ftvan, GlancM nunwoue
n prc,dl.lotd (,porogcmyj which can be
lttld to a l'ltW l'IOlf,
noe. __,_.,.,,,. rn doftleitlc mammal•
art widely dlltl'lbutld, partfeularty In IUbtroplcal and
troplcal ar111 withs. blgemlna and S. bovla ae the moet
Important speclN In cattle (► Table 5.8). In Europe
B. dl�na (tranemltted by lxodes rtclnu1) occurs
regloriilly, S. maJor (vector: Haemaphyssl,. punctata) '
Is ecarce. Sheep are host of B. ovla and S. motal.
B. canls In dogs (vector: Dermscentor retlcultltua) 19
endemic In southern and eastern Europe with some
foci In Central Europe. Furthermore, S. VOf/81/ ocan
in southern Europe. Babeslosls In horaee, caused by 8.
cabal/I, occurs in western, southern and eastern Europe,
and cases are occasionally Imported to non-endemic
European regions.
• Epldemlology. In Europe lxodid ticks are mostly focally
distributed and show seasonal activity whereas year­
round activity prevails In tropical and subtropical
areas. Babeslae may persist In tick populations for 3-4
generations due to vertical (transovarlal) transmission,
followed by stage-to-stage transmission. In populations
of grazing animals Babesla Infections often persist In a
status of endemic stablllty (► Glossary, p. 620).
• Immunology. In mammals humoral and cellular Immune
mechanisms limit the parasltaemla, which may persist
for months to years. Concomitant immunity protects
against clinical babeslosls.
• Cllnloal 1lgn1. Major cllnlcal signs In acute Infections
Include apathy, high fever, anorexia, anaemia, sometimes
haemogloblnurla, Jaundice, and neurological disorders. 1
The chronic Infection Is usually asymptomatic.
• Diagnosis. Case history (tick Infestation, stay In
endemic areas) and clinical signs provide clues for a
preliminary diagnosis. Aetiological diagnosis: detection
of parasites in Glemsa-stalned blood smears (caplllary
blood) Is mostly successful in acute disease, but less
reliable in chronic cases. A sensitive alternative is
DNA analysis of a blood sample. Serology for specific
antibody detection (IFAT, ELISA, other assays) In
unapparent, subac1:1te and chronic Infections.
Therapy. Acute babeslosls Is an emergency case.
Chemotherapy In cattle, horses and dogs with
lmldocarb (licensed only In some European countries).
Caution: side effects of lmldocarb and shoe -like
ctlons after treatment. Palllatlve m
ently recommend
T
 Part II. Parasites and parasitoses: protozoa

0.3-5 µm long merozoites, which are usually pairwise

located in erythrocytes (rarely more than two stages)
(► Table 5.8; ► Figure 5.21). Besides this, there are also
other forms (see life cycle). Based on the morphology of
the merozoites, babesiae are described as 'large species'
(>2.5 µm long) or 'small species' ( <2.5 µm long). Various
genotypes are known in addition to the named species.

Life cycle. In the natural cycle infection of vertebrates

Agents. Babesia spp. infect vertebrates; most species
are found in rodents, carnivores and ruminants, a
few species also in birds. All domestic mammals may
be hosts of particular Babesia species ( ► Table 5.8).
Characteristics are drop- or pear-shaped, mononuclear,
with Babesia spp. occurs through the bite of ixodid ticks
(► Figure 5.22). Inoculated sporozoites exclusively
infect erythrocytes where they initially develop to ring­
shaped or amoeboid trophozoites that multiply asexually
by binary fission, forming mostly two drop- or pear­
shaped merozoites. They are released from the host cell

• •' o:,
�:\,
- ..
I•

a Babesia bigemina b Babesia major C Babesia bovis

d Babesia divergens e Babesia ovis f Babesia caballi

Q)
TC
5
'6
Q)
�
�
cu
C
·;::::
Q)

C
>,
Ol
0
0 g Babesia canis h Babesia gibsoni
·u5
cu Figure 5.21. Babesia spp. in Giemsa-stained blood smears (characteristics of the species ► Table 5.8 ) (Photos: a-d, g, h:
co
a.. ITPB, E. Schein; e, f: IPH , K. F.).
 5. Phylum Alveolata

Table 5.8. Babesia species in domestic and wild animals (selection).

Hpst Sebeela ep. Merozottee Vectot'92 Pathoget\lcity3 O.Ographlc distribution

.,
.,
IAngth AnQle1 Poetuon ln
wm>
.I
e,ytt,�.
··- C'Cl

acute central Tropics and subtropics

"O
Cattle B. bigemina 4-5 Rhipicephalus I++ 1
(Boophllus) spp., 1 (Africa, Asia, Australia,
I=?. evertsl I America), southern
C'Cl
0..
- --- - -- - · Europe
t s� 8. big�mina
J 0
ci
obtuse central
---· -----
B. bovis -2.4 Rhlpicephalus (B.) +++
- - spe.:____ - -
B.divergens -1.7 obtuse marginal lxodes ricinus; Europe
I
++
northern Europe:
>--·---- - ----� -- I. per�_0catu� - --- ----
I Europe, Asia
B. major 3.3-3.5 acute central Haemaphysalls
/
+
- - ----
B. ovis
- --- -- - .. -- _ (JtJ_:!ctata- - -
---+ -----
Sheep, 1.5-2.5 acute central e.g. Rhlpicephalus +++ ; southern Europe, Africa,
goats ·--- - -- -·- --·· ----·--- ----
bursa - -- I Asia
B. motasl acute
-
central
- ·-
southern Europe, Africa. I
(virulent)
3.4
--
H. punctata
---
++
a I
r
� ----- - ---- ------ - -
B. motasi - Europe
(avirulent)
H. punctata
I
Equids B.caballi 2.5-4 acute central Oermacentor spp., +++ 1 Tropics and sub-tropics
Hyalomma spp.4 (except Australia, USA,
Japan), Europe
Wild B. capreoli 1.5-2.4 obtuse mostly I. ricinus? + Central Europe
ruminants marginal - --·
B. venatorum5 1.5-2.4 obtuse mostly I. ricinus? + Central Europe
marginal --
Dogs, B. canis 4-5 acute central Dermacentor I++
+ southern and eastern
other reticulatus I Europe, foci in Central
canids
B.vogeli 4-5 acute central
- --- --
Rhipicephalus
l
I
+
Europe
southern Europe, tropics
sanguineus (Africa, America, Asia,
.. - --- Australia)
B. rossi 4-5 acute central Haemaphysalis +++ South Africa
leach/ (syn.
H.elliptica)__ ------ -
B. gibson,f3 1-2 (3) . central R. sanguineus, ++ USA (California), Asia,
H. bispinosa northern Africa, Europe
B. conradae 1-2 . central R. sanguineus? ++ USA (California)
B. annae 7 1-2 . central I.hexagonus? ++ southern and Central
Europe, North America,
Israel
Cats B. felis 0.3-0.9 MK central H. leachi (syn. + South Africa, Zimbabwe
--------- .
H. elliptica)
Rodents B. microti 1-3 MK central I. ricinus, ? Central Europe
Q)
I. trianguliceps C
·c3
/. scapularis ++ North America
Q)
1 Acute: angle between members of a pair of merozoites is small; obtuse: angle is large; MK: Maltese cross.
2
2 ?: questionable or unknown.
3 Degree of pathogenicity: +++ high, ++ moderate, + low. C'Cl
4 In southern Russia, probably Rhipicephalus bursa. C
·;::
5 Previously Babesia sp. EU-1.
6 Probably a complex of species, other vectors in East and South Asia.
7 Previously Theileria annae, proposed new name Babesia vulpes. C
>,
Ol
0
0
·u5
C'Cl
C'Cl
Cl..
Part II. Parasites and parasitoses: protozoa
Hard tick
Sporogony
.....___
Salivary gland of L, N, A
Figure 5.22. Developmental cycle of Babesia vogeli (L: larva, N: nymphal stage, A: adult stage of Rhipicephalus sanguineus)
(Graphics: IPZ, S. Ehrat, modified by S. Amrein).
and enter other erythrocytes. In this way the parasites
may persist for years in the blood of a host. Some
merozoites transform into spheroid stages, the gamonts.
Blood-feeding female ticks ingest infected erythrocytes
which disintegrate in the tick's intestine. Whereas
the released merozoites are digested, the gamonts
differentiate into gametes, the so-called ray-bodies
that are characterised by thin, cytoplasmic processes
(described 1906 as 'Strahlenkorper' by Robert Koch). By
Gamogony
---:::='<---=..- Spheroid
stage
Gametes
=----F,..'1-- Zygote
Tick intestine �
fusion of two uninucleate gametes (syngamy), a zygote
is formed. Zygotes enter intestinal cells, multiply and
form sporokinetes which pass into the haemolymph and
infect subsequently haematocytes and cells of various
organs in which further multiplications occur. Following
the infection of ovary and oocytes Babesia stages may
be transmitted in the egg (transovarial transmission) to
the next tick generation (vertical transmission). After
the hatching of a tick from an infected egg, sporokinetes

infect salivary gland cells in which sporozoites are
produced that can be transmitted to a vertebrate host.
Due to vertical transmission to 3-4 daughter generations,
tick populations may remain infected for several years
in the absence of Babesia-infected mammalian hosts as
infection sources.
However, vertical transmission is limited in that only
~ 10-20% of the eggs are infected and egg production
of infected females is reduced when compared with
uninfected ticks. Nevertheless, vertical transmission is
an essential pathway in the epidemiology of babesiae.
The transmission modes of the various Babesia species
are very complex, particularly in 1- and 2-host ticks
( ► Chapter 14.1.1, p. 396), and must be considered
separately for the respective species. Some (atypical)
Babesia species (babesiae of rodents, 'small' species
in canids and felids) which are genetically related to
theileriae, are not transmitted transovarially, but only
transstadially.
Occurrence and epidemiology. General
information on the geographic distribution of Babesia
spp. is listed in ► Table 5.8. Apart from climate and
environmental conditions the tick populations and the
mammalian hosts play a central role in the epidemiology
of babesioses. Only vector-borne Babesia infections
are epidemiologically important; transplacental (e.g. B.
caballi, B. canis) or iatrogenic transmissions are rarely
observed.
• Spatial distribution patterns of ticks and
Babesia spp. Tick species live in special habitats
(► Ixodida, p. 396). This explains the usually focal
occurrence (natural foci) of particular tick species and
their restriction to particular areas. In such foci certain
Babesia spp. may persist for many months within tick
populations by transovarial transmission (see above).
Infection rates in ticks have been previously estimated
at >1% in case of B. divergens and at ~0.04% in case of
B. bovis. In recent years ticks have been examined for
the presence of species-specific Babesia DNA. Positive
findings indicate that the ticks had contact with Babesia­
infected vertebrates recently or some time ago. For
example, a study in eastern Poland revealed that 2.8%
of 853 Ixodes ricinus ticks were positive for B. microti,
1.2% for B. venatorum, and 0.2% for B. divergens. In
Norway 0.9% of 1,908 I. ricinus indicated the presence of
a Babesia species (B. venatorum, B. divergens, B. capreoli
and an undescribed species). Of a large number of I.
ricinus ticks collected (2009/2010) in public parks in
different Bavarian cities, 0.4-0. 7% contained Babesia
DNA (B. venatorum [syn. EUl], B. divergens, B.
divergenslcapreoli). In Belgium Babesia DNA was found
in up to 14% of I. ricinus. In the Netherlands 1.64% of 855
Dermacentor reticulatus were positive for B. canis, and a
few ticks for B. caballi (one infected tick from Belgium).
5. Phylum Alveolata
Hard ticks harbouring developmental stages of babesiae
can survive long starving periods and, depending on
the species, periods of dryn ess or cold. This explains
the occurrence of babesiae in arid environments or in
areas of cold climates up to north of the Arctic Circle.
• Spreading of babesioses. Spreading from
endemic to non-endemic areas is possible by displace­
ment of animals carrying Babesia spp. and/or ticks. Thus,
Boophilus ticks have been transferred to the Americas
and to Australia in past centuries and now number
amongst the most important parasites of cattle on these
continents. Likewise, Rhipicephalus sanguineus and
Dermaceritor reticulatus, which are important vectors
of babesiae, became endemic in suitable habitats in
Central Europe. Migrating birds can transport ticks over
long distances, including ticks containing Babesia DNA.
• Seasonal occurrence of babesioses. The
seasonal occurrence of babesioses is highly variable
depending on the areas and the transmitting tick species.
For example, Ixodes ricinus, the vector of B. divergens
of cattle, shows a bimodal seasonal activity in Central
Europe. Correspondingly, outbreaks of babesiosis in
grazing animals are predominantly observed in May and
June as well as in September and October. Dermacentor
reticulatus, which transmits B. canis, shows activity from
March until June and from September to November,
sometimes until December. Therefore, infections of dogs
may occur relatively early and relatively late in the year.
Seasonality of babesial infections in the tropics is less
distinct since certain tick species are active year-round
in these regions.
• Parasite reservoirs in mammals. The principal
hosts of the various Babesia species ( ► Table 5.8)
represent parasite reservoirs, particularly in the chronic,
asymptomatic phase of the infection. For example, on
Belgian farms 11-20% of cows tested in spring, summer
and autumn were seropositive for Babesia spp. Wild
anin1als may also serve as reservoirs. For example, B.
divergens has been found in wild ruminants, including
roe deer, red deer, mouflon, and reindeer, but some of
these findings need to be confirmed. Generally, current
knowledge of the epidemiological role of wildlife is
limited but respective studies using molecular techniques
Q)
are ongoing.
·u
C
'6
• Incidence of babesioses. The incidence of Q)
�
clinical babesioses in grazing animals, e.g. cattle, is low
under conditions of endemic stability. This may develop cu
C
when cattle are infected in the first 9 months of life. ·c
Q)
Throughout this period, the animals are protected by
an age-related resistance so that parasite transmission C
by infected ticks usually results in low parasitaemia >,
CJ)
without clinical signs. In contrast, disease is regularly 0
0
observed when young animals grow up under tick free .ui
conditions and are exposed to infected ticks at an age of
cu
>9 months. Age-related resistance to babesiae is largely a..
 Part II. Parasites and parasitoses: protozoa
limited to bovines and horses. Small ruminants and dogs
are generally sensitive to Babesia infections throughout
their life.
Immunology. The reasons for the low susceptibility
of young cattle and horses are not fully understood.
Maternal antibodies are apparently not involved as calves
are resistant to babesiosis independently of whether the
mother was exposed to Babesia spp. or not. Particular
plasma factors in calves may play a role. Likewise, a
more effective and fast-acting innate immune response
to babesiae is thought to occur in calves (characterised
by rapid IL-12 and IFN-y synthesis) when compared
with adult cattle. The spleen plays an essential role since
splenectomy of infected calves is followed rapidly by an
exacerbation of the infection.
Primary Babesia infections induce partial immunity,
which does not fully prevent infections but protects
from disease for a certain period of time. It is a
concomitant type of immunity. Primary infections
without superinfections persist for a few months, up
t to 1 year (B. motasi, B. caballi), rarely for 2-4 years (B.
I
L
I divergens, B. bovis). Subsequently, a short period of
sterile immunity may develop but disappears in the
absence of new infections.
The immunological elimination of babesiae mainly
occurs by sequestration of infected erythrocytes in the
spleen by activated macrophages and by phagocytosis
of free merozoites and infected cells after opsonisation
by specific antibodies (in cattle, predominantly IgG2).
In the case of B. bovis, the immunodominant antigen,
VESA I ( Variable Erythrocyte Surface Antigen I), plays
a crucial role. It is expressed on the surface of infected
erythrocytes and mediates adherence of infected cells
to endothelial cells of capillaries and postcapillarial
vessels. It seems to be a mechanism that prevents the
erythrocytes from being captured in the spleen, thus
protecting the infected cells from early sequestration.
VESAl is encoded by a multigene family (ves) and
underlies clonal variation. Obviously, it is part of the
immune evasion strategy of the parasite, enabling it
to continuously change the surface antigenicity of
infected cells( ► Chapter 1.5, p. 25).
Pathogenesis and clinical signs. The clinical
manifestation of Babesia infections is determined by
the pathogenicity of the species, the virulence of the
particular parasite strain, and the age and immune
status of the host. Infections may be asymptomatic or
become clinically manifest, mostly as acute or even
peracute disease, partly with high case fatality rates.
Acute babesiosis is associated with apathy, often high
fever, anorexia, parasitaemia, haemolytic anaemia,
thrombocytopenia, haemoglobinuria, icterus, circula­
tory disorders (oedemas, shock), and neurological
disorders, resulting in a multiple organ dysfunction
syndrome (MODS). Some of th.e symptoms are only
caused by particular species or occur only irregularly
or temporarily (e.g. haemoglobinuria, neurological
disorders).
Mechanisms of pathogenicity have been mainly studied
in B. bovis infections and Babesia infections of dogs.
They are complex and only partially understood. Some
aspects are discussed below.
• Anaemia and haemoglobinuria. Anaemia and
haemoglobinuria are common clinical signs. Lysis of
erythrocytes due to an enhanced osmotic fragility of
parasitised cells and cell damage during parasite release is
one of the important mechanisms. An immunologically
mediated lysis by anti-erythrocyte antibodies seems
probable in B. gibsoni and B. vogeli infections but may
be insignificant in B. canis infections. There is evidence
that oxidative stress and a haemolytic factor (in B.
gibsoni infection) may contribute to erythrocyte lysis.
Lysis is accompanied with increased phagocytosis of
erythrocytes by macrophages.
• Systemic inflammatory reactions. Systemic
inflammatory reactions associated with disseminated
intravasal coagulation (DIC) may be involved, as
shown in canine B. canis infections. Enhanced platelet
aggregation and degranulation and release of vasoactive
molecules reduce blood pressure and explain the acute
or peracute course of the disease and hyp otensive shock
reactions.
• Cytoadherence. Cytoadherence is an important
factor in the pathogenicity of B. bovis infections (see
immunology above: VESA I antigen of the ves family).
Infected erythrocytes accumulate in the capillaries of
various organs (brain, kidney and others), hampering
blood circulation and causing arterial occlusions with
post thrombotic acidosis. Cerebral disorders and MODS
may result.
• Neurological disorders. Neurological disorders,
which are rare in B. canis but more frequent in B.
rossi infections, have another pathogenesis than the
one described for B. bovis (see above). In dogs they
are a result of hypoglycaemia or tissue hypoperfusion,
resulting in tissue hypoxia and hypermetabolism (and
signs of azotaemia).
• Fever. The development of fever correlates with the
concentration of specific parasite antigens in serum.
These antigens and other components, released during
lysis of erythrocytes, are considered to induce fever.
For further information on Babesia spp. in various host
species see below.

Diagnosis. Case history (tick infestation, stay in
endemic areas) and symptoms (fever, paleness, possibly
haemoglobinuria) may justify a preliminary clinical
diagnosis. Direct demonstration of parasites in Giemsa­
stained blood smears is usually limited to cases of acute
babesiosis. Differentiation of 'large' and 'small' Babesia
spp. according to the lengths of the merozoites (larger
or smaller than the erythrocyte radius), angular pitch
(pointed or obtuse), and position within the erythrocyte
(central or peripheral) ( ► Table 5.8; ► Figure 5.21)
may provide species-specific diagnoses. Sensitivity
of parasite detection can be improved by preparing
smears with erythrocytic material obtained directly
from the border of the huffy coat after microhaematocrit
centrifugation (infected erythrocytes accumulate in that
layer). Serology is not usually helpful during the acute
phases since seroconversion needs 2-3 weeks p.l. but
gives reliable results in chronic unapparent infections.
In several countries, import or export of horses requires
serological investigations by accredited laboratories and
prescribed tests (e.g. USA) to preclude the introduction
of piroplasm-infected horses. In any case, DNA analyses
allow sensitive diagnoses and species differentiation.
Therapy. Acute babesiosis is a medical emergency.
Therapy must be started as early as possible. High
parasitaemia and severe clinical symptoms imply a poor
prognosis. High parasite density includes the risk of
treatment-induced fatal shock reactions. Imidocarb is
recommended for treatment of Babesia-infected cattle,
horses and dogs. The clinical course after treatment
may be complicated; therefore, treatment should
be performed by experienced clinicians. Common
side effects of imidocarb are salivation, lacrimation,
restlessness, colic and others (antidote: atropine).
Generally, palliative measures are recommended
for treated animals (e.g. in dogs, shock therapy and
rehydration). The effect of imidocarb against 'small'
babesiae is not always satisfactory. A combination of
atovaquone and azithromycin or buparavaquone has
been described as more effective for small Babesia
species in dogs (off-label treatment).
Control measures. Control measures are described
below.
5. Phylum Alveolata
Babesiosis in cattle
B. bovis and B. bigemina occur in tropical and subtropical
areas of various continents, including southern Europe
( ► Table 5.8). B. divergens is regionally endemic in
Europe, whereas B. major was hitherto rarely reported in ctl
"O
western and southern Europe, but has recently also been .E
found in Hungary. Other Babesia species in cattle ate B. (/)
ctl
ovata (Asia), B. beliceri (Russian Asia), and B. occultans
e
0.
(South Africa, recently Italy). B. orientalis parasitises 0:::
predominantly water buffaloes in Asia.
Babesia divergens
··· e:,Babesloals In cattle, haemoglObinuria ,ni
cattle. ti:
Agent. B. divergens is a small babesia (1.7x0.4 µm);
paired, divergent forms are found in marginal positions
in the erythrocyte ( ► Figure 5.21; ► Table 5.8).
Occurrence. B. divergens occurs focally or regionally
in the distribution areas of I. ricinus and J. persulcatus
in Europe from Finland to the Mediterranean Sea, in
Turkey (Black Sea Coast), and in regions of higher
altitude in the Near East (Lebanon Mountains) and
North Africa.
Epidemiology. I. ricinus is the vector of B. divergens
in western and Central Europe, and /. persulcatus
in northern Europe. Infections are often limited to
particular pastures (close to forests and scrubland)
of individual farms or to larger areas, e.g. valleys in
mountainous regions.
Clinical outbreaks are rare in areas of endemic
stability where all animals are usually infected and
are concomitantly immune to infections. Under such
conditions, clinical disease is generally limited to
bought-in heifers and older non-resistant animals. Single
or repeated outbreaks may be due to temporary tick
habitats, e.g. after introduction of ticks by birds, deer,
etc. Disease outbreaks are mainly observed in May,
June and September, the main periods of activity of the Q)
various tick stages. B. divergens infections in cattle are C
·o
known to occur in many European countries (e.g. FR, '6
IE, BE, CH, DE, AT, IT, HU, PL) but reliable data on the Q)
current general incidence are lacking.
cu
C
·;;::
Clinical signs. The incubation period lasts 8-15 days. Q)
Calves show mild symptoms (age-related resistance),
cattle of the second grazing period, without previous C
exposure, develop acute disease. With increasing
parasitaemia, animals present with fever up to >40 °C,
malaise, impaired general condition, anorexia and, in
dairy cows, significantly reduced milk yields, anaemia
 Part II. Parasites and parasitoses: protozoa
and haemoglobinuria, followed by icterus, tachycardia
and atony of the rumen. Deaths may occur.
Babesia major
Small endemic foci are observed in areas where the
vector Haemaphysalis punctata is present(UK, NL, FR,
HU, eastern Europe; in DE only on some North Sea
islands). Infections cause almost no clinical signs.
Babesia bigemina
•1
rDisease:-Ca�le tick ��ver, red water �e�e;, Texa�
fever (the disease in Texas has since been
eradicated).
Agent. B. bigemina is a large Babesia(4-5x2 µm), lying
in pairs at an acute angle. Round or irregularly shaped
forms may also be found in the course of replication
(► Figure 5.21).
Occurrence, epidemiology. B. bigemina is found
in tropical and subtropical areas of Africa, Australia,
L Central and South America and, sporadically, in
southern Europe(the Balkans, coastal areas of other
Mediterranean countries, PT). Infections have also been
reported from water buffaloes and some wild ruminants.
Transmission occurs by Rhipicephalus (Boophilus)
microplus, R. (B.) decoloratus, R. (B). annulatus and
R. evertsi.
Clinical signs. Asymptomatic infections or weak
symptoms are observed in areas of endemic stability.
In other cases, the incubation period lasts 8-15 days.
Virulent strains cause high fever, haemoglobinuria and
icterus in older cattle, particularly of European high­
yielding breeds(mortality ~50%). Infected animals
may di.e 5-8 days after onset of symptoms. Parasitaemia
levels may rise up to 40%. Infections with strains of
lower virulence are associated with moderate fever,
diarrhoea, constipation and rarely haemoglobinuria.
Animals recover within a few weeks. Regular Infections
of calves lead to enwotic stability.
Babesia bovis
Agent. B. bovis is a small Babesia(2.4x 1.5 µm) lying
usually in the centre of the erythrocyte; vacuolated signet
ring forms are common(► Figure 5.21). Due to its
wide distribution and high pathogenicity, it is the most
important Babesia species in cattle from an economical
point of view.
Occurrence, epidemiology. B. bovis infects cattle
in southern Europe, South East Asia, northern, western,
central and southern Africa, Australia, Central and
South America. Since B. bovis and B. bigemina are
transmitted by the same tick species they often coexist
geographically(except in South Africa).
Clinical signs. B. bovis is more pathogenic than B.
bigemina and may cause shock and CNS symptoms
(for pathogenesis ► p. 134) in susceptible cattle(>9
months of age). Peracute courses of disease are observed
in spite of low parasitaemia levels of <1%. Zebus and
zebu cross-breeds are distinctly less susceptible to B.
bovis than taurine breeds.
Control of bovine babesiosis
B. divergens. An effective control of the vector I. ricinus is
almost impossible under practical conditions. Moreover,
it must be considered that the endemic stability may
be disturbed by tick control measures. Commercial
vaccines are not available.
B. bigemina, B. bovis. Control measures consist of tick
control, vaccination and cross breeding of European
breeds with Babesia-resistant breeds(e.g. zebus). Tick
control is predominately based on regular application
of acaricides to cattle(spray, pour-on, dip, systemic
application). Vaccination with live vaccines containing
attenuated strains of B. bovis and B. bigemina is a
common, successful practice in many countries(e.g.
South Africa, Australia, Israel).
■ Babesiosis in sheep and goats
Two Babesia species infect domestic sheep and goats:
B. motasi and B. ovis.
B. motasi. The large B. motasi(► Table 5.8) occurs in a
large European area, from Portugal up to the Caucasus,
in central Asia, the Near and Middle East, and India. In
western, central and northern Europe only an avirulent
strain ls found, transmitted by lxodes ricinus(northern
DE) or Haemaphysalis punctata (UK !Wales], FR,
NL, SE). A pathogenic strain occurs in North Africa
(Maghreb region) and India causing fever, dyspnoea,
haemoglobinuria, with approximately l 0% mortality.
Goats seem to be resistant.
B. ovis. The widely distributed small B. ovis( ► Table
5.8; ► Figure 5.21) occurs in tropical and subtropical
areas in southern Europe, from Portugal to the Caucasus
region, coinciding with the distribution of the vectors
Rhipicephalus bursa, R. turanicus and Hyalomma
anato/icum. The distribution area has its northern limits
in Croatia and in the Massif Central in France. B. ovis is
highly pathogenic; clinical signs resemble those of the
B. bovis infection in cattle; mortality in sheep can be up
to 30-50%. Goats seem to fall ill only rarely.

■ Babesiosis in wild ruminants
Several Babesia species occur in European wild
ruminants, including B. divergens(red deer, reindeer),
B. capreoli(roe deer, chamois), B. motasi(chamois, ibex)
and B. venatorum(roe deer, chamois, ibex). B. odocoilei
(reindeer) and B. jakimovi(reindeer, cattle) are further
species occurring in North America and Russia(Siberia),
respectively. B. divergens and B. venatorum are zoonotic
agents(► p. 131).
■ Babesiosis in equids
Babesia caballi
Agent B. caballi is a large species resembling B.
bigemina. Parasites are usually found paired, often
joined at their posterior ends, and measure 2.5-4x2 µm
(► Table 5.8; ► Figure 5.21). Horses, donkeys, mules
and zebras are susceptible. Due to common vectors
(Dermacentor spp., Hyalomma spp., Rhipicephalus spp.),
this species is often associated with Theileria equi( ► p.
144).
Occurrence, epidemiology. B. caballi occurs in
southern Europe, Asia, Africa, Cuba, South and Central
America, and certain parts of the USA. The distribution
area in Europe extends from Portugal and Spain to
France, Italy, Hungary, Romania, Ukraine and Russia.
Recently, indigenous infections have been reported from
the Netherlands. The situation in other Central European
countries is unclear although specific antibodies have
been found on various occasions in indigenous horses,
and potential vectors are present in various Central
European areas.
Clinical signs. Clinical pictures vary from
asymptomatic to peracute forms and death. Horses in
endemic areas rarely fall ill ( endemic stability), however,
losses may be high if susceptible, older animals are
imported into such regions. The incubation period lasts
10-30 days. Symptoms are often non-specific; in the
most common acute form: high fever(>41 °C), malaise,
dyspnoea, constipation, colic and - in advanced stages
- exsiccosis and icterus, rarely with haemoglobinuria.
Documented case fatality is 10-50%. Subacute and
chronic for ms are accompanied by weight loss and
intermittent fever. The spleen is enlarged (detected by
rectal examinali011). Parasitaemia is usually low(mostly
< 1%), even i.n acute cases. The infection may persist in
horses up to four years, but can also resolve in just a
few months.
Diagnosis. Apart from the clinical importance of
equine piroplasmosis, B. caballi and Theileria equi
infections (► p. 144) represent an international
hindrance for travelling with horses, e.g. to horse
shows and race meetings. In some countries(Canada,
USA, Australia, Japan) permission for temporary or
5. Phylum Alveolata
permanent importation of horses depends on the
absence of antibodies to equine piroplasms. For a
long time, the complement fixation test (CFT) was
considered the test of choice. More recently, opinion
has changed and the CFT has been replaced by lFAT
and a competitive ELISA (c-ELISA; binding of serum Cil
""CJ
antibodies to recombinant antigens has to compete with .E(/)
that of monoclonal antibodies). These tests are more Cil
reliable for detecting infected animals and horses treated Q.
0
previously with antiparasitic drugs. Test details are given a:
in the OIE Manual of Diagnostic Tests and Vaccines for
Terrestrial Animals. For reference laboratories see http://
tinyurl.com/puy9csx.
Control. Vaccines are not available. Tick control in
endemic areas is essential(► lxodida, p. 396). Serological
examination of horses for sale is recommended.
■ Babesiosis in dogs and other carnivores
Causative agents of canine babesiosis are B. canis,
B. vogeli and B. rossi(large babesiae; formerly three
subspecies of B. canis) and B. annae, B. gibsoni and
B. conradae (small Babesia sp.). The most important
species in Europe is B. canis due to its high pathogenicity
( ► Table 5.8). In a recent study, based on DNA analysis
of 394 blood samples of dogs with suspected babesiosis
from 9 European countries, 98.3% were positive for
B. canis and the rest for B. vogeli. Cats and wild felids
are hosts of B. felis (South Africa and Zimbabwe). B.
herpailuri (syn. B. pantherae) (southern Africa), and
B. cati(cats in India).
Large Babesia spp. in canids
Babesia canis
Parasites a.re relatively pleomorphic; pyriform stages
measure 4-5x2 µm ( ► Table 5.8; ► Figure 5.21) but
amoeboid and ring forms and multiple infections
of erythrocytes are common and may appear
simultaneously.
Occurrence, epidemiology. The geographical
distribution of canine babesiosis is dependent on the
occurrence of Dermacentor reticulatus, which occurs in
(])
Europe from Portugal to the Ural Mountains, focally in C
Central Europe. B. canis is usually transmitted by adult ·o
'6
Q)
ticks (larvae and nymphs of D. reticulatus infest other 2
hosts, e.g. rodents). In nine European countries, several
genotypes of B. canis have been identified differing in
cCil
C
·;::
geographical distribution and prevalence. It is believed
that genetic diversity may influence the outcome of
vaccination. .S
>.
Ol
Different epidemiological patterns may be present in 0
0
Europe:(a) co-existence of several species of piroplasms :'=
(/)
(and other vector-borne pathogens) and endemic
Cil
stability in the local dog population, but many cases of 0..
 Part II. Parasites and parasitoses: protozoa
acute infections in newly introduced (nai've) animals,
like in Spain; (b) countries with an overall presence of
canine babesiosis and local differences in the occurrence
like in PL, HU and FR, the latter which is known to be
endemic, with hyper-endemic areas in the south-western
part of the country; and (c) countries, in which the
disease was considered as exotic and known as a travel­
disease, but with low prevalence and local transmission
related either to imported cases or to small indigenous
foci of B. canis e.g. in Europe in the Benelux, DE, CH
and AT.
Clinical signs. Dogs are susceptible independent of age
I.' •,
·, I
and breed; however, parasite strains may markedly differ
I
'
•,
' I
in virulence. Prepatency lasts 7-21 days. Episodes of
I
I
11
'
high (>40 °C} fever are common and initially observed.
Parasitaemia is generally low (1 % ) and lasts for 4-7
days. In spite of this, animals with low parasitaemia
I •:
sometimes die within 24 hours (after parasite appearance
in the blood) from hypotensive shock. Acute B. canis
infections are characterised by fever, apathy, paleness
(anaemia), haemoglobinuria and cerebral disorders.
I
I ,
Disseminated intravascuJar coagulation (DIC) associated
with acute renal or multiple organ failures are common
l complications in acutely diseased dogs. Chronic cases
,
j
''
! t' � show apathy, emaciation, signs of anaemia, episodes of
fever, liver insufficiency, icterus. Signs at necropsy reflect
the clinical symptoms, e.g. by hepato-and splenomegaly,
serosal petechiae, ecchymosis and haemorrhagic
diatheses.
Babesia vogeli
The species resembles morphologically B. canis. It
is transmitted by Dermacentor variabilis (American
dog tick) and by Rhipicephalus sanguineus, the brown
dog tick, which is endemic in tropical and subtropical
areas and in parts of the temperate zone, approximately
from 35° south to 56 ° north. All stages, larvae, nymphs
and adults, may transmit B, vogeli. The infection is
endemic in the whole Mediterranean area (around
the Mediterranean basin) and in the tropics. Cases
imported into Central Europe often originate from
southern European countries (IT, FR, ES) and Turkey.
Indigenous B. vogeli infections in Europe north of the
Alps have so far not been observed. B. vogeli infections
are often asymptomatic or accompanied by mild fever
and weak anaemia. Parasitaemia is low ( < 1 %) and lasts
for 3-7 days.
Babesia rossi
This is the most pathogenic species in dogs. It occurs in
Africa (reports from South Africa, Uganda, Nigeria), in
accordance with the distribution range of Haemaphysalis
leachi (syn. H. elliptica).
Small Babesia spp. in canids
B. gibsoni (► Table 5.8; ► Figure 5.21) infects dogs
and other canids in Asia, Australia, North Africa, North
America; it is rarely found in Europe (mainly imported).
Haemaphysalis spp. and R. sanguineus are vectors. In
the USA this species has spread in kennels of certain
dog breeds (pit bulls, American Staffordshire terrier),
presumably due to direct transmission from dog to dog
by biting. Parasitaemia starts 3 days p.i. and increases
for 2 weeks to levels exceeding 40%. Infected animals
may show fever, anaemia, apathy, thrombocytopenia
and haemoglobinuria. There is a tendency to a chronic
course of the disease.
A further pathogenic species of small babesiae, B. annae
(formerly Theileria annae, proposed new name B.
vulpes), has been reported in dogs in ES, PT, HR, Israel,
and USA, and it was found in red foxes in additional
countries (DE, AT, HU, IT, and CA). It is probably
transmitted by Ixodes hexagonus. In addition, a small
species, B. conradae, was detected in California, USA.
Immunity in canine babesiosis
In dogs, there is no age-related resistance to Babesia
infections but puppies may temporarily be protected
by maternal antibodies. Convalescent dogs develop
concomitant immunity, which persists in unchallenged
dogs for approximately ½ to 1 year. Superinfections
induce long-lasting immunity. Effective therapy of
Babesia infected dogs with imidocarb reduces immunity,
rendering animals susceptible to new infections to a
limited extent. Cross-immunity to Babesia species
other than the immunising species is generally lacking.
Immunity may even be limited to particular parasite
strains.
Therapy and prophylaxis of canine
babesiosls
Tick prophylaxis by collars releasing acaricides or by
administering acaricidal compounds in other application
forms (► p. 602) reduces the risk of tick infestation but
cannot completely exclude Babesia infections. This form
of prophylaxis can be combined with vaccination. A
subunit vaccine against B. canis (Pirodof) is licensed
and available in several European countries. The vaccine
does not fully protect against infections but may reduce
severe clinical consequences. Efficacies vary and depend
on the strains of B. canis to which dogs are exposed.
Protection induced by the vaccine lasts for 6 months if
no interjacent infection occurs.
Prophylactic treatment of dogs with imidocarb (6 mg/kg
b.w., s.c.) has been described as an option to protect dogs
that stay temporarily in endemic regions or are exposed
to a high infection risk, for example after splenectomy.

Protection lasts for approximately 4 weeks. However,
this method is usually restricted to special cases.
■ Babesiosis in rodents
Numerous (>30) Babesia species have been described
in rodents, including B. microti ( ► Table 5.8) which
is a zoonotic agent (see below, zoonotic importance).
Zoonotic importance
Babesiosis is a rare but clinically important disease in
humans. At least 15 Babesia species or genotypes have
been identified as causing agents of human babesioses.
Besides natural transmission of the agents by ticks,
transmission by means of blood transfusion from
infected to non-infected individuals plays a significant
role.
B. diverge11s occurs in Europe (and northern Africa) and
has caused to date approximately 40 human cases, 80%
in splenectomised individuals. The disease is usually
severe. Also closely related species/isolates have caused
human infections: B. venatorum (previously Babesia
sp. EUl) (Europe), Babesia sp. (MOl) (USA), and
Babesia sp. KOl (Korea). Case fatalities reach 40%.
Human infections with small Babesia spp. of the B.
microti group, including B. duncani, are predominantly
observed in North America, rarely in other regions,
including Europe. Natural hosts are predominantly
cricetid rodents, vectors are various ixodid ticks. Recent
studies in Europe indicate the co-circulation of zoonotic
and presumed non-zoonotic B. microti strains in the
same species of rodents. Disease in humans develops 1-9
weeks after exposure, especially in immunosuppressed
patients, with case fatalities of 20%. Immunocompetent
individuals may also be affected by the disease.
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5. Phylum Alveolata
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Schnittger L, Rodriguez AE, Florin-Christensen M, Morrison
DA (2012) Babesia: a world emerging. Infect Genet Evol
12: 1788-809.
Solano-Gallego L, Baneth G (2011) Babesiosis in dogs and
cats - expanding parasitological and clinical aspects. Vet
Parasitol 141: 48-60.
Vannier EG, Diuk-Wasser MA, Ben Mamoun C, Krause PJ
(2015) Babesiosis. Infect Dis Clin North Am 29: 357-370.
Wise LN, Kappmeyer LS, Mealey RH, Knowles DP (2013)
Review of equine piroplasmosis. J Vet Intern Med 27: 1334-
1346.
Wojcik-Fatla A, Zajc\c V, Sawczyn A, Cisak E, Dutkiewicz J
(2015) Babesia spp. in questing ticks from eastern Poland:
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Yabsley MJ, Shock BC (2012) Natural history of zoonotic
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Wildl 2: 18-31.
 Part II. Parasites and parasitoses: protozoa

Family Theileriidae

Genus Theileria
Disease: Theileriosis.
Sir Arnold Theiler (1867-1936), veterinarian of Swiss
origin, scientist and pioneer of the South African
veterinary service.
Theileria species multiply in mammalian hosts by
merogony in mononuclear leukocytes and subsequently
in erythrocytes. They are transmitted by ixodid ticks but,
in contrast to babesiae, they are not transmitted in the
tick population verticaUy but only from stage to stage
(transstadial transmission).
Summary
• Agenta. Memblrlofthlg9'111 .,,,.,,.,,,.,.parult•of
domNtlc and wild rumrnanta, 1quld1, and IOl'M other
rnammall, lncfudlng mnuplala. Thly n l'NP()nllble
for rtnportam dlil•-· iluCh a e. Coat....,.."' cattte
fnAfrtcaandthlll4itolrlof equfdl. 0tlncterlltlcltlgll
In the rnammallaff halt n fflllOntl In mononuclelr
llukooytaand ln�;theerythn)cytlcstagee
fflNIUr9 0.8-2 1,11'11.
• Ufe oyole. I� b(odld tlckl Inoculate aporozoit•
durtng feldlr1g llttP a nwnmallan host. The sporozoites
nflct � �. d.velop Into meronta
�'I�•� by merogony and generate
maozoltN whfch Invade erythrocyte,. During a
aubleqµlnt fNdlng cycle Infected erythrocytes are
� t,fllvit' or nymphal ttck1, the parasite
...,_ nni•klln the VICtor'I lntlltlne, undergo
#/ri species (e.g.
munology. The varloua
lstfnct linmunl>I
uencee. 0ependlng on the paraifte IP8Cfee, aterl1e
or ooncomttant lmmuntty to new li'lf«:ttons oocura In
convale8cent anknall.
• Pathog1M11l1, cllnlcal llgn1. Pathogenic stages of
tranatormlng 1pecle1 (e.g. T. parva, T. annulata and
��•�-.; �rf) are the meronts In leukocytes, causing
nla, dyspnoea and necroses in the
Ina! tract. In non-transforming spec
� the •rythrocytlc stages Induce fe
ta, humogloblnurla and lcterus.
1gnOIII. Cue hfatory, cllnlcal signs and labor t
mlnatlonl n diagnostic components. The detect
of parulte atagN In Glemsa-stalned blood or ly
node.,,,..,. preparatlona Is a routine procedure w
II often oomplll'T1lnt8d or replaced by DNA analysis.
Serology II Important In equine Infections because of
apeclal Import/export regulations In various cou tries.
• Therapy, control. Chemotherapy In cattle with
buparvaquone and parvaquone, In horses with
lmldocarb. Live vaccines are available regionally for
cattle and sheep. Measures against ticks are important
for control.
Agents. Various Thei/eria species are parasites of
domestic and wild ruminants, T. equi infects equines
( ► Table 5.9), and some species occur in other mammals,
including marsupials. T. an nae, a species described as a
parasite of carnivores, has been allocated to the genus
and named Babesia based on genetic criteria and the
fact that it docs not develop in leukocytes in mammals.

of--·••--.._
• oornplJdd dlvllopmental cycle In thl tick rNUltlng
tit._...._. era. lllfv.-y gland1 and production Characteristic stages of the genus Theileria spp. in
lftlr' moulting of the tick and mammals are meronts in mononuclear leukocytes
_.....,-"Af feeding• n trlnlmlttld In the
_.. .,.,, ,- (dltalll IN below). In thl tick
(mostly lymphocytes) and erythrocytic forms. The
former are small bodies (2-12 µm in size) of circular
IPP• .,. only tranamlttld from or irregular shape, containing a few large nuclei in an
lht next genntlon Ukl Sabella early stage of development (so-called macromeronts)
of the genua TMllerl• can bl and numerous small nuclei in a later phase (so-called
�'lnUlllomllng' and 'non-tranafonnlng'
micromeronts). They are known as Koch's bodies, named
IPtcfN .,. highly pathogenic
the Infected llukocyte hoet celll after the discoverer Robert Koch. The erythrocytic
.... to oonthJoul prollferatlon. stages (merozoites) measure approximately 0.8-2 µm,
Q)
C • 11Ntletfa app. are widely are round, oval rod- or comma-shaped, sometimes also
Q forming a Maltese cross ( ► Figure 5.23). In addition,
'6 In Afrtca, Alla, Aultralla/New
Q)
...... 8b'llnl of T. P111V8 CIUN Eat spherical stages develop in red blood cells that are
�
cro dlNue, and the Zimbabwe
Afttaa. T. IIMUlata and T. leatoquardl
regarded as gamonts.
C
c
·Q) JiGpe and aome other reglonl, Life cycle. The following description refers mainly
,. tropical) thelllrioell of to the pathogenic, transforming Theileria species in
� of lheep and goats, ruminants ( ► Figure 5.24). Theileriae are transmitted to
C en Important parasite of honel
>­ mammals as sporozoites in the saliva of ixodid ticks. The
CJ) It lrvs,leal and subtropical countries
0
ilnd Iii IOUthem Europe. Vectors sporozoites infect mononuclear leukocytes and develop
0 into meronts (see above) ( ► Figure 5.25).
·v; n hard tlcka of various genera
ro
ro
a.
 5. Phylum Alveolata

Table 5.9. Theileria species in domestic and wild mammals {selection ).

T
- ,_

Hosts thellt1rla si,ecles Vectors. . Pathogenlclty1 0li88M and dlitrlbutlort

-
Cattle, African buffalo T. parva2 Rhipicephalus +++ East Coast fever
(Syncerus caffen) appendiculatus East and Central Africa
. - ----- ------

T. parva2 R. appendiculatus, +++ Corridor disease

---- R. zambeziensis ----· -- East, Central
South, --- --- Africa
T. parva2 R. appendiculatus, + Zimbabwe theileriosis
R. zambeziensis Zimbabwe
T. mutans Amblyomma spp, + Benign bovine theileriosis
Sub-Saharan
- -- Africa, Caribbean
Cattle, water buffalo T. annulata Hyalomma spp. +++ Tropical or Mediterranean theileriosis
(Buba/is bubalis) Mediterranean countries, Near and
-- -- · · ·- -- ---- Middle East,
-- --Asia
Cattle, eland, (sheep) T. taurotragi3 Rhlplcephalus sp. + Benign African theileriosis
southern
. - ·- Africa
--------
Cattle, African and T. orientalis Haemaphysa/is spp. - Oriental theileriosis
water buffalo ---- -· Eurasia, Australia, New Zealand
Sheep, goat T. lestoquardi4 Hyalomma spp. +++ Malignant theileriosis of sheep and
goats
South-eastern Europe, northern Africa,
I
T-------. - -- ... -- ----· Middle East
T. ovis f-1yaJorr ,,r,,J sp., + Benign theileriosis of sheep and
Rhipicepl1alus? goats
southern Europe, northern Africa,
- ------- --- ----- Middle East, southern Russia
Roe deer, red deer, T. capreoll /xodes ricinus ? Europe
fallow deer --- ---- --- - - ---------·-· -- - -·------
Horse, donkey, T. equi Dermacentor spp., +++ Equine theileriosis
giraffe Hyalomma spp., Tropics and subtropics (except
Rhlpicephalus spp., Australia), southern Europe
Amblyomma sp.
1 Degree of pathogenicity: +++ high; ++ moderate + low.
2 Strains of T. parva differing in biology and epidemiology; markers for the ir differentiation currently not available; historically known as
T. parva parva. T. parva lawrenci and T. parva bovls.
3 Formerly known as T. sergenti or T. buffeli.
4 Syn. T. hirci.

Figure 5.23. Theileria species in Giemsa-stained blood smears: (a) Theileria parva {Photo: H. Mehlhorn); (b) Theileria equi
(Photo IPH, K.F.).

Meronts of T. parva develop predominantly in ap+ T
lymphocytes, those of T. annulata in MHCII expressing
cells (B lymphocytes, monocytes, macrophages) and
meronts of T. equi in a broad range of host cells (B
and T lymphocytes, macrophages, monocytes). The
meronts of transforming species ( T. parva, T. annulata,
T. lestoquardi) divide into daughter meronts and release
mediators that transform the host cells to lymphoblastoid
cells and prevent apoptosis, resulting in immortalisation.
These cells divide rapidly, and in the course of mitosis,
daughter meronts cross over to daughter host cells.
After a number of replications as meronts, numerous
 Part II. Parasites and parasitoses: protozoa

.,,..­
''
'\
/
/
/
I
(
I I
I Sporozoites
Merogonles
In lymphocytes Blood circulation I
: �;�=tted --�-

I � "'/'4 \
�/�e<C
0

I Merozo
erythrocytes

Hard ticks

Moulting

Gamogony
,,;:,(_..,...e:,,.__ Spheroid stage
-..;;;.��r-�•�- Gametes
,---�;_r:.�•- Zygote

Salivary gland of adult tick �

Intestine of a tick nymph

Q)

·o
C

'6 Figure 5.24. Developmental cycle of Theileria parva in cattle (Graphics: IPZ, S. Ehrat, modified by S. Amrein).
Q)
�
c
co (up to 100) merozoites are generated which are released Infected erythrocytes are ingested by a susceptible tick
C
·c and invade erythrocytes. Apart from '/: parva, the stage (larval or nymphal stage), the intraerythrocytic
Q)
erythrocytic stages divide continuously. The resulting stages are released, and gamonts develop to gametes
.S merozoites, released from lysed erythrocytes, infect new ('ray-bodies') that form zygotes by syngamy. Zygotes
>- erythrocytes thus inducing a persistent parasitaemia. developing in intestinal cells of the tick give rise to
0)
0 ln non-transforming Theileria species there is no sporokinetes that enter via the haemolymph salivary
0
""in evidence that multiplication in leukocytes continues gland cells where sporozoites are formed. After moulting
after establishment of the erythrocytic phase. and commencement of blood feeding, sporozoites are
co
CL transmitted to a new host.

Figure 5.25. Theileria parva: macromeronts (MA) In bovine
lymphocytes and disintegrating micromeront (Ml) (Photo: H.
Mehlhorn).
Occurrence and epidemiology. The occurrence
of theileriae depends on the availability of suitable tick
species in the area ( ► Table 5.9). Various mammalian
hosts serve as reservoir hosts in which erythrocytic
stages of the parasite may persist for years or even
lifelong thus remaining an infection source for the
vectors. Whereas babesiae may persist over several
generations in the tick population, Theileria infections
are eliminated from transmitting ticks so that they do
not function as reservoirs. The pathogenic theileriae of
cattle in Africa persist in wild ruminants. The primary
host of T. parva is the African buffalo (Syncerus cafferi).
In cattle T. parva has developed into a complex of various
strains. In the case of corridor disease (named after a
corridor between the Hluhluwe and the Umfolozi game
parks in South Africa), buffaloes are essential for the
persistence of the infection since parasitaemia levels in
cattle are too low to guarantee efficient transmission.
African buffaloes may be co-infected with various strains
of T. parva. Reservoirs of T. annulata and T. orientalis
are water buffaloes (Buba/is bubalis).
T. equi occurs in parts of southern Europe. For
instance, 8.2% of 294 horses in northern Italy showed
specific antibodies to T. equi, and T. equi DNA could
be demonstrated in 33% of these animals. In France T.
equi was detected in bone marrow of clinically healthy
horses, suggesting that bone marrow is a reservoir site.
This species is not endemic in Central Europe, although
potential vectors exist in the area.
Immunology. The course of a primary infection
of ruminants with pathogenic theileriae is signi­
ficantly determined by immunosuppressive and
immunopathological factors (see pathogenesis, below).
Surviving animals develop a sterile immunity (T. parva)
or a concomitant immunity (T. annulata, T. equi) to
new infections. Protection is mostly strain-specific in
the case of T. parva, and species-specific in the case of
T. annulata. Specific antibodies are involved in partial
immunity to free merozoites and sporozoites. Cellular
5. Phylum Alveolata
mechanisms are more efficient and act, in particular,
against intracellular meronts. In the case of T. parva,
the main effector cells are cos + T cells whereas co4+
Th 1 cells and macrophages are more effective against T.
annulata. Unapparent carriers of T. equi are protected
from disease or new infection. T. equi-infected horses Ctl
"O
produce antibodies against immunodominant merozoite .EU)
antigens. These antibodies are associated with control of Ctl
parasitaemia. After natural infection horses seroconvert
e
Q.
within 1-2 weeks with peak levels at 30-45 days. 0:::
Pathogenesis. Bovine theilerioses, caused by
transforming, pathogenic Theileria spp. usually
progresses through three phases. Phase 1: After an
incubation period of approximately 2 weeks, a massive
hyperplasia of mononucleated cells develops within
a few weeks, followed by lymphocytolysis. At the
beginning an uncontrolled proliferation of infected
leukocytes and a polyclonal T and B cell activation
play a decisive role. Proliferation of mononuclear
cells occurs initially in regional lymph nodes at the
site of the tick bite and expands subsequently in an
almost uncontrolled manner throughout the whole
body, including spleen, liver, kidney, thymus, bone
marrow, abomasum and intestine, and produces
tumour-like infiltrations ( ► Figure 5.26). Phase 2:
Infected macrophages are activated and show enhanced
phagocytic activity (erythrophagia) and upregulated
TNF synthesis, causing fever, chronic inflammation and,
subsequently, emaciation. Infected lymphocytes secrete
IFN-y and IL-10 as potent immunomodulators. Phase
3: In the final stage, progressive lymphocytolysis and
suppressed leukopoiesis result in lymphoid depletion
and disorganisation of lymphoid organs associated
with necroses and disseminated haemorrhaging in the
gastrointestinal tract, as well as pulmonary disorders.
In T. mutans infections, extensive proliferation of
intraerythrocytic stages may cause severe anaemia.
Infections with non-transforming Theileria species of
cattle (e.g. T. orientalis) or sheep (e.g. T. ovis) are usually
associated with comparatively low number of meronts
(l)
C
·u
"O
(l)
�
co
C
·;::
(l)
C
>,
CJ)
0
0
·en
Figure 5.26. Theileria parva: lymphoid alterations in bovine
co
kidney (Photo: W.O. Neitz; see A. Latif). 0...
 Part II. Parasites and parasitoses: protozoa
and low parasitaemia levels. Disease symptoms in T.
equi infections are limited to the erythrocytic phase,
and the pathogenesis may broadly correspond with that
of babesial infections.
Clinical signs. Pathogenic Theileria spp. of ruminants
(T. parva, T. annulata, T. orientalis) cause fever, swelling
of lymph nodes, leukopenia, dyspnoea, constipation and,
subsequently, diarrhoea, sometimes CNS disorders and
anaemia. T. equi infections in horses are associated with
fever, anaemia, haemoglobinuria and icterus.
• Theilerioses of cattle, East Coast fever. The
agent of East Coast fever, T. parva, is highly pathogenic.
Copious stages of proliferation in lymphoid cells and
erythrocytes are produced in susceptible hosts in which
mortality rates may reach l 00%. Only young and immune
animals survive the infection. Typical symptoms, after
a 2 week incubation period, are: swelling of regional
and later on all lymph nodes; fever (40-41 °C); after 4-5
more days, dyspnoea, constipation and, subsequently,
diarrhoea and bloody mucus in the faeces, sometimes
CNS disorders, death after 2-4 weeks or, in peracute
cases, death may occur within 4-5 days p.i., i.e. before
the onset of parasitaemia ( ► Figure 5.27).
Necropsy performed in the final phase shows emphysema
and oedema of the lungs, disseminated haemorrhages,
ulcers in the gastrointestinal tract, particularly in the
abomasum and small intestine, and effusions into the
body cavities. The lymph nodes are oedematous, partly
necrotic. In liver and kidneys, but also in other organs,
focal, partly diffuse lymphocytic infiltrations are found
( ► Figure 5.28).
• Corridor disease and Zimbabwe theileriosis
resemble East Coast fever, but differ in epidemiology.
Benign bovine theileriosis is usually associated with
less severe clinical symptoms; however, some strains of
T. mutans may cause high parasitaemia levels leading
to anaemia, icterus and sometimes death.
Q)
C
·o
'5
Q)
�
cro
C
·c
Q)
j
C
>­
-
CT)
0
0
"in
ro Figure 5.27. Theileria parva: heifer with East Coast fever, severe
ro
0. dyspnoea (Photo: G. Buscher).
• Tropical or Mediterranean theileriosis and
theileriosis in sheep and goats. The clinical
course resembles East Coast fever but is less severe.
Nevertheless, a massive accumulation of meronts may
occur and, due to high parasitaemia levels of up to 80%,
anaemia develops. Mortality rates in susceptible cattle
may reach 50-60%. With declining meront formation,
the parasitaemia ceases but may persist at low levels for
years. Such animals are immune to new infections but
may serve as reservoirs for a long time. The malignant
theileriosis of sheep and goats, caused by T. lestoquardi,
resembles the Mediterranean theileriosis in cattle.
• Equine theileriosis. Only the erythrocytic stages
of 1: equi are pathogenic. After primary infections
the parasitaemia levels are usually at 1-5%, but may
occasionally be much higher. Clinical signs in the acute
phase are high, intermittent fever (39.5-42 °C), lethargy,
pale mucous membranes, anaemia, thrombocytopenia,
dyspnoea, constipation, colic, and in advanced stages
exsiccosis, icterus and haemoglobinuria. Mortality
rates of 10-50% occur in susceptible, untreated horses.
Chronic infections are associated with low-grade
anaemia, splenomegaly and a moderate decline in
performance. In several European regions (DE, CH,
northern IT) 1.7-8.2% of several hundred investigated
native horses had serum antibodies against T. equi, and
some of them were positive in PCR. This may be an
indication for an unapparent persistence of the agent
in a 'refugium' (e.g. bone marrow, see above). Latent,
asymptomatic infections may persist for years.
Diagnosis. Case history (stay of horses in endemic
areas, tick infestation), clinical signs and the direct
or indirect detection of the causative agent allow an
accurate diagnosis. Meronts (e.g. 7� parva, T. annulata,
7: /rirci) and erythrocytic stages (all Tf1ei/eria species) are
detectable in smears of lymph node aspirates and blood,
respectively, after Giemsa staining. DNA analyses allow
a sensitive and specific species and strain diagnosis.
Serologlc a. says are used for diagnosing Theileria
Infections ruminants and horses. Approved assays are of
Figure 5.28. Theileria parva: lung of a bovine with East Coast
fever showing high-grade oedema and emphysema (Photo:
G. Buscher).

special importance for the export and import of horses.
Due to legal regulations in several countries, imported
horses have to be free of specific antibodies to T. equi and
Babesia caballi. According to OIE regulations, special
assays (IFAT, c-ELISA, in the latter case employing
particular recombinant antigens) have to be performed
in certified laboratories ( ► B. caballi, p. 137).
Therapy. T. parva and T. annulata infections in cattle
are treated with derivatives of naphthochinone, i.e.
buparvaquone or parvaquone, which are active ag.iinst
meronts. Imidocarb {2.4 mg/kg b.w., i.m., twice in 72 h
interval) is used in T. equi-infected horses. Side effects
are common; dosages should not be increased. Complete
parasite elimination is generally not achieved.
Control. Measures against theileriosis in cattle (East
Coast fever, Mediterranean theileriosis) include tick
control ( ► lxodida, p. 396) and vaccination.
• East Coast fever. Tick control is the basic measure.
Its combination with vaccination may be economically
worthwhile in valuable stocks. Tick control is performed
by limiting the movement of cattle and preventing access
of foreign herds and wild ruminants to grasslands by
fences, etc. and by repeated treatment with acaricides
(dips, sprays). In areas of high infection risk, acaricidal
treatments must be repeated twice a week to prevent
sporozoite transmission (sporozoites are generally not
released by the ticks until the 4th day after infestation).
Vaccination is carried out by inoculation of sporozoites
of a virulent stabilate together with the application of
long-acting tetracycline to prevent disease. Due to
the existence of immunologically different strains of
T. parva, a cocktail of several strains must usually be
administered.
• Mediterranean theileriosis and malignant
theileriosis in sheep. Permanent housing is practised
in some areas ( e.g. in Israel) particularly to protect
imported European dairy stock from tick infestation.
Vaccination is performed by injection of merozoites of in
vitro-attenuated strains. The system is cheap and reliable
and is currently broadly used. A similar technique of
vaccination is utilised to control malignant theileriosis
in sheep.
• Equine theileriosis. Vaccines are not available and
antiparasitic treatments do not completely eliminate
the parasites, i.e. horses, once infected, remain carriers
of T. equi for a long time, possibly for life. Prevention,
therefore, depends on individual tick prophylaxis or
avoidance of stays in endemic areas.
5. Phylum Alveolata
• Genus Cytauxzoon
Kytos (G): cell; auxano (G): to proliferate, grow; zoon
(G): animal. Refers to the increase of cell numbers in
an animal.
Cytauxzoon spp. replicate in mammalian hosts by
rnerogony in macrophages or monocytes and infect
subsequently erythrocytes. They are transmitted by
ixodid ticks to vertebrate hosts and from stage to stage
within the tick population.
Agt'I 1ts. Cytauxzoon felis infects macrophages and
monocytes of wild felids and domestic cats forming
macromeronts in myeloid ceUs releasing numerous
merozoites that invade erythrocytes. Merozoites in
erythrocytes are <2 µm, rod- or comma-shaped.
Cytauxzoon manul parasitises Pallas's cats (Otocolobus
mamtl) in Mongolia, and a genetically closely related
Cytauxzoon was first found in Iberian lynx, and later
on in domestic cats in Central Europe.
Life cycle. C. felis is transmitted to feline hosts as
sporozoites in the saliva of ixodid ticks. The sporozoites
invade mononuclear leukocytes of myeloid origin
(CD34 + blast, monocyte, macrophage, dendritic ceU
or Langerhans cell). In these cells the parasite forms
meronts, undergoes asexual multiplication and generates
merozoites that infect circulating erythrocytes.
The specific mechanism by which sporozoites target
the host cells and whether or not meront-infected
cells replicate is not known. However, the fact that
serial passage with smaU volumes of parasitised tissue
is possible suggests that infected cells replicate as
described for transforming Theileria spp. Also, 'lateral
transmission' from meronts to other uninfected
myeloid cells is discussed. Merozoites invade circulating
erythrocytes. Infected erythrocytes are ingested by
susceptible ticks in which gamogony occurs in the gut,
followed by sporokinete invasion of the salivary glands
and sporogony (see Theileria development).
Part II. Parasites and parasitoses: protozoa
Occurrence and epidemiology. The occurrence
of C. felis in North and South America depends on
the availability of the suitable tick species as vectors,
including Amblyomma americanum, Dermacentor
variabilis and maybe other Dermacentor species. Wild
felids (bobcats, mountain lions, ocelots, spotted cats and
jaguars) represent classical reservoirs of C. felis, mostly
remaining asymptomatic. Another infection source for
ticks are possibly chronically infected domestic cats.
Cytauxzoonosis often occurs in young outdoor cats with
a history of tick infestations. Geographic hot spots are
known with prevalences in domestic cats as high as 30%.
In Europe, Cytauxzoon has been diagnosed in Iberian
lynx and domestic cats in Spain, and in domestic cats in
IT, FR and CH. The tick vectors are not known (most
likely Dermacentor spp. or Jxodes ricinus). Recently
(2012), cytauxzoonosis was diagnosed in three cats in
north-eastern Italy, and Cytauxzoo11 sp. was detected in
15% of 118 domestic cats by blood smear and in 23%
by DNA analysis.
Pathogenesis. The high pathogenic potential of C.
felis is associated with the development of the parasite
in the mononuclear phagocyte system. Cells filled with
schizonts line blood vessels, causing obstruction of the
blood flow, especially in the liver, spleen and lungs.
The disseminated infection results in thrombosis,
circulatory impairment, tissue infection and a severe
systemic inflammatory response that can lead to multi­
organ dysfunction or failure and death within 3 weeks
of infection.
Clinical signs. Natural persistent, subclinical
infections have been diagnosed in wild bobcats, but
clinical disease was observed in captive lions and tigers.
In domestic cats, cytauxzoonosis is typicaUy an acute
or peracute severe febrile disease. General clinical signs
are depression, anorexia, high fever, icterus, dyspnoea,
tachycardia , generalised pain and vocalisation. Signs
of haemolytic an.aemia are frequent. (pale mucous
membranes, pigmenturia, plenomegaly, hepatomegaly).
Many cats die within l week of the onset of clinical
signs. Cytauxz.oon infections reported in cats in Europe
showed a milder course of disease with low-levels of
parasilaemia and anaemia.
Therapy. Chemotherapy in domestic cats should be
initiated immediately in combination with supportive
care treatment (fluid, oxygen and anti-thrombotic
therapies) with atovaquone {15 mg/kg b.w., p.o., every
8 h for 10 days) and azithromycin (IO mg/kg b.w., p.o.,
every 24 h for JO days). The survival rate of cats was
60% in a clinical trial.
, Selected references
Bazarusanga T, Vercruysse J, Marcotti T, Geysen D (2007)
Epidemiological studies on theileriosis and the dynamics
of Thei/eria parva infections in Rwanda. Vet Parasitol 143:
214-221.
Birkenheuer A (2015) Cytauxzoonosis. In: Beugnet F, Halos L
(eds.) Parasitoses & vector borne diseases of cats. Lyon ,
France: Merial S.A.S.. pp. 229-233. ISBN 978-2-9550805-
0-4.
Carli E, Trotta M, Chinelli R, Drigo M, Sinigoi L, Tosolini
P, Furlanello T, Millotti A, Caldin M, Solano-Gallego L
(2012) Cytauxzoon sp. infection in the first endemic focus
described in domestic cats in Europe. Vet Parasitol 183:
343-352.
Gomes J, Soares R, Santos M, Santos-Gomes G, Botelho
A, Amaro A, Inacio J (2013) Detection of Theileria and
Babesia infections amongst asymptomatic cattle in Portugal.
ncks Tlck Borne Dis 4: 148-151.
Grandi G, Molinari G, Tlttarelli M, Sassera D, Kramer LH
(2011) Prevalence of Thefleria equi and Babesia caballi
infections in horses from northern Italy. Vector Borne Zoonotic
Dis 11: 955-956.
Guidi E, Pradier S, Lebert I, Leblond A (2015) Piroplasmosis
in an endemic area: analysis of the risk factors and their
implications on the control of theileriosis and babesiosis in
horses. Parasitol Res 114: 71-83.
Lawrence JA, Perry BO, Williamson SM, De Vos AJ, Irvin
AD, Pipano E, Shkap V (2004) Theileriosis. In: Coetzer JA,
Tustin RC (eds.). Infectious diseases of livestock. 2nd ed.
Vol. 1. Oxford, UK: Oxford University Press, pp. 447-501.
ISBN 0-19-576169.
Lloret A, Addie DD, Boucraut-Baralon C, Egberlnk H,
Frymus T, Gruffydd-Jones T, Hartmann K, Horzinek
MC, Hosie MJ, Lutz H, Marsllio F, Pennisi MG, Radford
AD, Thiry E, Truyen U, Mijstl K, European Advisory
Board on Cat Diseases (2015) Cytauxzoonosis in cats:
ABCD guidelines on prevention and management. J Feline
Med Surg 17: 637-641.
Mana BJ, Plenaar R, Latif AA (2015) A review of Thel1eria
diagnostics and epidemiology. Int J Parasitol Parasites Wildl
4: 104-118.
Perera PK, Gasaer RB, Anderson GA, Jeffers M, Bell CM,
Jabber A (2013) Epidemiological survey following oriental
thetlerios1s outbreaks in Victoria, Australia, on selected cattle
farms. Vet Parasitol 197: 509-521.
Pitel PH, Pronost S, Scrlve T, Leon A, Richard E, Fortier
G (2010) Molecular detection of Theileria equi and Babesia
cabal/1 ,n the bone marrow of asymptomatic horses. Vet
ParaSltol 170: 182-184.
Ramsay JP, Uetl NW, Johnson W C, Scole GA, Knowles
DP, Mealey RH (2013) Lymphocytes and macrophages
are infected by Theileria equi, but T cells and B cells are not
required to establish infection in vivo. PLoS One 8: e76996.
 5. Phylum Afveolata

Schein E, Rehbein G, Voigt WP, Zweygart E (1981) Babesia

equi: development in horses and in lymphocyte culture. Trap
Med Parasitol 32: 223-233.
Sivakumar T, Hayashida K, Sugimoto C, Yokoyama N (2014)
Evolution and genetic diversity of Theileria. Infect Genet Evol
27: 250-263.
Ueti MW, Mealey RH, Kappmeyer LS, White SN, Kumpula•
McWhirter N, Pelzel AM, Grause JF, Bunn TO, Schwartz
A, Traub-Dargatz JL, Hendrickson A, Espy B, Guthrie
AJ, Fowler WK, Knowles DP (2012) Re-emergence of the
apicomplexan Theileria equi in the United States: elimination
of persistent infection and transmission risk. PLoS One 7:
e444713.
Walker JG, Klein EV, Levin SA (2014) Disease at the wlldlife­
lifestock interface: acaricide use on domestic cattle does not
prevent transmission of a tick-borne pathogen with multiple
hosts. Vet Parasitol 199: 206-214.
Wise LN, Pelzel-McCluskey AM, Mealey RH, Knowles DP • Therapy, oo I. Tetracycline (e.g.
(2014) Equine piroplasmosls. Vet Clin North Am Equine Pract m plua aulfonlmldee (efllcll0Vlir•1G11llflllllllfll
30: 677-693. lmportanoe. s. COIi le tranem
humane, o.nllly resulting In mild or
cllrtlp.i P.f88811tatlona,
- Subphylum Ciliophora
Cilium (L): ciliary, phorein (G): to carry. Agent. Balantidium coli is common in pigs, more rare
in humans, monkeys, rats, dogs and cats. The supposed
Characteristics of the subphylum Ciliophora (pre­ infection of ruminants with B. coli is due to confusion
viously Ciliatea or Ciliata) are hair-like cilia, the specially with Buxtonella sulcata (see below). B. coli exists in
structured cell wall (cortex) with characteristics of the the form of motile trophozoites and immobile cysts.
Alveolata, the existence of two nuclei (macronucleus and The oval trophozoites vary in size (S0-100x40-75 µm)
micronucleus responsible for cytoplasmic processes and and are completely (holotrichously) covered with cilia
reproduction, respectively) and conjugation, a special arranged in longitudinal rows. A cytostome with dense
variant of sexual reproduction. ciliation is subterminally located at the narrower end.
The kidney-shaped macronudeus lies in an almost
central position, the micronucleus is localised in a notch
5.3 Classes Litostomatea and of the macronucleus. The almost colourless, spheroidal
Oligohymenophorea cysts measure 40-65 µm; the nuclei are visible after
staining ( ► Figure 5.29).
5.3.1 Orders Vestibuliferida and
others Life cycle. After oral ingestion of cysts, trophozoites
hatch in the small intestine, settle in the lumina of caecum
Family Balantidiidae and colon and feed on bacteria, starch and other particles
in the intestine. Trophozoites multiply predominantly,
Genus Balantidium by transverse binary fission; conjugations are observed
rather rarely. Tissue damage occurs when the parasites
Balantidium coli invade the intestinal mucosa. Cysts are formed in the
colon. These are shed in the faeces, often together with
r- -�
f Disease: Balantidiosis in pigs and other mammals.
-- - .__
.

..-Uc--��,:al
■
.
i
trophozoites. Trophozoites die rapidly outside the host
but cysts survive for weeks in moist environments.

Occurrence and epidemiology. B. coli is globally

Balantion (G): bag; refers to the shape of the trophozoites;
kolon (G): colon.
distributed. Domestic pigs and wild boars are the major
reservoir hosts. Prevalences in suckling piglets are
usually low, but up to 100% of pigs older than 4 weeks
may be infected. In Central Europe, prevalences in sows
vary from 0 to 80%. The intensity of cyst excretion
increases with age; in particular, lactating sows shed large
numbers of cysts. B. coli infections are common both in
free-living or captive primates and other monkeys, e.g.
in sanctuaries. Regarding human infections see below.
 Part II. Parasites and parasitoses: protozoa

Macronucleus
Micronucleus

Figure 5.29. Balantidium coli: (a) vegetative form (trophozolte) (50-100x40-75 µm); (b) cyst (40x65 µm); (c) trophozoite, native
preparation, iodine staining (Graphics a, b: IPZ, A. Seeger; after Geigy and Herbig 1955; Photo c: IPZ).

Pathogenesis and clinical signs. Since B. coli is

of low virulence most infections of pigs, humans and
other hosts remain unapparent. Trophozoites rarely
invade the intestinal wall and induce extended, multiple
necroses with haemorrhages, predominantly in caecum
and colon, occasionally also in the small intestine or even
the stomach. Finally, ulcers develop which are covered
with yellowish, suppurative material. In histological
sections of ulcers and in adjacent parts of the mucosa
and submucosa, trophozoites with the characteristic
macronucleus can be found ( ► Figure 5.30). The ability
of B. coli to invade tissue is ascribed to the production
of hyaluronidase by the parasite. Sometimes infections
accumulate in particular piggeries and are associated
with diarrhoea and tenesmus.

Diagnosis, therapy and con trol. Cysts can be

detected by faecal examination using a flotation
technique, and trophozoites (in fresh faeces) by means
of the Baermann funnel technique. Detection of cysts
or trophozoites is not indicative for disease, since
asymptomatic B. coli infections are common In pigs (see
above). Diseased pigs may be treated with tetracylines
such as doxycycline: 10 mg/kg b.w. p.o. for S days, or
trimethoprim plus sulfadimidine: 2x 15 mg/kg b.w. p.o.
daily for 3-5 days.

Zoonotic importance. The estimated worldwide 8.

Q)
't
C coli prevalence in humans is low (0.02-1 %), but the rates Flgure 6.30. Balantidium coll Infection in a pig: histological
5
:a in some geographic regions (e.g. in Asia, Latin America, section through the wall of the large Intestine with numerous
Q)
� Middle East) may reach values >20%. Transmission is B. coli trophozoites, recognisable by the darkl y stained
enhanced by close contact between pigs and humans, macronuclei (Photo: IPH, K.F.).
co poor sanitary conditions and climatic conditions
C
·c favouring survival of cysts. Occasionally the infections
Q)

result in clinical presentations with diarrhoea.

C
>-
0)
0
0
'in
co
co
0.
 5. Phylum Alveolata

Family Pycnotrichidae I. multifiliis occurs worldwide and parasitises the skin

and gills of many freshwater fish species, particularly
Genus Buxtonella salmonids, in natural water bodies, fish tanks and
aquaria. The life cycle is depicted in ► Figure 5.31. Q)
Buxtonella su/cata Holotrichously ciliated, spherical trophozoites .c
(trophonts) (300-1000 µm) inhabit small epithelial 0
-0
Buxtonella sulcata is a very common parasite in the cavities. They multiply and release ciliated stages C
ct!
caecum of ruminants. It is presumed to be harmless. (trophozoltes, tomonts) which encyst, e.g. on the lake ct!
-0
Round cysts (0 50-130 µm) resemble those of B. coli. bed or the bottom of an aquarium. There, they divide ·c
into multiple daughter cells (tomites), which transform �
'S
Families lchthyophthiriidae and into ciliated swarmers (theronts, approximately 40 µm .0

Chilodonellidae in size) and invade the skin and gills of new hosts. iE
Alterations are macroscopically visible, whitish spots. �
Numerous species of these genera are parasites of fish Sometimes, extended necroses are observed in the
(see special literature). Here we briefly describe some epithelia of skin and gills. Deaths are common.
frequently observed agents.
Genus Chilodonella
Genus /chthyophthirius

/chthyophthirius multifiliis Disease: Clllilodonellosis.

Disease: lchthyophthiriosis (white spot disease). Cheilos (G): lip, margin; odon (G): tooth. Refers to lip­
and tooth-like structures at the cytostome.

Ichthys (G): fish; phtheiros (G): louse, skin parasites. Skin

alterations are macroscopically visible and reminiscent
of lice.

Swarmer with
terminal cilium
Penetration of a swarmer Into
the skin and encystatlon
(I Trophozolte

t Q)
C
·o
i5
Q)
Encysted �
trophozoite C'
ct!
C
·c
Q)

.£
>.
0)
0
Multiplication 0
·u5
e
Figure 5.31. Developmental cycle of lchthyophthirius multifiliis (Graphics: IPZ, S. Ehrat; after Mehlhorn and Piekarski 2002). 8:
Part II. Parasites and parasitoses: protozoa
Chi/odonella piscicola
Worldwide distribution in freshwater fishes (predomi­
nantly carps), brackwater and aquarium fishes. The
heart-shaped, holotrichously ciliated parasite (30-80 µm)
inhabits gills and skin. It multiplies by binary fission and
the resulting stages settle on the same or another host.
C. piscicola induces enhanced mucus production and
hyperplasia of the epithelium. Hyperplastic epithelium
extends over the respiratory epithelium and reduces
the respiratory surface of the gills. The parasite occurs
under a wide range of temperatures (slightly above zero
to 25-30 °C) and accounts for great economic losses in
the fish industry.
5.3.2 Orders Sessilida and Mobilida
Families Epistylidae and Trichodinidae
Peri (G): around, above; trichos (G): hair, bristle.
Sessilida: genera Epistylis, Apiosoma, Ambiphrya attach
to skin and gills of freshwater fishes. The cytostome
is surrounded by a collar of ciliae. They reproduce by
binary fission. Resulting swarmers attach to new hosts.
Sessilida do not feed on host substances. The damage
caused by massive infections consists of impaired gas
exchange of the gills and impaired movement.
Mobilida: genera Trichodina, Trichodinella, Tripartiella
are frequent parasites on freshwater and saltwater
fishes, infesting skin and gills. Trophozoiles are discoid,
measure 60 µm (Trlchodina) or 30-40 µm (Trichodinella,
Tripartiella), move on the skin/gill surface by ciliae and
attach to the epithelium with collars of spines. Damage
occurs only in case of heavy infections.
Selected references
Abdel-Hafez G, Lahnsteiner F, Mansour N, Licek E (2014)
Pathophysiology of lchthyphthirius multifiliis Infection in
rainbow trout (Oncorrynchus mykiss) and chub (Leuciscus
cephalus). J Comp Pathol 151: 394-399.
Dickerson HW (2006) lchthyphthirius multifiliis and Cryptocaryon
irritans (Phylum Ciliophora). In: Woo PTK (ed.) Fish diseases
and disorders. 2nd ed. Vol. 1: Protozoan and metazoan
infections. Wallingford, UK: GABI. pp. 116-153. ISBN-10:
0-85190-015-0.
Labes EM, Hegglin D, Grimm F, Nurcahyo W, Harrison
ME, Bastian ML, Deplazes P (2010) Intestinal parasites
of endangered orangutans (Pongo pygmaeus) in Central
and East Kalimantan, Borneo, Indonesia. Parasitology 127:
123-135,
Pomajblkova K, Obornik M, Horak A, Petrzelkova KJ, Grim
JN, Levecke B, Todd A, Mulama M, Kiyang J, Modry D
(2013) Novel insights into the genetic diversity of Balantidium
and Balantidium-llke cyst forming ciliates. PLoS Negl Trop
Dis 7: 32140.
Ryan SJ, Brahares JS, Walsh C, Milbers K, Kilroy C,
Chapman CA (2012) A survey of gastrointestinal parasites
of olive baboons (Papio annubis) in human settlement areas
of Mole National Park, Ghana. J Parasltol 98: 885-888.
Schuster FL, Ramirez-Avila L (2008) Current world status of
Balantdium coli. Clin Microblol Rev 21: 626-638.
6. Phyla Amoebozoa and Percolozoa:
amoebae
Amoibos (G): changing; zoon (G): animal, creature;
heteros (G): different; /obos (G): lobe.
Summary
• Agents. Amoebae are organisms Of variable shape
that move by means of pseudopodia and feed l:1y
phagocytosis. They are phyiogenetlcally heterogeneoue
and may be, for pragmatic reasons, divided Into
parasitic and free-living groups. Many species form
tysts.
Parasitic amoebae
• Occumtnce and clinical signs. Entamoeba hlstolytlca
Is a pathogenic species which occurs worldwide In
humans, monkeys and occasionally in dogs and cats.
Clinical cases in humans occur predominantly in areas
with warm climates. E. histolytica, primarily a parasite
of the large intestine, may cause dysentery and also
systemic infections, particularly of the liver. Entamoeba
invadens may cause severe intestinal and systemic
disease in reptiles.
• Zoonotlc importance. E histolytica is rarely transmitted
from monkeys to humans. Transmission from humans
to animals is more likely.
Free-living, opportunistic pathogenic species
• Occurrence and clinical signs. Various genera (amongst
others Naegleria, Acanthamoeba, Hartmannella) Inhabit
mainly moist, but also dry, environmental habitats.
Occasionally, they cross over to humans and animals
as opportunistic agents and sometimes cause severe
diseases, e.g. primary amoebic menlngoencephaRtls
in humans. Free-living amoeba may disseminate
pathogenic bacteria (e.g. Leg/one/la pneumophlla, the
agent of human legionnaires disease).
L--. . ·---- -�
The cellular body of amoebae is delimited by a plasma
membrane and is highly variable in shape. The
cytoplasm is usually separated into a clear peripheral
ectoplasm and a rather turbid endoplasm, and contains
nucleus, lysosomes, i n some groups, mitochondria
or - in case of E. histolytica - mitosomes. Amoebae
generate plasma protuberances - pseudopodia - for
locomotion and feeding by phagocytosis. Multiplication
is by binary fission. Encystation is common. Cysts are
resistant to environmental influences and important
in transmission.
co
"O
6.1 Classes Entamoebidea, :.a
Lobosea and Heterolobosea Q)
0
E
6.1.1 Order Entamoebida c
w
Family Entamoebidae
Various genera of the family (Entamoeba, lodamoeba,
Endolimax) inhabit the intestinal tract of vertebrates
(► Table 2.1, p. 45).
Genus Entamoeba
The genus Entamoeba comprises approximately 50
species of which E. histolytica is most important as a
pathogenic agent in humans and other primates.
Entamoeba histolytica
Disease: Entamoebosis (amoebic dysentery,
II'
amoebosis) in humans and animals.
Agent. E. histolytica and at least two morphological
identical, non-pathogenic species (E. dispar and E.
moshkovskii) inhabit the large intestine of humans. E.
moshkovskii is mainly considered a free-living species
which occurs in sewage as well as in sediments of fresh
and brackish water. However, this species has also been
found in many countries in humans with prevalences up
to 50%. Recent observations suggest that £. moshkovskii
may be pathogenic, causing diarrhoea in humans. All
these species form cysts that contain four nuclei in the
mature stage. These cysts can be differentiated from
morphologically distinct cysts of other apathogenic
amoebae occurring in primates (Entamoeba coli,
lodamoeba biitschlii, Endolimax nana).
Trophozoites of E. histolytica are very variable in size
(10-60 µm). Under suitable conditions, they show a
broad, lobate pseudopodium that is jerkily extruded.
The vesicular nucleus, with a central karyosome and
regular chromatin granules attached to the nuclear
membrane, are characteristics of the genus, visible in
stained preparations. E. histolytica trophozoites invading
the intestinal wall incorporate erythrocytes(a diagnostic
characteristic of the pathogenic forms). Mature cysts
(0 10-16 µm) contain four nuclei and rod-shaped
chromatin bodies with rounded ends( ► Figure 6.1).
 Part II. Parasites and parasitoses: protozoa
', ,
'·,
,J
.f,�:;:;l��{K�&�?':,
c:�r;�'.1K
4t_
{'!-:';' ·:�'-l ,;�·:.
Er ythroc yte
Nucleus
a Pseudop odium
Chromatoid
���'".1t""--body
���--Nucleus
Figure 6.1. Entamoeba hlstolytica: (a) trophozolte (length 20·
60 µm) with phagocytlsed erythrocytes; (b) cyst (10-16 µm)
with four nuclei (Graphics: IPZ. A. Seeger; after Geigy and
I • Herbig 1955).
Life cycle. E. histolytica and the other species
mentioned above have direct life cycles in which
mature cysts are transmitted from host to host. Natural
infections with E. histolytica occur in humans and almost
all other primates and, occasionally, in dogs and cats.
Trophozoites inhabit the mucosal surface of the large
intestine and multiply by binary fission. In the course of
cyst formation, a trophozolte is enclosed by a cyst wall
and generates four nuclei by fission, Cysts are excreted
in the faeces; fully developed cysts are Immediately
infectious. Aft.er oral Ingestion of cysts by n ultoble
host, trophozoites ore released Into the lumen of the
colon, where they may stay and multiply for month
without causing any detectable harm to the host. Under
particular circumstances. however, they may invade the
intestinal wa.11 causing disease (see below). E. dlsparand
E. moshkovskii do not invade tissues.
Occurrence and epidemiology. Approximately
500 million people are infected with E. liistolytica/E.
dispar/E. moshkovskii lhroughout the world. fn 5-15%
of cases, the agent is£. l,isto/ytica. ln most geographical
areas £. dispar prevails. Prevalences of E. moslikovskii
in some countries varied between 5% (Iran) and SO%
(Australia). On average prevalences of Entamoeba spp.
in humans in Europe and the USA amount to ~4%, and
up to ~SO% in tropical and subtropical areas. Worldwide,
E. histolytica is responsible for approximately 40 million
new clinical cases per year, and a death toll of SS,000
people (in 20 l O). Amoebic dysentery is also observed
in monkeys in zoos.
Trophozoites degenerate rapidly outside the host but
cysts survive on the ground for at least 8 days at 28-
34 °C. Cysts are often transmitted with contaminated
vegetables or drinking water and by contaminated hands,
etc. Arthropods (cockroaches, flies) may spread the
agent.
Pathogenesis, clinical signs, immunology.
Receptors and surface lectins enable the trophozoites
to adhere to enterocytes. Subsequently, cytolysis occurs
by pore-forming proteins (amoebapor types A-C) and
proteases. Initially, small necrotic foci develop followed
by ulcers and dysentery. In acute cases, the faeces consist
mainly of mucus and blood, containing masses of
trophozoites. Trophozoites may be haematogenously
spread into the liver or other organs (lungs, brain, spleen,
skin) where, sometimes large, necrotic lesions (so-called
abscesses) may arise due to massive cell damage that can
cause fatal disease. Cell-mediated immunity plays a role
in limiting systemic infections since immunosuppression
(e.g. by corticosteroids) can result in enhanced spread
of the infection to various organs in humans. Recurrent
asymptomatic intestinal infections with E. histolytica
and E. dispar have been reported.
Diagnosis, therapy, control. Intestinal infections
are diagnosed by detecting trophozoites and/or cysts
using coproscopy (► SAFC technique, p. 530), intestinal
lesions may be detected by endoscopy. E. histolytica
can be distinguished from some of the apathogenic
species (e.g. E. coli, lodamoeba) by cyst morphology,
but generally by DNA analyses or by detection of E.
histolytica-specific coproantigens. Serology indicates
cases of tissue infections (luminal infections do not
induce specific antibodies). Extraintestinal forms
are diagnosed by imaging techniques (X-ray, CT)
In conjunction with serological detection of specific
antibodies.
Drug11, llccn!lcd for human amoeblosis. can be employed
In animal Infections (paromomycin, diloxanlde furoatc,
nltrolmldazolc). Infections In monkeys arc common;
control In zoological gardens or sanctuaries Is difficult
and requires effective hygienic measures.
Zoonotic importance. Proven human cases of
transmission of amoebae from animals (monkeys) to
humans are very rare. Human to animal transmission
is more likely.

Genus Entamoeba in domestic and pet
animals
Various Entamoeba species are described as parasites
of the large intestine of animals, e.g. E. equi (horse), E.
bovis (cattle, buffalo), E. ovis (sheep, goat), E. suis (pig),
E. polecki (pig, monkey, human), E. cuniculi (rabbit),
E. muris (various rodents), E. caviae (syn. E. cobayae)
(guinea pig), E. anatis (duck) E. gallinarum (chicken,
other fowl), and E. invadens (reptiles). E. apis is an
intestinal parasite of bees. The oral cavity of humans,
monkeys, horses, pigs, cats and dogs may be inhabited
by E. gingivalis (syn. E. equibuccalis) which does not
produce cysts. Most of these species are considered
apathogenic, except E. invadens.
Entamoeba invadens
Agent and life cycle. Entamoeba invadens parasitises
the intestine of reptiles. The species resembles,
morphologically and biologically, E. histolytica but is
adapted to temperatures of 27-29 °C and, therefore, is not
transmittable to endothermic hosts. The development
corresponds in principle to that of E. histolytica. Many
reptile species can fall ill from E. invadens. Turtles are
often asymptomatically infected and may shed cysts
continuously; they are regarded as reservoir hosts.
Pathogenesis and clinical signs. E. invadens is
pathogenic for saurians and snakes. After oral ingestion
of cysts, small necroses and ulcers develop in the colon.
They may expand gradually to the cloaca and into the
midgut. Secondarily other organs may be infected (liver,
kidney, heart, brain, eyes, skin). Symptoms include
anorexia, obstipation or excretion of bloody mucus,
enhanced water uptake, apathy and spastic movements.
Diagnosis . Trophozoites can be microscopically
detected in bloody, mucous excrements or in the content
of the colon (sampling with cotton swaps). Faecal
examination by the SAFC technique ( ► p. 530) allows
the detection of trophozoites and cysts. Organ lesions
and demonstration of amoebae confirm the diagnosis
at necropsy.
Th erapy. Nitroimidazole derivatives and tetracyclines
are recommended for therapy. For prevention, terrariums
and equipment should be disinfected with boiling water.
Importation of cysts with equipment, feed, etc. must
be avoided. Insects or mites (accidental vectors) have
to be eliminated.
6. Phyla Arnoebozoa and Percolozoa: amoebae
6.1.2 Order Centramoebida and
other orders
Family Acantharnoebidae and other
families "O
C
Cll
Cll �
Free-living amoebae as opportunistic parasites and "O Q)
reservoirs of pathogens :o-e
Q) 0
0 ,._
E CD
Agents and life cycle. All free-living amoebae ,._ ....
Cll .C
(nucleus with large karyosome, pulsating vacuole and co
Q)
mitochondria) form trophozoites and cysts (the genus (.)
Naegleria [Family Vahlkampfiidae] in addition shows
flagellated stages with two flagella). The trophozoites
( 12-30 µm, sometimes >60 µm) vary in shape and
generate broad or slender pseudopodia. The round or
polygonal cysts measure 8-30 µm. The genus Balamuthia
contains only one species (B. mandril/is), the genera
Naegleria and Hartmanella (family Hartmanellidae)
include few species (e.g. Naegleriafowleri, Hartmannella
cantabrigensis), whilst the genus Acanthamoeba contains
at least 17 species (A. culbertsoni and others). In addition,
multiple other genera exist.
Occurrence and epidemiology. Members of the
genera Naegleria, Acanthamoeba and Hartmanella
are cosmopolitan, but Balamuthia is found only in
warm climates. Potentially pathogenic species live in
freshwater (particularly in warmed-up water, e.g. in
swimming pools, water containers, aquaria, other heated
bodies of water). They usually tolerate a broad range
of temperatures (2-40 °C). Cysts may persist under
moist conditions for long periods. The particularly
resistant cysts of Acanthamoeba spp. even survive
dryness for several years. Pathogenic bacteria have been
demonstrated in cysts of Acanthamoeba, Naegleria and
Hartmanella spp. (e.g. Legionella pneumophila, Listeria
monocytogenes, Pseudomonas spp.).
Clinical signs. Free-living amoebae may cause diseases
in animals. Thus, infections of the CNS and other tissues
have been reported in amphibia, reptiles, fishes, birds
and mammals. Amoebic meningoencephalitis has been
observed in tapirs, horses and orang-utans. Clinical cases
in humans are rare but often severe and sometimes even
fatal, e.g. primary amoebic meningoencephalitis (PAM) Q)
(agent Naegleria fowleri) or granulomatous amoebic
·u
C
encephalitis (GAE) caused by Acanthamoeba spp. and B. '6
Q)
mandrillaris. Acanthamoeba spp. are agents of keratitis, 2
in particular in people wearing contact lenses. c
Cll
C
·;::
Diagnosis, therapy. Free-living amoebae may be
J
Q)
cultured in various in vitro systems (see special literature)
and identified in tissue by histology and DNA analysis. .!;
There is currently no reliable therapeutic approach. >,
Ol
0
....
0
"cii
Cll
Cll
CL
 Part II. Parasites and parasitoses: protozoa

Selected references

Ali IKM (2015) Intestinal amebae. Clin Lab Med 35: 393-422.
Cateau E, Delafont V, Hechard Y, Rodier MH (2014) Free-living
amoebae: what part do they play in healthcare-associated
infections? J Hosp Infect 87: 131-140.
Bradford CM, Denver MC, Cranfield MR (2008) Development
of a poly merase chain reaction for Entamoeba invadens. J
Zoo Wildl Med 39: 201-207.
Hooshyar H, Rostamkhani P, Rezaeian M (2015) An annotated
checklist of the human and animal Entamoeba (Amoebida:
Endamoebidae) species - a review article. Iran J Parasitol
10: 146-156.
Jacobson ER (2007) Infectious diseases and pathology of
reptiles. Color atlas and text. CRC press, Boca Raton, FL.
USA. ISBN 0-8493-2321-5.
Matsubayashi M, Suzuta F, Terayama Y, Shimojo K, Haritanl
M, Shibahara T (2014) Ultrastructural characteristics and
molecular identification of Entamoaba suis isolated from
pigs with haemorrhagic colitis: implications for pathogenicity.
Parasitol Res 113: 3023-3028.
Parija SC, Manda! J, Ponnambath DK (2014) Laboratory
methods of icientification of Entamoeba histolytica and its
differentiation from look-alike Entamoeba spp. Trap Parasitol
4: 90-95.
Walochnlk J, Schelkl U, Haller-Schober EM (2015) Twenty
years of acanthamoeba diagnost1CS in Austria. J Eukaryot
Microblol 6 2: 3-11.

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7. Phylum Microsporidia (syn. Microspora)

7.1 Class Microsporea ctl

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·;;::::
7.1.1 Order Microsporida 0
a.
(/)

Disease: Microsporidiosls.
1II.. ,

Mikros (G): small; spora (G.): seed.

Microsporidia are small, unicellular, spore-forming

parasites with intracellular development. Previously
regarded as protozoans, they are now thought to be
a sister group of fungi and are therefore assigned to a
separate phylum within the superkingdom Opisthokonta
(► p. 46). There has been a proposal to indicate their
systematic affiliation by using the term 'Opisthokonta:
Microsporidia' instead of 'Fungi: Microsporidia'.

Summary
• Agents. To date, the phylum Mlcrosporidla comprises
at least 180 genera with 1,300-1,500 species which
parasltise a wide host range from protozoans to
mammals in terrestrial and aquatic environments. They
form characteristic, small (1-3 pm, rarely up to 9 µm
long), thick-walled spores ith typical orgar.ielles (e.g.
anchoring disk, polaroplast, polar tube, sporoplasm). General features. Microsporidia are small,
Spores are resistant In the environment and can remain unicellular, spore-forming parasites with intracellular
Infectious for long peri s. development. Previously regarded as one of the most
• Life cycle. Terrestrial ve ebrates become Infected by primitive eukaryotic lineages or as protozoans, they
Ingestion (presumably also by Inhalation) of spores or by are now thought to be a sister group of fungi and are
transplacental transmission of the agents. In the host, therefore assigned to a separate phylum within the
the nucleated sporopl m Is Injected by means of the superkingdom Opisthokonta. Relationships to fungi
polar tube from the spore Into a cell of the target organ,
are inter alia indicated by the presence of chitin and
predominantly the Intestine. The following Intracellular
trehalose in spores, as well as characteristics of protein­
development inclutles a proliferative phase with multiple
divisions (merogony) and the formation of sporea
coding and rRNA genes. Microsporidia have the smallest
(sporogony). eukaryotic genomes so far identified (2.3-19.5 Mb),
• Occurrence anct epldemlology. Mlcrosporldla h prokaryotic-size ribosomes, vesicular Golgi structures
a global distrib411on: about half of the gen and mitosomes, a relic version of mitochondria.
aquatic anim e wide host range al
parasites (e.g. todes, cestodes, Although related to fungi, Microsporidia exhibit Q)
which Micros live as 'hyp different and unique features, as manifested in the
·u
C

species are of I veterln morphology of spores. They are small (1-3, rarely up '6
Encephalitozoon cunicull In 9 µm long), their thick wall consists of a protein- and
Q)
�
osts, Encepha1 ozoon he/le carbohydrate-containing outer layer (exospore) and �
d N. ceranae in bees, and ctl
a chitin-rich inner layer (endospore). The spore wall C
lugea, Loma and Plelstoph ·;;::::
llem, E. lntestinalls, Ente
encloses the cytoplasm (sporoplasm) with one or two Q)

me other species are nuclei, a vacuole, and an extrusion apparatus. The latter
mans, especially In I consists of a polaroplast and a typical polar tube which is C

ludln AIDS attached to a mushroom-like anchoring disk and often >­

CJ)
0
coiled up around the sporoplasm with a genus-specific 0
number of coils (1 to >30) (► Figure 7.1). It is one of 'ui
the most remarkable features of Microsporidia that all ctl
these complicated structures are formed in a single cell. 0..
Part II. Parasites and parasitoses: protozoa

In infected cells, Microsporidia usually develop directly

Anchoring disk in the cytoplasm, separated only by the parasite's plasma
membrane which is often covered with a glycocalyx.
Exceptions are Encephalitozoon spp. which are enclosed
in a parasitophorous vacuole. Initially, the sporoplasm
develops into meronts, which multiply by binary or
multiple fissions (merogony). Subsequently, meronts
form sporonts, giving rise to sporoblasts that differentiate
to mature spores (sporogony).
Polar
tube
Pathogenesis and clinical signs. Throughout
merogony, Microsporidia do not induce serious cell
danrnge, which occurs only later in the sporulation
phase and is characterised by cell destruction and focal
granulomatous inflammation of surrounding tissues.
Depending on their location and extent, the clinical
picture varies. In clinical cases, infections may affect
individual organs (e.g. intestine, eye) or multiple organs.
Figure 7 .1. Microsporidia. Scheme of a spore (Graphics: IPZ, Infections in immunocompetent vertebrates (including
M. Mathys; after Curry 1998). humans) often take a chronic course and remain
asymptomatic. However, immunocompromised or other
predisposed hosts may suffer from serious disease with a
In contrast to other developmental stages, spores can fatal outcome. For example, in monkeys, dogs and foxes,
survive outside the host cell. particularly in young animals, acute infections with
high morbidity may occur, and rabbits can be affected
Microsporidia are of veterinary importance as agents by progressive and often fatal neurological forms of
of infections in domestic rabbits, cats, laboratory the disease.
animals, fur-bearing animals, dogs, birds, monkeys
in zoos, fish and insects (bees, silkworms). Since the Diagnosis. Although spores are small, they can be
beginning of the HIV pandemic, Microsporidia have detected in excreta (urine, faeces, sputum), tissues or
attained medical significance, mainly as opportunistic cerebrospinal fluid by light microscopy using sensitive
parasites in immunocompromised patients. staining methods (chromotrope and several fluorescent
stainings, e.g. Uvitex 2B•, Calcofluor•). However, these
Microsporidia infection in mammals methods do not usually allow a species-specific diagnosis.
Using electron microscopy, important features of
Life cycle. Microsporidia have rather uniform life genera or species can be detected. Serological methods
cycles. Here we refer to cycles involving terrestrial (ELISA, IFAT) to detect specific antibodies are now the
vertebrates which become infected by peroral uptake methods of choice for diagnosing persistent, unapparent
of spores or by transplacental transmission of the agents infections of E. cuniculi in rabbits, rodents, carnivores
(► Figure 7.2). Airborne infections are presumably and monkeys. Antibody detection is also suitable for
possible. When spores have passed to the digestive diagnosing clinical cases, serocpidemiological studies
tract, the polar tube is extruded explosively within <2 and monitoring animal populations (rabbits, laboratory
seconds and thereby extended up to several I 00 µ111 animals, etc.). DNA-based methods (amplification,
length (diameter 0.1-0.2 µm). The elongation of the sequencing) for the detectIon of pathogens in excreta
polar tube might be due to recoiling and high elasticity, and tissues arc available for E. cuniculi and many
but the addition of material to the tip of the polar tube other Microsporidia species. E. cuniculi and other
has also been discussed. The vacuole of the spore is Microsporidia species (but not E. bieneusi) can be
regarded as a 'pressure vessel: providing the force for cultivated in several mammalian cell lines.
extruding the polar tube. Upon contact with a host cell,
the polar tube penetrates deep into the cytoplasm and
injects the nucleated sporoplasm. The mechanisms of
parasite spreading within the body are not yet fully
understood. In vitro, Microsporidia infect adjacent cells
in the same manner as described above. In addition,
spores can be phagocytised by macrophages and other
cells and probably transported therein. The subsequent
intracellular development includes a proliferative phase
(merogony) and the formation of spores (sporogony).
r 7. Phylum Microsporidia (syn. Microspora)
Family Nosematidae
Genus Encephalitozoon
Encepha/itozoon cunicu/i
Disease: Encephalitozoonosls.
En- (G prefix.): in; keplwle (G): head; zoon (G): animal.
Reference to location of parasites in the CNS.
Encephalitozoonosis in rabbits
Agent. E. cuniculi is morphologically uniform, but
several strains can be genetically and biologlcalJy
distinguished: strain I in rabbits and humans, strain ll
in mice, rats, cats and polar foxes, especially blue foxes
(Alopex lagopus), strain Ill in dogs (South Africa, USA)
as well as in South American monkeys and in humans,
and strain IV in humans, cats and dogs. These strains are
not strictly host specific; strains I-III are experimentally
infectious for mice or rabbits.
Life cycle. Rabbits become infected predominantly
by ingestion of spores, which are mainly excreted
in the urine of infected rabbits ( ► Figure 7.2). It is
probable that intestinal epithelial cells, macrophages or
endothelial cells are initially infected before the parasites
disseminate in the animal body and settle in various
organs (liver, lungs, kidneys, central nervous system,
etc.). After about 3-4 months, the kidneys in particular,
the brain and, less frequently, the heart are affected. In
addition, intrauterine infections occur.
Occurrence and epidemiology. E. cuniculi (strain
I) is the only known microsporidian species in rabbits.
In some European countries, larger groups of healthy
domestic rabbits exhibited seroprevalences of around
8% to >40%, but prevalences of 85-96% were recorded
from rabbits with neurological symptoms. Horizontal
infections by ingestion of spores are the rule, whereas
intrauterine infections are rare. Main reservoir hosts
are domestic rabbits with asymptomatic infections; wild
rabbits can regionally play a role as infection sources. E.
cuniculi has apparently not been demonstrated in hares.
The spores of E. cuniculi can remain infective for months
in a moist, cool environment. Spreading of spores within
a group of animals occurs through the contamination
of the environment and food. The infection can be
introduced into colonies by asymptomatic infected
rabbits.
Immunology. In immunocompetent mammals, an
infection with E. cuniculi usually takes a chronic course,
characterised by persistent inflammation and high
antibody titres. Crucial for effective protection is the
cell-mediated immunity. Similar to other intracellular
ectiona, unrculfiiifRt:ioi'iscinirul�b-stantia:l
IL-12 production by macrophages or dendritic cells
This leads to the meue of Th 1 cytokines in tissues
and in the circulation, particularly of IFN-y, but no
of Tb2 cytokines, e.g. IL-4. The induction of a CDS
T-cell response hu an important prot«tlve function. CCI
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·;::
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Pathogenesis and pathology. The pathogenesi a.
e
Cl)
is chancterlsed by focal inflammatory processes. A
(.)
n«ropsy, only a few lesions may be found or m� �
Irregular, indented foci in the renal cortex. HJstological
findings: Kidneys: focal or segmental lympho
plasmacellular, interstitial nephritis with differen
sr-�...'--"'"''"'-'Obro J • br in· focal non uppur-ativ
meningoencephalitis with perivascular lymphocytic
inflltrates and astroglJosls. In histological sections of
foci of inflammation, parasites are often invisible (this is
especially true for HE-stained sections) ( ► Figure 7.3).
On the other hand, nests of E. cuniculi can occasionally
be found in appa. rently intact tissue. Parasites are rarely
detected in lungs, liver and heart. Clinical symptoms are
primarily due to lesions in the CNS.
Clinical signs. £. cuniculi infections can remain
asymptomatic for years. The reason why clinical signs
occur in a proportion of infected rabbits, regardless of
age, is not known. The disease most commonly manifests
in torticollis, opisthotonus or ataxia, hyp eresthesia or
paralysis, weight loss and wasting. Furthermore, cases
of uveitis are described ( ► Figure 7.3b).
Diagnosis. In cases of suspected encephalitozoonosis,
an investigation of specific serum antibodies is indicated.
In the differential diagnosis, infestations with Psoroptes
ear mites and pasteurellosis have to b e taken into
account, among others. Post mortem diagnosis is based
on histological finding of characteristic lesions.
Therapy and control. In rabbits, treatment with
fenbendazole (daily 20 mg/kg b.w. for 4 weeks directly
per os or administered in feed pellets) has proven to
be effective. In cases with neurological symptoms,
corticosteroids (e.g. dexamethasone) may additionally
be applied to inhibit inflammatory processes in the
brain. The dosage must be in the anti-inflammatory
and not in the immunosuppressive range. Albendazole
is used successfully in humans against Encephalitozoon
species. However, this benzimidazole is not approved
for rabbits (risk of side effects).
As preventive measure against the introduction
of E. cuniculi spores into rabbit p opulations, a high
standard of hygiene should always be maintained. In
breeding flocks at risk, spreading of the infection can C
be largely controlled by serological surveillance and >.
-
0)
isolation of seropositive animals. Animal exhibitions 0
0
and group maintenance of young animals in pet shops ·en
are associated with an infection risk for the involved �
CCI
rabbits. Prophylactic administration of fenbendazole Q_
Part II. Parasites and parasitoses: protozoa

Infection of intestine,
kidney and brain

Excretion of spores
in urine

Transplacental
Infection infection
per os

-
Nucleus

Sporo­
plasma '. : -� 0z' . ·" .
i\ 'c.'\ �,· ( ·:'
,... eront
t·
� '

), --..., .

•�f-i==---,,,�-
I

@
:, •,. ·-.'.!'.;:-.' ·"' Spore
of a cell
- - - - -

Parasitophorous
vacuole

Spore

Agure 7.2. Life cycle of Encsphalitoz.oon cuniculi (Graphics: IPZ, S. Ehrat).

at therapeutic doses suppressed the infection in rabbits

after experimental admini tratfon of spores.£. cuniculi
spores can be killed by heat >70 °C and disinfectants
(2% lysol, 10% formalin or 70% alcohol, application
tjme al least 10 min).

Encephalitozoonosis in other species
• Dog, fox and mink. E. cuniculi infections in dogs
(strains III and IV) and blue foxes (strain II) occur
as sporadic, acute encephalitis-nephritis syndrome in
puppies which was previously confused with distemper.
Horizontal and vertical (intrauterine) infections ensure
the persistence of E. cuniculi in infected dog and fox
populations. Dogs, excreting spores in the urine, are
infection reservoirs. Furthermore, spores from rodents
can contaminate food in fur farms (blue foxes, minks).
In Iceland, the prevalence of E. cuniculi in wild polar
foxes (Alopex lagopus) was 12%, in American minks
(Mustela vison) 8%.
• Cats. Recently (2011 ), E. cuniculi was diagnosed in
Vienna as the causative agent of recurrent uveitis and
cataracts in 11 cats. All these cats had positive antibody
titres in an E. cuniculi-IFAT. Molecular analyses revealed
in 7 cases the strain II (commonly found in rodents) of
E. cuniculi, but in 4 cases genotype IV was identified. In
cats, ocular encephalitozoonosis should be considered
in differential diagnosis.
• Monkeys. Spontaneous infections with Encepha­
litozoon-like Microsporidia have been described
previously in red titi monkeys ( Callicebus moloch
cupreus) and squirrel monkeys (Saimiri sciureus) in
US zoos. In emperor tamarins (Saguinus imperator) and
golden lion tamarins (Leontopithecus r. rosalia) from
European zoos, E. cuniculi strain III (found in dogs)
has been identified.
• Horses. In some countries, serum antibodies
against E. cuniculi were detected in horses, e.g. in 4.8%
of 105 horses in the USA. Of 377 horses in CZ, 6.9%
excreted E. cuniculi and 17.3% E. bieneusi in faecal
samples as determined with a nested PCR. E. cuniculi
has rarely been reported as cause of abortion and
placentitis in mares. After experimental oral infection
of horses with spores of E. cuniculi, parasite DNA was
7. Phylum Microsporidia (syn. Microspora)
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·;::
0
Q.
Cl)
g
2
first detected in spleen (7 d p.i.), thereafter in many
organs (including brain, liver, intestine etc.) as well in
faeces (28-42 d p.i.), and finally (63 d p.i.) only in lung,
kidney and caecum. Histological examinations did not
reveal any parasite stages.
• Birds. Encephalitozoon-like spores have been
detected in various disease outbreaks in aviaries, mainly
in parrot species (Psittacidae). E. hellem was identified
as cause of mass mortality of budgerigar chicks, and
as a first record in a yellow-streaked lori ( Chalcopsitta
scintillata) imported from Indonesia to Switzerland. E.
hellem can persist in birds and cause disease outbreak
under stress, such as transportation or overcrowding
of cages. Birds represent potential infection sources
for humans.
Genus Nosema
Nosema apis and Nosema ceranae
- Diseases: Nosernosls and type C nosem0sis in
h0ney bees.
Nosos (G): disease; apis (L): bee.
Agents and life cycles. Nosema species are mainly
found in insects. Nosema apis and N. ceranae are of
special significance as causative disease agents in adult
honey bees (Apis mellifera). These two species can be
distinguished using genetic and morphological criteria,
including spore morphology. N. apis has large spores
(6.0x3.0 µm) with more than 30 coils of the polar
tube, compared to spores of N. ceranae (4.4x2.2 µm)
with 18-21 coils. The direct life cycle of both species
starts with the ingestion of mature spores with food or
water. The parasites infect epithelial midgut cells, in
which parasite stages develop directly in the cytoplasm
(without parasitophorous vacuole) by formation of
Part II. Parasites and parasitoses: protozoa

meronts, sporonts and sporoblasts which give rise to

spores. After disintegration of infected cells, spores
are released and infect adjacent epithelial cells or are
excreted in faeces.

Occurrence and epidemiology. For decades, N.

apis was thought to be the only cause of nosemosis
in honey bee colonies worldwide. However, after N.
ceranae was described as a new species in Asia (1996),
this species was later identified in naturally infected bee
colonies in Asia, Europe, North and South America.
In many regions, N. ceranae is now the predominant
species causing the so-called type C nosemosis, which
is of special significance in countries where professional
beekeeping is practiced. Simultaneous infections of
bee colonies with both species have been recorded; for
example, 3 out of 9 Swiss bee colonies infected with N.
ceranae also harboured N. apis. It seems that N. ceranae is
better adapted than N. apis to complete its reproductive
cycle under variable temperature and environmental
conditions (see specialised literature). Spores of both
species can contaminate the honey.

Signs of disease. Lysis of infected midgut epithelial

cells leads to metabolic and behavioural disorders,
starvation, and eventually death of infected bees. The
infection can spread from the midgut to other tissues,
such as malpighian tubules, salivary glands and fat body.
Mortality is variable, depending on many factors; it
ranged between 11 and 93% in bees experimentally
infected with nosema spores. Pathogenicity is not
always expressed, indicated by frequent asymptomatic
infections of bees shedding Nosema spores.
Both Nosema species were associated with the Colony
Collapse Disorder (CCD), a multifactorial condition
which has caused major losses of honey bee colonies
in the northern hemisphere (USA, Europe) over the
past decade. Studies in Spain have suggested a causative
role of N. ceranae in the aetiology of CCD, but in colder
climates such an involvement was ruled out. On the
other hand, there is evidence that Varroa destructor
( ► p. 424) can play a major role as cause of winter
colony losses, due to its direct detrimental effects and
its role as a vector of several bee viruses. Three viruses
are held responsible for large-scale winter losses of
bees, namely d.eformed wing virus (DWV), acute bee
paralysis virus (ABPV), and Israeli acute bee paralysis
virus (IABPV). Currently, it cannot be ruled out that
various synergistic pathogens contribute to the aetiology
of CCD and similar conditions.
Diagnosis. Microscopic detection of spores in the
bee's gut ( ► Figure 7.4) indicates only the presence
of the parasite in a bee colony, but does not alJow
conclusions to be drawn regarding pathogenic effects
as spores are also excreted by healthy bees. Therefore,
other parameters have to be considered, such as losses
of bees and epidemiological conditions.
Figure 7.4. Nosema ap/s: spores (5-9x3-4 µm) in the gut of a
bee, stained (Photo: IPH, K. Friedhoff).
Control. Authorised therapeutic drugs to control
nosemosis are currently not available. Heavily infected
bee colonies are eliminated. [n less heavily infected
colonies attempts should be made to create favourable
conditions for self-control (combs contaminated
with faeces or equipment should not be used; clean
hives, good location, breeding selection for vitality,
etc.). Official preventive or control measures are only
prescribed in a few countries ( ► p. 607).
Microsporidia infections in fish
Family Pleistophoridae
Numerous species from 20 microsporidian genera
occur in fish. The infected host tissue can respond
by producing so-called xenomes which are due to
enormous hypertrophy (0 up tol4 mm) and structural
changes of host cells (mostly connective tissue or
cells of mesenchymal origin). Just a few examples of
Microsporidia pathogenic to fish are presented herein.
Genus Loma
Loma salmonae
L. salmonae forms on secondary gill lamellae in trout
whitish xenomes (S:0.4 mm) which substantially restrict
the functions of the gills in heavy infections.

Genus G/ugea
G/ugea anomala
In almost all organs of sticklebacks ( Gaste rosteus
aculeatus), G. anomala causes xenomes which are easily
recognisable as prominent bumps (�4 mm) on the skin.
Genus Pleistophora
Pleistophora hyphessobryconis affects about 18 species
of ornamental fish (tetras, barbs, goldfish, etc.), infecting
muscles and oocytes in the ovary. Infected fish lose
their colour, affected muscles appear as white spots
under the skin, heavily infected fish die. Most spores
are concentrated in subcutaneous tissues; they penetrate
the skin and are thus released to the environment. They
can be detected microscopically in skin swabs. Decaying
fish release more spores.
Zoonotic importance. Until the mid-1980s there
were very few reports of human infections with
microsporidia. After the outbreak of the HIV pandemic,
several genera of Microsporidia have been identified as
opportunistic parasites, mostly in immunocompromised
patients (AIDS, organ transplantation, etc.), including
Encephalitozoon, Ente rocytozoon, Pleistophora, Trachi­
pleistophora, Anncaliia (previously Brachiola), Nosema,
Microsporidium and Vittaforma. Species of the first 3
genera mentioned are also found in vertebrate animals,
thus making them potentially zoonotic. Before the
introduction of the antiretroviral chemotherapy against
HIV infections, the most common species in humans,
Enterocytozoon bieneusi, was responsible for about
15% of AIDS-associated diarrhoea cases in Europe.
This species causes rarely self-limiting traveller's
diarrhoea in immunocompetent persons. E. bieneusi
also occurs in various vertebrate animals (primates,
dog, cat, pig, cattle, chicken). However, most of these
isolates genetically differ from human isolates. Currently,
there is no evidence of zoonotic transmission of E.
bieneusi. Zoonotic transmission is likely to occur in
Encephalitozoon cuniculi (all strains) (animal hosts:
rabbits, carnivores, etc.), E. intestinalis (animal hosts:
primates, cattle, pig, dog, chicken, etc.), E. hellem
(animal hosts: birds), and Pleistophora sp. (animal hosts:
fish). E. cuniculi can cause disseminated infections in
immunodeficient persons affecting especially kidneys
and CNS, but also other organs.
7. Phylum Microsporidia (syn. Microspora)
Selected references-=------•
Benz P, Maass G, Csokai J, Fuchs-Baumgartinger A,
Schwendenwein I, Tichy A, Nell B (2011) Detection of
Encephafitozoon cunicufi in the feline cataractous lens. Vet
Ophthalmol 14: 37-47. co
"O
Capella-Gutierrez S, Marcet-Houben M, Gabald6n T (2012) ·;:::
0
Phylogenomics supports microsporidia as the earliest Cl
(/)
diverging clade of sequenced fungi. BMC Biol 10: 47.
Dainat B, Van Engelsdorp D, Neumann P (2012) Colony
collapse disorder in Europe. Environ Microbiol Rep 4: 123-
125.
Dalnat B, Evans JD, Chen VP, Gauthier L, Neumann P (2012)
Predictive markers of honey bee colony collapse. PLoS One
7(2):e32151.
Guscettl F, Mathis A, Hatt JM, Deplazes P (2003) Overt
fatal and chronic subcllnical Encephalitozoon cuniculi
microsporidiosis In a colony of captive emperor tamarins
(Sagulnus /mperator). J Med Primatol 32: 111-119.
Hlges M, Meana A, Bartolome C, Botfas C, M artfn­
Hernandez R (2013) Nosema ceranae (Microsporidia), a
controversial 21st century honey bee pathogen. Environ
Microbial Rep 5: 17-29.
Holt HL, Aronstein KA, Grozinger CM (2013) Chronic
parasitization by Nosema microsporidia causes global
expression changes in core nutritional, metabolic and
behavioral pathways in honey bee workers f,4pis mellifera).
BMC Genomics 14: 799.
Mathis A, Weber R, Deplazes P (2005) Zoonotic potential of
the microsporidia. Clin Microbial Rev 18: 423-445.
Stentlford GD, Feist SW, Stone OM, Bateman KS, Dunn
AM (2013) Microsporidia: diverse, dynamic, and emergent
pathogens in aquatic systems. Trends Parasitol 29: 567-578.
Suter C, Mathis A, Hoop R, Deplazes P (1998) Encephalitozoon
heffem infection in a yellow-streaked lory (Chalcopsitta
scintiffata) imported from Indonesia. Vet Rec 143: 694-695.
Suter C, M0ller-Doblles UU, Hatt JM, Deplazes P (2001)
Prevention and treatment of Encephalitozoon cuniculi
infection in rabbits with fenbendazole. Vet Rec 148: 478-480.
Vavra J, Luke§ J (2013) Microsporidia and 'the art of living
together'. Adv Parasitol 82: 253-319.
Wagnerova P, Sak B, Kvetoi\ova D, Marsalek M, Langrova I,
Kvac M (2013) Humoral immune response and spreading of
Encephalitozoon cuniculi infection in experimentally infected
ponies. Vet Parasitol 197: 1-6.
Weiss LM (2011) Microsporidiosis. In: Palmer S, Soulsby
L, Torgerson PR, Brown DWG (eds.) Oxford textbook of
zoonoses. 2nd ed. Oxford, UK: Oxford University Press, pp.
596-612. ISBN 978-0-19-857002-8.
 8. Phylum Myxozoa

8.1 Classes Myxosporea and Table 8.1. Selective and simplified classification of the phylum
Malacosporea Myxozoa (also ► Table 1.1, p. 17).

I
Myxa (G): mucus; zoon (G): animal, living being. .
�tr�Jj'1\[i}L,i.',o�:1,;i_1,1,0 ,\'11-11 1,.,',i·,,Jy:.,)-
�"' '
Class Order Genus
Summary
Myxosporea Bivalvulida Enteromyxum,
• Agents. Myxozoa are microscopically small, multicellular Henneguya, Hofere/lus,
parasites related to the Cnidaria. They are characterised Myxidium, rtyxobolus,

--
by spores, containing one to several polar capsules and Sphaerosr,,.: ·a,
one to many infective germs (sporoplasms). The/ohanc · 'L'S
• Life cycle. Life cycles are only known from a relatively Multivaivulida Kudoa
small number of fish parasites. Most of them have 1--·

two-host cycles with asexual reproduction and �cosporea Malacovalvullda Tetracapsu:aides

spore formation In fish and sexual development In
, I Invertebrates (e.g. annelids), also with formation of ( ► Figure 8.1). The polar capsules are morphologically
spores. Direct cycles with fish to fish transmission have almost identical to nematocysts of Narcomedusae
been described for species of the genus Enteromyxum. (Coelenterata). Myxozoa are also genetically closely
• O ccurrence and epidemiology. Most of the >2,000 related to the Narcomedusae. Like other metazo ans,
species of Myxozoa are cosmopolitan parasites of fish,
Myxozoa are characterised by a high degree of cell
both In marine and freshwater environments. Some
species can cause considerable economic losses In
differentiation (1 generative cell type and 3 somatic
wild or cultured fish populations. Some species have
types); they form desmosomes, tight junctions and
been recorded from reptiles and amphibians and very collagen and possess mitochondria.
few from birds and mammals.
• Clinical signs. Examples of fish diseases caused by Current knowledge on life cycles ofMyxozoa parasitising
Myxozoa are: whirling disease of salmonlds (agent: fish is still sketchy. About 35 species have a heteroxenous
I cycle, including the following phases: (a) asexu al
Myxobo/us cerebra/ls), proliferative kidney disease of
salmonlds (agent: Tetracapsulo/des bryosalmonae), development in fish with production of myxospores
swimming bladder and kidney sphaerosporosls of carps( = myxospora spores), which are infective for
(agent: Sphaerospora dykovae) and a muscle Infection
invertebrates (e.g. Oligochaeta); (b) sexual development
(agent: Kudoa thyrsltes).
in invertebrates with formation of another type of spore,
• Control. National directives regarding preventlo!'.1 and
control of some of these diseases should be followed.
the actinospores, which are infectious to fish. The
formation of two types of spores within a single species
is a peculiarity of the Myxozoa. In a few species of the
General features. Myxozoa are microscopically small genus Enteromyxum, monoxenic cycles (direct fish to
metazoan parasites, which were originally classified as fish transmission) have been described.
protozoans, but are now regarded as organisms related to
the Cnidaria, Most of the more than 2,000 known species The two spore types that develop from polynuclear
are parasites of marine and freshwater fish, including precursors have the following features:
some of economic importance. Some species are strictly • Myxospores (abbreviation: M-spores) (0 usually
host specific, while others have a wide host range. In 10-20 µm) are round, oval or have another shape
addition to fish, some myxozoan species have been and are often equipped with species-specific annexes
Q)
found in invertebrates (see below), reptiles, amphibians, designed to delay sedimentation in water ( ► Figure
·o
C

'6 birds (ducks) and mammals (mole, shrews). Infections 8.1). A multi-valved, usually hard shell spore coat
Q)
� with Myxidium anatidum in ducks are more widespread surrounds up to 6 polar capsules and the infectious
cco in the USA than previously thought. Some myxozoan sporoplasm. Each polar capsule contains a spirally
coiled 'filament' (which is essentially a tubule) which
C species are listed in ► Table 8.1 and 8.2.
·;::
Q) is extruded upon infection of a host. M-spores are
Myxozoa are characterised by multicellular spores, formed in vertebrate hosts.
£ containing one to several polar capsules and one to • Actinospores (abbreviation: A-spores) with a basic
>,
0)
many amoeboid infective germs (sporoplasms). The triradiate symmetry, exhibit a wide range of different
0 polar capsules contain an extrudable filament (which shapes and are equipped with star or anchor-shaped
0
'iJi is essentially a tubule) with an anchoring function. The attachments. The spore contains sporoplasms and
spores are covered with a wall (shell), composed of one polar capsules ( ► Figure 8.1 ). These spores are
co
(L or several valves, which originate from transformed cells formed in invertebrate hosts.
 8. Phylum Myxozoa

...,...... ....
Table 8.2. Selected Myxozoa species.

SpeclH Fllhhoat Dlltrtbutlon Pr8clllollon ....

Myxobolus cerebra/is rainbow trout, other Eurasia, North and cartilage (especially Tublfex tubffex1
salmonids South America, head, gills, vertebral
Australia. New Zealand column)
M. encephallcus carp South-east Europe brain , ?3
M. neurobius river trout Eurasia CNS ?
M. cyprinl cyprinld fish Eurasia, North America muscles -
7
Tetracapsuloides salmonlds, pike Europe.USA kidneys Pfumstella sp. 2,
bryosalmonae
Sphaerospora ren/co/a carp
- - --
Europe, Israel, Australia blood, awlm bladder,
Frederlcella sp.2
8ranchlura sowerby,1,
-- - -- kl(!neya T. tublfex1
S. tincae tench Eurooe kidneys-- ,-
?
S. trottae river trout Central Europe kidney tubull Lumbrlcus sp. 1,
T. tublfex1
S. molnari carp Europe gills ?
Hoferellus cyprinl carp Eurasia kidney tubull Nais sp. 1
Myxidium lieberkuehnl pike Europe, North America kidney tubull, urinary 7
bladder
M. giardl eel worldwide? skin, gills, Intestine, T. tubifex 1
kidneys
M. anatldum duck USA bile ducts ?
Kudoa thyrsltes salmonids, other fislil worldwide muscles, especially of ?
species marine fish
, So.
_ JiclmyXY_m fegatl shrews CZ,PL bile ducts, liver ?
1 Annelida fjointed worms).
2 Bryozoa.
3 ? = unknown.

A selection of Myxozoa species of fish is listed in
► Table 8.2. Ribosomal DNA sequences are known
from about 60 myxozoan species and can be used for
species identification and phylogenetic studies.
8.1.1 Order Bivalvulida
Genus Myxobolus
Myxobolus cerebra/is
Disease: Whirling disease ira salrmionil!ls.
Agent. Myxobolus cerebralis, the causative agent of the
whirling disease of rainbow trout and other salmonids,
forms ovoid, 2-valved M-spores(about 9x7 µm) with 2
ro
0
were formerly regarded as distinct species parasitising
Tubifex).
X
>,
�
The spores inject the tips of the extruded polar filaments
into glandular openings or into epithelial cells, thereby
allowing the sporoplasms to invade the tissue. From the
portal of entry the parasite migrates through intercellular
spaces into the cartilage of head and skeleton. At the
same time, a complicated cycle of cell division takes place
that ends with the formation of sporoblasts, multicellular
pansporoblasts and finally with the development of
myxospores( ► Figure 8.1). These spores, released after
death of the fish, are taken up by Tubifex worms. In these
invertebrates, multinuclear actinospores are formed after
asexual multiple fissions and a gamogony. These spores
Q)
are enclosed in multi-valved shells and are equipped with C
·c3
anchor-shaped attachments( ► Figure 8.1). The cycle
is closed when sporoplasms from A-spores penetrate Q)

polar capsules. The sporoplasm contains 2 nuclei; further into tissue of fish where they continue to develop.
nuclei are present in polar capsules and the valves of the Since the sexual phase of development takes place in cu
C
shell( ► Figure 8.1). invertebrates, they are classified as definitive hosts and ·;::
Q)
fish as intermediate hosts.
Life cycle. Trout or other fish acquire the infection by .s
ingestion of mud tube worms( Tubifex tubifex, Annelida) Occurrence and epidemiology. M. cerebralis, >,
Ol
containing infectious A-spores, or by spores that float first described in 1898 as the cause of whirling disease 0
in the water. Floating spores can also attach to the skin, of rainbow trout in German fish farms, was probably
the mouth or the epithelium of the gills(these A-spores initially a harmless parasite of river trout (Salmo trutta) in
·encu
Central Europe and north-east Asia. After introduction
 Part Ill. Parasites and parasitoses: metazoa

Infection with
free A spores
�--�
---
Infection with
G) � �
A spores in / Asexual multiplication in fish
Polar
--
with formation of M spores
il
Tubifex
---�-- _ capsules
Sporoplasm
,o;;t

M spore

Polar capsule
of A spore
i;,;

Sporoplas,ns

A spore

In Intermediate host asexual and sexual

multiplication involving intermediate stages
(not sho n), and formation of A spores

Figure 8.1. Life cycle of Myxobo/us cerebra/is (Graphics: IPZ, S. Ehrat; after Mehlhorn and Piekarski 2002).

of rainbow trout (Sa/mo gairdneri), the parasite spilled
over to this highly susceptible fish species and was
distributed by fish trade to other European countries as
well as to North and South America, Australia and New
Zealand. This process was associated with an increase
of virulence, so that mortality rates of 80-90% occurred
in river trout. Overall, about 11 salmonid species arc
susceptible to M. cerebralfs, including species of trout,
char, and salmon.
A water temperature of 16 °C is most favourable for the
development oflhe parasite. In Central European rivers,
such favourable temperatures are reached in spring or
early summer, when young fish (fry, fingerlings) are at the
most susceptible age, because the proportion of cartilage
in the skeleton is high. Young fish acquire the infection
as early as in the yd week of life. Tubifex worms become
infected with M-spores that are released after the death
of infected fish to the water and the bottom sediment
where they can survive for years. The development
of the parasite in the worms until release of A-spores
takes 2-3 months; these spores remain infectious for
approximately 2 weeks. Developmental stages in Tubifex
do not survive at ambient temperatures >25 °C.
Pathogenesis and clinical signs. The agents
multiply in intercellular spaces in the cartilage tissue
offish. The so-called 'plasmodial stages' of M. cerebra/is,
with finely branched processes ('pseudopodia') and a
diameter of 20-40 µm, divide and form large foci in
the cartilage, which is enzymatically lysed. In addition,
chondrocytes are phagocytised by the plasmodia. This
especially concerns the cartilage of the head (skull, jaw,
gills) and spine. Symptoms appear 2-3 months p.i. and
include circular and uncoordinated movements due to
disturbance of balance, and blackening of the posterior
third of the body. This discoloration is attributable to
disorders of innervation of the skin and the control of
melanocytes. In young, susceptible fish mortality can
reach 90%. With increasing ossification of the skeleton,
fish become resistant. Older fish that survive an infectio n
often suffer from deformities of skull and spine.

Diagnosis. Symptoms of the whirling disease and
the detection of parasite stages (sporoblasts, spores)
in histological sections of head cartilage or in touch
preparations of tissues (Giemsa staining) lead to a
diagnosis. Species identification is possible using
morphological features and molecular techniques.
Serological methods have not been successful.
Control. To protect juveniles from high exposure, it
is recommended to transfer trout fry to earthen ponds
only around the age of 4 months (5-7 cm in length).
The rearing ponds should have a sediment-free ground
(concrete or plastic cover) that can easily be cleaned
and disinfected. Whirling disease is notifiable in many
countries.
Genus Sphaerospora
Sphaerospora dykovae (previously S. renicola)
Disease: Swim bladder Inflammation (S81) and
kidney sphaerosporosis In carps.
Agent and life cycle. Sphaerospora dykovae is
the causative agent of two diseases, chronic swim
bladder inflammation (SBI) in carp fry and kidney
sphaerosporosis in carps. S. dykovae forms multicellular,
proliferative stages floating in the blood of fish, so-called
Csaba cells (blood phase). Continuing divisions can lead
to a significant increase of these stages in blood. After
migration of such cells to the swim bladder, complexes
of up to 30 primary cells are formed (so-called K cells),
whose function is still unclear (swim bladder phase). A
third phase follows in renal tubules with sporogony and
formation of spherical spores M (0 6-8 µm).
Occurrence. SBI has been described so far in Europe
and in Israel. Prevalences reached 70-100% in young
carps under intensive rearing conditions. Only carp
fry is affected by acute disease; carps in the 2nd and 3rd
year of age are resistant.
Pathogenesis and clinical signs. In the swim
bladder the parasites cause an exudative-proliferative
inflammation with bleeding, oedema, and an enormous
thickening of the wall due to intensive proliferation
of connective tissue. In this case, the lumina of
bladder chambers are narrowed. In the acute phase,
the infection can also lead to peritonitis and kidney
hyperplasia. Clinical signs occur predominantly in
3-4 months old carps, which exhibit disturbances of
balance and movement as well as growth retardation.
The mortality cannot be clearly determined because
additional infections with Sphaerospora molnari, other
Myxozoa, coccidia, cestodes ectoparasites, etc., usually
occur in summer, possibly contributing to pathogenicity.
8. Phylum Myxozoa
Sporogony stages in renal tubules initially cause
hypertrophy and dystrophy of epithelial cells as well
as dilatation of tubules, which are massively filled with
parasites and are thus clogged. Despite these changes,
renal function may remain largely intact. The gross co
lesions are usually inconspicuous. -0
::i
>
Diagnosis and control. Microscopic detection of S. co>
0
dykovae stages in touch and compression preparations (.)
co
of swim bladder and kidney, in blood smears and in co
histological sections of the swim bladder. Necropsy 2
findings: swim bladders or yellowish brown, peritonitis
and adhesions to adjacent organs (kidney, liver, and
intestines). Specific control measures are not available.
8.1.2 Order Malacovalvulida
Genus Tetracapsula
Tetracapsu/oldes bryosalmonae (syn.
T. renlcola)
Disease: Proliferative kidney disease (PKD) in
salmon Ids.
Agent. The nature of the agent, previously designated
as PKX pathogen, has long been a mystery until
comparisons of 18S rDNA revealed that it is genetically
Cu
identical to parasite stages from bryozoans (Bryowa). 0
N
These stages have previously been described as a distinct 0
X
species under the name Tetracapsuloides bryosalmonae. >,
2
Today, the name is valid for the causative agent of PKD
whose developmental stages use both fish and bryowans
as hosts.
Life cycle. Current knowledge of the life cycle of
T. bryosalmonae is still incomplete. Infectious stages
originating from bryozoans infect fish through the gills
and are probably transported via the blood to various
internal organs. There, first multiplication stages occur
that are not involved in sporulation and are therefore
referred to as extrasporogenous or presporogonous
stages. Following this, sporogonic stages and spores
develop in the lumen of renal tubules. In experiments,
kidney homogenate of infected trout was infectious to
bryozoans.
Occurrence. Outbreaks of PKD have been observed in
rainbow trout, river trout, brook trout and Arctic char,
Atlantic salmon, grayling and pike. PKD occurs both
in fish farms and in the wild, and is one of the major
diseases of rainbow trout in Europe and North America,
and there also of the Pacific salmon (Oncorhynchus spp.).
In Europe, PKD occurs seasonally, beginning with rising
water temperatures in summer until autumn. Surviving
fish seem to be protected against reinfection.
 Part Ill. Parasites and parasitoses: metazoa
Pathogenesis and clinical signs. In kidneys, the
infection causes lesions from mild hyperplasia of the
interstitial kidney tissue to massive granulomatous
reactions with intensive proliferation of connective
tissue and displacement of glomeruli and tubules. In
other organs (spleen, liver) inflammatory reactions
occur. Symptoms include apathy, skin darkening,
exophthalmus, swelling of the abdomen, anaemic gills
and abnormal swimming movements.
Diagnosis. Necropsy findings: swelling of the kidney
with nodular protrusions and characteristic whitish grey
spots (granulomas), which coalesce in advanced cases;
granulomas in spleen and liver; ascites. Histological and
immunohistochemical detection of the agent.
Control. So far there are no specific control measures
available. Official directives, existing in some countries,
should be followed. Vaccine development and breeding
of resistant trout are ongoing.
8.1.3 Order Multivalvulida
GenusKudoa
Kudoa thyrsites (muscle parasite of fish)
Agent and life cycle. Kudoa thyrsites forms star­
shaped, 4-valved M-spores with 4 polar capsules.
Probably, K. thyrsites has an indirect life cycle. Most
Kudoa species are intracellular muscle parasites. In fish,
M-spores develop within 5-6 months p.i.
Occurrence. K. thyrsites is a globally common
parasite that can occur in many marine fish species
(e.g. Atlantic and Pacific salmon, Pacific halibut) and
river trout. There are also numerous other Kudoa species
parasitising fish. K. thyrsites has become a significant
problem in aquaculture (e.g. in salmon farms), where
prevalences of 50-70% have been reported.
Clinical signs. Kudoa infections cause unsightly
whitish cysts or soft spots in muscles, which appear
only after a few days in fresh, chilled fillets or after
smoking, thus dramatically reducing the market value.
lo rare cases, the infection causes disease.
Q)
C spores in terrestrial mammals: Soricimyxum fegati gen. et
·c::;
'6 Diagnosis. Typical star-shaped spores can be
Q)
� microscopically detected in native fluid pressed out of
muscle tissue. A PCR assay is described.
co
C
·;::
Q) Zoonotic importance. ln a few cases, Myxozoa spores
(Myxobo/us, Henneguya) have been found in human
,!; faecal samples, but it remained unclear whether they
>- originated from an infection or were 'pseudoparasites'
0)
passing through the human gut after consumption
'iii of infected fish. An infection was more likely in an
co immunosuppressed patient with diarrhoea and shedding
co
Cl. of spores of Myxobolus sp. persisting for 2 months.
In Japan, Kudoa septempunctata was recently (2012)
identified as a novel food poisoning agent. Affected
persons developed emesis and diarrhoea within 2-20
hours after consumption of raw fish (olive flounders).
- Selected references a:=::a::mm:::az:==aa
Bartholomew JL, Atkinson SD, Hallett SL, Lowenstine W,
Garner MM, Gardiner CH, Rideout BA, Keel MK, Brown
JD (2008) Myxozoan parasitism in waterfowl. Int J Parasitol
38: 1199-1207.
Canning EU, Okamura B (2004) Biodiversity und evolutio n of
the Myxozoa. Adv Parasitol 56: 43-131.
Eiras JC, Molnar, Lu VS (2005) Synopsis of the species
of Myxobolus Butschli, 1882 (Myxozoa: Myxosporea:
Myxobolldae). Syst Parasitol 61: 1-46.
EI-Matboull M, Hoffmann AW (1998) Light and electron
microscopic studies on the chronological development of
Myxobolus cerebra/is to the actinosporean stage in Tubifex
tubifex. Int J Parasitol 28: 195-217.
Grabner DS, EI-Matbouli M (2010) Tetracapsuloides
bryosalmonae (Myxozoa: Malacosporea) portal of entry into
the fish host. Dis Aquat Organ 90: 197-206.
Holzer AS, Hartigan A, Petra S, Peckova H, Eszterbauer E
(2014) Molecular fingerprinting of the myxozoan community
in common carp suffering swim bladder inflammation (S81)
Identifies multiple etiological agents. Parasit Vectors 7: 398.
Kawai T, Seklzuka T, Yahata Y, Kuroda M, Kumeda Y,
lijima Y, Kamata Y, Sugita-Konishi Y, Ohnishi T (2012)
Identification of Kudoa septempunctata as the causative
agent of novel food poisoning outbreaks in Japan by
consumption of Paralichthys olivaceus in raw fish. Clin Infect
Dis 54: 1046-1052.
Lorn J, Dykova I (2006) Myxozoan genera: definition and notes
on taxonomy, life-cycle, terminology and pathogenic species.
Folia Parasitol 53: 1-36.
Mackenzie K, Kalavati C (2014) Myxosporean parasites
of marine fishes: their distribution In the world's oceans.
Parasitology 141 : 1709-1717.
Moncada LI, L6pez MC, Murcia Ml, Nicholls S, Le6n F, Guio
OL, Corredor A (2001) Myxobo/us sp., another opportunistk:
parasite In lmmunosuppressed patients? J Clin Microbial
39: 1938-1940.
Pruneacu CC, Pruneacu P, Pucek Z, Lom J (2007) The first
finding of myxosporean development from plasmodia to
sp. n. (Myxozoa) from Sorex araneus (Soricomorpha). Falla
Parasitol 54: 159-164.
r.

Helminths

He/mim (G): worm.

Summary
, Tho torn, 'holmlnu,· 11 o colloctlvo nomo for vory
dllforont, parosltlo motoz.oons bolonglno to tho phyla
P1otynolr11lnthos (llotworms), Nomotodo (roundworms)
ond Aconthocopl'lolo (thorny-heodod worms).
Leeches (Annolldo) ore not regarded as helmlnths.
The flatworms Include the Trematode (flukes) and
the Cercomeromorpha with the Monogenea and the
Cestodo (tapeworms).
• Infections or diseases caused by helmlnths are referred
to as helmlnthoses: helmlnthology Is the science dealing
with helmlnths.

Table 9.1. Simplified and selective classification of helmlnths.

I
, I�) r'j� '.,1 11'• ,~{-j i-(II .I;�I "
',•1• ,,, •�lj ':1 >• -:;.;_r,� I 11)'
, I,,, II f 11' Jt
I

Order, Suborder (SO) Famlly Genua3

• Superfamlly -Subfamily

�lum: Pl�tyhelmln.!!_les (syn. Platyhelmlntha, Plathelmlnthes) (Flatworms)

Subphylum: Trematoda (Flukes)
en
_2!ass: Aspldog!strea (► p. 173) .c

-- ----
-
Class: Dlgenea (syn. Malacobothril) -
- -
� E
- --
-
Echinostomida Fasclolidae Fssclols, Fasclololdes, Fasclolopsls, Paratasciolopsls Q)

-- Echinostomatldae _§chin9£!!.ryphium,_Ichlnostoma, Hypoderaeum, �iophora

I

- -
Amphlstomida Paramphistomldae Callcophoron, Coty/ophoron, Explanatum, Gigantocotyle,

i Gastrothylaclda�
-Psramphlstomum
Rschoederius,
-- --
Gastrothytax
- Gastrodlscus
-- --

- -
-i--

Gaslrodiscldae Gastrodiscoides,

- -
t---
Plaglorchiida
- -
Dicrocoellldae . Dlcrocoellum, Eurytrema
Prosthogonlmldae
.... -
Prosthogonimus
J roglotrematld� _ C9!.lyriclum, Nanophyetus, Troglotrema

Opisthorchiida
Paragonimidae_
Oplsthorchlidae
.farag'lnlmus -
Clonorchls, Metort:his, Opisthorchis, Pseudamphistomum
Heterophyidae Apophallus, Heterophyes, Matagonimus
Strigeatida 4
Strigeidae Apatemon, Cotylurus, Parastrigea, Strigea Q)
C
Dlplostomidae5 A/aria ·c3
Bilharziella, Austrobilharzia, Gigantobilharzia, Heterobilharzia,
'5
Schistosomatidae Q)
Orientobilharzia, Ornithobilharzia, Schistosoma, Trichobilharzia
C'
�phylum: Cercomeromorpha ro
C
Class: Mon�enea (syn. PectobothriQ ·;::
__§yrodaotylida Gyrodactylidae Gyrodactylus

>-
Dactytogyrida Dactylogyridae Dactylogyrus, Neodactylogyrus C
PolvopiSJhOCOMifl" Dl�OCOMidae Diplozoon, Discocotyle 0)

'in
ro
D.
 Part Ill. Parasites and parasitoses: metazoa

Table 9.1. Continued.

karyota, Sub
(collective term)2
!
Order, Suborder (SO) I Family Genus3
• Superfamily - Subfamily
1
Class: Cestoda (Tapeworms), Subclass: Eucestoda
Diphyl/obothrium, Diplogonoporus, Ligula, Schistocephalus,
------
Pseudophyllida 0iphyllobothriidae
Spirometra
----- --------.l
!3othrlo�epha�ae B0!!_1riocephalus
Tr�a�nophoridae Eubori1rium, Triaenophorus
Cyclophyllida Mesocestoidldae Mesocesto/des ---------
Anoeiocephalldae
Bertie/la, Clttotaenia, Anop/ocephsls, Kllllgrewla, Monlezia,
Mosgovoyia, Paranoplocephala
- Anoplocephallnae

- T"y_�mosomatinae Av/tel/Ina, Stjlesia� T hysaniezia, Tlwsano_E0!!!_B__

!

Davaineidaa Davslnea, Ra/11/etlna

_Dilepldidae
Diplopylldlum, Dlpylldlum, Joyeuxlella__
Amoebotaenls, Choanotaenls
Dipylid�dae
Dlcranotaenia, Diorchis, Drepanidotaenia, Echinocotyle, Echinolepis,
Flmbriaria, Gastrotaenia, Hymenolepls, Microsomacanthus,
Hymenolepididae

____, Rodent�epls, Sobolevicanthus, Vamplrolepis

Taeniidae Ec_h _ln_o _coccus, T_ a_ e_ nl_ a____ _____
Ph um: Nem_!ltoda (sy� Nematozoa) (Roundworms or Threadworms)
--------------------.
Class: �cement� (Phasm_id_ia.,_)__
Rhabdilida Rhabditidae Caenorhabditis, Pelodera, Rhabditis
Cephalobid�e___ Ha!icephalob_us_ ,_Ti_ u_rb_a_ t�_ix ______ _
1---------+-----------------

--- Strongyli�
• Strongyloldea
Strongyloid�da� _Strongy_lo_ lde
_ _ s__ _________

_ a_ e_ ___-+-----------------------1
§!ro�gylld
Bidentostomum, Craterostomum, Oesophagodontus, Strongylus,
_!!lodontoph_ _ o_ ru_s ___________
- Strongylinae

- Cyathostominae Caballonema, Coronocyc/us, Cyathostomum, Cylicocyc/us,

Cyl/codontophorus, Cyl/costephanus, Cyllndropharynx,

- Gyalocepha�nae__ Gy�/0�P!}B!US-
Pe!!:_ovlf!__e"]_a, !!_o!erlostom_um
_ __

Chabertlldae
- Chabertllnae Chabertla
- Oe�ph��ostomlnae Oeso_h�fl0St0!!J_u_m__ _________ ____....
Syn9amldae ___ __ __
- Syn9a'!!)nae -- _!Jyathostoma, Mam!!1omono amus, St1]9B'!!_US
- Stephanurln!3e _ 1 s_Jephanurus____ _____ _ __

--
• Ancylostomatoidea Ancylostomatidae
� �cylos�omatlnae7 Ancylostoma, Globoce_pha�s. UtJE'!Jaria- - ---1
Q)

Bunostomum, Grammocephalus, Monodontef/a, Necator

·u
C

- Bunostominae
Amidostomatldae __ Amldostomum, Epomidiostomum
'6 -------1
• Trichostrongyloidea
Q)
�
c.' Trlchostrongylidae Apteragia, Cooperia, Graphidium, Haemonchus, Hyostrongy/us,
Marshallagia, Mecistocirrus, Obe/iscoides, Ostertag/a, Rinadia,
co
_ _ ___ Spiculopteragi� Teladorsagia, Trichostron!J�, fY u s -----1
-
C
·;::
::: ::..
Molineidae
Ornithostro� y_i
l _d ae_ _ Ornithostrongylus
Moline us,Nemato�d�ff�us�,�O�l/�u�la�n�u_______
�s ____,

+-
Nippostrongylus, Heligmosomoides
C
>-
0) Heligmonellidae
0
0 Dictyocaulidae Dlctyocaulus
·1n
co
0..
 Helminths

Table 9.1. Continued.

'"'"_ Allrilli•
........... tt
IQlllotlve 1Mn)I
-�ala)
�- .•

Order, Suborder (SO) Famltr Oenue3

• Sup«famltr -Subfamlly

-
.
• Melastrongyloidea 1 Metastrongylidae
r Protostrongytidae . Metastrongylus
Capreoca11AJs. Cystocaulus. Elaphostrongylus, Mueller/us,

- -
, Parela/:Jhostrongylus. Protostrongylus, Neostrongylus,
Spiculocaulus. Varestrongylus
--
- , -
Crenosornatidae ; Crenosoma. Otostrongylus. Troglostrongylus
Angiostrongyildae '. Anglostrongylus. Aelurostrongylus -
i -
L•--·
Fllaroididae Filaroldes, Os/erus
Pseudallldoe l Psouda/lus. Halocorcus --
-
-
Ascaridlda

�·-- • Cosmocercoldea Atraclldae Probst mo yr/a ---

• Ascaridoidea Ascaridldae - -
r---· -- ---- �scarfs, Bayllsascorls, Paro.scarfs, Toxasco.rls -
- Ascarldinae - -
-Toxocarinae -------- -
Toxocara -- -
--- -- --
Anisakidae Anlsakls, Contracaecum, Phocanema, Porrocaecum,
Pseudoterranova, Terranova --
• Heterakoidea Heterakidae
Ascaridiidae
Heterakis
Ascar/dla
---- - --
-
Oxyurida Oxyuridae Aspiculuris, Enterobius, Oxy�!!_s, Passalurus, Skrfal}inema, Syphacia
Spirurida -- -- -- ·-
SO Camallanina Camallanidae Carnal/anus -
Anguillicolidae Anguillicola ---
Philometridae Phllometra,
·- Philometroldes
--- ---- -- Cl)
.c.
Dracunculidae Dracunculus, Avioserpens
SO Spirurina .E
<D
• Gnathostomatoidea Gnathostomatidae Gnathostoma I
• Physalopteroidea Physalopteridae Physaloptera
• Thelazioidea Thelaziidae Thelazla._ Oxy__!pirura
• Rictularioidea Rictularlldae Pterygodermatites
• Spiruroidea Gongylonematidae Gongylonema
Spiruridae Parasplrura, Pff?!_osp.!_rura, Spirura
Splrocercldae Ascarops, Cyathospirura, Physocephalus, Simondsia, Spirocerca,
- Stref)_fopharagus
• Habronematoidea Habronematldae Draschla, Habronema, Parabronema, Procyrnea
Tetramerldae Tetrameres, Microtetrameres
Cystidlcolidae Cystidicola
• Acuarioidea Acuariidae Acuaria, Cheilospirura, Dispharynx, Echinuria, Streptocara,
Synhimantus Q)
C
• Filarioidea Filariidae Parafilaria, Stephanofi/aria, Suifilaria ·u
'6
Onchocercidae Q)
�
-Setariinae Setaria C'
Cll
- Dirofilariinae Dirofilaria, Loa C

- Onchocercinae Acanthocheilonema, Brugia, Cercopithifi/aria, Cutifilaria, -�

Dipetalonema, Elaeophora, Litomosoides, Mansonella, Onchocerca,
Wuchereria -�
-Splendidofilariinae Aproctella, Cardiofilaria, Chandtere/la, Pelecitus, Splendidofilaria >,
0)
0
- Lemdaninae Eufi/aria, Eulimdana, Sarconema 0
'cii
Cll
Cll
Q_
 Part Ill. Parasites and parasitoses: metazoa

Table 9.1. Continued.

um1: Anlmalla
)2

Order, Suborder (SO) Family Genus3

• Superfamily · - Subfamily

Class: Adenophorea (Ap�asmidia)

Enoplida
• Dioctophymatoidea Dioctophyma_ti_da_e__ o_,_o· c_ t_op
.c.. hy
-' - ng=y_li_d_es,_ _H�y_s_tl_ic_h_is______
' m_ a--',_6u_ _s_t�_o-'
__
+-1

• Trichinelloidea Trichuridae \
- Trichurinae Trichuris
- Capillariinae Aonchotheca, Bawscapillaria, Capillaria, Ca/odium, Euco/eus
Pearsonema
- Trichosomoidinae Anatrichosoma, Trichosomoides
Trichinellidae Trich inella
i------------�-- ..:_____.,________________________
Phylum: Acanthocephala (Thorny-headed worms)
Oligacanthorhynchida Macracanthorhynchus, Prosthenorchis
Echinorhynchida Acanthocephalus, Echinorhynchus
Polymorphida Filicollis, Po/ymorphus
Neoechinorhynchida Neoechinomynchus
1 Latin names of taxonomic categories ► Table 1.2, p. 18.
2 Collective term without phylogenetic and taxonomic significance.
3 In bold letters genera with particular importance for veterinary medicine, as zoonotic agents or as typical examples of the family; alphabetical
order of the genera.
• Syn. Strigeidida, Strigeida, Strigeatea.
5 Syn. Diplostomatidae.
6 Based on morphological and genetic findings it has been proposed to repeal the order Pseudophyllida and replace it by the new orders
Diphyllobothriida and Bothriocephalida (Kuchta el al., 2008).

Q)
C
13

�
ro
C:
·c:

J
.£
>­
CJ)
0
0
"iii
ro
.....
co
0..
p
9. Phylum Platyhelminthes (flatworms)
- Subphylum Trematoda
(flukes)
9.1 Class Digenea
Platyhelminthes: platys (G): flat, wide, he/mis (G): worm.
Trematoda: Trema (G): hole. Refers to the structure of
suckers.
The subphylum Trematoda contains parasitic
metazoans belonging to the classes Aspidognstren (syn.
Aspidobothrii) (about I 00 species) and Dlgenen {syn.
Malacobothrii) (digenetic trematodes) (approximately
18,000 species). Aspidogastrea are mostly small, up to
10 mm long trematodes with direct life cycles (egg -t
larva -+ adults) that parnsitise snails and mussels, as
well as the intestine or biliary tract of fish and turtles
(water tortoises); they are not considered here in detail.
The Digenea are of great importance in veterinary and
human medicine as causative agents of diseases.
Characteristics and properties. The body of
the Digenea has a bilaterally-symmetrical structure;
it is usually dorso-ventrally flattened and leaf-shaped
or lanceolate, sometimes pear-shaped, cylindrical,
filamentous or of another shape ( ► Figure 9.1). The
body length of the Digenea usually varies between <1
mm and several centimetres, but reaches enormous
proportions in Nematobibothrioides histoidii, a trematode
parasite of the sun fish (Mola mo/a), which is up to 12
m long and only 1-3 mm wide.
Oral sucker----
Oesophagus---J�-.Jlloi.._--\----Pharynx
Intestine
Seminal vesicle--1--=i =-----
Figure 9.1. Scheme of a trematode of the class Digenea (Graphics: IPZ, A. Seeger; after Schell 1985).
The integument (body surface) consists of a syncytial
plasmatic outer layer without nuclei, which is connected
by cytoplasmatic bridges with lower, nucleated parts
portions of the syncytium ( ► Figure 9.2). Integument
and musculature (longitudinal, circular and dorso­
ventral muscles) of the digeneans and other flatworms
are closely linked. In the adult stages of the digeneans
the integument is folded and partly covered with scales
or spines. In different species an outer glycocalyx
composed of polysaccharides has been demonstrated.
the space between the ectodermal integument and
the entodermal digestive epithelium is filled with a
mcsodermnl parenchyma in which the internal organs
are embedded.
Usually two muscular suckers serve as adhesive organs.
The sucker at the front end surrounds the mouth (oral
sucker); the ventral abdominal sucker has no access to
internal organs ( ► Figure 9.1 ). Arrangements and forms
of the suckers vary in different groups of Digcnea. In some
species further adhesive structures occur, for example a
collar of spines at the anterior end. The digestive tract
consists of the foregut with mouth, pharynx (may be
absent), and midgut, which usually ends blindly and
can be forked or divided into more branches ( ► Figure
9.1). Circulatory and respiratory systems are missing.
The excretory system consists of protonephridia and
branched channels. The reproductive organs are usually
very complex and hermaphroditic; only in a few groups
they are dioecious (e.g. Schistosomatidae) ( ► Figure
9.1). The eggs produced by the Digenea contain a zygote
and yolk cells, the egg shell is often provided with a lid
Cirrus and
cirrus pouch
Uterus with egg
 Part Ill. Parasites and parasitoses: metazoa
Figure 9.2. Fasciola hepatica, adult stage: Scheme of the Integument (Graphics: IPZ, A. Seeger; after Threadgold 1984).
..: (operculum) at one pole. At the time of elimination
from the host, the eggs may already contain a larva
(miracidium). The nervous system (cerebral ganglion
= nerve ring, surrounding the pharynx) is connected
with nerves extending anteriorly and posteriorly and
with sensory cells. In adults, sensory cells are located
in the integument, usually aggregated on suckers. Free­
living larval stages can have simple photosensitive organs
('eye-spots').
The uptake of nutrients takes place through the mouth
opening, and selectively through the integument. The
energy production of adult trematodes is mainly
based on anaerobic utilisation of carbohydrates,
which are partially metabolised to propionate, acetate,
succinate and lactate which are excreted. Free-living
stages (miracidia, cercariae) with access to oxygen can
completely break down carbohydrates to CO2 and water.
Trematodes and some other helminths are capable of
protein and pyrimidine synthesis, but they cannot
synthesise purine nucleotides. The fat metabolism
is limited because the ability to synthesise long-chain
fatty acids is missing.
The life cycle of digeneans comprises several stages
(► Figure 9.4): adult stage - egg - miracidium -
sporocyst (partly daughter sporocyst) - redia ( usually
several generations) - cercaria - metacercaria (may
C be absent) - juvenile trematode - adult stage (in some
>­
Ol
groups of the Digenea there are deviations from this
0 basic scheme). The adult stages reproduce sexually and
'il, are parasites of vertebrates, the sporocysts and rediae
reproduce asexually in invertebrate intermediate
co
0... hosts. The miracidia and cercariae, and partly also
the metacercariae live (mostly short-term) in the
environment. The life cycle is characterised by an
alternation of generations (sexual-asexual) (heterogony)
and an obligate alternation of hosts (heteroxeny),
including the definitive host (vertebrate) and one or
two intermediate hosts. (The first intermediate host is
almost always a mollusc: snail or mussel). In most species
the life cycle is bound to aquatic or wetland habitats.
Selected references
Gibson DI, Jones A, Bray RA (2002) Keys to the Trematoda. Yd.
1 . Wallingford, UK: CASI International; ISBN 085· 1995-470.
Jones A, Bray RA, Gibson DI (2OO5a) Key to the Trematoda. VrJ
2. Wallingford, UK: CASI International; ISBN 085-19958-?X.
Jones A, Bray RA, Gibson DI (2OO5b) Key to the Trematoda. Yd.
3. Wallingford, UK: GABI International; ISBN 085-1995·888.
Kassal T (1999) Veterinary helminthology. Oxford , UK: Butt0fW()'lh
Heinemann; ISBN 0-7506-3563-0.
Kostadlnova A, Perez-del-Olmo A (2014) The systematicsol
the Trematoda. Adv Exp Med Biol 766: 21-44.
Maule AG, Marks NJ (eds.) (2006) Parasitic flatworms:
molecular biology, biochemistry, immunology and physiolog/.
Wallingford, UK: CASI International; ISBN-1O: 085-199·
027-4.
Mehlhorn H (ed .) (2008) Encyclopedia of parasitology. 3rd ed.
Berlin, Germany: Sp ringer; ISBN : 978-3-540-48994·8.
Peoples RC, Fried B (2014) Form and function in the Digenea
Adv Exp Med Biol 766: 3-20.
Schell CS (19 85) Hand book of Trematodes of North Ameri:a
North of Mexico. Moscow, ID, USA: University Press of ldal'o;
ISBN 0-89 301-09 5-2.

9.1.1 Order Echinostomida
£chinos (G): Hedgehog; stoma (G): mouth. Refers to a
collar of spines surrounding the mouth of species in the
family Echinostomatidae.
The Echinostomida are elongated trematodes with a flat
body, often with a spiny integument. The front end can
be transformed into a so-called apical conus (Fasciolidae)
or may be equipped with a collar of spines around
the mouth opening (Echinostomatidae). Among the
numerous families the Fasciolidae and Echinostomatidae
are of particular veterinary importance.
Family Fasciolidae
Fascia (L): band. Refers to the leaf-like appearance of
the parasites.
Summary
• Agent. Fasclo/a hepatics (common liver fluke) Is the
most important representative of the Echinostomlda.
Adult stage leaf-like, up to about 5 cm long. Other
species of the family(► Table 9.2).
• LHe cycle, epidemiology. Development indirect and
bound to wetlands. Definitive hosts are herbivores,
especially sheep, goats and cattle. Intermediate hosts
in Europe: almost exclusively Galba truncatula (syn.
Lymnaea truncatula)(dwarf pond snail, liver fluke snail).
Infection of definitive hosts per os: uptake of encysted
metacercarlae with plants or rarely with drinking water
(floating cysts). In Central Europe greatest infection risk
In late summer and autumn. Migration of juvenile flukes
in the definitive host from small Intestine ..... peritoneal
cavity ..... liver tissue (migration phase 6-7 weeks) -+
bile ducts. Prepatent period 8-10 weeks.
• Occurrence. F. hepatics: worldwide In temperate
climates, F. g/gantlca: In subtropical and tropical regions
(Asia, Africa). F. hepatics Is an Important liver parasite of
ruminants, which also occurs In other herbivores (e.g.
horse, donkey, rabbit), omnivores(pig) and occasionally
in humans.
• Pathogenesis, cllnlcal signs. Juvenile flukes destroy
the liver parenchyma, adults damage bile ducts and
suck blood. Consequences: various forms of fasclolosls
(acute, subacute, chronic) or subcllnlcal adverse effects
(reduced productivity).
• Diagnosis. lntravital diagnosis by detection of Fasclola
eggs in faeces(sedimentation technique); copro-antigen
detection is feasible. Detection of specific antibodies in
milk(bulk-tank samples) for herd surveillance.
• Therapy control. Effective anthelmintics are available
(trlclabendazole, etc.), comtrol options include preventive
measures in conjunction with strategic anthelmintic
treatments.
• Zoonotlc import ance. F. hepatics and F. gigantica
cause fasciolosls in humans.
• Other species of the famlly. Fasciola glgantica,
Fascioioides magna
9. Phylum Platyhelminthes(flatworms)
The representatives of the family Fasciolidae ( ► Table
9.2) are quite large, leaf-shaped flukes that parasitise the
liver or the small intestine of mammals and undergo
diheteroxenous developmental cycles with water snails
as intermediate hosts. Of particular importance are
co
Fasciola hepatica and F. gigantica. -0
.E
Genus Fascia/a
0
C
.c
•
Fasciola l,epatica (common liver fluke) (.)
w
Disease: F'asclolosls.
Fascia (L): band; hepar (G): liver.
Agent. The adult stages are flattened, laurel-leaf like,
brownish-grey, about 18-50 mm long and 7-14 mm wide
( ► Figure 9.3). The conical anterior end (apical conus)
is demarcated by a shoulder-like broadening from the
rest of the body, which gradually tapers to the posterior
end. The oral sucker is apical, the ventral sucker at the
base of the apical cone. A striking feature is the strong
branching of internal organs (testes, vitelline glands,
ovary, intestine), the uterus is irregularly coiled, located
in the anterior third of the body. Tegument with spines.
Eggs oval, thin-shelled, with operculum, 130-145x70-90
µm, golden-yellow. When expelled from the host they
contain the fertilised egg cell and yolk cells. Some strains
of F. hepatica produce large eggs up to 180 µm long.
Life cycle. In the adult stage, F. hepatica parasitises
mainly domestic ruminants (sheep, goat, cattle, buffalo),
but also other, mostly herbivorous mammalian species
and humans. The life cycle is diheteroxenous (mammal,
snail), and includes the following stages: egg ---+
miracidium---+ sporocyst---+ redia (up to 3 generations)
---+ cercaria---+ metacercaria ---+ juvenile stage ---+ adult
stage ( ► Figure 9.4).
• Development from egg to miracidium. The
sexually mature flukes live in the bile ducts of their
definitive hosts. F. hepatica has a high reproductive
capacity (daily approximately 4,000-50,000 eggs per
parasite in sheep), which is subject to large fluctuations
depending on the intensity and stage of infection and
the host species (see epidemiology). Eggs are passed
with the flow of bile into the intestine and then with
the faeces to the environment. A portion of the eggs
can remain longer (8-16 weeks) in the gallbladder and
is released in batches. In an aqueous environment,
embryonic development to a ciliated miracidium takes
place in the eggs if sufficient oxygen is available and the
temperatures are above 10 °C. In Central Europe this
development takes 2-4 weeks at suitable temperatures
during summer.
Part Ill. Parasites and parasitoses: metazoa

Table 9.2. Species (selection) of the family Fasciolidae.1

Species, size, distribution (D) Intermediate hosts Definitive hosts Predilection sites
adults
ot1 I

'
Fascio/a hepatica2 I Galba (syn. Lymnaea) cattle, sheep, goat, buffalo, bile ducts
(common liver fluke) truncatula, other horse, pig, wild ruminants,
18-50x7-14111m ; Lymnaeidae man3 {
D: Worldv1ide in temperate
·- zcnes
- __,1 I
Fasciola gigantica Radix (syn. Lymnaea) cattle, buffalo, sheep, goat, bile ducts
· (large liver fluke) 1 auricu/aria complex horse, donkey, camel, man
i 24-75x5-12 mm I
D: Subtropical and tropical regions in Africa,
�ia, eastern Mediterranean region I ·- I

Fascioloides magna2 I Ga/ba (s�-;;_Ly�n�aea) wapiti, white-tailed deer, liver parenchyma

(large American liver fluke) I truncatula, Lymnaea caribo u , red deer, fallow
70-100x20-30 mm modicella, L. caperata deer, sheep, goat, cattle
D: North Americ_§l,_Europe
Parafascio/opsis
-
fasciolaemorpha2
- j
I

Planorbarius corneus
-
elk, roe deer, red deer,
-- ·-
small intestine, gallbladcte-,
(elk liver fluke) bison, sl1eep bile ducts
3-7x1 .0-2.5 mm
D: Europe
1 Data without claim of completeness.
2 Species occurring in Central Europe.
3 In Australia isolated cases in birds (emus: acci dental hosts).

Cirrus
Ventral sucker
Partial view
of intestine

Testes

Figure 9.3. Fasclola hepatlca: (a) scheme; (b) adult stage unstained; branched intestine filled with blood (a: Graphics: IPZ,J,
Peter, adapted from A. Wiegand and 0. Mattes, 1958, b: IPZ, K. Wolff).

The mature miracidium (length about 130 µm) formed
in the egg detects by means of its light sensory organ
(ocellum) light stimuli that act as signals for hatching
which occurs only in water. The glycogen stores of the
miracidia allow them only a short life of 20-30 h in
which they are searching for a suitable intermediate host.
In Europe this is Galba (syn. Lymnaea) truncatula, an
amphibious freshwater snail, which is often stil)1ing al
light-exposed edges of small water bodies, just bdo1i
the water level (epidemiology, see below). Initially,
the miracidia perform undirected, fast swi mming
movements; then they orient themselves to the light
and the water surface and are thus led to the habita1of
the snails. There, they are attracted chemotactically by
 9. Phylum Platyhelminthes (flatworms)

ro
"'O
.E0
en
0
C
:E
u
w

/��"
�.. Adult stage
Ouvenlle stages not shown)
°' ·0
0 ",,0
,

c\ 0 c, 9
'ii I'

Metacercaria
on a plant

Cercaria

Sporocyst

Reclla
, tup to S ge eratlon�)

Figure 9.4. Life cycle of Fascia/a hepatlca (Graphics: IPZ, S. Ehrat),

glycoconjugatcs of the snails within distances ofless than
15 cm. Although other snail species (Lym11aea palustris,
L. stagnalis, Radix peregra) may also be attractive, the
miracidia find favourable conditions for penetration
and further development only in specific intermediate
hosts. The penetration is preceded by the attachment
of the miracidium to the epidermis which is stimulated
by short-chain fatty acids (C 7-C9) in the mucus of the
snail. The infection process is temperature dependent,
does not take place below 5 °C and proceeds optimally
at 15-26 °C.
 Part Ill. Parasites and parasitoses: metazoa
• Developmental stages in the intermediate
host. The penetration of the miracidium into the snail
is accomplished by eversion and introversion of the
'anterior papilla' (a conical projection), supported by
secreted proteolytic enzymes. The miracidium then
loses its cilia and transforms into a young sporocyst (up
to 500 µm long). Sporocysts migrate into the digestive
gland where their germ cells give rise to rediae (mother
rediae, generation I) that penetrate the sporocyst wall
and invade the tissue of the digestive gland. The rediae
are about 1.5-2.5 mm long, cylindrical organisms with
oral sucker, pharynx, intestine, and two lateral lobe-like
lappets in the posterior third of the body ( ► Figure 9.4).
,I
Each redia contains 16-28 masses of germ cells (germ
'I
:, balls), from which more rediae (generations II and III)
or cercariae emerge. The mature cercariae leave the
rediae through a birth pore. The oval cercariae (up to
400x220 µm) have a long tail (up to about 800-1000
µm), they are equipped with an oral and ventral sucker,
pharynx, oesophagus, a forked intestine, and with
glands that are important for subsequent encystment.
The cercariae migrate through the tissue and leave
the snail not earlier than 7 weeks p.i. However, not all
cercariae reach maturity at the same time, so that from
an infected snail, cercariae can be released repeatedly
over a few weeks or several months. The potential of
asexual reproduction in the snail is considerable because
several hundred cercariae may develop from a single
miracidium. The development in the snail takes 5-8
weeks under favourable conditions; it is temporarily
interrupted at lower temperatures.
• Development of the metacercaria. After escape
from the snail, the cercariae swim around vigorously in
the water and attach themselves, usually within a few
minutes, with their ventral sucker to plants or other
objects. Then, the cercaria detaches its tail and produces a
spherical cyst of about 250 µm in size with a multilayered
cyst wall consisting of tanned and keratinised proteins,
mucoproteins and mucopolysaccharides. Thus, the
cercaria has become a metacercaria that is infectious
shortly after encystation. Some of the cercariae (<I 0%)
may encyst on the water surface, forming floating
cysts. The metacercariae are viable for long periods
(epidemiology, see below).
Q)
• Infection of a definitive host and migration to
·o
C
'6 the liver. The infection of a host occurs by ingestion of
Q)
�
metacercariae adhering to plants or on rare occasions
by uptakte of floating cysts with drinking water. In the
ro forestomach system of ruminants, the metacercariae
C
·c
Q) are activated by the higher temperature (compared to
the environment), the presence of CO 2 and reducing
.� conditions. Initially they perform vigorous movements
>,
Ol
in the cysts, and during a subsequent resting period
0 they release from their intestine proteases (cathepsins)
·w which act on the inner cyst wall thus allowing the
emergence of the metacercaria. The hatching process
C'il
Q_
is stimulated by bile components in the small intestine.
The hatched young flukes attach to the surface of the
intestinal mucosa, distal to the opening of the Ductus
choledochus. Then, they penetrate the intestinal wall,
migrate within 24 h through the intestinal wall into
the peritoneal cavity and from there to the liver, where
most of them are present after 4-6 days. The young
flukes migrate though the liver tissue for 6-7 weeks, and
thereafter they reach the bile ducts where they gradually
develop to sexual maturity. Eggs are excreted in the
faeces at the earliest 2-3 months p.i. (prepatency in sheep
55-57 days, in cattle 56-77 days). The average life-span
of the parasites in cattle is 9 months, but much longer
in sheep. Migrating young flukes occasionally invade
blood vessels and reach various organs via the circulatory
system, for example the lung. A direct migration to
organs other than the liver is possible. In this way
occasional prenatal infections are possible which have
been observed in calves.
Occurrence and epidemiology. F. hepatica
occurs worldwide in temperate regions where suitable
intermediate hosts live. In many regions of Africa and
Asia, the areas of distribution of F. hepatica and F.
giganlica overlap ( ► p. 184). The life cycle of F. hepatica
depends on many factors as described in the following
paragraphs. Accordingly, the spatial distribution and the
prevalence of F. hepatica in definitive hosts are subject to
great local and regional fluctuations. Thus, for example
in northern Switzerland, an average of 18% of cattle (n
~ 1,300) was infected with F. hepatica, but prevalences
of about 60% were found in highly endemic regions. In
recent years, valuable information on the prevalence
of F. hepatica in dairy herds was obtained in studies
of bulk-tank milk samples for antibodies in the milk
serum (diagnosis, see below). Prevalences determined
in this way ('herd prevalences') showed, for example,
in southern Sweden low average values (6-7%), but
higher ones in Belgium ( ~60%) and Germany (East
Friesland 45-57%, Schleswig-Holstein ~50%, Bavaria
32%, including one district with 95%).
• Definitive hosts. Worldwide, domestic ruminants,
especially sheep, goats and cattle, are the main definitive
hosts of F. hepntica, but also buffalo, horse, pig, wild
ruminants, rabbit, hare, nutria, kangaroos, other
herbivores and man can be carriers of the parasite. Sheep
have a special epidemiological significance because they
are highly susceptible to F. hepatica and the parasites
can survive for several years with high egg production.
Cattle usually excrete lower egg numbers and eliminate
the parasite burden - if re-infections are excluded -
usually after about 9 months. Fasciola eggs are passed
to the habitats of the intermediate hosts in the faeces of
fluke carriers or in liquid manure.
• Eggs in the environment. For the development
of eggs in the environment a minimum temperature of

10 °C is required; the upper tolerance limit is about 35 °C.
At optimal temperatures of23-25 °C, the development of
miracidia takes about2- 3 weeks; at 16 °C, it is extended
to2-3 months. Although high temperatures facilitate a
rapid development of miracidia, they are increasingly
becoming inhibitory or lethal. At low temperatures, the
eggs remain viable for long periods, e.g. at 4 °C for more
than 2 years. Under frost of -5 °C the eggs survive barely
3 weeks. Eggs enclosed in wet faeces of the host can
survive in Europe for about 10 weeks during summer
and up to 6 months during the cooler season, when
they can partially develop. Complete development and
hatching of the miracidia is only possible when the
eggs areflushed out of the faeces and remain constantly
surrounded by a film of water or when they have been
directly passed into the water. When drying, the eggs
die offquickly. Eggs which have been passed by housed
definitive hosts are killed in a manure pile in 10 days,
whereas a portion remains viable in liquid manure
during summer (at ~18 °C) for approximately 8 weeks
and in winter ( ~8 °C) for 11 weeks.
• Intermediate hosts. Various species of freshwater
snails of the family Lymnaeidae serve as intermediate
hosts for F. hepatica worldwide. In Europe, Galba (syn.
Lymnaea) truncatula (dwarf pond snail, liverfluke snail)
is the most important and typically the only intermediate
host. Some other lymnaeids, particulary juvenile snails,
are considered as less efficient intermediate hosts of
potential local importance, such as Omphiscola (syn.
Lymnaea) glabra in France or Lymnaeafuscus in Sweden.
In extra-European regions, other species play also a
role as intermediate hosts, for example in Africa G.
truncatula and Pseudosuccinea (syn. Lymnaea) co/umella,
in North America Fossaria (syn. Lymnaea) humilis, F.
bulimoides and F. cubensis, and in Australia Austropeplea
(syn. Lymnaea) tomentosa and Pseudosuccinea (syn.
Lymnaea) columella. Such snails can be distributed over
long distances (e.g. in water with aquarium fish) and
possibly settle in foreign habitats.
G. truncatula is a freshwater snail, belonging to the
Pulmonata (air breathing snails), has a cone-shaped,
clockwise twisted shell, 7-12 mm high with an umbilicus
(► Figure 9.5, left). G. truncatu/a is found in all European
countries, including most of the islands, and is also
present in regions of Africa, Asia, as well as in North
and South America. In Europe, these snails inhabit
both lowlands and mountainous areas ( up to 2,800 m
altitude; in Bolivia up to 4,100 m). Their amphibious
properties allow the snails to live in water or on wet
ground ( ► Figure 9.6). They are found mainly in shallow
marginal zones of ditches, streams, ponds, rivers, smaller
pools of water, such as wheel ruts or footprints of grazing
animals, or in damp parts of pastures or meadows.
G. truncatula prefers clear, oxygen-rich, standing or
slow-flowing waters with pH values between 5 and 9
(optimum around 7-8) with muddy, loamy or clayey
9. Phylum Platyhelminthes (flatworms)
ground. They can survive temporary desiccation of the
habitat for months by hiding in crevices of the soil or by
pressing the shell opening on the ground thus avoiding
large fluid losses. Furthermore, the snails can survive
the winter. Spreading into new habitats occurs mainly
by passive transport in water (in watercourses, by heavy
rainfalls or floods) and less often by transport of snails
or their eggs by birds and other carriers; actively they
migrate only very short distances.
In Central Europe, the development of G. truncatula
from the egg to the adult stage takes about 3 months.
Preconditions are adequate moisture and suitable
temperatures(> 10-25 °C). In spring, overwintered older
snails lay eggs. In May the first young snails hatch, which
reach reproductive maturity after ~8 weeks and begin
laying eggs. In the following period there is an increase
in snail numbers, which reach a peak around August.
From September onwards old snails die, but some of
the young snails survive the winter.
• Development of F. hepatics in snails and
infection risk for definitive hosts. Depending on
the local temperatures, F. hepatica develops in the snails
within one or two vegetation periods ( 1-year cycle and
2-year cycle, respectively):
Figure 9.5. Gslbs (syn. Lymnses) truncatuls, shell; height of
the shell about 7 mm (Photo: IPZ).
(1)
C
·u
i5
(1)
�
(1j
C
·.::
(1)
j
C
>,
CJ)
0
0
Figure 9.6. Galba (syn. Lymnaea) truncatula at a moist spot of
·u5
a pasture (Photo: IPZ, H. Hertzberg). (1j
(1j
CL
 Part Ill. Parasites and parasitoses: metazoa

I-year cycle. Infection of snails with miracidia
occurs mainly in early summer. In the warm season,
the development of F. hepatica in the intermediate
hosts is completed within 5-8 weeks, so that in late
summer and fall numerous cercariae are released
and develop into metacercariae. Therefore, from late
summer until the end of the grazing period there
is an increased infection risk for definitive hosts.
2-year cycle. The snails are infected by miracidia
in the fall. In winter, the development of F. hepatica
in the snails is inhibited or interrupted, and will be
completed only when the temperature rises in the
following year. In spring or later, cercariae emerge
from the snails and transform into metacercariae
which represent an infection risk.
Corresponding to this sequence, in Central Europe
periods with increased infection risk (= main infection
periods) for definitive hosts are the late summer and
autumn (greatest risk) and early summer (lower risk).
However, an infection risk also exists during the rest
of the vegetation period, as metacercariae on pasture
remain viable for long periods. In higher mountain
areas, the 2-year cycle is the rule.
• Metacercariae and routes of infection.
Herbivores acquire the infection most frequently during
the grazing period by ingesting metacercariae with
plants or, more rarely, with drinking water. Prenatal
infections have occasionally been observed in cattle.
Infections in stables are possible if grass with adhering
metacercariae is fed to the animals. Such grass may
come from ungrazed pasture which is inhabited by G.
truncatula and has been contaminated with Fasciola
eggs by spreading slurry. Occasionally, infections are
caused by poorly dried hay, in which metacercariae can
survive several months. In grass silage, metacercaria die
in about 2 weeks.
wall, together with fibrin deposits and adhesions at the
intestinal serosa. These changes are usually mild and
without clinical relevance, but peritonitis and severe
serous exudation occur in massive infections. In such
cases, there is an increased tendency of parasites to
migrate not only to the liver but also to other organs
(including the diaphragm, lung, pancreas, uterus).
• Phase 2. Migration of juvenile stages in the liver
parenchyma (from day 4 to 6-7 weeks p.i.). The juvenile
liver flukes migrating from the peritoneal cavity through
the serosa of the liver into the parenchyma ingest liver
tissue with the oral sucker and use it as food. Juvenile and
adult flukes secrete a mixture of several cathepsins with
different functions: lysis of host tissue during migration,
degradation of proteins into peptides that are taken up by
the parasite, and cleavage of host immunoglobulins. The
laller plays a role in immune evasion ( ► p. 36). During
the migration phase, usually lasting 6-7 weeks, the liver
flukes grow from about 0.3 mm in length to 3-14 mm.
The migrating flukes leave behind winding tracks that
contain destroyed liver tissue and blood, accompanied by
inflammatory cells (including eosinophilic leukocytes,
macrophages, foreign-body giant cells) ( ► Figure 9.7
and 9.8). Resorptive processes take place and granulation
tissue is formed that is later replaced by connective
tissue. At this stage, histological signs of portal vein
inflammation are detectable, leading to vascular
occlusion and subsequently to liver cell necrosis, bile
duct proliferation and production of connective tissue.
The lobules are gradually surrounded and restricted by
connective tissue. This interstitial hepatitis is manjfested
by an increased demarcation of the liver lobules. Severe
changes may lead to cirrhosis in later phases due to the
shrinkage of connective tissue.

Pathogenesis and pathology. Symptoms caused

by fasciolosis are mainly due to the activities of the
parasites in the liver and the related pathophysiological
disorders and lesions (►Figure 9.7). Type and degree of
the disorders depend upon the intensity of the Fasciola
infection, the mode of reaction of the liver (inter alia
depending on animal species and age), the nutritional
Q)
C status of the host and other factors. At the same infection
·c3
'6 dose, sheep prove to be much more susceptible than
Q)
2 cattle, which have a higher natural resistance to Fasciola
>- (see below). The pathogenesis can be divided into
aJ
C different phases ( ► Table 9.3 ).
·;::
(1)

j • Phase 1. Migration o f juvenile stages f rom

C the small intestine into the peritoneal cavity
>- (approximately until day 6 p.i.). During the migration Figure 9. 7. Cattle liver with subacute fasciolosis: liver surface
0)
0 of juvenile stages of F hepatica (length about 0.25 mm) and gallbladder with fibrin deposits, migration tracks of the
0
-�
<f)
from the small intestine into the peritoneal cavity, local parasites in the parenchyma (see enlarged detail in ► Figure
tissue damage and bleedings occur in the intestinal 9.8) (Photo: IPZ).
a..
OJ
 9. Phylum Platyhelminthes (flatworms)

small bleedings in the damaged bile duct wall blood

Figure 9.8. Cattle liver with subacute fasclolosis: surface with
migrating tracks of parasites (scale: mm) (Photo: IPZ).
Macroscopically, various changes are visible on the liver
surface and in the parenchyma: winding, thread-like,
reddish or grey-white migration tracks, punctate foci
or larger areas of necrosis, and haemorrhages. Later,
the liver appears marbled in colour as a result of the
coexistence of fresh and scarred migration tracks
with the adjacent liver parenchyma. The liver may be
enlarged, and the liver capsule may be partly covered
with fibrinous deposits. Some flukes migrate from the
liver back into the peritoneal cavity and cause small,
round and sharp-edged outlet openings on the liver
surface. Further changes may include: peritonitis,
serous or bloody effusions into the peritoneal cavity,
enlargement of lymph nodes of the liver and changes
in various other organs (lung, pancreas, etc.).
loss takes place. In cattle, (from the 16th week p.i.),
hyaline degeneration of the connective tissue and focal
mineral deposits may occur, causing tubular linings and
thickening of the bile duct. However, bile ducts and liver
parenchyma may regenerate in the course of several �
"O
months (up to 1 ½ years) after elimination of the flukes. .E0
0
Macroscopically, the liver at this stage shows more or C
less severe fibrosis or cirrhosis, as well as thickening and E
(.)
some partial extensions of the bile ducts ( ► Figure 9.9 w
and 9.1 O). In cattle, the strongly thickened bile ducts
occur partly as finger-thick, coarse strands. When
cutting the bile ducts, mineral deposits cause a grinding
noise. In sheep and goats, the bile ducts are usualJy
less strongly thickened, but they often exhibit nodular
or wavy extensions containing aggregates of parasites;
mineral incrustations are missing. In swine and horses,
the bile ducts are usually moderately thickened and
visible as local spindle- or sausage-shaped strands. In
all animal species, bacterial colonisation of the bile
ducts may cause secondary inflammation and abscess
formation.
During the stages of infection, detailed above, various
pathophysiological processes are induced which are
summarised in a simplified form in ► Table 9.3. Of
these, anaemia, dysproteinaemia and metabolic disorders

• Phase 3. Colonisation of the bile ducts by juvenile

and adult liver flukes. By 6 weeks p.i., the liver flukes
that have grown up to about 3-14 mm colonise small
bile ducts and migrate with increasing size to their final
location in the major bile ducts. The proportion of
migrating stages in the parenchyma decreases gradually,
but in massive infections or in relatively resistant hosts
(e.g. cattle) longer persistence is possible. In this phase,
one finds recent or old changes of traumatic hepatitis,
and already signs of cholangitis with greater prominence
of the thickened bile ducts. Figure 9.9. Sheep liver with chronic fasciolosis: thickened and
extended bile ducts and slight fibrosis of the liver parenchyma
After migration to the bile ducts, the parasites grow (Photo: IPZ).
gradually up to 20-30 mm and attain sexual maturity
at the earliest 8-9 weeks p.i. Liver flukes remaining
in the parenchyma can be encapsulated by tissue
reactions (particularly common in cattle). Under the
influence of the parasite, a chronic inflammation of
the bile duct wall develops, with local proliferation
of granulation tissue into the lumen and eventually
fibrosis of the bile duct wall. Causes of the cholangitis
are thought to be mechanical factors ('browsing' of the
epithelium by the parasite and damage to the mucosa
by integumental spines) and chemical effects (Fascia/a
secretes cathepsins [see above] and large amounts of
praline; high concentrations of praline promote the
formation of connective tissue and collagen synthesis). Figure 9.10. Section of a cow liver with chronic fasciolosis:
Due to the blood-sucking activities of the flukes and the thickened bile ducts (Photo: IPZ).
 Part Ill. Parasites and parasitoses: metazoa

Table 9.3. Essentials of the pathophysiology of fasciolosis.

'
Phases of the Activity of liver flukes Host reactions or Signs (see also te>d)
infection consequences

Juvenile release of antigens immune reactions hypergammaglobulinaemia, eosinophilia

nukes in liver migration in liver internal bleedings anaemia
parenchyma parenchyma and release of intracellular enzymes increased concentrations in serum
destruction of liver tissue (AST, GLDH)1
reduction of albumin synthesis hypoalbuminaemia
disturbances of liver function metabolic disorders
Adult nukes in unknown inappetence2 disturbance of weight development,
bile ducts reduced performance
damage to the bile duct ----
release of GGT 1 from bile ducts increased concentrations in serum
mucosa and blood sucking loss of erythrocytes anaemia
loss of serum proteins Into 11,e hypoproteinaemia, predominantly
intestine hypoalbumlnaemia
- -
degradation of muscle proteins disturbance of weight development
1 AST: aspartate aminotransferase: GGT: y-glutamyltransferase: GLDH: glutamatedel1ydrogenase.
2 Responsible factors unknown.

play a prominent role. The anaemia - caused by internal
bleedings, blood loss into the bile ducts and blood
ingestion by the parasites - is equivalent to a haemorrhagic
anaemia of the normocytic and normochromic type.
During prolonged courses of the disease, the anaemia
can turn into a hypochromic, macrocytic type due to
increased iron loss. The dysproteinuemia is caused by
an increase in the y-globulin concentrations in the
serum (due to antigenic stimulation), and by the loss
of albumin (reduced synthesis in the liver and loss into
the intestine). Disturbances in metabolism (e.g. albumin
synthesis, carbohydrate metab olism, detoxification
function) are consequences of the liver damage. Among
other factors, inappetence and degradation of muscle
protein (to compensate protein loss into the intestine)
are made responsible for reduced weight gain. Signs of
impairment of the energy metabolism in sheep with
heavy F. hepalica burdens (~75-245 adult parasites
per animal) are reduced glucose levels and increased
concentrations of �-hydroxybutyrate in the serum. The
latter is one of the ketone bodies and results from the
compensatory mobilisation of free fatty acids.
Resistance and immunology. Various species of
Q)
C definitive hosts exhibit a natural resistance to the F.
·c::; hepatica infection which is classified as low (in sheep,
'6
�
Q)
goat, rabbit, hare), moderate (cattle, horse, red deer,
�
fallow deer, roe deer, man) or high (pig, dog, cat).
co
C These gradations are partly attributed to the fact that
·;::
the definitive hosts have varying capabilities to trap
J
Q)
migrating stages of Fascia/a by means offtbrotic reactions
C in the liver parenchyma or to eliminate them from the
>,
OJ
bile ducts. The mechanisms involved are still unclear.
0 In addition to these properties of the animal species,
0
·u5 other factors play a role in the efficiency of resistance,
such as the infection dose. For example, after a primary
co
0....
infection of cattle with 200-1,300 metacercariae per
animal, around 30% of the parasites reach the bile ducts,
but at higher doses of 2,500-15,000 metacercariae, only
3%. Differences in resistance may also exist between
different races or age groups of the same host species
(juvenile animals are more susceptible than older ones).
• Sheep. Sheep are highly susceptible to F. hepatica
and unable to develop sufficient immunity under natural
infection conditions. Therefore, heavy infections quite
frequently lead to disease and death. Survivors or less
heavily infected animals may remain fluke carriers for a
long time (up toll years). Although previous infections
may lead to an inhibition of growth and of the migration
capability of liver flukes originating from a reinfection,
they do not stimulate significant immunity.
• Cattle. Cattle have a higher resistance to F.
hepalica than sheep and arc able to eliminate most of
the flukes approximntely 9-26 months after a primary
infection. After a primary infection with high doses
of mctaccrcariae, cattle acquire increased resistance
(60-84%) to reinfection with Fascia/a. However, under
natural conditions in endemic ureas the immune
response is often weak. Therefore, new light infections
are possible, even in older animals.
Immunity in chronic fasciolosis is characterised
by a predominance of Th2-associated responses
simultaneously with an inhibition of Th 1 -cell activity.
Like other parasites, F. hepatica has also developed
mechanisms of immune evasion, such as the change
of antigens in the integument during different
developmental stages or the ability for enzymatic
cleavage of immunoglobulins, which are involved in
cytotoxic, antiparasitic host react ions.
 9. Phylum Platyhelminthes (flatworms)

Table 9.4. Forms of fasciolosis in cattle and sheep.

Parameter Forms of fascloloils

,-
Acute
- ') l

Subacute Chronic
- -
Involved animal species sheep, very rare in cattle sheep, rare in cattle sheep and cattle (most
common form)
Predominate occurrence in September-November October-December December-April
Central Europe sheep: -4-7 weeks p.i. sheep: -7-12 weeks p.i. sheep: >12 weeks p.i.
Clinical signs weakness, abdominal pain, inappetence, impaired productivity (milk, meal, wool) rapid or
pale mucous membranes, gradual weight loss, pale mucous membranes, subcu1aneous
sudden lethal cases oedema (frequently submandibular. predominantly in subacu1e
fasclolosis of sheep)
Duration of disease few days few weeks weeks to months
Laboratory findings
•Anaemia normochromic, normocytlc or normochromlc, normocytic to hypochromic and makrocytic,
missing partially missing
• Hypoalbuminaemia + + + In moderate and severe
cases
• Eosinophilia + + +/-
• Liver enzymes in serum elevated elevated typically normal or GGT2
elevated
Pathology of the liver migration tracks of Fascia/a in migration tracks in fibrosis and cirrhosis,
liver parenchyma, bleedings, parenchyma, enlarged bile thickened bile ducts, in cattle
fibrinous exudate, peritonitis ducts, fibrosis with mineralised incrustations
Parasitological findings
• Parasite stages: juveniles in liver parenchyma: juveniles in liver parenchyma adults in bile ducts (possibly
approximate number and and adults in bile ducts some stages in parenchyma)
localisation 1 sheep: >1,500 sheep: >800-1,500 sheep:<100
cattle: >4,000 cattle: 2,000-4,000 cattle: <250
• Eggs in faeces none present present
1 The data on the number of parasites are based on experimental studies and should be regarded as approximate Infection intensities that
cause clinical signs of disease. Lower infection intensities can cause subclinical changes (e.g. anaemia) and also reduced performance.
2 GGT: y-glutamyl transferase.

Clinical signs and adverse effects. At low

infection intensity, all phases of the infection can be
asymptomatic. In heavy infections, the disease manifests
as acute, subacute or chronic fasciolosis(► Table 9.4).

F. hepatica is an economically important parasite that

in severe infections causes serious illness and death, the
latter particularly in sheep and goats(► Figure 9.11).
Lower worm burdens may result in chronic diseases and
decreasing performance(milk, meat and wool) in cattle
and small ruminants. Livers infected with F. hepatica
are unsuitable for human consumption. According to Figure 9.11. Sheep with fasciolosis: distinct submandibular
surveys conducted in Belgium, chronic fasciolosis in oedema (so-called bottle yaw) (Photo: IPZ, J. Boray).
cattle herds is considered a production-reducing factor if
at least 25% of the animals are infected and the infection
intensity is at least 10 liver flukes per animal. Under Diagnosis
these conditions, the annual losses were estimated at€
30 per dairy cow. Calculations in Switzerland involving • lntravital diagnosis. The method of choice during
all infected cattle(independently of the worm burden) the patent period is the sedimentation technique, which
resulted in annual losses of€ 299 per animal. Worldwide, has a high methodological sensitivity(near 100%}, if egg
the losses caused by fasciolosis in animal production are counts are>10 epg(► p. 526). Since the epg values are
estimated at 2 billion US$ annually. often lower and also subject to significant fluctuations,
a lower diagnostic sensitivity of a single examination of
 Part Ill. Parasites and parasitoses: metazoa
an individual animal has to be expected (e.g. in cattle
55-80%). An increase in sensitivity to approximately
90% is possible by using 10 g of faeces per sample
and examination of three samples per animal. Since
fasciolosis is usually a herd problem, a reliable diagnosis
can usually be made by single (or repeated) faecal
examinations of an adequate number of animals. For
herd surveillance, the detection of specific antibodies
in blood serum or in bulk milk samples by ELISA is
suitable. A commercially available test for detecting
antibodies in milk (Pourquier� ELISA fascioliasis serum
milk) had, in one study, a mean sensitivity of 88% and
a specificity of 84%. It should be noted that specific
antibodies in serum occur about 2-7 weeks after a
primary infection in sheep and cattle, depending on
the dose of infection, and persist for many months; after
successful chemotherapy an antibody persistence of 8
months has to be expected in cattle. By copro-antigen
ELISA, patent Fascia/a infections can be diagnosed
with high sensitivity and specificity (>90%) as well as
prepatent infections (in sheep 1-5 weeks before onset:
of egg shedding), if a high quality test system is used.
l
• Subacute fasciolosis. Subacute fasciolosis is often
associated with low egg excretion; it is missing in the
acute form. In Fascia/a infections of horses and pigs, the
excretion of eggs is often low or absent.
For the diagnosis of fasciolosis, blood parameters can
contribute important information, particularly elevated
liver enzymes (AST and GLDH in acute and subacute,
GGT in chronic fasciolosis) and eosinophilia, anaemia,
hypoalbuminaemia and the serological detection of
specific antibodies. The puncture of the gall bladder
under sonographic control in cattle with subsequent
microscopic examination of bile for eggs of Fascia/a
and Dicracaelium is a sensitive diagnostic method that
is limited to individual cases in the clinic.
• Post mortem diagnosis. Assessment of liver
changes, cutting and squeezing the bile ducts and the
liver parenchyma for the detection of adult or juvenile
liver flukes, examination of bile sediment for Fascia/a
eggs. The routine examination of slaughtered cattle
detects only about 60% of the livers infected with
P. hepatica.
Q}
·o
C
'6 Therapy. Various drugs are available for the treatment
�
Q}
of fasciolosis, for example closantcl, netobimin, and
c triclabendazole. In their application the different
<O
C efficacies against juvenile and adult stages have to be
·c: considered ( ► Table I 9.2, p. 579). Triclabendazole
j is regarded as a reference, since it is highly effective
£ against juvenile and adult Fascia/a stages (sheep: I 0
>, mg/kg b.w. p.o., cattle: I 2 mg/kg b.w. p.o.). In some
Ol
0 countries, F. hepatica strains from sheep have been
0
'ui found with resistance to fasciolicides (including
co rafoxanide, closantel and triclabendazole). For example,
co
0... triclabendazole resistance has been diagnosed in the UK
and the Netherlands. For all fasciolicides withdrawal
periods or other restrictions have to be observed
(► Table 19.2; ► Table 19.6, ► p. 585 ff).
Control. Control against fasciolosis is carried out
within integrated programs by preventive measures
in conjunction with 'strategic' anthelmintic treatments
(metaphylaxis) (► Glossary, p. 620) of the liver fluke
carriers at epidemiologically relevant time points, under
consideration of the lactation period of cows or milking
sheep (details ► p. 576).
Zoonotic importance. There are reports from
many regions of all continents on sporadic or endemic
infections of humans with F. hepatica (in the north of
Bolivia local prevalences over 70%). Worldwide, the
number of infected people is estimated at 2.4 to 17
million. In Europe, over 5,000 cases from 19 countries are
known in recent times, especially from France, Portugal
and Spain. In Asia and Africa, F. gigantica infections have
also been diagnosed in humans. The infection of humans
happens by ingestion of metacercariae that adhere to
contaminated plants (e.g. watercress, vegetables) or with
water (floating cysts). Pigs could be experimentally
infected by administration of fresh liver containing
juvenile stages of F. hepatica. Infection in humans are
unapparent or associated with hepato-cholangitic signs.
Diagnostic options are coproscopic detection of eggs
(after a prepatent period of 2-4 months), copro-antigen
detection, serological testing for specific antibodies and
imaging techniques for liver alterations.
Fascia/a gigantica (large liver fluke)
Disease: Tropical fasciolosis. I
Fasciola (L): band; giganteus (L): huge, gigantic.
Agent. F. gigantica is similar to F. hepatica, but longer
(24-75 mm) and relatively slender (5-12 mm), the 'apical
conus' is shorter, the 'shoulders' are less pronounced and
the posterior end is more rounded. The eggs correspond
morphologically to those of F. hepatica, but are usually
larger ( l 50-190x90-100 µm). Within the species F.
gigantica there are several strains with slightly different
biological properties.
Life cycle and epidemiology. Definitive hosts are
mainly cattle and buffaloes, to which the parasite is
particularly well adapted, but also sheep, goats, horses,
donkeys, camels and other herbivores. Humans are
also occasionally affected (see above). The life
cycle corresponds in principle to that of F. hepatica.
Epidemiologically important intermediate hosts
are various subspecies of the Radix (syn. Lymnaea)
auricu/aria complex (including Radix auricularia, R.
natalensis, R. rufescens). These snails live in stagnant
.,.......--
or slow-flowing, oxygen-rich fresh water, such as lakes,
rivers, or often on irrigated rice fields. The development
of miracidia in the eggs of F. gigantica takes at +25 °C
about 3 weeks, that of cercariae in the intermediate host
4 weeks. The development is suspended at temperatures
below+ 16 °C. Up to 1/3 of the cercariae can develop into
floating metacercariae (floating cysts), the remaining
attach themselves to plants or other objects. Floating
cysts apparently play a greater role in the infection of
definitive hosts than in F. hepatica. The infection risk
for definitive hosts varies in most habitats throughout
the year depending on rainy and dry seasons. At cooler
temperatures, the metacercariae of F. gigantica cnn
remain viable in forage plants up to 6 months. The
development in the definitive host follows in principle
the same course as in F. hepatica. Prepatent period: 13-16
weeks. In cattle, the parasites usually survive less than
I year, but some 3-4 years.
Occurrence and adverse effects. F. gigantica
occurs in subtropical and tropical areas in Africa
(especially Sub-Saharan Africa) and Asia (belt from
Turkey across southern Asia to the Philippines and
Indonesia), which overlap in part with endemic areas of
F. hepatica. Tropical fasciolosis with prevalences around
90% is regionally considered as the most important
helminthosis of cattle and water buffaloes.
Pathogenesis and clinical signs. Changes and
forms of tropical fasciolosis are similar to those of the F.
hepatica infection, but cattle more frequently have liver
lesions corresponding to those caused by F. hepatica in
sheep. More severe infections of F. gigantica manifest
themselves in inappetence, weight loss, anaemia,
diarrhoea and oedema formation.
Immunology. In contrast to F. hepatica, a primary F.
gigantica infection in sheep and goats induces significant
immune protection against further homologous
infections. Therefore, the prospects for developing
a vaccine against F. gigantica are likely to be more
favourable than in F. hepatica.
Diagnosis. Coproscopic detection of eggs using the
sedimentation technique. With a copro-antigen ELISA
100% of cattle infected with more than 15 specimens of
F. gigantica could be identified.
Therapy and control. In sheep and cattle trida­
bendazole (10 mg/kg or 12 mg/kg b.w. p.o.) is highly
effective against juvenile and adult F. gigantica, but in
buffaloes only at an increased dose (24 mg/kg b.w.).
Depending on the age of the infection and the dosage,
clorsulon and dosan tel are also effective (► Table
19.2). The control strategies are similar to those against
F. hepatica.
9. Phylum Platyhelminthes (flatworms)
Genus Fascio/oides
Fascioloides magna (large American liver
fluke, giant liver fluke)
Adults about 70-100 mm long and 30-40 mm wide,
leaf-shaped, eggs similar to F. hepatica, average 145x94
µm. F. magna is in North America (USA, Canada)
regionally a fairly common parasite of cervids, including
wapiti (Cervus elaph11s), white-tailed deer (Odocoileus
virgi11ia1111s) and caribou (Rangifer tarandus caribou) in
which the parasite attains sexual maturity. In endemic
areas, other wild ruminants(moose, bison) or domestic
ruminants(cattle, sheep) can be infected, but the parasite
usually docs not reach sexual maturity in these hosts.
Probably introduced with American cervids to Europe,
I� magna was first found in red deer in a Turin zoo and
later sporadically elsewhere. Today, F. magna is endemic
in some areas in roe deer, red deer and fallow deer(free­
living or in an enclosure), predominantly in CZ, SK, AT,
HU, HR, DE and IT (2006: in HR prevalences in red and
fallow deer 13-90%, in the Austrian Danube floodplains
on average 6%, locally up to 100%).
The life cycle is similar to that of F. hepatica. Intermediate
hosts are snails of the family Lymnaeidae, in Europe
Galba truncatula; the cercariae encyst on plants. In
the definitive host, the parasites migrate from the
intestine through the peritoneal cavity to the liver
and occasionally to other organs. In cervids, serving
as natural hosts, the juvenile stages of F. magna -
after a migration phase in the liver parenchyma - are
enclosed in walnut-sized, thin-walled cysts in which
the parasites reach sexual maturity. Since the cysts
are openly connected with the biliary tract, shedding
of eggs to the environment is possible. The prepatent
period lasts about 6 months. In contrast, in bovids the
parasites are usually completely enclosed in thick-walled
capsules. In sheep and goats, the juveniles permanently
move about in the liver parenchyma and cause severe
liver damage, but rarely induce the formation of thin­
walled capsules. Triclabendazole or closantel are used
for therapy(► Table 19.2).
Genus Parafasciolopsis
Parafascio/opsis fascio/aemorpha (elk liver
fluke)
Adult flukes are lanceolate, with a well-defined head
cone, only about 3-7xl.0-2.5 mm in size (► Figure
9.12), eggs brownish 120-130x80-84 µm. The life
cycle is similar to other fasciolids but with planorbid
snails (Planorbarius corneus) as intermediate hosts.
The cercariae encyst on the water surface and plants
and are taken up with them or with drinking water. In
the definitive host, the juveniles that hatch from the
metacercarial cysts settle initially in the small intestine
where they develop to preadult or sexually mature stages
 Part Ill. Parasites and parasitoses: metazoa

Family Echinostomatidae

Echinos (G): hedgehog; stoma (G): mouth. Refers to a

collar of spines around the oral sucker.

Summary
The adults of this family parasitise iA the intestine of
amphibians, reptiles, birds, mammals and humans.
• Their integument is often covered with spines, the oral
sucker is surrounded by a collar of spines (► Figure
9.13).
• First intermediate hosts are snails, second inter­
mediate hosts invertebrates or vertebrates. The
Echinostomatidae are mainly of practical importance
as parasites of waterfowl.
Figure 9.12. Parafascio/opsis sp. (Graphics: IPZ, A. Seeger;
after Skrjabin 1948).

and then migrate through the Ductus choledochus into

the gallbladder and bile ducts, where egg-producing
stages are predominantly found. Occasionally there
is also a migration into the pancreatic ducts. The elk
(= moose) (Alces alces) is regarded as the original
host in which the parasite causes a chronic bile duct
inflammation with mineral deposits. Natural infections
with the 'elk Liver fluke' also occur in deer, red deer, bison
and sheep; cattle and rabbits proved to be susceptible
experimentally. In moose and sheep heavy infections
can cause severe liver damage and death. Distribution:
eastern and south-eastern Europe (Poland, Russia,
Hungary, former Yugoslavia).

a b

Figure 9.13. (a) Echinostoms revolutum; (b) E. revolutum:

anterior end with collar of spines (Graphics: IPZ, A. Seeger;
after Kotlan 1960).

The species of the gencrn Echinostoma and Hypo­

derac11m listed in ► Table 9.5 are causative agents of
echlnostomatidosls of birds. They mainly play a role in
Q)
outdoor rearing of water fowl which acquire the infection
·u
C

'5 by ingestion of metacercariae-containing freshwater

Q) snails or other intermediate hosts. Pigeons and chickens
�
�
occasionally consume water snails at the edge of stagnant
(1j
C
water or on damp ground thus becoming infected. In
·;;::
heavy infections the echinostomatids cause catarrhaJ
or haemorrhagic enteritis, diarrhoea or emaciation and
C even death. Diagnosis is usually made by detection of
>,
0)
the parasite at necropsy. Flubendazole and praziquantel
0 are effective according to some reports. Isthmioplwra
0
·en me/is (syn. Euparyphium melis) was found in northern
Germany in around 1 % of foxes and cats and in 32% of
74 raccoon dogs (Nyctereutes procyonoides).
 9. Phylum Platyhelminthes (flatworms)

Table 9.5. Species (selection) of the family Echinostomatidae. 1

Species, slze1 dlstrlbutloh (D) httennedlate hosts (IH) beflnltlve hoita Pl'edllectlon altea
of adults

Echinostoma revolutum 2 1 st IH: fresh water snails Lyrnnaeidae: duck. goose, pigeon, ileum, caeca,
6.5-30x0.6-1.6 mm L. palustris, L. stagnalis. Galba tnmcatula chicken. turkey rectum Cil
-0
D: Europe, Asia 2nd IH: fresh water snails Physidae.
Planorbidae
.E0
Echinoparyphium recurvatum 2 1st IH: fresh water snails Lymnaea. Physa, duck. goose, other small intestine
en
0
1.5-4.5x0.7 mm C
Planorbis, etc. water birds, rarely E
_ 2nd �fresh water snails. frogs galliformes, pigeon (.)

Hypoderaeum conoldeum 2 1s t IH: fresh water snails Lymnaea duck. goose, other small Intestine
12x2 mm stagnalis, etc. water birds. chicken,
D: Europe, Africa.'.. Asia, North America 2nd IH: fresh water snails frogs, leeches pigeon
/sthmiophora melis2 1•t IH: fresh water snails Lymnaea mustellcls. rox, small intestine
2.4-11x0.7-1.6 stagna/ls, etc. hedgehog, cat, pig,
D: Holarctlc 2nd IH: amphlbla, fish etc.
1 Date without claim to completeness.
2 Species occurring in Central Europe.

Selected references Knubben-Schwelzer G, Torgerson PR (2015) Bovine

Bennema SC, Ducheyne E, Vercruysse J, Claerebout E,
Hendrickx G, Charlier J (2011) Relative importance of
management, meteorological and environmental factors in
the spatial distribution of Fasciola hepatica in dairy cattle
in a temperate climate zone. Int J Parasitol 41: 225-233.
Bennema SC, Vercruysse J, Claerebout E, Schnieder T,
Strube C, Ducheyne E, Hendrickx G, Charlier J (2009)
The use of bulk-tank milk ELISAs to assess the spatial
distribution of Fascia/a hepatica, Ostertagia ostertagi and
Dictyocaulus viviparus in dairy cattle in Flanders (Belgium).
Vet Parasitol 165: 51-57.
Baray JC (1969) Experimental fasciollasis In Australia. Adv
Parasitol 7: 95-210.
Charller J, Bennema SC, Caron Y, Counotte M, Ducheyne E,
Hendrickx G, Vercruysse J (2011) Towards assessing fine­
scale indicators for the spatial transmission risk of Fascia/a
hepatica in cattle. Geospat Health 5: 239-245.
Charlier J, Vercruysse J, Morgan E, van Dljk J, Williams
DJ (2014) Recent advances in the diagnosis, Impact on
production and prediction of Fascia/a hepatica In cattle.
Parasitology 141: 326-335.
Flynn RJ, Mulcahy G, Elsheikha HM (2010) Coordinating
innate and adaptive immunity in Fascia/a hepatlca Infection:
implications for control. Vet Parasitol 169: 235-240.
Forbes AB, Reddick D, Stear MJ (2014) Efficacy of treatment
of cattle for liver fluke at housing: influence of differences
in flukicidal activity against juvenile Fascia/a hepatica. Vet
Rec 176: 333
Gordon DK, Zadoks RN, Stevenson H, Sargison ND, Skuce
PJ (2012) On farm evaluation of the coproantigen ELISA
and coproantigen reduction test in Scottish sheep naturally
infected with Fasciola hepatica. Vet Parasitol 187: 436-444.
Knubben-Schweizer G, Ruegg S, Torgerson PR, Rapsch C,
Grimm F, Hassig M, Deplazes P, Braun U (201O) Control of
bovine fasciolosis in dairy cattle in Switzerland with emphasis
on pasture management. Vet J 186: 188-191.
fasclolosis: control strategies based on the location of Galba
truncatula habitats on farms. Vet Parasltol 208: 77-83.
Kralova-Hromadova I, Bazsalovlcsova E, Stefka J,
Spakulova M, Vavrova S, Szemes T, Tkach V, Trudgett
A, Pybus M (2011) Multiple origins of European populations
of the giant liver fluke Fascioloides magna (Trematoda:
Fasclolidae), a liver parasite of ruminants. Int J Parasitol
41: 373-383.
Mas-Coma S, Bargues MD, Valero MA (2005) Fasioliasis
and other plant-borne trematode zoonoses. Int J Parasitol
35: 1255-1278.
Moskwa B (1990) Immunological reactions of sheep and lambs
to experimental Infection of Parafasciolopsis fasciolaemorpha.
Acta Parasitol Polonica 35: 223-231.
Novobilsky A, Engstrom A, Sollenberg S, Gustafsson K,
Morrison DA, Hoglund J (2014) Transmission patterns
of Fasciola hepatica to ruminants in Sweden. Vet Parasitol
203: 276-286.
Palmer DG, Lyon J, Palmer MA, Forshaw D (2014) Evaluation
of a copro-antigen ELISA to detect Fasciola hepatica infection
In sheep, cattle and horses. Aust Vet J 92: 357-361.
Rapsch C, Schweizer G, Grimm F, Kohler L, Bauer C,
Deplazes P, Braun U, Torgerson PR (2006) Estimating
the true prevalence of Fascia/a hepatica in cattle slaughtered
in Switzerland in the absence of an absolute diagnostic test.
Q)
Int J Parasitol 36: 1153-1158. C
Sattmann H, Horweg C, Gaub L, Feix AS, Haider M,
·c::;
'6
Walochnik J, Rabitsch W, Prosl H (2014) Wherefrom and Q)
whereabouts of an alien: the American liver fluke Fascioloides
magna in Austria: an overview. Wien Klin Wochenschr 126 Cil
C
Suppl 1: S23-31. ·.::
Q)
Schweizer G, Braun U, Deplazes P, Torgerson PR (2005)
Estimating the financial losses due to bovine fasciolosis in -�
Switzerland. Vet Rec 157: 188-193. >.
Ol
0
0
"cii
Cil
0...
 Part Ill. Parasites and parasitoses: metazoa

9.1.2 Order Amphistomida

Amphi (G): on both sides; stoma (G): mouth. Refers to
two suckers, one at the anterior and the other at the Pharynx
posterior end of the body.

Summary
• Agents. Amphistomida are trematodes of a mostly
pear-like or conical body shape with the ventral sucker
located at the posterior end. Numerous species
parasitise fish, amphibians, reptiles, birds and mammals.
In Europe, several species are of interest, living In the Acetabulum
adult stage in the rumen of ruminants (rumen flukes), (sucker)
e.g. Paramphistomum cervi and Calicophoron daubneyl.
• Life cycle. Indirect cycle with water snails (Planorbidae,
Lymnaeidae) as Intermediate hosts. Infection of
definitive hosts by ingesting encysted metacercariae.
The juvenile stages initially colonise the small Intestine Figure 9.14. Paramph/stomum sp.: histological sagittal section
and then migrate into the rumen.
(Photo: IPZ).
• Pathogenesis, clinical signs. Adverse effects in
severe infections are caused by the Juvenile stages
in the intestine, but they rarely occur under European
conditions. Calicophoron microbothrium). Of these, P. cervi and C.
• Diagnosis, therapy. Coproscopic detection of eggs daubneyi probably have the widest distribution. Since
(sedimentation technique). For therapy, see below. these parasites live in the adult stage in the rumen, they
are referred to as 'rumen flukes'(► Table 9.6).

The majority of the Amphistomida have a pear-like or
conical body shape. The oral sucker is replaced by a strong
pharynx; the ventral sucker (acetabulum) is located at
the rear end and is usually strongly developed (► Figure
9.14). In Central Europe several Paramphistomum
species occur in domestic and wild ruminants, including
Paramphistomum cervi, Calicophoron daubneyi (syn.
P. daubneyi), P. ichikawai and P. microbothrium (syn.
In various areas, especially in warm countries, other
species of rumen flukes are endemic, including the
genera Paramphistomum, Cotylophoron, Calicophoron,
Gastrothylax and Fischoederius. The family Gastrodiscidae
includes Gastrodiscus aegyptiacus (caecum and colon of
equids in Africa) and Gastrodiscoides hominis (caecum
and colon of pigs and humans in Asia).

Table 9.6. Species (selection) of the family Paramphistomidae.1

8peclN. .., dl81rtbutlon (DJ Intermediate hoeta Definitive hoeta Predlleotlon lltea
(heh water anallaJ of■dulta

Paramphlstomum cervl 2 Planorbldao: e.g. Plonorbls cattle. buttalO. sheep, 9oa1. rumon
(rumen fluke) planorbls, Anlsus vortex wild ruminants (ro<:I ond fOIIOw
6-12x2-4 mm door. roo door. hlson, otc.)
D:_Europe, North America. Asia
Callcophoron daubneyl 2 (syn. Lymnaolldae: Gn/lJ(J C8IIIO, buffnlO. shQop, wllel rumon
Paramphlstomum daubneyl 2 ) truncatulll, possibly Lynmaon rurn1nants
(rumen fluke) fuscus and L, palustns
4.6-9.8x2.4-6.4 mm
D: Europe, Africa
Paramphlstomum lchlkawai 2 Planort>1dae: e.g. Amsus spp. cattle, sheep, wild ruminants rumen
(rumen fluke)
5-7x2-3mm
D: Europe, Russia, Australia
Explanatum (syn. Gigantocotyle) Planorbidae: Gyraulus sp. catlle, buffalo, w,ld rumll'lanlS bile ducts, gall
explanatum) bladder
8-13x3.5-6 mm
D: Central and East Asia Africa, Canbbean
1 --- - -------'----- ------'--------
Data without claim to complete�-----
2 Species occurring in Central Eur ope.
+"
Family Paramphistomidae (rumen
flukes)
Genus Paramphistomum
Paramphistomum cervi
Disease: Paramphlstomosis.
Agents. In the adult stage P. cervi is 5-12 mm long,
2-4 mm wide and about as thick, pear-shaped, with a
large acetabulum and a striking reddish colour(caused
by the parasite's own haemoglobin)( ► Figure 9.15 and
9.16). Other species are morphologically similar. The
species identification of the rumen flukes is difficult and
possible on sagittal sections based on the morphology
of the internal organs and the acetabulum. Eggs: oval,
with operculum, similar to eggs of Fasciola hepatica,
but they are almost colourless and on average larger
(140-180x76-95 µm).
Life cycle. The eggs expelled in the faeces of definitive
hosts( ► Table 9.6) are undeveloped and susceptible
to dehydration, but can survive for months in a humid
environment, especially at low temperatures(at 10 °C
Figure 9.15. Paramphistomum sp. from a cow; length about
11 mm (Photo: IPZ).
Figure 9.16. Paramphistomum sp. in the rumen of bison (Photo:
IPZ).
9. Phylum Platyhelminthes (flatworms)
for about 6 months). In an aqueous environment at
temperatures between 15-25 °C miracidia develop in
about 3 weeks that hatch from the eggs and invade
intermediate host snails(Planorbidae)( ► Figure 9.17)
and develop into cercariae. The cercariae released from
the snails encyst on plants and change into metacercariae ca
D
(diameter about 250 µm), which soon become infective .E
and may remain viable under sufficiently moist
conditions for 3-5 months, but quickly perish in dry ..c
a.
conditions(e.g. during hay drying). E
<(
Definitive hosts become infected by ingesting infectious
metacercariae with fodder plants. The juvenile rumen
flukes hatch in the small intestine, they initially colonise
the duodenum for I ½-2 months growing there to 1-3
mm in length before migrating to the rumen where they
attach with the acetabu.1um to the villi. The prepatent
period in cattle and sheep lasts 3 ½ months, and is slightly
shorter in roe deer. In heavy infections, juvenile stages
may persist for several months in the small intestine.
Occurrence and epidemiology. C. daubneyi
uses the same intermediate host ( Galba truncatula)
as Fasciola hepatica, and is known to occur in several
European countries, e.g. France, Spain, UK, and Ireland.
According to recent reports(2014), this species appears
to be the most common if not the only species in Ireland
where it occurs in cattle regionally in high prevalences up
to 100% and significant infection intensities, associated
with morbidity. Cl)
..c
C
The intermediate hosts of P. cervi are water snails o f
the family Planorbidae ( ► Table 9.6), which live i n
.E
Q)
shallow, plant-rich waters (ponds, pools, ditches) and :r:
partly in marshy areas. Larval stages of the flukes may
overwinter in the snails. It is assumed that the cercariae
are swarming out of the snails predominantly in May
and June, so that from this time on there is an increased
infection risk. Wild ruminants serve as reservoir hosts
for P. cervi.
Pathogenesis and clinical signs. Intestinal
infections are pathogenically significant when hosts
are infected with large numbers of parasites (several
thousand to ten thousand worms). Juvenile rumen flukes
destroy plugs of the mucosa by means of the acetabulum Q)
and cause small local haemorrhages, inflammation
·u
C
i5
Q)
�
ca
C
·;::
C
>-
0)
0
0
·u5
Figure 9.17. Shell of Planorbis sp. (diameter about 24 mm) ca
C1:l
(Photo: IPZ). Q..
 Part Ill. Parasites and parasitoses: metazoa
(enteritis) and necrosis, often accompanied by a
significant loss of albumin into the intestinal tract.
Consequently diarrhoea, inappetence, weight loss,
weakness, and death may occur. During the ruminal
phase of the infection the adult stages usually cause
only minor tissue damage that is clinically insignificant.
Clinical signs of intestinal paramphistomosis are mainly
observed in lambs and young cattle in warm regions.
In Central Europe, infections with paramphistomes in
domestic and wild ruminants are mostly unapparent,
but regionally some losses of productivity may occur,
as reported from Britain and Ireland.
Immunology. The infection with P. microbothrium
stimulates a certain degree of immunity that leads to a
reduction of the number of juveniles in the intestine,
thereby reducing the risk of disease.
Diagnosis. In living animals eggs can be detected by
coproscopy (sedimentation technique). Paramphistonwm
eggs are on average larger and colourless compared to
the very similar Fascia/a eggs ( ► Figure 16.8, p. 539).
Egg shedding of Calicophoron or other species should
be considered as potential confounding factor in liver
fluke diagnosis and in field tests used to determine drug
resistance against F. hepatica. In clinically suspected
cases washing of faeces through a sieve (with small
mesh sizes) and examination of the sieve residue using
a stereomicroscope for juvenile stages is recommended.
Post mortem: examination of the small intestine for
juvenile stages (sieving and washing technique) and the
rumen wall for adults (macroscopically).
Therapy and control. Oxcyclozanide ( I 5 mg/kg. b. w.
p.o.) and closantel (IO mg/kg. b.w. p.o.) have shown high
efficacy against adult C. daubney in catt.le. Albendazole
in an increased dose ( 15-20 mg/kg b.w. p.o.) has a partial
effect on intestinal stages. A prophylactic option is to
prevent access of the grazing animals to the sources of
infection, e.g. by fencing in snail habitats (see Pasciola
hepatica, ► p. 576).
Further Paramphistomidae
For information on the distribution of other species sec
► Table 9.6. The life cycles of these species nre similar
(1)
C to that of P. cervi, with the exception of Gigantocotyle
·o
'6(1) explanatum (syn. Expla11at111n explmratum) in callle and
�
buffaloes. The adults of this species, common in Asia,
c
ro
colonise the bile ducts and the gallbladder and cause
C chronic bile duct inflammation with severe thickening
·c
(1) of the bile duct wall. In this regard, the changes arc
similar to fasciolosis.
C:
>
Cl
0
·1n
co
co
0..
Selected references
Abrous M, Rondelaud D, Dreyfuss G (2000) A field study of
natural infections in three freshwater snails with Fasciola
hepatica and/or Paramphistomum daubneyi in central France.
J Helminthol 74: 189-194.
Arias MS, Sanchfs J, Francisco I, Francisco R, Pineiro
P, Cazapal-Monteiro C, Cortinas FJ, Suarez JL,
Sanchez-Andrade R, Paz-Silva A (2013) The efficacy of
four anthelmintics against Calicophoron daubneyi in naturally
infected dairy cattle. Vet Parasitol 197: 126-129.
Dorchies P, Bergeaud JP, Duranton C, Prevot F, Tessier
P (1998) Prevalence of bovine paramphistomosis: results
of a field survey in France. Rev Med Vet; 149: 1029-1032.
Ferreras MC, Gonzalez-Lanza C, Perez V, Fuertes M,
Benavides J, Mezo M, Gonzalez-Warleta M, Giraldez
J, Martfnez-lbeas AM, Delgado L, Fernandez M, Manga­
Gonzalez MY (2014) Ca/lcophoron daubneyi daubneyi
(Paramphistomldae) in slaughtered cattle in Castilla y Le6n
(Spain). Vet Parasitol 199: 268-271.
Gordon DK, Roberts LC, Lean N, Zadoks RN, Sargison
ND, Skuce PJ (2013) Identification of the rumen fluke,
Calicophoron daubneyi, in GB livestock: possible implications
for liver fluke diagnosis. Vet Parasitol 195: 65-71.
Lotty WM, Brant SV, Ashmawy Kl, Devkota R, Mkoji GM,
Loker ES (2010) A molecular approach for identification of
paramphistomes from Africa and Asia. Vet Parasitol 174:
234-240.
Rolfe PF, Boray JC, Nichols P, Collins GH (1991) Epidemiology
of paramphistomosis in cattle. Int J Parasitol 21: 813-819.
Sey O (2001) Amphistomes of the World. Budapest, Hungary:
Hungarian Natural History Museum & University of Pees;
ISBN 963-641-865-9.
Vignoles P, Rondelaud D, Dreyfuss G (2008) Paramphistomum
daubneyi: production dynamics and infectlvity of
metacercariae originating from snails dissected at regular
intervals. J Helminthol 82: 175-180.
Zlntl A, Garcia-Campos A, Trudgett A, Chryssofidis AL,
Talavera-Arce S, Fu Y, Egan S, Lawlor A, Negredo C,
Brennan G, Hanna RE, De Wool T, Mulcahy G (2014)
Bovine poramphlstomes In lroloncl. Vet Parositol 204:
109-208.

9.1.3 Order Plagiorchiida
Plagios (G): oblique; orchis (G): testis. Refers to the
oblique positioning of the testes in many species.
Summary
• Agents. In Europe, the small llver fluke (lancet fluke)
Dlcrocoe/ium dendriticum, Is the most Important
representative of tliis order. Wltli about 1 ctn body
length D. dendriticum is tnucli smaller than the iarge
liver fluke (Fascia/a hepatics); In some areas tlii!9e
species occur sympatrically.
• Ufa cycle and occurrence. D. dendrltlcum Is a bile
duct parasite especially In ruminants, but also In other
herbivores (horse, donkey, hare, rabbit, etc.) and rarely
in omnivorous animals and humans. T he development
of D. dendriticum takes place In a terrestrial cycle with
two Intermediate hosts (land snails and ants). Infection
of definitive hosts: ingestion of ants that contain
metacercariae. In infected ants, a metacercaria in the
brain ('brain worm') Induces a change in their behaviour
so that they remain during the cooler night and morning
hours on the tips of plants, thus favouring their uptake
by definitive hosts. In the host, the juvenile lancet flukes
migrate from the small intestine tl:lrough the Duetus
choledochus into the bile ducts (compare Fascia/al) an<!I
develop there into adults. Prepatent period 7 weeks.
• Pathogenesis, clinical signs. D. dendritlcum is ef low
pathenicity, but can cause cholangltis and fibrosis of
the liver, reduced performance and on rare occasior;is
ether symptoms.
Diagnosis. In the living animal diagnosis Is
unsatisfactory because of the low sensitivity ef the
available techniques for detecting eggs In the faeces.
In sheep and cattle specific antibodies were detected in
the serum with high sensitivity (>85%) using an ELISA.
• Therapy, control. Chemotherapy is possible with
different anthelmintics; effective and sustainable control
strategies do not yet exist.
Zoonotic importance. Infections of humans with
the lancet fluke are very rare; more common Is the
gastrointestinal passage of lancet fluke eggs after
consumption of liver products originating from sheep
or cattle.
From the other families of the Plaglorchlldae (► Table
9.7 and 9.8) Paragonimus species have to be considered
as a cause o f lung disease in dogs imported from
endemic areas.
The Plagiorchiida are trematodes with different body
shapes, usually with a 3-host cycle (definitive host and
two intermediate hosts). They parasitise mammals and
birds (intestine, bile ducts, oviduct, lung, etc.), as well
as fish, amphibians and reptiles.
9. Phylum Platyhelminthes (flatworms)
Family Dicrocoeliidae
The members of this family ( ► Table 9.7) are small to
medium-sized, lanceolate trematodes, which as adult
stages mainly inhabit the bile ducts, gaU bladder or
pancreatic ducts of mammals, birds and reptiles. In the C1J
-0
life cycles of almost all species terrestrial intermediate
hosts are involved. An adaption to such cycles is that 2
0
their eggs already contain a miracidium when expelled "6,
C1J
from the host. In some areas ofEurope the lancet fluke,
Dicrocoe/ium dendriticum, is a common parasite of
domestic and wild ruminants.
Genus Dicrocoelium
Dicrocoelium dendriticum (syn. D. lanceolatum)
(lancet fluke, small liver fluke)
■
Disease: Dlcrocoellosls.
Dikroos (G): double, forked; koilos (G): hoUow; dendron
(G): tree. Refers to the forked intestine and the tree-like
branched uterus.
Agents. The adult parasites are 5-10 mm long and 2
mm wide and have a lancet-shaped, flattened, body of
brownish colour, integument without spines ( ► Figure
9.18 and 9.19). Other features include the slightly lobed
and tandemly arranged testes in the front third of the
body, the lateral vitelline glands and the meandering
uterus loops filled with eggs. Eggs: 38-45x22-30 µm,
oval, slightly asymmetrical, dark brown, thick-shelled,
with operculum. The egg, when passed in the faeces,
contains a fully developed miracidium in which two
spherical structures (germinal cells) are easily visible.
A very similar species is Dicrocoe/ium chinensis, but the
testes are arranged in a parallel position (epidemiology,
see below).
Life cycle. The sexually mature lancet flukes live in the
bile ducts and gall bladder of the definitive hosts (sheep,
goat, cattle, etc.) ( ► Figure 9.20). The eggs produced by
the parasites pass through the bile ducts to the intestine
and in the faeces to the environment. The miracidium
in the egg is well protected against environmental
influences by the resistant egg shell and can survive
long periods of time (epidemiology, see below).
The further development is dependent on two
intermediate hosts. First intermediate hosts are
numerous species of shell-bearing land snails. Plant
residues in the faeces ofruminants or other herbivores
are for the snails a sought-after food with which they
ingest eggs of the lancet fluke. The miracidia, ciliated
only at the anterior end and bearing an apical stylet,
hatch in the snail's intestine, they migrate to the digestive
gland and transform into irregularly shaped sporocysts.
 Part Ill. Parasites and parasitoses: metazoa

Table 9.7. Species (selection) of the family Dicrocoeliidae. 1

Species, size, distribution (D) Intermediate hosts (IH) Definitive hosts Predilection 8lte9
of adults

Dicrocoelium dendriticum 2 1 st IH: land snails domestic and wild ruminants, bile ducts, gall
(small liver fluke, lancet fluke) 2nd IH: ants (see text) camel, south american camelids, bladder
8-12x1.5-2.5 mm rabbit, hare, horse, rarely man
D: Europe, America, North Africa, Asia
Dicrocoelium hospes 1st IH: land snails Umicolaria sheep, goat. cattle, buffalo, pig, bile ducts, gall
(African lancet fluke) 2nd IH: ants Dory/us, rabbit, rarely man bladder
4.8-6.?x0.7-0.9 mm Camponotus, Crematogaster
0: Sub-Saharan Africa
Eurytrema pancreaticum 1st IH: land snails: Bradybaena, domestic ruminants, pig, camel, pancreas ducts
(pancreatic fluke) Ganesella monkeys
8-16x5-8 mm 2nd IH: grasshoppers
0: Asia, South America -- Co�ocephalinae -
Eurytrema procyonis 151 IH: land snails Mesodon raccoon, rarely cat pancreas ducts
(pancreatic fluke) thyroidus
1.7-2.Sx0.7-1.3 mm 2nd IH: presumably arthropods
0:USA
1
Data without claim to completeness.
2 Species occurring In Central Europe.

1,,

Figure 9.19. Dicrocoelium dendriticum (length about 11 mm)

and Fasciola hepatics (length about 49 mm) (Photo: IPZ).

From germ cells in these mother sporocysts, tubular

Figure 9.18. Dlcrocoellum dendritlcum: stained; length about
11 mm (Photo: IPZ).
daughter sporocysts emerge that are provided with a
birth opening. Finally, each of the daughter sporocyst
produces I 0-40 ccrcnrlne which are equipped with two
suckers, an apical stylet, tubular glands and a long tail.
The development until the formation of cercariae takes
3-5 months, but may be prolonged at lower temperatures.
If the snails are reactivated after a resting phase (e.g. dry
rest) by wet weather, the cercariae leave the daughter
sporocysts and migrate into the respiratory cavity of
the snail. There, they release a slimy secretion from
their glands in which they wrap up the cercariae, and
form aggregates of usually a few hundred individuals,
the so-called 'slime balls'. These are covered by the snail
with another layer of mucus and expelled from the
respiratory cavity. Slime balls sticking together can form
berry-like conglomerates (3-12 mm), containing up to
6,000 cercariae. In the rapidly decaying slime balls the
cercariae survive at best only a few days ( ► Figure 9.21 ).
 I ; •

Cl]
'Q
E.
u
0
g>
a:

Ants attached · --�

to plant
Adult stage
(Immature stages not shown)

- - - - - - - - - - - - - - - - -Q ��.;� -
t/
Slime ball with

��,�- f: --.. (b
0
Hatched

/
mlracidium

K
\ Cercarla
Ant \
Land snall Mother

�-�--;--,
sporocyst

�� ,
'Brain worm' ercarla
penetrating
the crop wall
Daughter sporocyst

Figur e 9.20. Life cycle of Dicrocoellum dendritlcum (Graphics: IPZ, S. Ehrat).

Sec ond interm ediate hosts are various species of ants,
mainly ofthe genus Formica, which consume the slime
ball thereby ingesting cercariae of D. dendriticum. In
the ant the cercariae penetrate the wall of the digestive
tract in the area of the crop leaving the tail behind,
thus passing into the abdominal body cavity. The holes
caused by the penetration process are carefully sealed.
After a short period of inactivity, some cercariae begin
to migrate cranially to the head of the ant. There, one
cercaria (rarely 2-3) penetrates the brain where it is
surrounded by a thin envelope. As soon as this so-called
'brain worm' is established, the remaining cercariae
retreat caudaHy. In the abdomen, rarely in the thorax,
the cercariae undergo morphological changes; they are
enclosed by a capsule about 20 µm thick and mature
into metacercariae (size of encysted metacercariae
 Part Ill. Parasites and parasitoses: metazoa
Figure 9.21. He/ice/la sp. releasing 'slime balls' of Dicrocoelium
dendriticum (Photo: IPZ).
about 400x280 µm) ( ► Figure 9.20 and 9.22). The
development of the metacercariae in the ants takes at
least 40 days at 25 °C. These encysted metacercariae are
infective for the definitive host, but not the 'brain worm'.
Most of the naturally infected ants contain up to 100
metacercariae, some over 400. After maturation of the
metacercariae the ants show a biologically interesting
change in behaviour, triggered by the 'brain worm':
they do not return to their nests in the evening at
temperatures< 15 °C, but migrate to the tips of plants
and firmly attach to them with their mouthparts in a
spasmodic manner. This favours the ingestion of infected
ants by grazing animals. The spasm is released when
the temperature rises, so that during the day the ants
resume their usual activity. Ants infected with a 'brain
worm' of D. hospes remain on plants, but they are not
attached by their mouthparts.
After ingestion by a susceptible definitive host the
metacercariae are activated in the small intestine, leave
the capsule and migrate through the Ductus choledochus
into the bile ducts of the liver, where they reach sexual
maturity. The prepatent period is about 7 weeks, and
the life span of the lancet fluke in the definitive host is
estimated at I ½-6 years. Mixed infections with Fasciola
hepatica are not uncommon in endemic areas.
Distribution, occurrence and epidemiology. D.
dendriticum is regionally endemic in North America,
Europe, North Africa and Asia(Turkey, Middle East to
China, Japan, Philippines) and in some South American
(])
countries. 1n Europe, the area of distribution includes
·u
C
'6 numerous countries from the Iberian Peninsula to Russia
(]) and from Scandinavia to southern and south-eastern
�
�
Europe. Within these countries, the distribution is
co
C
heterogeneous and depends on the habitat conditions.
·;:: Locally, the prevalence of the parasite can be high, e.g. at
J-�
(])
about 50% in slaughter cattle, 30% in sheep and 48% in
goats in Switzerland. Definitive hosts of D. dendriticum
>,
0)
are mainly ruminants(sheep, goat, cattle, buffalo, roe
0 deer, deer species, ibex, chamois, elk, etc.), as well as
0
'iii
other herbivores(e.g. horse, donkey, South American
co camelids, rabbits, hare, marmot) and rarely, pig and
co
0... man. Domestic ruminants are primarily responsible
l
Figure 9.22. Dicrocoelium dendriticum: metacercariae: size
approximately 480x280 µm (Photo: IPZ, K. Wolff).
for the contamination of pastures with eggs of D.
dendriticum. Sheep, which are infected with about
300-900 adult lancet flukes can expel per gram of
faeces about 5,000 eggs every day. These eggs are very
resistant, and can overwinter and remain viable in the
faeces at temperatures between + 18 °C and - IO °C for
about 3 months, occasionally even up to 11 months.
Little is known about D. chinensis, a species probably
imported with Sika deer from Asia to Austria, which has
subsequently been found there and in northern Italy in
native wild ruminants(bighorn sheep, deer).
As first intermediate host numerous species(>90) of
shell-bearing land snails(Pulmonata, Stylommatophora)
have been described in Europe, including He/ice/la
itala ( ► Figure 9.21), He/ice/la obvia(syn. Xerolenta
obvia) and Zebrina detrita. These species prefer dry
and calcareous soils. Cochlicopa lubrica(syn. Cione/la
lubrica) is another intermediate host species, which
lives in moderately moist habitats in Europe and is
widespread both in lowland areas and in alpine regions
(2,600 m above sea level)( ► Figure 9.23). Therefore,
the development of the lancet fluke is possible both in
dry and in wet habitats under the condition that first
and second intermediate hosts are present. The long
life span of the snails (e.g. H. itala up to 3 years) is
epidemiologically significant.
Second intermediate hosts arc mainly ants of the genus
Formica(in Europe, among others, Formica cunicu/aria,
F. rufibarbis, F. prate11sis and F.fusca). In extensively used
pastures, especially in hilly and mountainous regions,
favourable conditions exist for the cycle of the lancet
fluke. Grassland, intensively cultivated mechanically,
is not suitable for nesting of ants; here the nests are
especially found in border areas and along fences. The
developmental stages of D. dendriticum can overwinter
both in the snails and ants and also survive periods of
inactivity of their intermediate hosts. At temperatures
below +5 °C the development of the parasite in the
snails is arrested.
In Central Europe, ants are found after hibernation
in large numbers in April/May outside the nests.
►
Figure 9.23. Dicrocoelium dendriticum: Intermediate host
Cochlicopa lubrica (height of the shell 6 mm) (Photo: IPZ).
In an endemic area of Germany, about 25% of the
overwintered snails (H. obvla) contained mature
sporocysts of D. dendriticum in spring. According to
studies in DE, FR and CH definitive hosts can acquire
the infection with D. dendriticum throughout the whole
grazing season. Usually, however, the infection risk is
highest at the beginning of the grazing period until
May/June; thereafter it decreases gradually, but it may
rise somewhat in autumn. Infections are possible even
in housed animals by feeding grass to which infected
ants adhere.
Pathogenesis. The lancet fluke generally causes
less damage than Fascia/a because it neither migrates
through the liver parenchyma nor sucks blood. The
degree of damage depends on the time and intensity
of infection. In sheep and goats, and especially in
South American camelids, the changes are often
more pronounced than in cattle. In livers recently
infected with lancet flukes, the central vein and the
periportal vessels of the liver lobules are expanded.
The bile ducts show signs of catarrhal inflammation
(cholangitis) with increased mucus production, oedema
and cellular infiltration of the mucosa. Adenoma-like
glandular proliferation and proliferation of smooth
muscles, connective tissue and ground substance result
eventually in thickening of the bile duct wall in the
further course of the infection (► Figure 9.24 and
Figure 9.25. Dicrocoe/ium dendriticum: histological section
through an infected bile duct in the liver of a sheep (Photo:
IPZ, K. Wolff, B. Hauser, P. Wild).
9. Phylum Platyhelminthes (flatworms)
Figure 9.24. Dlcrocoellum dendrltlcum: sheep liver with severe
Infection, thickened bile ducts (Photo: IPZ).
9.25). Furthermore, local extensions of the bile ducts
occur (cholangiectases). Longer existing cholangitis can
lead in the liver parenchyma to increasing formation of
connective tissue (fibrosis), which completely encloses
the liver lobules (monolobular fibrosis), and to cirrhosis
with destruction of hepatocytes. Hepatic dicrocoeliosis
can induce proliferative changes in lung arteries in New
World camelids. In experimental infections of hamsters
and sheep with D. dendriticum elevated levels of liver­
specific serum enzymes (ALT, AST) were detected. In
golden hamsters there was evidence of liver cell damage
by oxidative stress and formation of fatty acid peroxides.
Macroscopically weakly infected livers often appear
unchanged. In heavy infections larger bile ducts - when
their walls become thicker - are more prominent as spots
or strands, and the fibrosis of the parenchyma leads to an
enhanced demarcation of the lobules (► Figure 9.24). In
liver sections the thickened bile ducts are conspicuous,
from which lancet flukes can be squeezed out with
the bile. Due to the uterine loops filled with dark­
coloured eggs, the parasites appear as black-brownish,
often clumped objects that can be easily overlooked in
weak infections. Infection intensities often vary from
a few specimens to >20,000 per animal (► Figure
9.26). In southern Germany and Switzerland heavy
natural Dicrocoe/iwn infections were observed in South
American camelids (llamas and alpacas) associated with
Q)
·o
C
'o
Q)
�
ro
C
·;::
Q)
j
C
>,
0)
0
0
Figure 9.26. Dicrocoelium dendriticum: worm burden (20,500 "cij
specimens) from an older sheep (Photo: IPZ, K. Wolff). ro
ro
0...
 Part Ill. Parasites and parasitoses: metazoa
unusually violent reactions of the liver with granulomas
and abscesses in the liver parenchyma.
Clinical signs and adverse effects. In cattle and
small ruminants even moderate to severe infections
with Dicrocoelium remain usually unapparent. In some
cases in sheep anaemia and elevated serum levels of
liver enzymes as well decreasing performance (weight,
milk production) were described. Losses caused by
Dicrocoelium are primarily due to the confiscation of
infected livers at meat inspection.
Immunology. In sheep, the numbers of lancet flukes
per animal gradually increase during one or several
grazing seasons. This indicates that adequate immunity
does not develop. However, the infection induces
humoral and local cell-mediated immune responses.
An age-dependet decline in Dicrocoelium burdens was
observed in Canadian elks (wapitis), but not in co­
grazing beef cattle.
Diagnosis. Intravital diagnosis by egg detection in
faeces (e.g. flotation technique using a special flotation
liquid with specific gravity> 1.3). In general, coproscopic
! techniques have a very low sensitivity (for example,
I
! .
sedimentation technique about 40%) ( ► p. 526). The
detection of specific antibodies in the serum of sheep
and cattle in the ELISA had a sensitivity of 88% and a
specificity of 84%. Post mortem, the lancet flukes in the
bile ducts and gall bladder are detectable macroscopically,
and the eggs in the bile sediment microscopically.
Therapy and control. Treatment of dicrocoeliosis
is possible with some (pro)benzimidazoles, but
higher doses than those for controlling nematodes are
needed, e.g. in sheep albendazole (2x 15 mg/kg b.w.
p.o. at intervals of 15-20 days) or fenbendazole (Sx
20 mg/kg b.w. p.o. on consecutive days), and in cattle
netobimin (20 mg/kg b.w. p.o.) ( ► Table I 9.4 and 19.6).
Praziquantel (SO mg/kg b.w., p.o.) is highly effective and
safe, both in sheep and New World camelids.
Because of the low clinical significance of dicrocoeliosls,
measures that are aimed only at this parasitosls are
in general not justified. However, dicrocoeliosis can
be integrated into control measures against other
<l)
parasitoses. Control measures against intermediate hosts
·u
C
'6 cannot be considered for ecological reasons.
<l)
Zoonotic importance. Rarely do humans become
co infected with D. dendriticum by accidental ingestion
C
·c of infected ants. The infection can cause symptoms
<l)
of cholangitis. More common is the intestinal passage
-� of Dicrocoelium eggs by eating liver or liver products
>,
0)
of infected animals. For the diagnostic clarification
0 of such cases the consumption of such food has to be
0
'iii stopped for a few days, followed by repeated coproscopic
co examinations. There are some reports of infection of
co
0... humans with D. hospes from Africa.
Further species of the order Plagiorchiida
In► Table 9.7 some other species of the family Dicro­
coeliidae are listed. In sheep and cattle Eurytrema
pancreaticum and Eurytrema coelomaticum can cause
pancreatitis, pancreatic fibrosis with clinical symptoms.
► Table 9.8 provides information on representatives of
other families of the order.
Selected references c::a::tm=:ma-===-•
Beck MA, Goater CP, Colwell DD, van Paridon BJ (2014)
Fluke abundance versus host age for an invasive trematode
(Dicrocoelium dendriticum) of sympatric elk and beef cattle
in southeastern Alberta. Canada. Int J Parasitol Parasites
Wild! 3: 263-268.
Broglla A, Heidrich J, Lanfranchl P, Nockler K, Schuster
R (2009) Experimental ELISA for diagnosis of ovine
dlcrocoellosls and application in a field survey. Parasitol
Res 104: 949-953.
Colwell DD, Goater CP (2010) Dicrocoe/ium dendriticum
In cattle from Cypress Hills, Canada: humeral response
and preliminary evaluation of an ELISA. Vet Parasitol 174:
162-165.
Dadak AM, Wieser C, Joachim A, Franz S (2013) Efficacy and
safety of oral praziquantel against Dicrocoefium dendriticum
in llamas. Vet Parasitol 197: 122-125.
Hertzberg H, Kohler L (2006) Prevalence and significance of
gastrointestinal helmlnths and protozoa in South American
camelids in Switzerland [in German]. Berl Munch Tierarztl
Wochenschr 119: 291-294.
Mange-Gonzalez MY, Gonzalez-Lanza C, Cabanas E,
Campo R (2001) Contributions to and review of dicroceollosis,
with special reference to intermediate hosts of Dicrocoefium
dendriticum. Parasitology 123: 91-114.
Otranto D, Traversa D (2002) A review of dicrocoellosis of
ruminants including recent advances in the diagnosis and
treatment. Vet Parasitol 107: 317-335.
Otranto D, Rehbein S, Weigl S, Cantacessl C, Parisi A,
Lia RP, Olson PD. (2007) Morphological and molecular
differentiation between Dlcrocoeffum dendrlticum (Rudolph!,
1819) and Olcrocoeffum chlnensls (Sudarikov and Ryjlkov,
1951) Tang and Tang, 1978 (Platyhelminthes: Dlgenea). Acta
Trop 104: 91-98.
Procop GW (2009) North American paragonlmlasis (caused by
Paragon/mus ke//icott1) in context of global paragonlmiasis.
Clin Microbial Rev 22: 415-446.
Schuster R (1993) Infection patterns in the first intermediate
host of Dicrocoelium dendriticum. Vet Parasitol 47: 235-243.
Wolff K, Hauser B, Wild P ( 1984) Dicrocoeliose des Schafes:
Untersuchungen zur Pathogenese und zur Regeneration
der Leber nach T herapie. Berl Munch Tierarztl Wochenschr
97: 378-387.
 9. Phylum Platyhelminthes (flatworms)

Tab le 9.8. Further species (selection) of the order Plagiorchiida. 1

Family, species, size, distribution (D) Intermediate hosts (IH), definitive , Significance
hosts (DH) and (predllectlon sites In
definitive hosts)
� "

Prosthogonlmidee ---- -
Prostllogonimus cuneatus 2 1 st IH: water snails (Bithynia) causative agent of prostho-
(oviduct fluke) 2 nd IH: dragonflies (Ubel/ula, etc.) gonimosis: inflammation of oviduct,
10-12x5-7 mm DH: chicken, turkey, duck. goose. wild disorders of egg production; in
D: Europe, Asia, Africa, America birds (oviduct, rectum. Bursa Fabricii) Central Europe very rare In domestic
poultry
Troglotrematldee --
Troglotrema acutum 2 1 81 IH: water snails (Byt/Jinella) inflammation and bone lesions,
(nasal fluke) 2 nd IH: frogs especially on frontal bones
3.3x2.2 mm DH: mustellds (polecat, weasel, mink,
D: Europe badger), lox (cranla���Ues)
Nanopllyetus salmincola 1 11 IH: Jugs spp. N. selmlncole is the vector of the
(salmon poisoning fluke) 2 nd IH: fish (salmonlds, etc.) agent (Neorlckettsle helmlnthoeca) of
0.8-2.5x0.3-0.5 mm DH: carnivores: raccoon, skunk, fox, mink, the 'salmon poisoning disease'
D: north-western USA, north-eastern dog, cat, man (small Intestine)
Russia
Paragonimidae
Paragonimus kellicotti 1 st IH: snails (Pomatiopsis) agent of paragonlmosls of dogs
(lung fluke) 2 nd IH: Crustacea (Cambarus, etc.) and cats: dyspnoea chronic cough,
8-16x5-7 mm DH: mink, fox, raccoon, dog, cat, pig, haemoptysis, etc.
D: North America, southern Asia, South man, etc. (lung)
Africa, Israel
1 Data without claim lo completeness.
2 Species occurring in Central Europe.

Family Opisthorchiidae
9.1.4 Order Opisthorchiida
Various species of this family(► Table 9.9) are regionally
Opisthen(G): at the rear, caudal; orchis(G): testis. Refers significant causes of liver disease, particularly in
to the position of the testes in the posterior body region. carnivores and humans. In Central Europe, Opisthorchis
felineus, the cat liver fluke, deserves particular attention.
Summary The representatives of this family are small to medium­
sized, trematodes with a smooth or finely spined
• Agents, distribution. Oplsthorchllda are small to
integument, similar to the lancet fluke, but with testes
medium-sized trematodes, an essential feature of which
Is the position of the testes In the posterior body region.
located in the posterior part of the body(► Figure 9.27).
Of the family Opisthorchlldae the following species are
Furthermore, similarities exist with the Dicrocoeliidae
known to occur in Central Europe: 0plsthorch/s fellneus regarding the life cycle, but in the Opisthorchiidae
(cat liver fluke), Metorchls bills and Pseudamph/stomum freshwater snails and fish are l st and 2nd intermediate
truncatum as parasites of the bile ducts and gall bladder hosts, respectively.
in cats and other carnivores. The family Heterophyldae Is
represented inter alia by Intestinal parasites Apopha//us Genus Opisthorchis
donicus and Metagonlmus yokogawal (In foxes, etc.).
Life cycle. Indirect cycle with water snails as first and Opisthorchis felineus (cat liver fluke).
usually with fish as second intermediate hosts.
Diagnosis, therapy. Detection 0f eggs by coproscopy,
more recently also by PCR. Praziquantel is effective
against 0. felineus.
Elisease: Opisthorchiosis. fl
Zoonotic importance. 0. felineus and related species
(0. viverrini, Clonorchis sinensis) are important causative
ager:its-0f wo oses es ecially in Asia. Opisthen(G): at the rear, caudal; orchis (G): testis,feles
(L): cat.

Agent. Lancet-shaped flukes, 8-13 mm long, with

features of the genus. Lobed testes located in the
posterior third of the body (► Figure 9.27). Eggs: oval,
26-30x11-15 µm, with slightly protruding edges at the
 Part Ill. Parasites and parasitoses: metazoa

Table 9.9. Species (selection) of the family Opisthorchiidae. 1

- - - ·- . --
::�1.��D(kfC�. .!f:.t"�\JO'�
-��....?;;,(lb:�-,..,. (0)
. -
1m·�XJl1-ZZ6Wuu1muJi
,ICw:1lu'Cf l,J!fl�(U,:(l;
ft,

"
" .. .. ' .•l
�� . .l'�I
Opisthorchis felineus 2 1 st IH: snails cat, dog, fox, pig, man bile ducts, gall
(cat liver fluke) 2nd IH: fish bladder
8-13x1 .2-3.0 mm
D: Europe, Asia
Opisthorchis viverrini 1 st IH: snails cat, dog, man, etc . bile ducts, gall
6.0x2.0mm 2nd IH: fish bladder
D: South East Asia
Clonorchis sinensis 1 st lH: snails cat, dog, pig, man bile ducts, gall
(Chinese liver fluke) 2nd IH: fish bladder
10-28x25 - mm
D: East Asia: China, Korea, etc.
Metorchis bilis2 1 st IH: snails dog, cat. fox, raccoon dog, bile ducts, gall
2.34- 3. x1.0-1.4 2nd IH: fish mustellds, seals, birds bladder
D: Europe, North America
Pseudamphistomum truncatum2 1 at IH: snails dog, cat, fox, common seal, man bile ducts, gall
2x0.5mm 2nd IH: fish bladder
D: Euro�. GIS, India
1 Data without claim to completeness,
2 Species occurring in Central Europe,

latter emerge from the snails, and adopt a characteristic

position when floating in the water(► Figure 9.28):
the curved body is directed downwards and the tail
upwards('tobacco pipe posture'). Cercariae present in
the bottom zone of the water are triggered by vibrations
and differences in brightness, such as caused by a fish,
to rapid upward movements. When the cercaria comes
in contact with a fish, it penetrates the skin, leaving the
tail behind, encysts in the subcutaneous tissue or in
the muscles and develops into a metacercaria(about
290x200 µm). Metacercariae can also simply adhere to
the skin. After uptake of metacercariae with raw fish
by a definitive host, the parasites hatch in the intestine
and migrate through the Ductus choledochus into the
bile ducts and gallbladder, where they become sexually
mature. The prepatent period is 3-4 weeks. Occasionally
the parasites inhabit the pancreatic ducts.
Figure 9.27. Opisthorchis fe/ineus (Graphics: IPZ, A. Seeger;
after Kotlan 1960). Distribution, occurrence and epidemiology. The
main distribution areas of 0. felineus are rivers and lakes
in regions of eastern Europe and Asia(Belarus, Ukraine,
interface of the operculum, containing a miracidium Russia, Kazakhstan). The parasite is also focally present
when passed in the faeces. in the Baltic States and in northern areas of Poland,
Q)
C Germany and Italy.
'<3 Life cycle. Definitive hosts for 0. felineus are fish­
'6
Q)
consuming mammals(e.g. cat, dog, fox, raccoon dog, ln an endemic focus in Brandenburg(DE), 16% of 155
otter, mink, polecat, pigs, seals) and man. The eggs cats were infected with 0. felineus(data from I 999).
co
C passed by the definitive hosts in the faeces already Foxes were infected in several northern states of
·;::
contain a miracidium. For further development the Germany(Brandenburg, Berlin, Schleswig-Holstein)
eggs need to reach still or slow-flowing freshwater (prevalence in Berlin: I 8% of 396 foxes). Further hosts
C bodies, where appropriate intermediate hosts live. After in Central Europe are the raccoon dog, mink, polecat,
>,
0)
sedimentation to the bottom the eggs can be ingested otter, muskrat and probably the brown rat. The limiting
0 there by water snails (Bithynia leachi, regionaJly other factor for the distribution of 0. felineus is the occurrence
0
·u; species). In the snails development from miracidia to of Bythina leachi, which is one of Germany's rather rare
sporocysts, to rediae and cercariae takes place. The species of freshwater snails. As second intermediate hosts
co
(L
 9. Phylum Platyhelminthes (flatworms)

co
:g
:.c0
..c
U)
·a.
0

Figure 9.28. Opisthorchls fellneus: cercarla In typical floating Figure 9.29. Metorchls bills (Graphics: IPZ, A. Seeger; after
position in the water (Graphics: iPZ, A. Seeger; after Skrjabin Skrjabln 1950).
1950.)

several species of freshwater fish have been identified
in Brandenburg and B erlin, including ide (Leuciscus
idus), silver bream (Blicca bjoerkna) and bleak (Alburnus
a/burnus).
Pathogenesis and clinical signs. 0pisthorchis
infection initially causes desquamation of bile duct
epithelia as well as cellular infiltration into the bile
duct wall and the periportal tissue. Later changes
are hyperplasia of bile duct epithelia, adenoma- and
papilloma-like proliferation of the mucosa, cyst-like
extensions (cholangiectases), fibrous thickening of
the bile ducts and proliferation of connective tissue
in the liver parenchyma. The proliferations of the bile
duct mucosa can turn into cholangio-carcinoma(cases
known in humans, dogs and cats). In addition to the
parasite, nitrosamines derived from food play a causal
role. Macroscopically, especially the knot- and cyst­
like expanded bile ducts are conspicuous at higher
infection intensities. Clinical signs include vomiting,
loss of appetite, jaundice, digestive disorders, oedema,
and ascites.
are frequent. According to WHO, about 10 million
people in Russia and Asia are infected with 0pisthorchis
species(0. felineus and 0. viverrini). The very similar
Chinese liver fluke ( Clonorchis sinensis) occurs in
parts of Asia(Russia, China, Korea, Vietnam, etc.); the
number of people infected with this species is estimated
at around35 million.
Further species of the family Opisthorchiidae
Metorchis bi/is(syn. Metorchis a/bidus) is a liver parasite
of mammals and birds(► Table 9.9; ► Figure 9.29).
In northern Germany, this species occurs regionally
frequently. In Brandenburg, it was detected in over 50%
of the red foxes, furthermore in 3% of 155 cats and
in 8% of 74 raccoon dogs (Nyctereutes procyonoides).
Pseudamphistomum truncaturn occurs in foxes and cats
in northern Germany(e.g. in Berlin in 2% of396 foxes).
Family Heterophyidae

Diagnosis. Diagnosis is performed by coproscopic egg Agents of intestinal infections.

detection(► p. 526), species diagnosis can be confirmed
Q)
by PCR; post mortem detection of the parasite in the
·u
C

bile ducts and the gallbladder. This family includes several species with indirect
life cycles (water snails - fish) parasitic in the small 2
Q)

Therapy and control. Treatment with praziquantel

(dogs: 2x 20 mg/kg b.w. p.o.). Prophylaxis by heating
intestine of carnivores and other vertebrates. Apophallus
donicus has been detected in 3% of foxes in Germany
cco
C
(>70 °C) or freezing the fish before eating or feeding to and Metagonimus yokogawai in 1.6% of foxes in Austria. ·;;::::
Q)
animals(-10 °C for 5 d or -28 °C for 3 h). Heterophyes heterophyes occurs in the Mediterranean j
region in dogs, cats and foxes, and rarely in humans. .s
Zoonotic importance. In Germany(Mecklenburg­ >-
0')
West Pomerania) sporadic cases of 0. felineus infections 0
have been described in humans. In the main endemic 'ci'i
areas, mentioned above, human 0pisthorchis infections
co
CL
Part Ill. Parasites and parasitoses: metazoa
Selected references
Beugnet F, Franc M, Tielemans, E (2015) Gastro-intestinal
helminthoses. In: Beugnet F, Halos L (eds.) Parasitoses &
vector borne diseases of cats. Lyon, France: Merial S.A.S.,
pp. 15-49; ISBN 978-2-9550805-0-4.
De Liberato C, Scaramozzino P, Brozzi A, Lorenzetti R, Di
Cave D, Martini E, Lucangeli C, Pozio E, Berrilli F, Bossu
T (2011) Investigation on Opisthorchis felineus occurrence
and life cycle in Italy. Vet Parasitol 177: 67-71.
Schuster R (2002) Leberegelbefall. In: Aspock H (ed.) Amoben,
Bandwurrner, Zecken. Parasiten und Parasitare Erkrankungen
des Menschen in Mitteleuropa. Denisia 6; Neue Folge Nr.
184, pp. 291-315; ISBN 3-854 74-088-3.
Petney TN, Andrews RH, Saijuntha W, Wenz-MOcke A,
Sithithaworn P (2013) The zoonotic, fish-borne liver flukes
Clonorchis sinensis, Opisthorchis felineus and Opisthorchis
viverrini. Int J Parasltol 43: 1031-1046.
Schuster RK, Heidrich J, Pauly A, N6ckler K (2007) Liver
flukes in dogs and treatment with praziquantel. Vet Parasitol
150: 362-365.
Traverso A, Repetto E, Magnani S, Meloni T, Natrella
M, Marchisio P, Giacomazzi C, Bernardi P, Gatti S,
Gomez Morales MA, Pozlo E (2012) A large outbreak of
Opisthorchis felineus in Italy suggests that opisthorchiasis
develops as a febrile eosinophilic syndrome with cholestasls
rather than a hepatitis-like syndrome. Eur J Clin Microblol
Infect Dis 31: 1089-1093.
9.1.5 Order Strigeatida
Trematodes of this order are characterised by cercariae
with a forked tail (furcocercariae). The family
Schistosomatidae is the most important one.
Summary
Famlty SchlatoeomatldH
• Agentl and life cycln. The species of this famlly are
about 0.5-3.5 em long and have usually a cylindrical,
thin body. They are dloeclous, but In certain phases of
their development the males and females live pairwise
In venout veaets (blood flukee). Freshwater snalls are
Intermediate hosts In which furcocercarlae develop,
that IW8ffl'I out Into the water, Invade the final hosts
through the lkln and reach their predilection sltee In the
blood V8IIIII after an extensive ayatemlc migration.
• Epidemiology and occurrence. In tropical and
eubtropical .,.., n,mlnants ere pa,tlculatty affected
by vll'loua Schl,toaoma apeclee Oncludlng S. bovls,
S. ,plndale, S. n.u/e) that cauee vlaceral or nasal
forms of IChlltolomolll. In Europe (Hungary, Turkey)
Orlentob/1""1zlll turlcestanla occurs in wild n,minants.
In the USA HeterobllltMzia amerlcana is a parasite
In the meaentaric veins of the dog and other animal
lf)ldel. In W8ffl'I countries, about 200 million people
ant Infected with Schistosoma species (especially
with S. haematobium, S. mansoni and S. JIIPOlllCUm).
Different host species (buffalo, pig, dog, etc.) play an
Important role as reservoir hosts of S. Japon,cum and
some related species.
y
�
• Pathogenesis, clinical signs. Lesions in the form of
multiple granulomas arise in various organs caused
by schistosome eggs, which penetrate through blood
vessel walls to reach the lumen of various organs
Qntestine, urinary bladder, etc.) and subsequently
the environment. Eggs remaining in the tissues act
as pathogenic agents. Cercariae of various animal­
pathogenic species of the Schistosomatidae can invade
the skin of humans without further development and
cause pathological changes (cercarial dermatitis,
swimmer's itch).
Families Strlgeldae and Diplostomldae
Different species of the family Strigeidae are intestinal
parasites, predominantly in waterfowl, but they generally
play a minor role. Of the Diplostomidae only A/aria alata
Is mentioned here.
Family Strigeidae
Strigeidae are usually small, about 1-3 mm long
trematodes with a body divided into two parts by an
annular groove. The cup-shaped anterior part bears
a small oral sucker, in some species associated with
a pseudosucker on each side, a ventral sucker and
a bilobular attachment organ (tribocytic organ).
The usually cylindrical posterior part contains the
reproductive organs and in a terminal depression
the genital cone. The adults are intestinal parasites of
birds and mammals. The eggs (with an operculum)
are unembryonated when excreted in the faeces. The
life cycle is triheteroxenous. Several species are of
veterinary interest, especially as parasites of aquatic
birds ( ► Table 9.1 O).
Family Diplostomidae
The body of species belonging to this family is also
divided into two parts, but the anterior part is more
leaf-shaped (compare Strigeidae). Only A/aria alata is
mentioned here: The adult parasites (2.5-6x0.5-2 mm)
inhabit the small intestine, especially of wild canids
(wolf, fox. raccoon dog. etc.). and rarely of the dog. in
Central Europe and Asia. Prevalences in European foxes
between <1% and >50%, and in DE in the rnccoon dog
up to 70%. First intermediate hosts are freshwater snails
(Planorbidac) in which cercariac develop. The latter
infect tadpoles or adult frogs ( econd intermediate hosts)
in which so-called me ocercariae are formed (stages
between cercaria and metacercaria). Upon ingestion
b)' definitive hosts the mesocercariae migrate via the
pt'ritoneal cavity and diaphragm to the lungs where they
transform to mt'tacercariae that move on via the trachea
into the intestine and develop to adults. Paratenic hosts
(amphibians, reptiles, mammals) may become infected
by ingestion of second intermediate hosts containing
mesocercariae that persist in their tissues. An infection
 9. Phylum Platyhelminthes (flatworms)

Tabl e 9.10. Species (selection) of the family Strigeidae. 1

Species, elze, distribution (D) lntennedlate hoata (IH) Definitive hom lltee of adults
(DH)

Apatemon gracilis 2 191 IH: fresh water snails Lymnaea palustris, Radix goose, duck, wild small intestine
(syn. Strigea gracilis) peregra. Planorbis planorbis, etc. waterfowl, rarely
Cl)
1.0-2.Sx0.4 mm 2 nd IH: fresh water fish pigeon "D
D: Europe, Africa, America, Asia
Cotylurus comutus 2 111 IH: fresh water snails Lymnaea stagnalis, duck, other water small intestine Ol
·;::
1.2-1.4x0.5 mm L. palustris, etc, fowl. galliformes, and rectum if)
0: Wortdwide 2 nd IH: fresh water snalls or leeches (Pisclco/8, etc.) pigeon
Parastrlgea robusta 2 1 •t IH: fresh water snails Planorbis p/anorbis, Anisus domestic and wild small intestine
2-2.Sx0.5 mm vortex, etc. duck, pigeon
D: Europe, Asia 2nd IH: tadpoles - frQQS
- - -- ·
-- -
1 Data without claim to completeness.
2 Species occurring in Central Europe.

of the definitive hosts is also possible by ingestion of
infected paratenic hosts. Occasionally wild boars( 1.8%
in Croatia) harbour in their muscles mesocercariae
of A. alata, formerly called Agamodistomum suis or
in the German literature 'Dunckerscher Muskelegel'.
Mesocercariae (0.4-0.7x0.2 mm), surrounded by a
thin cyst wall, are mainly found in the fatty parts of the
muscles and can be detected using a modified funnel
technique(► p. 530 and special literature). Special
sites are recommended for collecting samples, such as
muscles(with fat) of the masseter, diaphragm, tongue,
and larynx. A PCR is available for species identification.
A. alata is considered potentially pathogenic for humans.
Only a few cases of alariosis in humans are known from
the USA and Canada caused by A/aria americana or
unidentified mesocercariae.
Family Schistosomatidae (blood flukes)
Agents. Schistosomes are parasites in venous vessels of
reptiles(crocodiles), birds, mammals and humans. They
differ from other trematodes mainly by their usually
elongated, thread-like shape, the sexual dimorphism
and the pairwise association of males and females.
The relatively short and thick male forms a body fold,
the ventral groove(canalis gynaecophorus), which is
differently expressed in the subfamilies. It looks like a
longitudinal slit (schistoma: split body), and encloses
the thin, thread-like, slightly longer female(► Figure
9.30). The integument of many species forms wart-like
structures. The suckers located near the anterior end
are poorly developed or absent. The bifurcated intestine
joins to form a posterior blind end. Eggs: large, oval or
spindle-shaped, without operculum, some with terminal
or lateral spine, contain a fully developed miracidium
when released from the host. The cercariae have a
forked tail.

■
Life cycle. The sexually mature schistosomes live
Disease: Schistosormatidoses. in domestic animals mainly in the mesenteric veins,
some in the portal veins, or venous plexus of the nasal
mucosa. The females lay eggs containing an immature
Schizein(G): to divide, separate; soma(G): body. Refers miracidium, which matures during its persistence
to the body shape of the male(see below). A previous in the host within 6-10 days, and remains viable for
name of the genus was Bilharzia(honouring Theodor about three weeks. Eggs penetrate the vessel wall
Bilharz [1825-1862] a German physician and discoverer and the surrounding tissue, and some finally reach
of schistosomes in blood vessels of humans). Therefore, the lumen of the intestines or the urinary bladder
the human disease caused by these parasites is still today (in case of S. nasale and Trichobilharzia regenti the
Q)
denominated as bilharziosis. nasal cavity). The penetration process is assisted by C
immunologically induced inflammatory responses,
·o
'o
Q)
Schistosomatidae (short form: schistosomes) have a partly by proteinases, which are secreted through the �
special importance, as some species are widespread eggshell into the environment. In the excretions of the
in tropical regions and cause schistosomosis which definitive host (faeces, urine, nasal mucus) the eggs Cl)
C
·;::
currently affects about 200 million people. Schistosomes reach the environment. In freshwater, the miracidia are Q)
of veterinary significance are primarily parasites of stimulated mainly by a drop in temperature(<32 °C} and j
domestic ruminants in subtropical and tropical areas salinity(below 0.7%) for immediate hatching from the C
of Africa and Asia. Some species occur in mammals egg shell. Miracidia of T. regenti hatch already on the >,
0)
or waterfowl in temperate climate zones and can play a nasal mucosa of the definitive host(duck). 0
0
role as zoonotic agents(► Table 9.11). +-'
·u5
Cl)
co
0..
 Part Ill. Parasites and parasitoses: metazoa

Table 9.11. Species (selection) of the family Schistosomatidae of veterinary importance. 1

Subfamily, speeies, length ef females (F), lnternnediate heats llt)eflnltive heats, predileetien sites ef adults
distribution (D) (fresh water snails) (S), prepatency

Subfamily: Schistosomatinae
Schistosoma bovis 2 (F: 13-34 mm) Bulinus species (8. cattle, sheep, goats, pigs, horses, camels,
D: Mediterranean (Corsica, Sardinia, Sicily, tropicus, B. truncatus, antelopes, rodents, monkeys, (man)
Spain), Middle East, North, West and East etc.), Planorbarius sp. S: mesenteric and portal veins
Africa, south to Angola and Zambia prepatency: 41days
Schistosoma curassoni (F: 18-26 mm) Bulinus umbilicatus cattle, sheep
D: Africa (Mauritania, Senegal, Mali, Nigeria) S: mesenteric veins
prepatency: 40 days
Schistosoma mattheei (F: 17-25 mm) Bulinus africanus group cattle, sheep, goats, wild ruminants, zebra,
D: southern Africa rodents, monkeys, (man)
S: mesenteric and portal veins
prepatency: 42 days
Schistosoma japonicum (F: 15-30 mm) Oncomelania species buffalo, cattle, pig, dog, other domestic animals,
D: East Asia (China, Philippines, Sulawesi, wild animals (including rodents, carnivores,
Celebes) ruminants, macaques), man
S: mesenteric and portal veins
prepatency: 34 days
Schistosoma indicum (F: 5-26 mm) lndoplanorbis exustus cattle, buffalo, sheep, goat, equines, rodents
D: India, Pakistan S: mesenteric and portal veins
prepatency: 52 days
Schistosoma Spindale (F: 7-16 mm) lndoplanorbis exustus cattle, buffalo, cattle, sheep, goat, equines,
D: India, South East Asia rodents
S: mesenteric and intestinal veins
prepatency: 46 days
Schistosoma nasale (F: 7-12 mm) lndoplanorbis exustus, cattle, buffalo, sheep, goat
D: India, South East and East Asia Lymnaea (syn. Radix) S: veins of nasal mucosa
luteola, etc. prepatency: 77 days
Schistosoma turkestanicum (syn. Lymnaeid snails cattle, sheep, goat, water buffalo, horse, camel,
Orientobilharzia turkestanicum)2 (F: 7 mm) etc.; roe deer, red deer
D: East Asia, Russia, Middle East, Turkey, S: mesenteric and portal veins
Hungary prepatency: ?
Heterobilharzia americana (F: 9-18 mm) Lymnaea cubensis raccoon, lynx, opossum, rare dog, white-tailed
D:USA deerl, etc.
S: mesenteric veins
prepatency: 70 days
Subfamily: Bilharziellinae
Bilharziella po/on/ca 2 (F: 2 mm) Lymnaeidae, Plsnorbarlus goose, duck. other water birds
D: Europe, Asia, Africa, North America and Plsnorbls species S: mesenterlc and portal veins
---- p�patency: 84 da�
Trlchobl/harzia szldatl 2 (F: 3 mm)4 Lymnaea stagna/1s ducks and other water birds
D: Europe, Asia S: mesenterlc veins and Intestinal wall
prepatency: ?
Trichobilharzia frank/ 2 (F: 4.2-4.6 mm) Radix auricularia ducks
D: Europe S: liver and mesenteric veins
prepatency: 13 days
Q)
Trichobilharzia regent/ 2 (-7 mm) Radix peregra, R. ovata ducks
·o
C
D: Europe S: veins of nasal mucosa.
'5 prepatency: ?
Q)
1 Data without claim to completeness.
2 Species occurring In Central Europe.
ro 3 Accidental host of immature stages.
·cCQ) 4
Unclear if synonymous with T. ocellata; ? no data.

C In water the miracidia with their short life span of only to swarm out to the water not earlier than 3-6 weeks
>,
0) 10-24 h try to find a suitable intermediate host. Various after infection. The cercariae are approximately 300-
0 species of freshwater snails act as intermediate hosts 600 µm long and morphologically characterised by a
0
·u5 ( ► Table 9.11) in which numerous cercariae arise from forked tail. They float around freely or adhere to the
ro the invading miracidia by asexual multiplication in water surface. Upon contact with a definitive host they
ro
a.. mother and daughter sporocysts. T he cercariae begin penetrate the skin within a few minutes, but rarely
►
Man as definitive host
,, -
�d
Fme fu,coce,cous ceroarla
_, I �EV' -_'
/' ·
Oncomelania
.t snail
Redia
Figure 9.30. Life cycle of Schistosoma japonicum (Graphics: IPZ, S.Ehrat).
the mucosa of the upper digestive tract after uptake
of cercariae with drinking water. During the infection
process, which is accomplished by cercarial movements
and secreted enzymes, the cercaria loses its tail, strips
off the superficial glycocalyx, forms a new integument,
and thus becomes a schistosomulum.
The migration of schistosomes in the definitive host
of those species that inhabit the veins of abdominal
organs as adult stages, can be summarised as follows:
schistosomula migrate through the subcutaneous
tissue --+ searching venous capillaries or lymphatics
--+ migration through the venous circulation to the
right heart ventricle and the lung --+ haematogenous
migration to the intrahepatic branches of the portal
vein--+ there development into adult worms and pairing
of males and females shortly before reaching sexual
maturity --+ retrograde migration of the pairs to the
mesenteric veins or the venous plexus of the urinary
bladder. Prepatent periods, depending on the species,
last about 5-11 weeks (► Table 9.11 ). After infection
of a host, juvenile stages of 1: sergenti follow peripheral
nerves, enter the spinal cord and brain, stay there in
9. Phylum Platyhelminthes (flatworms)
Reservoir hosts:
cattle, buffalo,
pig. etc.
/
/1(------ ,,
Egg with
mlracldlum
\
Free miracldium
Sporocyst
extravascular spaces and then migrate to their sites in the
nasal mucosa. Schistosomes in their mammalian hosts
can survive for years (in humans: average 2-5 years, some
up to 40 years; S. curassoni in sheep at least 8 years).
Distribution, occurrence and epidemiology.
Information on the geographic distribution of
Schistosomatidae is presented in ► Table 9.11.
Schistosomes are found only in wetlands, where
freshwater snails serving as· intermediate hosts find
suitable living conditions. T hese snails live in standing
or slow-flowing waters (e.g. Bulinus or Planorbarius
species), some are amphibious and live on wetlands,
e.g. in rice fields ( Oncomelania species). Most important
are the schistosomes in subtropical and tropical areas.
In Europe, S. bovis occurs in domestic ruminants, wild
ruminants are hosts of Orientobilharzia turkestania
and waterfowl of different species of the subfamily
Bilharziellinae (► Table 9.11).
Pathogenesis. Upon infection with schistosomes
changes in the skin and various internal organs may
occur.
 Part Ill. Parasites and parasitoses: metazoa
• Skin lesions. A primary penetration of cercariae
into the skin often remains asymptomatic, but it can
lead to itching and usually mild skin changes (erythema,
urticaria, papules). With repeated exposure, symptoms
appear faster and are intensified. Schistoma species
which are not host-specific can also cause such changes
(see below).
• Changes of internal organs. In the course of
infection with host-specific Schistosoma species, the
eggs play a crucial role in the pathogenesis. Significant
proportions of eggs (up 50%) remain in the organs of
the definitive host. The eggs are distributed from the
location of the parasites through the bloodstream to
various organs where they get stuck in small blood
vessels. The miracidia produce antigens (proteins,
glycoproteins), which pass through the eggshell into the
tissue. Due to the stimulation ofT-lymphocytes and with
the participation of cytokines, foci of granulomatous
reactions arise, called egg granulomas. Here, around
one or more eggs in the centre, mainly macrophages,
neutrophils, eosinophils, and fibroblasts are aggregated
( ► Figure 9.31 ). These lesions may coalesce and form
the basis of larger granulomatous proliferations. The
eggs deposited in the tissues die off within about 3
weeks. They are degraded or calcified; the granulomas
are replaced by connective tissue.Thus, fibrous changes
occur at an increasing rate. This can lead to cirrhosis
of the liver with destruction of liver tissue and serious
malfunctioning. In the bowel or bladder wall the
parasites in the blood vessels cause small haemorrhages,
and later nodular granulomas are formed around eggs.
Fibrosis may also occur in the intestinal wall.
Clinical signs. Among the Schistosoma species
( ► Table 9.11) S. nasa/e has a special position due to its
location in the veins of the nasal mucosa. The formation
of pinhead-si1,ed, nodular granulomas in the mucosa
of the nose, with inflammation and fibrosis ultimately
•�".
t��!'
. for application in practice.
Re�
(I)
C or in nasal mucus (direct smear or sedimentation
"[j
'6
(I)
�
co
C
·;:::
-...�.��
J-�
>-
. Therapy and control. In cattle, goats and pigs
0>
0 .::' ...
� praziquantel (>20 mg/kg b.w. p.o.) is highly effective
"ui
Figure 9.31. Schistosoma granuloma in the liver tissue of a
mouse, caused by an egg located in the centre (Photo: IPZ) .
co
CL
leading to rhinitis with mucopurulent nasal discharge,
sneezing and in severe cases to dyspnoea.
Other species o f the genus Schistosoma and
Orientobilharzia cause changes in the bowel (initial
pinpoint bleedings, and later formation of egggranulomas,
inflammatory reactions and fibrosis) and in the liver (egg
granulomas, fibrosis, cirrhosis). Egg granulomas and
other lesions can also occur in the urinary bladder and
in genital organs (especially in S. bovis infections), in
the lungs, pancreas and other organs. Clinical signs are
anorexia, enteritis (partly haemorrhagic), emaciation,
anaemia, hypoalbuminaemia, eosinophilia, dehydration,
less commonly, haematuria (S. bovis). The clinical
presentation is influenced by the infection intensity,
the host species and the immune status.
In dogs infected with Heterobilharzia americana, bloody
diarrhoea anorexia, emaciation, and hypoalbuminaemia
were observed.
Depending on the worm burden and the immune
status of the hosts, infections with schistosomes is often
clinically unapparent, but associated with shedding
of Schistosoma eggs. Such 'silent' parasite carriers are
epidemiologically important.
Immunology. In endemic areas, humans and other
hosts (sheep, goat, etc.) acquire immunity by multiple
infections with schistosomes, which completely or
partially protects against super-infections with cercariae,
but does not eliminate the schistosomes already
established in the body (concomitant immunity). The
immune response is primarily directed against the few­
hours-old schistosomula invading the body. Older stages
escape the immune defence by immune evasion(► p.
36),
Extensive work on the development of vaccines against
schistosomosis in animals and humans have yielded
valuable new insights, however, without results ready
Diagnosis. Intravital diagnosis in animals by detection
of Schistosoma eggs in fresh faeces (sedimentation
technique with physiological saline, not with water!)
technique); also, biopsy samples of the rectal or nasal
mucosa can be examined for eggs, and egg granulomas.
In the serum of infected animals, such as goats with
S. bovis infection, specific antibodies and circulating
antigens are detectable. Post mortem the egg granulomas
are especially characteristic.
against different Schistosoma species (S. bovis, S. spindale,
S. japonicum, S. nasale). but a therapy is usually not

possible for economic reasons. According to case reports
praziquantel (details on dosage are not available) is also
effective against the heterobilharziosis of the dog. The
access of animals to water with infected intermediate
hosts should be prevented, if possible.
Zoonotic importance. Among the Schistosoma species
parasitising humans, S. japonicum and some related
species are of zoonotic importance because animals
(cattle, buffaloes, pigs, etc.) contribute significantly to
the excretion and dispersal of the eggs of this species. On
the other hand, in other human-pathogenic Schistosoma
species (S. haematobium, S. mansoni, etc.), domestic or
wild animals play only a minor or no role as reservoir
hosts. Human schistosomosis is widely distributed
in tropical regions while Europe was thought to be
free from this disease since the I 960s. However, an
authochthonous focus of S. haematobium with several
human cases was detected 2013 in Corsica.
The cercariae of animal-pathogenic species of the
Schistosomatidae can penetrate the human skin
and cause cercarial dermatitis. Primary infections
often remain unnoticed or are associated with mild
symptoms (temporary itching, formation of papules).
Shortly after repeated exposure itching, erythema and
the formation of papules or blisters may occur due to
skin sensitisation. Having invaded an aberrant host, the
cercariae perish in a short time; therefore symptoms
usually fade away within 10-20 days. After a primary
experimental infection of mammals (rodents, rabbits,
monkeys) cercariae of Trichobilharzia and Bilharziella
species occasionally migrate to the lungs or other organs
and survive there for 3-10 days. Trichobi/harzia regen ti
(► Table 9.11) exhibits a pronounced neurotropism in
the mouse. Skin lesions in humans can also be caused
by human-pathogenic species, e.g. S. haematobium,
S. mansoni and S. japonicum. In animals, cercarial
dermatitis is rarely observed.
Cercarial dermatitis of humans occurs worldwide,
also in Central Europe (e.g. AT, CH, CZ, DE, FR). In
Europe, species of Trichobilharzia, Bilharziella and
Gigantobilharzia are known as causative agents; the
intermediate hosts live in fresh water. The disease
occurs in the warm season after bathing or swimming
in ponds or lakes; therefore is also termed 'Swimmer's
itch' (a misleading common name is 'duck flea itch' ). In
some regions, infections are also possible in brackish
water, as the intermediate hosts of some genera (e.g.
Austrobilharzia, Ornithobilharzia) occur in this habitat.
9. Phylum Platyhelminthes (flatworms)
Selected references
Holtfreter MC, Mone H, MOiier-Stover I, Mouahld G, Richter
J (2014) Schistosoma haematobium infections acquired in
Corsica. France. August 2013. Euro Surveill 19 (22). pii:
20821.
Horak P, Kolafova L, Mike§ L (2014) Schistosomaloidea and
diplostomoidea. Adv Exp Med Biol 766: 331-364.
Horak P, Mike§ L, Llchtenbergova L, Skala V, Soldanova
M, Brant SV (2015) Avian schistosomes and outbreaks of
cercarial dermatitis. Clln Microblol Rev 28: 165-190.
Lewis FA, Tucker MS (2014) Schistosomiasis. Adv Exp Med
Blol 766: 47-75.
a,
MaJoroa Dan A, Erd,lyl K (2010) A natural focus of the blood
lluke Orlentobllharzla turkestanlca (Skrjabin, 913) (Trematoda:
Schistosomatldae) In red deer (CeNus elaphus) in Hungary.
Vet Parasltol 70: 218-223.
Mohl K, QroBBe K, Hamedy A, Desert T, Kabelltz P, LOcker
E (2009) Biology of A/aria spp. and human exposure risk to
A/aria mesocercariae - a review. Parasltol Res 105: 1-15.
Rlehn K, Lalkovskl N, Hamedy A, LOcker E (2014) First
detection of A/aria alata mesocercarlae in wild boars (Sus
scrota Linnaeus, 1758) from Bulgaria. J Helminthol 88:
247-249.
Rollinson D, Simpson AJG (eds.) (1987) T he biology of
Schistosomes. From genes to latrines. London, UK:
Academic Press, Harcourt Brace Jovanovich Publishers:
ISBN 0-12-593692·3.
9.2 Class Monogenea
Monos (G): single; generatio (L): generation. Refers to
the direct life cycle with a single generation (in contrast
to Digenea with alternating generations).
The class of Monogenea (syn. Pectobothrii) belongs to
the subphylum Cercomeromorpha together with the
Cestoda (tapeworms). Certain stages of both groups
are characterised by a more or less separated posterior
part of the body with 6-16 hooks (the cercomer) or a
modification of it (see procercoid ► Figure 9.34, p.
209), but they differ significantly in other characteristics.
Whereas the Monogenea are mainly fish parasites, the
host range of cestodes comprises all classes of vertebrates.
Q)
In marine and freshwater fish the Monogenea are
·o
C
parasites of the skin, the gills and organs having
contact with the environment (e.g. nose, mouth). The �
adult stages are usually small, about 0.2-8 mm long
with a characteristic body shape and a conspicuous cu
C
adhesive organ called an opisthaptor. This consists of ·;::
a large sucker with 1-3 pairs of centrally located hooks
(anchors) and 12-16 peripheral, smaller hooks or several C
small suckers. The life cycle is monoxenous: release >,
0)
of eggs into the water ___. the ciliated, free-swimming 0
0
larva with a cercomer (oncomiracidium) arising from ·u5
the egg attaches itself to the host___. development to the cu
adult stage. The viviparous Gyrodactylidae complete cu
0..
 Part Ill. Parasites and parasitoses: metazoa
their entire life cycle on the host. Among some others,
the genera Gyrodactylus, Dactylogyrus, Discocotyle and
Diplozoon are important as fish parasites. The life cycle
of Diplozoon paradoxum ( ~ 7 mm long), a parasite from
the gills of fish, is unique. Two juvenile, hermaphroditic
individuals combine to make a pair, and their bodies fuse
completely close to the site of the reproductive organs,
thus making cross-fertilisation possible after maturation.
Selected references -�=====::==:::1
Mehlhorn H (ed.) (2008) Encyclopedia of parasitology. 3rd ed.
Berlin, Germany: Springer; ISBN: 978-3-540-48994-8.
I I 'I,
I
Roberts RJ (ed.) (2012) Fish pathology. 4th ed. Chichester, UK:
I Wiley-Blackwell; ISBN 978-1-4443-3282-7.
I I
(:
'
9.3 Class Cestoda (tapeworms)
- Subclass Eucestoda
Kestos (G): tape, ribbon. Refers to the tape-like shape
of the body.
Summary
• Representatives of the subclass Eucestoda are parasites
of animals (fish, amphibians, reptiles, birds, mammals)
or humans and causative agents of significant zoonoses
such as taenlosls, cystlcercosls and echlnococcosls.
• Main characteristics: body dorsoventrally flattened,
tape-like, composed of a head (scolex), an unsegmented
proliferative section (neck region) and a chain of
segments (proglottlds) named stroblla. The scolex Is
equipped with attachment organs: a pair of longitudinal
grooves (bothr1a), tube- or leaf-like structures (bothridla)
or with four acetabula (suckers). In some groups
the scolex bears a retractable cylindrical organ, the
rostellum, which Is usually armed with hooks. The
integument is a syncytlum with superficial, mlcrovllll-llke
structures (mlcrotr1ches). The length of adult cestodes
varies between a few mllllmetres and approximately
25m.
• A dlgestlv, tract Is lacking, nutrients are exclusively
absorbed through the body 11urface, Calcareous
co,;puscles are embedded In the tissue,
• Reproductive organ• are hermaphroditic, rarely
dloeclous. Each segment (p!'OQlottld) contains ono,
sometimes two sets of male and female reproductive
organs.
• The life cycle Involves a definitive host and one
(Cyclophylllda) or two Intermediate hosts (Pseudo­
phylllda) In which larval stages develop.
• The adult stages of the Eucestoda Inhabit the Intestine
(predominantly the small Intestine), but some species
C live In the large Intestine or In bile ducts; the larval stages
>,
Ol Invade various organ systems in natural Intermediate
0 or accidental hosts.
'ciJ
co
co
0..
Characteristics and properties. ► Figure 9.32
and 9.33. Body dorsoventrally flattened, ribbon-shaped,
tapered at the anterior end. Typically subdivided into
scolex (head), an unsegmented proliferative section
(neck) and the strobila. The latter consists of a few up
to many {>4,000) proglottids that are separated from
each other by deep transverse constrictions, which
do not correspond to an internal segmentation (this
subdivision of the body is lacking or indistinct in some
cestode groups) ( ► Figure 9.32). The neck region gives
rise to a sequence of proglottids with male and female
reproductive organs which progressively mature as
the proglottids move distally. A body cavity is lacking,
the internal organs are embedded in a parenchymal
meshwork. The length of adult cestodes varies between
a few millimetres and 25 m.
• Scolex. The scolex has an elongated or spherical­
ellipsoid shape and is equipped with attachment organs,
consisting in the Pseudophyllida of long, narrow grooves
(bothria) or tube- or leaf-like structures (bothridia) and
in the Cyclophyllida of 4 suckers (acetabula); the latter
can be armed with small hooks. The scolex of some
cyclophyllidean groups has a cylindrical or globular
retractable organ, the rostellum, usually armed with one
to several rings of hooks. Number, shape and size of the
rostellar hooks are diagnostically significant ( ► Figure
9.32b, c).
• Integument. The integument of the adults is similar
to that of trematodes, but with numerous superficial
cytoplasmic protrusions (microtriches) (thrix [G]: hair)
( ► Figure 9.32d). The microtriches cause a significant
increase in the absorptive surface, like the microvilli of
the enterocytes in mammals.
• Digestive tract. A digestive tract is lacking,
substrates are exclusively absorbed via the integument.
The energy metabolism is mainly an anaerobic
catabolism with incomplete degradation of organic
substances and excretion of volatile fatty acids (such as
acetic acid, propionic acid, succinic acid, lactic acid).
• Calcareous corpuscles. Calcareous corpuscles
(CC) are oval structures of variable diameters (5-15 �,m),
formed in parenchymal cells, composed of an organic
matrix with concentrically deposited layers of inorganic
substances and surrounded by a membrane. Principal
inorganic components are Ca and Mg, predominantly as
carbonate or phosphate, together with traces of various
elements, such as Al, Cr, Fe, Mn and Cu. CC represent at
least I 0% of the dry matter of the body, and may differ
according to cestode species and their geographical
origin. Although known for a long time, the function
of the corpuscles is still a matter of speculation (e.g.
phosphate reservoir, buffer against endogenous or
exogenous acids).
., 9. Phylum Platyhelminthes (flatworms)

Echinococcus Dipylidium

Scolex hooks

Microtriches

Cf)
.s::::.

.E
Q)
I

Figure 9.32. Characteristics of tapeworms (Eucestodla): (a) diagram of a tapeworm, (b) scolex (head) of Echinococcus and
Dipylidium, (c) scolex hooks, (d) surface of the integument with mlcrotriches (TEM) of Strobilocercus fasciolaris, (e) rostellum
of Echinococcus sp. (SEM) (Graphics: a-c: IPZ, M. Mathys; d: IPZ; e: H. Mehlhorn).

• Reproductive organs. Reproductive organs are
hermaphroditic, rarely dioecious. Each proglottid
contains one, sometimes two complete sets of male
and female sexual organs( ► Figure 9.33a, b). In the
anterior part of the strobila, the sexual organs develop
gradually to full functionality, while further down the
reproductive parts become stunted, and the extended
uterus is gradually filled with eggs. Pseudophyllida
have an opening of the uterus, through which eggs are
released. In the Cyclophillida, which do not have such
an opening, proglottids containing mature eggs(= gravid
proglottids) detach from the strobila and are excreted.
Eggs are released when the proglottids are damaged
either within or outside the host or if they disintegrate
in the environment.
• Eggs. Eggs of the Pseudophyllida are similar to those
of digenetic trematodes and contain a fertilised egg cell
and vitelline cells( ► Figure 9.34 and 9.35). In contrast,
cyclophyllidean eggs contain an oncosphere, a spherical
larval stage equipped with 6 embryonic booklets ( =
hexacanth larva or first stage larva)( ► Figure 9.36).
Life cycle. The life cycle is typically diheteroxenous
(Cyclophyllida) with one intermediate host or
triheteroxenous(Pseudophyllida) with two intermediate
hosts, in which various larval stages develop(second or
third larva). The predominant site of adult tapeworms in
definitive hosts is the small intestine, but some species
inhabit the colon or the bile ducts. Metacestodes(second
larval stages) develop in extraintestinal locations of
intermediate hosts, such as body cavities and internal
organs.
 Part Ill. Parasites and parasitoses: metazoa

�-Uterus with eggs

Genital pore

Vagina

Vitellarium

a b

Figure 9.33. Characteristics of tapeworms (Eucestoda): (a) sexually mature proglottld of Tsenla sp., (b) gravid proglottid of
Tsenis sp. (Graphics: IPZ, A. Seeger; after Furmaga and Wysocki 1951).

• Reproduction. In many species with a high 9.3.1 Order Pseudophyllida

reproductive potential, multiplication occurs in the
definitive host through sexual multiplication (with egg Among the order Pseudophyllida, belonging to the so­
production) in proglottids, which are continuously called 'lower' Eucestoda, the genera Diphyllobothrium
formed over months to years. In some species, significant and Spirometra (family Diphyllobothriidae) are parasites
asexual multiplication of larval stages occurs in the of vertebrate animals and humans. Some genera of
intermediate host. the families Diphyllobothriidae (e.g. Ligula, Schisto­
cephalus) and Bothriocephalidae (e.g. Bothriocephalus,
Triaenophorus and Eubothrium) play a role as fish
Selected references parasites. Fish are parasitised by further genera of
other orders belonging to the 'lower' tapeworms, e.g.
Arma C, Pappas PW (eds.) (1983) Biology of the Eucestoda. Vol. Caryophyllaeus and Khawia (order Caryophyllida) that
I and II. London, UK: Academic Press; ISBN 0-12-062102-9. are not further considered here.
Chalar C, Salome M, Sel\orale-Pose M, Marin M, Williams
CT, Dauphin Y (2013) A high resolution analysis of the Family Diphyllobothriidae
structure and chemical composition of the calcareous
corpuscles from Mesocestoldes cortl. Micron 44: 185-192. Genus Diphyllobothrium
Khalil LF, Jones A, Bray RA (eds.) (1994) Keys to the Cestode
parasites of Vertebrates. Wallingford, UK: CAB International; Diphyllobothrium latum (fish tapeworm, broad
ISBN 0-85198-879-2. tapeworm) and further species
Loos-Frank B, Gottsteln B (2006) Helmlnthen. In: Hlepe
T, Lucius R, Gottsteln B (eds.) Allgemelne Parasilologle.
Stuttgart, Germany: Paray, pp. 110-140; ISBN 3-8304- Disease: Dlphyllobothrlosls.
4101-0.
Mehlhorn H (ed). (2008) Encyclopedia of parasitology. 3rd ed.
Q)
C Bertin, Germany: Springer; ISBN: 978-3-540-48994-8. Di- (G): double; phyllon (G): leaf; bothros (G): groove;
·o Odening K (1993) Stamm Plathelminthes. In: Gruner HE (ed.) latus (L): broad. Reference to leaf-like shaped scolex
'6
Q) Lehrbuch der Speziellen Zoologie. 5. Aufl. Band I: Wtrbellose with bothria and broad proglottids.
T iere. 2. Teil. Jena, Germany: G. Fischer, pp. 341-442; ISBN
cu 3-334-00339-6.
C
·;::
Summary
Schmidt GD ( 1986) CRC handbook of tapeworm identification.
• Agent. Dlphyllobothrium latum is several meters long,
Boca Raton, FL. USA: CRC Press; ISBN 0-8493-3280-X.
scolex with 2 slot-like grooves (bothria), proglottids
C Spakulova M, Orosova M, Mackiewicz JS (2011) Cytogenetics
usually wider than long with a rosette-like coiled
>, and chromosomes of tapeworms (Platyhelminthes, Cestoda).
CJ) uterus. Parasites in the small intestine of humans and
0 Adv Parasitol 74: 177-230.
0 in fish-eating mammals (including dog, fox, pig). Eggs
'iii similar to those of trematodes: golden-yellowish with
cu
(l.. • operculum. Numerous other species.
 9. Phylum Platyhelminthes (flatworms)

•
, Life cycle, occurrence and epidemiology. Devel-
opment in water: egg -+ ciliated larva with embryonic
hooklets (coracidium) -+ hatching of the coracidium
-+ development of a procercoid In small crustaceans
and of a -+ plerocercoid in fish -+ infection of definitive
hosts directly or via paratenic hosts (predatory fish).
Distribution in lake and river areas of the northern
hemisphere (North America, Asia, Europe, including
lakes in the Alpine region).
• Clinical signs, diagnosis, treatment, prophylaxis. In
animals, usually asymptomatic infection, diagnosis by
detection of eggs in faeces, therapy of dogs or cats
with praziquantel (► Table 19.14, p. 600). Prophylaxis:
cooking or deep-freezing of fish prior to human
consumption or feeding to carnivores or pigs.
Agent. The genus Diphyllobothrium comprises about
50 species, including 14 species reported in humans.
One of the most important species is Diphyllobothrium
latum (► Figure 9.34): Adult parasite 1-15 m long
(maximum 25 m), scolex with 2 slot-like bothria, strobila
�
composed of numerous(up to 4,000) proglottids. These :Q
are wider than long(width about 12-20 mm), but exhibit >,
.c
a square form in the posterior part of the tapeworm. a.
0
Characteristics are the rosette-like-coiled uterus located -0
:::i
in the centre of the proglottid, a medio-ventrally located Q)
Cl)
genital pore and closely behind it a uterine opening.
Eggs: 55-76x37-56 µm, oval, golden-yellowish with
operculum, similar to those of trematodes(► Figure
9.34). Humans and piscivorous terrestrial mammaJs
(e.g. bear, dog, fox, cat, and pig) are definitive hosts,
and fresh water fish(pike, perch, burbot, etc.) serve as
second intermediate hosts.

Fish as facultative
paratenic hosts
Adult parasite in definitive host

-
,I/
-----
,�
Proglottid
Egg

J
'
·.•

2nd Intermediate host 1 st intermediate host

Coracidium

/
Plerocercoid

Coracidium without
Procercoid ciliated embryophore

Figure 9.34. Life cycle of Diphollobothrium latum (Graphics: IPZ, S. Ehrat).

 Part Ill. Parasites and parasitoses: metazoa
Further species (selection): D. dendriticum: 2 nd
intermediate hosts [IH]: freshwater fish, definitive hosts
- [DH]: gulls, terns, also dog, cat, fox, man; northern
Europe, Asia, Alaska. D. nihonkaiense: 2nd IH: salmon
species - DH: man, brown bear; Pacific coasts of Asia
and North America. D. pacificum: 2nd IH: marine fish
- DH: seal species, man; American Pacific coast, Japan.
In the following chapter only D. latum is considered.
Life cycle. The development of D. latum takes place in
a 3-host (triheteroxenous) cycle with optional inclusion
of paratenic hosts ( ► Figure 9.34). Each adult tapeworm
in the small intestine of a definitive host can produce up
to 1 million eggs per day, which are released continuously
through the uterine opening and passed with the gut
contents to the environment. In water, a first larval
stage (coracidium) develops within a few days or weeks,
depending on the ambient temperature. This stage,
about 40-50 µm in diameter, is covered with a ciliated
epithelial layer and equipped with 6 embryonic hooklets.
It hatches from the egg and floats around in the water.
After ingestion of the coracidium by a small crustacean
(Copeoda, such as Cyclops, Ettdiaptomus), a second larva,
the procercoid, develops in the body cavity in 2-3 weeks.
The procercoid is about 500 µm long and characterised
by a cercomer with 6 hooks at its posterior end. If
infected crustaceans are ingested by plankton-eating
freshwater fish, the procercoids invade the peritoneal
cavity, muscles or organs of the fish and mature to 1-3
cm long third larvae, the plerocercoids, which already
show some morphological characteristics of the adult
tapeworm. If those fish containing mature plerocercoids
are eaten by predator fish, the plerocercoids can persist
in the new hosts, which may then function as paratenic
hosts. Definitive hosts become infected with D. latum by
ingestion of fish, containing mature plerocercoids. Quite
often, several tapeworms inhabit the same definitive
host (multiple infection). The prepatent period of D.
latum in dogs is 13-I 5 days, while the life span of the
tapeworm in man may exceed IO years.
Occurrence and epidemiology. D. latum is
distributed in lake and river areas of North America,
South America and Eurasia. The European endemic
areas include Sca.ndinavian countries (e.g. Sweden and
Finland ~20 or 20-50 human cases/year), the Baltic
Q)
states, Poland, as well as areas around sub-Alpine lakes in
·u
C
'6 Italy, France and Switzerland (330 human cases reported
Q)
between 2002 and 2007). In Lake Leman 8-12% of perch
�
(Perea fluviatilis) were infected with plerocercoids
(1j
C
of D. latum, and 7.8% in Lake Maggiore (data from
·c 1997). Sporadic human cases have been observed in
Q)
j several European countries, some of them presumably
-� due to the consumption of imported fish. In Europe,
>­ Diphy/lobothrium infections in animals (dog, fox, cat,
O'J
0 pig) are rare (e.g. regionally <0.1 % of dogs and 0.5% of
'in
foxes in DE, 0.4% in CH; 2% of lynxes in FI). D. latum
(1j
co
0...
also occurs in Russia, but in large areas D. nihonkaiense
is common. In recent years, several cases of human
infections with D. nihonkaiense or D. dendriticum have
been diagnosed (confirmed by molecular analyses)
in European countries (CH, FR or CH, FR, CZ, LI,
NL) and were attributed to the local consumption of
imported salmon. D. dendriticum, widely distributed
in arctic and subarctic regions, is a common parasite
of piscivorous birds and mammals. With regard to
prevention it is important to note that both freshwater
and marine species of fish can be involved as hosts of
various Diphyllobothrium species.
Pathogenesis and clinical signs. Diphyllobothrium
infections in humans and animals are frequently
asymptomatic and rarely associated with intestinal
discomfort. In about 2% of humans, heavy and prolonged
D. /atum infections may cause megaloblastic anaemia,
due to withdrawal of vitamin 812 by the tapeworm.
Diagnosis, treatment and prevention. The
intravital diagnosis is made by coproscopic detection
of eggs (sedimentation technique); sometimes parts
of the strobila are excreted. Since the morphological
identification of Diphyllobothrium species is difficult,
molecular techniques (e.g. PCR) are currently the
preferred diagnostic tools, having the advantage that
tissue from adult or larval stages and eggs can be used
as samples. Therapy in dogs and cats: praziquantel in an
increased dosage of lx 35-40 mg/kg b.w. p.o. Prevention:
wastewater treatment and cooking or freezing (at least
24 h at -18 °C) of fish before human consumption or
feeding to animals.
Zoonotic importance. Worldwide, the number of
humans infected with Diphyllobothrium spp. is estimated
at 20 million. D. /atum and D. nihonkaiense are the most
common species, whereas D. dendriticum is regarded as
a previously underdiagnosed causative agent. In some
European countries (e.g. Baltic region) the incidence
of endemic human diphyllobothriosis is apparently
declining. On the other hand sporadic cases are reported
from various European regions (including alpine areas
of CH, FR, IT). Changes in eating habits (for example,
'carpaccio', 'sushi' from raw fish, especially raw salmon)
are presumably related lo an increasing infection risk.
Salmon species are primarily regarded as sources of
infection, but trout, perch, pike and other species of
freshwater and marine fish also have to be considered.
Individual prophylaxis: heating (core temperature
>50 °C for at least 5 min.) or freezing offish (see above);
smoking or marinating is not sufficient.
►
9. Phylum Platyhelminthes (flatworms)

Genus Spirometra eri11aceie11ropaei) (cat, dog, other carnivores in Europe,

Asia, and Australia). The plcroccrcoids of Spirometra
species, called spargana (singular: sparganum), arc about
Diseases: Splrometrosis and sparganosis. 'II 1-40 cm long and a few millimetres wide, with superficial
pseudosegmcntation and a scolex with bothria. In this
ro
chapter S. eri11e1ceie11ropaei is predominantly considered.
�
Spira (L): winding, turn; metra (G): uterus. Refers to >­
.c:
uterine windings in the proglottid. Life cycle. S. cri11accie11rop11ei inhabits the small a.
0
intestine of the definitive hosts. The life cycle ( ► Figure -0
:J
Agent. The genera Spirometra (zipper tapeworm) and 9.35) is similar to that of Dipl1yllobotl1r/11m with small Q)
V,

Diplryllo/Jot/1rium arc closely related and morphologically
similar, but they differ genetically and biologically.
Plcroccrcoids of Diphyllobothri11m Inhabit fish, those of
Spirometra other vertebrates. Spirometra species arc IQ.
100 cm long, the scolcx has slot-like bothria, the uterus
in the proglottids is spirally wound in 2-7 coils, and the
eggs arc similar to those of Diphyllobotl1rhm1. Several
species are known, such as: Spirometra ma11s011oides (cat,
dog, wild felids and canids in North and South America)
and Spirometra erinaceieuropaei (syn. Diphyllobothrium
crustaccnns (copepods) as first intermedinte hosts a..
(procercoid) and amphibians, reptiles. birds and
mammals ns second Intermediate hosts (pleroccrcoid).
Definitive hosts acquire the infection by ingesting
intermediate hosts or paratenlc hosts containing
plerocercoicls. The prcpatent period Is 2-3 weeks. If
plerocercoids arc ingested by accidental hosts (for
example, rodents, pigs, monkeys, or humans), they
penetrate the Intestinal wall and invade serous cavities,
internal organs, the inter-muscular connective tissue

Infection with
procercolds In
1" intermediate hosts
Infection with plerocercoids
in 2nd lntennediate
hosts

2•ld intermediate
hosts with plerocercolds
I Egg

Coracidium

1" intennediate host

with procercoids

Figure 9.35. Life cycle of Spirometra sp. (Graphics: IPZ, S. Ehrat).

 Part Ill. Parasites and parasitoses: metazoa
or the subcutis. Such an infection is called sparganosis
which occasionally even occurs in definitive hosts (dogs,
cats, and other carnivores) (see below).
Occurrence and epidemiology. Spirometra species
are found worldwide in different prevalences. The water­
bound life cycle favours the infection of frogs, reptiles
(snakes, turtles), rodents and other animal species living
in moist habitats. In southern China, 30% of 124 snakes
contained spargana of various species, and in Florida
(USA) 5% of wild boars (n=4,476) were infected with
spargana of S. mansonoides. The infection of mammals
and humans occurs by ingestion of drinking water,
containing small crustaceans infected with procercoids,
or by eating unprocessed spargana-containing tissue
from intermediate or paratenic hosts. In the tissues of
dead hosts spargana survive at +5 °C for 14 days and at
least 1 day at room temperature.
Pathogenesis and clinical signs. Intestinal
infections of definitive hosts with Spirometra spp. rarely
cause disturbances with diarrhoea. T he spa.rganosis
is often asymptomatic in vertebrates, but it can cause
skin lesions, peritonitis, etc., depending on the organ
localisation of the spargana, for example in dogs. In
wild boars coiled spargana were found in foci of 1-3
cm in diameter, surrounded by cellular infiltrates
and connective tissue, predominantly in connective
tissue of muscles (abdomen, leg, shoulder) as well as
in subperitoneal locations. Spargana of S. mansonoides
excrete a multifunctional cysteine proteinase, which has
effects similar to growth hormones in mice leading to
increased body weight.
Diagnosis and therapy. Intestinal Spirometra
infections in definitive hosts are diagnosed by
coproscopic egg detection (sedimentation technique)
or by finding the tapeworms at necropsy. Treatment of
the intestinal infection with praziquantcl at an increased
dose (see above Dlphyllobothrium). In suspected
cases of sparganosis in dogs and cats, the choice
of diagnostic procedures depends on the presumed
organ localisation of the parasites (e.g. laparoscopy for
suspected abdominal sparganosis). Isolated parasites
can be identified as spargana using morphological
features, but species diagnosis requires DNA analyses.
Q)
Differential diagnosis has to consider other larval
·o
C
'6 cestodes, especially tetrathyridia of Mesocestoides. Dogs
Q)
� with abdominal sparganosis were successfully treated by
surgical intervention and subsequent chemotherapy with
cu several cycles of mebendazole for three months (daily
C
·c 20 mg/kg b.w. p.o. 3 weeks), followed by praziquantel
Q)
(daily 5 mg/kg b.w. p.o. 3 weeks).
C may be absent; genital pores in lateral position, except
>,
C1)
Zoonotic importance. In humans, spargana invade
0 various organs (subcutis, lung, peritoneal cavity, genital
0
·v; organs, brain, eyes, etc.) and can cause significant,
sometimes painful, inflammatory changes in the affected
cu
0..
organs. Cerebral sparganosis is of special significance.
Such infections are predominantly observed in East and
South East Asia and rarely in Europe (e.g. CZ, FR, IT).
- Selected references a:....;=======::i
Chai JV, Murrell KD, Lymbery AJ (2005) Fish-borne parasitic
zoonoses: status and issues. Int J Parasitol 35: 1233-1254.
De Marval F, Gottstein B, Weber M, Wicht B (2013) Imported
diphyllobothriasis in Switzerland: molecular methods
to define a clinical case of Diphyllobothrium infection as
Diphyllobothn'um dendriticum, August 2010. Euro Surveill
18: pii: 20355.
Denegrl GM, Reisin IL (1993) The complete biological cycle of
Diphyllobothn'um en'nsceieuropei (Cestoldea, Pseudophyllidea)
under experimental conditions. Helminthologla 30: 177-179.
Dupouy-Camet J, Peduzzi R (2004) Current situation of human
diphyllobothrlasis In Europe. Euro Survelll 9: 31-35.
Kuchta R, Scholz T, Bray RA (2008a) Revision of the order
Bothriocephalldea Kuchta, Scholz, Brabec & Bray, 2008
(Eucestoda) with amended generic diagnoses and keys to
families and genera. Syst Parasitol 71: 81-136.
Kuchta R, Scholz T, Brabec J, Bray RA (2008b) Suppression
of the tapeworm order Pseudoplyllidea (Platyhelminthes:
Eucestoda) and the proposal of two new orders,
Bothriocephalidea and Dlphyllobothildea. Int J Parasitol 38:
49-55.
Kuchta, R, Brabec J, Kubafkova P, Scholz T (2013) Tapeworm
Diphyllobothrium dendriticum (Cestoda)-neglected or
emerging human parasite? PLoS Negl Trop Dis 26: e2535.
Lloyd S (2011) Other adult and larval cestodes. In: Palmer SR,
Lord Soulsby, Torgerson PR, Brown DWG (eds.) Oxford
textbook of zoonoses. 2nd ed. Oxford, UK: Oxford University
Press, pp. 643-649; ISBN 978-0-19-857002-8.
Scholz T, Garcia H, Kuchta R, Wlcht B (2009) Update of the
human broad tapeworm (genus Diphyllobothn'um), including
clinical relevance. Clin Mlcroblol Rev 22: 146-160.
Wlcht B, Yanagida T, Scholz T, Ito A, Jimenez JA, Brabec
J (2010) Multiplex PCR for differential Identification of broad
tapeworms (Cestoda: Olphyllobot11rium) Infecting humans.
J Clln Mlcroblol 48: 311 I -3116.
9.3.2 Order Cyclophyllida
Kyklos (G): circle; phyl/011 (G): leaf. Refers to the scolex
with circularly arranged suckers.
This order includes most of the cestodes of veterinary
significance, including important agents of zoonoses
(1aenia and Echinococrns species). Characteristics of
the order: scolex with 4 suckers and a rostellurn, which
in the Mesocestoididae.
...
Family Mesocestoididae
Genus Mesocestoides
Diseases: Mesocestoidosls and latval
mesocestoldoSis (or tetrattiyridiosis).
Meso- (G): centre; kestos (G): belt; oideus (L): similar.
'Meso' refers to some characteristics of the family that
are 'between' the Pseudophyllida and Cyclophyllida.
Summary
• Agent. In the adult stage Masocesto/des species are
parasites of the small Intestine of carnivores, birds
and humans. In Europe there are at least 2 species:
Mesocestoldes lltteratus (most common species), and
Mesocestoides 1/neatus, both predominantly In red
foxes and raccoon dogs but less frequently In dogs
and cats.
• Life cycle. Probably 3-hosts cycle; first Intermediate
hosts have not yet been Identified (arthropods are
suspected); second lntennedlate hosts are numerous
species of vertebrates (amphibians, reptiles, birds,
mammals), In which Infective larvae (tetrathyrldla,
singular: tetrathyrldlum) develop In body cavities,
sub-pleural cysts, lung, liver and other organs. Such
Infections with tetrathyrldla also occur In dogs and
cats (LM: larval mesocestoldosls). Infection of definitive
hosts by Ingestion of Infected lntennedlate hosts.
• Diagnosis, therapy. Typical gravid proglottlds with
paruterlne organ. Therapy as In Taen/a Infections (► p.
238).
Agent. The taxonomy of the genus Mesocestoides is
complicated due to a high degree of morphological
variability. Over 12 species have been described,
Paruterine organ
containing eggs
a C
Figure 9.36. Mesocestoides sp.: (a) scolex; (b) gravid proglottid; (c) egg; (d) tetrathyridium of Mesocestoides vogae (syn. M.
cort,). (Graphics: IPZ, A. Seeger).
9. Phylum Platyhelminthes (flatworms)
but only a few of them can be reliably identified by
morphological features. In Europe, at least two species
are known to occur in carnivores: Mesocestoides
litteratus (most common species) and Mesocestoides
lineatus. These species are genetically distinct and can
be differentiated by discrete features of the reproductive C1l
:Q
organs. Length of both species is up to 15 cm, sometimes >-,
longer. Numerous proglottids, scolex with 4 suckers but .c:
a.
without rostellum; gravid proglottids barrel-shaped with 0
0
paruterine organ, ventromedian genital pore ( ► Figure
9.36a, b). (M. leptotlrylacus described in European
foxes is regarded as a variant of M. litteratus). Eggs (M.
1/neatus: 25-45x29-34 µm), thin-shelled, containing an
oncosphere. The infective larvae of Mesocestoides sp.
arc called tctrathyridia (singular: letrathyridium). They
arc characterised by an elongated or oval body about
2-70 mm long, filled with parenchyma; the scolex at the
anterior end is normally invaginated, it has 4 suckers
but no rostelJum.
M. lineatus and M. litteratus are parasites of the small
intestine of foxes, other wild carnivores as well as
domestic cats and dogs. Tetrathyridia of M. vogae
(syn. M. corti) and other, unidentified species are
known to cause peritoneal and other forms of larval
mesocestoidosis (LM) in dogs, cats and other mammals.
Several Mesocestoides species have been described in
birds of prey, for example, M. per/atus.
Life cycle. A 3-host life cycle is assumed for
en
Mesocestoides species. However, all attempts to identify ..c.
arthropods or other invertebrates (>40 species) as
first intermediate hosts have failed so far. Numerous
.E
Q)
vertebrate species (amphibians, reptiles, birds, I
mammals) are known as second intermediate hosts in
which tetrathyridia develop in body cavities, sub-serosal
cysts, lungs, liver, and other organs. If intermediate
hosts, containing mature tetrathyridia, are ingested
cC1l
C
·;::
<l)
C
>-
0)
d 0
0
·u5
C1l
0..
 Part Ill. Parasites and parasitoses: metazoa
by susceptible definitive hosts, adult stages develop in
their small intestine. Prepatent period 2-3 weeks. In the
definitive host, the parasites survive for many months.
After peroral infection, tetrathyridia of Mesocestoides
species (which are often not precisely identifiable) can
penetrate the intestinal wall of various animal species
(final or intermediate hosts) and invade body cavities
and internal organs. In intermediate hosts, tetrathyridia
of M. vogae (syn. M. corti) are capable of asexual
multiplication. T herefore, they can be maintained in
mice by intraperitoneal serial passages and used for
research purposes. In mice, tetrathyridia of M. vogae
are transmitted via the milk from the mother to the
offspring (lactogenic transmission). In experimentally
infected dogs, juvenile stages of M. vogae can multiply
asexually in the intestine.
Occurrence and epidemiology. Mesocestoides
species are widely distributed in the northern and
southern hemisphere, infecting wild and domestic
carnivores as definitive hosts, such as foxes, coyotes,
raccoon dogs, wolves, jackals, skunks, wild cats, and
domestic dogs or cats. For example, in Europe red
foxes are commonly infected with intestinal stages of
Mesocestoides sp. with variable prevalences up to 50-
78%. Domestic cats are less frequently infected (e.g.
DE, CH: 2-4%, IT : 1.2%, ES: 14%), and rarely dogs. In
southern Germany and Switzerland tetrathyridia of
Mesocestoides sp. were found in low prevalences ( < 1%)
in different rodent genera (Apodemus, Myodes [syn.
Cl.ethrionomys], Microtus). Tetrathyridia from rodents
(Apodemus, Myodes) in Poland were identified by nuclear
and mitochondrial DNA analyses mainly as M. litteratus
and less frequently as M. lineatus. Larval mesocestoidosis
of domestic carnivores is rare, but recent case reports
from various countries (e.g. IT, DE, Japan), suggest
that this infection may have been underdiagnosed in
previous periods.
Pathology and clinical signs. Massive infections of
definitive hosts with intestinal stages of Mesocestoides
sp. are usually asymptomatic, but lack of appetite,
diarrhoea and mucoid faeces have occasionally been
reported. In dogs and cats, the infection of the thoracic
and/or abdominal cavities and internal organs with
Q)
C tetrathyridia (LM: larval mesocestoidosis) may cause
·u anorexia, vomiting, peritonitis, ascites, abdominal
Q)
�
distension, respiratory symptoms, leukocytosis etc., as
well as tissu.e damage with granuloma formation and
co encapsulation of the parasites. If untreated, LM can
C
·c be a life-threatening disease. In a few recent cases, M.
(I)
lineatus and M. vogae have been identified as causative
-� agents by molecular techniques. Rarely, carnivores(dog,
>,
CJ>
cat) are simultaneously infected with both strobilated
0 stages in the intestine and tetrathyridia in body cavities.
'iii
co
ro
0..
Diagnosis and therapy. Infected definitive hosts
expel single proglottids or parts of the strobila,
consisting of several segments. A typical feature of the
barrel-shaped gravid Mesocestoides proglottid is the
paruterine organ, which is already visible in unstained
microscopic specimens(► Figure 9.36b). Thin-shelled
eggs, containing an oncosphere, are only rarely found
in faecal samples. Ultrasonographic examinations may
provide clues for LM. Tetrathyridia(sometimes atypical
and acephalic forms) can be obtained post mortem or
in vivo by aspiration of peritoneal fluid and used for
morphological examination and DNA analysis. Intestinal
Mesocestoides infections in cats and dogs are treated
with praziquantel (5 mg/kg b.w. p.o.) (► Table 19.14).
Praziquantel (5 mg/kg b.w. s.c. 2x with an interval of 2
weeks) seems to be more effective than fenbendazole(SO
mg/kg b.w./d, p.o., for at least 28 d) against peritoneal LM
in dogs. Proven prophylactic measures are not known.
Zoonotic importance. Intestinal Mesocestoides
infections of humans are very rare, caused by ingestion of
raw organs of intermediate hosts containing tetrathyridia
(e.g. snake liver in Asia).
Selected references
Boyce W, Shender L, Schultz L, Vickers W, Johnson C,
Ziccardi M, Beckett L, Padgett K, Crosbie P, Sykes
J (2011) Survival analysis of dogs diagnosed with canine
peritoneal larval cestodiasis (Mesocestoides spp.). Vet
Parasitol 180: 256-261.
Eleni C, Scaramozzino P, Busi M, lngrosso S, D' Amelio
S, De Liberato C (2007) Proliferative peritoneal and
pleural cestodiasis in a cat caused by metacestodes of
Mesocestoides sp. Anatomohistopathological findings and
genetic identification. Parasite 14: 71-76.
Hrtkova G, Miterpakova M, O'Connor A, Snabel V, Olson
PD (2011) Molecular and morphological circumscription of
Mesocestoldes tapeworms from red foxes (Vulpes vulpes)
In Central Europe. Parasitology 138: 638-647,
Paplnl R, Mattelnl A, Bandlnelll P, Pampurlnl F, Manclantl F
(2010) Effectiveness of prazlquantel for treatment of peritoneal
larval cestodlasls In dogs: a case report. Vet Parasltol 170:
158-161.
Vence L, Kramer L, Pagliaro L, Genchl C (2005) Ultrasono­
graphic features o f peritoneal cestoidlasls caused by
Mesocestoides sp. Vet Radiol Ultrasound 46: 417-422.
Wirtherle N, Wiemann A , Ottenjann M, Llnzmann H, Van
der Grinten E (2007) First case of canine peritoneal laNal
cestodosis caused by Mesocestoides lineatus in Germany.
Parasitol Int 56: 317-320.
Zalesny G, Hildebrand J (2012) Molecular identification of
Mesocestoides spp. from intermediate hosts (rodents) in
central Europe (Poland). Parasitol Res 110: 1055-1061.
I 9. Phylum Platyhelminthes (flatworms)

Family Anoplocephalidae An overview of different species occurring in Europe and

Anoplon (G): unarmed; kephale (G): head. Reference to
the 'unarmed' scolex.
Summary
; Agents and occurrence. Characteristics of Anoplo­
cephalldae: scolex with 4 suckers, but witfiout tosteilum
and hooks; usually numerous proglottld!l, wld� than
lo-ng: eggs pOlymorphlc, rather thick-shelled, containing
an oncosph8're, enclosed by an embryophore (pytlform
apparatus) charactel'lstlc within members of the
subfamily Anoplocepliallnae. Anoplocephalldae art
Intestinal parasites of herbivorous mammals, aome
species occur In humans, birds and reptiles (► Table
9.12). Worldwide, Monlezla and Anop/ocaphala species
are Important parasites of ruminants or horses,
respectively.
• Life cycle. Egg shedding In faeces of definitive hosts
➔ ingestion of eggs by moss mites (Orlbatlda) and
development of cystlcercolds In their body cavity -+
infection of definitive hosts by Ingestion of Infected
mites.
Cllnlcal signs: In lambs dlar�hoea and disorders of
weight gain; In horses diarrhoea, emaciation; colic.
Diagnosis, treatment, control. Detection of eggs
or proglottids In faeces; new option: copro-antlgen
detection in horses. Treatment of choice of sheep a11<:l
horses with prazlquantel. Control see below.
other regions is presented in ►Table 9.12. In addition,
reference is made here to some other species: Tf1ysaniezia
giardi (Europe, Asia, Africa, America), Avite/lina
centripunctata and Stilesia globipunctata (southern
Europe, Africa, Asia) in the small intestine of ruminants;
Stilesia lrepatica (tropical and southern Africa, Asia) in
bile ducts of domestic and wild ruminants; Thysanosoma
actinioides (North and South America) in bile ducts and
the small intestine of ruminants; Anoplocephala gigantea
(rhinoceros), A. manubriata (African and Indian
elephanl), A. gorillae (gorilla); Bertie/la studeri and B.
mucronata in the small intestine of Old World and New
World monkeys, rarely also In humans. Species of the
genera Avlte/lina, Stiles/a, Thysanlezla and Thysanosoma
(subfamily Thysanosomatinae) occurring in ruminants
differ from Moniezia (sec below): the mature proglottids
contain a single or several paruterine organs (fibrous egg
capsules) with eggs lacking a typical pyriform apparatus.
Genus Moniezia
Disease: Monezlosis in runnlnants.
Moniez, R.-L., French helminthologist (1852-1936).
Agent. Worldwide, Moniezia expansa and Moniezia
benedeni are the most important species (►Table 9.12).
Their main features are: length several meters; scolex
with 4 suckers, without rostellum; proglottids much

Table 9.12. Species (selection) of the family Anoplocephalldae.

-� ,,
Species and dlstilbutlon (D) Intermediate Definitive hosts Adults: Length (L), width (W),
hosts locallsatlon

Moniezia expansa oribatid mites sheep, goat, cattle, roe deer, L: up to 10 m; W: up to 2.5 cm
D: worldwide (moss mites) red deer, chamois, other Small intestine
ruminants
Moniezia benedeni oribatid mites cattle, buffalo, sheep, goat, roe L: up to 4 m; W: up to 1.6 cm
D: worldwide (moss mites) deer, other ruminants Small intestine
Anoplocephala pertoliata oribatid mites horse, donkey, other equids L: 2.5-4 (8) cm; W: up to 1.4 cm
D: worldwide (moss mites) lleocaecal junction, caecum,
terminal ileum
Anoplocephala magna oribatid mites horse, donkey, other equids L: up to 50 cm; W: up to 2.5 cm
D: worldwide --- (moss mites) Small intestine
Paranoplocephala mamillana oribatid mites horse, other equids L: 1_-4 cm; W: up to 0.6 cm
D: worldwide -- (moss mites) Small intestine
Cittotaenia ctenoides oribatid mites wild and domestic rabbit, hare L: 30-80 cm; W: up to 1.0 cm
(syn. Mosgovoyia ctenoides ) (moss mites) Small intestine
D: Europe, North America
Cittotaenia pectinata oribatid mites wild and domestic rabbit, hare, L: 5-18 cm; W: up to 1.5 cm
(syn. Mosgovoyia pectinata) (moss mites) marmot Small intestine
D: Europe, Asia, Africa, North- and
South America
Ki/Jigrewia delafondi probably oribatid pigeons, other columbiformes L: up to 23 cm; W: up to 0.5 cm
(syn. Aporina delafondi) mites Small intestine
D: Europe, Asia, Africa, North America (moss mites)
 Part Ill. Parasites and parasitoses: metazoa

wider than long; each proglottid with a double set of
reproductive organs and a genital pore on each lateral
margin; uterus reticulate, filled with numerous eggs
(► Figure 9.37 and 9.38). Eggs irregular polymorphic,
60-90 µm in size containing an oncosphere, surrounded
by a pear-shaped embryophore (pyriform apparatus).
Predominant hosts of M. expansa are sheep and goats,
whereas M. benedeni typically infects cattle.
Life cycle. The development is inextricably bound to
moss mites (Oribatida), of which numerous species can
act as intermediate hosts ( ► Figure 9.38), for example
species of the genera Galumna, Liebstadia, Scheloribates
and Trichoribates. After ingestion of Moniezia eggs by
the mites, infective cysticercoids develop in their body
cavity within 1-3 months, depending on the ambient
temperature. Definitive hosts acquire the infection by
uptake of infected moss mites. Prepatent period 30-52
days, patency often only 3 months, but can be prolonged
to 8 months.
Occurrence and epidemiology. M. expansa and
M. benedeni are widespread in the world. In Central
Europe and other regions, the prevalence of Moniezia
infections in lambs can reach >50%. Favourable habitats
for moss mites are soils with high humus content
and sufficient moisture. In mites, cysticercoids can
hibernate and survive up to 2 years. The percentage
of infected mites is usually low (2-3%). With warm
and humid conditions, the mites can be found in the
vegetation on the soil surface; in dry conditions and
sunshine they retreat a few centimetres into the ground.
Drought is detrimental to the mites, but can promote
their dissemination through dust and wind. Moniezia
eggs are quite resistant and can survive the European
winter in faeces on pasture. Although an infection risk
exists throughout the whole vegetation period in Central
Europe, lambs acquire the infection predominantly in
the first months of the grazing season (April to June) by
ingestion of infected overwintered moss mites. Multiple
infections with several tapeworms per animal are quite
frequent. Approximately 2-6 months after infection,
the majority of tapeworms are eliminated, but residual
worm burdens - partly as short tapeworms of about 5
cm in length - can overwinter in the host. The life cycle
of M. benedeni in cattle lasts a little longer; the highest
prevalences are observed in autumn.
Pathogenesis and clinical signs. At necropsy
of heavily infested lambs whitish-yellowish tapeworm
masses are often visible through the intestinal wall.
Slimy and fluid intestinal contents and occasionally
emaciation are the most obvious changes. Histological
examinations may reveal signs of catarrhal enteritis with
mild destruction of villus epithelia and light cellular
infiltration of the mucosa. It is still unclear whether
alterations found in Moniezia infections are due to the
tapeworm infection alone or whether co-infections
are involved (e.g. trichostrongyles). Heavy Moniezia
infections in lambs are associated with diarrhoea,
anaemia, insufficient weight gain, loss of weight and,
in rare cases, nervous disorders. In older sheep and
cattle the infection is usually asymptomatic.
Immunology. The partial elimination of M. expansa
burden by lambs 2-6 months p.i., and the fact that older
sheep - exposed to the same infection risk as lambs
- carry lower worm numbers and are less frequently
infected, can be regarded as an indirect sign of immune
responses, but little knowledge exists on this aspect.
Diagnosis, treatment and control. Diagnosis
in living animals: macroscopic observation of the
conspicuous yellowish-white chains of proglottids
expelled with the faeces or microscopic detection of
eggs (flotation technique) in faecal samples. The drug of
choice for treatment of sheep Is praziquantel (3.75 mg/kg

.'"',,.
b.w. p.o.). Moreover, various benzimidazole compounds
. - are effective in normal or increased dosages (►Table
19.3 ). In Central Europe. lambs should be treated late
. q I June to early July, In order to relieve the animals of heavy
tapeworm burdens in an early phase of the infection.
... If necessary, the treatment should be repeated once or
' more times in intervals of 4-6 weeks. In lambs which
Q)
�' are born later during the grazing period, a treatment

.
·o
C
.a 4 \.

.
at the beginning of their third month of life may be
'6 '-4 f'>
- ,. . '
�
Q)
I�
indicated. Treatment of cattle is normally not required.
. (r.,,,.• '., �;:;:
cco
�••

... . �- -
The Systamex• forte interval bolus ( ► Table l 9.3) is
.• effective against Moniezia in cattle.

--
C
·;;:: .. JJ. ., . ....
"..,.."._ �.
Q)

-�
·- - .._.... ...
.
.- ·r-
',,- ·•
'' ·�-' �
i��. �
._;-,.:�..,:

.,...,.
(
>,
0)
0 --·--' '.,IJ '
0
'ui Figure 9.37. Monezia sp., partial view of the tapeworm burden
co from the small intestine of a sheep (Photo: IPZ).
co
0..
 9. Phylum Platyhelminthes (flatworms)

ct!
;g
>­
.c
CL
0
u
>,
0

Mature proglottld

... l�1.iJ/i;/t(i;r.1g{:�;. Egg

Moss mite

Infected
moss mites
on plant

Q)
C

Cystlcercold ·13
'6
Q)
. �
Figure 9.38. Life cycle of Monlezla sp. (Graphies: IPZ, M. Mathys). c:­
co
C
·;::
Q)
j
,s;
>,
0)
0
0
+-'
"iii
.....
ct!
co
0..
 Part Ill. Parasites and parasitoses: metazoa
Genera Anoplocephala and
Paranoplocephala
Disease: Equine anoplocephalldosis.
Anoplos (G): unarmed; kephale (G): head. Refers to the
scolex without hooks.
Agents. Common features of the causative agents of
anoplocephalidosis in equines (►Table 9.12) are: scolex
without rostellum, proglottids much wider than long,
each with one set of reproductive organs and a genital
pore in unilateral position, uterus transverse and tubular.
The species can be distinguished morphologically.
Anoplocephala perfoliata: a few centimetres long, body
shape trapezoid-like, a small lappet behind each of
the four round suckers of the scolex (► Figure 9.39);
Anoplocephala magna: much longer, without lappets
behind the suckers; Paranoplocephaln mamillana: only
a few centimetres long, slit-like suckers. The organ
localisation of the tapeworms provides further hints
for diagnosing the species (►Table 9.12). Eggs are thick­
shelled and of irregular, rounded to quadrangular shape,
containing an oncosphere, surrounded by a pyriform
apparatus (see Moniezia).
Life cycle. Many species of moss mites (Oribatida),
including species of the genera Galumna, Liebstadia,
Scheloribates, etc. are obligatory intermediate hosts
in the life cycles of the above-mentioned equine
anoplocephalids. After ingestion of anoplocephalid
eggs by the mites, infective cysticercoids develop in
their body cavity within 2-4 months, depending on the
C these, 51% harboured up to 100 tapeworms and 14% over
>,
-
O>
0 of 912. Egg shedding in faeces does not correlate with
0
'ii, Figure 9.39. Anoplocephala perloliata: adult stages (natural
cu length approximately 2.5-4 cm); arrow: lappets on the scolex
cu
0... (Photo: IPH).
ambient temperature. The infection of horses occurs
through uptake of infected mites on pasture. Prepatent
period 6-10 weeks, sometimes longer. The lifetime of A.
perfoliata in horses is estimated at 6 months.
Occurrence and epidemiology. The species listed
in ►Table 9.12 with a worldwide distribution are also
found ubiquitously in Europe. The most common species
is A. perfoliata with regionally varying prevalences up to
70%, followed by the much rarer species A. magna and
P. mamillana, which usually occur in mixed infections
with the first-mentioned species. Horses or mules,
which have acquired the infection during the previous
grazing period, may remain parasite carriers up to 6
months and contaminate the pasture with proglottids
and eggs in the following spring. As excretors of parasite
eggs, both young and older horses have to be taken
into consideration. Important sources of infection are
permanent pastures, which have been used for several
years by horses, offering favourable living conditions for
moss mites. Moss mites of many genera and species are
widespread in various regions. Sche/oribates laevigatus,
especially important in the epidemiology of A. perfoliata
in Central Europe, prefers grassland of variable moisture
and occurs - according to studies in southern Germany
- during the whole grazing season in significant
population densities with maxima in the summer and
autumn months. Considerable differences regarding
moss mite species and their population densities
may exist between various grazing areas and regions,
depending on local habitat conditions. It is assumed that
the survival times of A. perfoliata eggs on pasture and
cysticercoids in mites are similar to Monezia (see above).
Little knowledge exists in Europe on the seasonal
dynamics of the infection. An increase in the prevalence
of A. perfoliata in the second and third quarter of the
year is indicative for an exposure rising from spring to
the summer and autumn months. In autumn, an increase
in serum antibodies against A. perfolia1<1 antigens was
observed in foals, about 2 months before egg excretion
in faeces was detectable. Furthermore, the highest egg
excretion occurred in the second half of the grazing
period. Necropsies revealed that juvenile stages of
A. perfolinta are present throughout the year in the
intestinal tract of horses. This fact can be explained by
repeated infections, resulting in several generations of
tapeworms with extended prepatent periods in parts of
the population (immune reactions see below).
Infection intensities with A. perfoliata are subject to
major fluctuations. In Sweden, 65% of 470 slaughter
horses were infected with A. perfo/iata in 1992/1993. Of
100 specimens per animal with an individual maximum
the intensity of the infection and is generally highly
variable (see below, diagnosis).

Immunology. According to Swedish studies(necropsy
findings of 470 horses), foals in their I st year of life were
less frequently (37%) infected with A. perfoliata than
2-30 years old horses(60-68%). This fact indicates that
protective immunity does not develop in the course of
repeated infections. In horses infected with A. perfoliata,
specific serum antibodies are detectable, which are
directed against different antigens of the parasite. In
the majority of animals, the concentrations of antibodies
against 12 and 13 kDa antigens show a significant
correlation with infection intensity and are particularly
indicative for early stages of the infection. A. perfoliata
induces marked inflammatory and specific immune
res ponses within the caecal mucosa, involving local
production oflgG andlgE antibody isotypes. However,
their potential role in parasite elimination or immune
protection is unclear.
Pathogenesis. A. perfoliata inhabits mainly the
ileocaecal junction, the proximal caecum, far less
frequently the terminal ileum and the ventral colon
(► Figure 9.40). Here, the parasites attach firmly
to the mucosa and are often found in dense groups,
predominantly around the ileocaecal junction. At
their attachment sites, they cause hyp eraemia, focal
ulceration, diphtheroid deposits, glandular atrophy,
Figure 9.40. Cestodes in the intestine of horses: (a) mass
infection with Anoplocephala perfoliata, (b) Paranoplocephala
mamillana (Photos: K. Tomczuk).
9. Phylum Platyhelminthes (flatworms)
fusion of villi, cellular infiltrations of the mucosa and
submucosa (including lymphocytes, plasma cells, and
eosinophils), submucosal oedema and occasionally
hyperthropy of the muscle layer. In heavy infections,
the changes may extend to further parts of the intestine.
After detachment of the parasites, the ulcers heal by
scar formation. :g
>..
.c
a.
Heavy colonisation around the ostium ileocaecale
u>-
0
can lead to obstructive stenosis. Secondary bacterial
0
infections with necrosis or abscess formation are
regarded as the cause of perforation of the bowel wall
with subsequent peritonitis. Furthermore, ilea! wall
thickening or obstruction and intussusception of
different sections of the intestine are associated with A.
perfoliata infection. In the ganglia of intestinal muscles,
degenerative and inflammatory changes were detected,
which could play a role in the pathogenesis of colic.
Even at low infection intensities with 1-20 tapeworms
per animal, pathological changes are detectable in the
intestine. There is a statistically significant correlation
between such changes and the infection intensity.
In Sweden, 21% of 470 horses (age 1-30 years) had
moderate and l l % severe changes with average worm
burdens of 67 and 240 per animal, respectively.
Mass infection with A. magna may cause catarrhal
and haemorrhagic enteritis and occasionally rupture
of the intestine. Specific data on pathological changes
or clinical symptoms potentially associated with P.
mamillana are not available.
Clinical signs. Mass infection with A. magna may
cause diarrhoea. Infections with A. perfoliata are
inapparent or can lead to indigestion, diarrhoea, colic
and emaciation. In one of the studies, 22% of clinical
cases with spastic colics were attributed to infections
with A. perfoliata. Other studies suggest that A. perfoliata
infections are associated with increased risks for colic
and impaction of the ileum.
Diagnosis. Detection of eggs and proglottids by
faecal examination. The sensitivity of egg detection
with the usual flotation technique (either with saturated
sodium chloride or zinc sulphate solution) is very low
(2-13%). Better sensitivities of about 54-58% can be
achieved by using large faecal samples (30-50 g) and
a combined sedimentation-flotation technique (with
zinc sulphate solution, specific gravity: 1.3, or saturated
sugar solution), especially at high worm burdens(> 100
per animal). The rectangular to rounded, thick-shelled
eggs of A. perfoliata and A. magna have a diameter
of about 65-80 µm, while the eggs of P. mamillana
are smaller (37-51 µm). There are certain differences
between the species in the structure of the pyriform
apparatus. For diagnosing the infection in groups
of horses, the detection of specific antibodies by
ELISA can be useful. In an ELISA, 68% of 38 horses
with A. perfoliata infection were seropositive; cross-
 Part Ill. Parasites and parasitoses: metazoa
reactions with nematodes apparently played no role.
In a comparative study of egg detection, serology and
a copra-antigen test, the latter showed the best results
(sensitivity, 74%; specificity, 92%) and had a positive
correlation with the infection intensity. PCR assays for
species-specific diagnosis using eggs concentrated by a
centrifugation/flotation technique are described.
Therapy and control. Benzimidazole compounds
are ineffective against Anoplocephalidae in equines.
The drug of choice is praziquantel (1.0 mg/kg b.w. p.o.).
At least 2 treatments (in Central Europe: June/July and
autumn) are considered useful in problematic herds,
but long-term studies on the best strategic concepts are
lacking. Alternative grazing of pastures by horses and
ruminants or pasture rotation systems are recommended
as complementary measures. Control measures against
the intermediate hosts (moss mites) are not feasible.
Selected references
Back H, Nyman A, Osterman Lind E (2013) The association
between Anoplocephala perfoliata and colic In Swedish
horses - a case control study. Vet Parasltol 197: 580-585.
Denegri G, Bernardina W, Perez-Serrano J, Rodgrlguez­
Caabeiro F (1998) Anoplocephalid cestodes of veterinary
and medical significance. Folla Parasitol 45: 1-8.
Gasser RB, Williamson RMC, Beveridge I (2005) Anoplo­
cephala perfoliata of horses - significant scope for further
research, improved diagnosis and control. Parasitology 131:
1-13.
Hoglund J, Nilsson 0, LJungstrom BL, Hellander J, Lind EO,
Uggla A (1998) Epidemiology of Anoplocephala perfoliata
infection in foals on a stud farm in south-western Sweden.
Vet Parasitol 75: 71-79.
Pavone S, Veronesi F, Genchi C, Fioretti DP, Briantl E,
Mandara MT (2011) Pathological changes caused by
Anoplocephala perfoliata In the mucosa/submucosa and in
the enteric nervous system of equine ileocecal junction. Vet
Parasltol 176: 43-52.
Pittaway CE, Lawson AL, Coles GC, WIison AD (2014)
Systemic and mucosa! lgE antibody responses of horses to
infection with Anoplocepllala perfollata. Vet Parasltol 199:
32-41.
Relnemeyer CR, Nielsen MK (2009) Parasitism and colic. Val
Q)
C Clin North Am Equine Pract 25: 233-245.
·c3
'5 Rehbein S, Lindner T, Visser M, Winter R (2011) Evaluation
Q)
of a double centrifugation technique for the detection of
Anop/ocepllala eggs in horse faeces. J Helminthol 85:
co
C
409-414.
·c Roelfstra L, Betschart B, Pfister K (2006) A study on the
Q)
seasonal epidemiology of Anoplocephala spp. infection in
_f; horses and the appropriate treatment using a praziquantel
>, gel (Droncit 9% oral gel). Ber1 Munch Tierarztl Wochenschr
CJ)
0 119: 312-325.
0
·u5
co
a..
Skotarek SL, Colwell DD, Goater CP (2010) Evaluation of
diagnostic techniques for Anoplocephala perfoliata in horses
from Alberta, Canada. Vet Parasitol 172: 249-255.
Tomczuk K, Kostro K, Szczepaniak KO, Grzybek M,
Studzinska M, Demkowska-Kutrzepa M, Roczen­
Karczmarz M (2014) Comparison of the sensitivity of
coprological methods in detecting Anoplocephala perfoliata
invasions. Parasitol Res 113: 2401-2406.
Families Davaineidae, Dilepididae and
Hymenolepididae
Davaineidae: Davaine, C.J. (1812-1882), French
physician and parasitologist; Dilepididae: Di- (G): two;
lepis (G): shell; Hymenolepididae: hymen (G): thin
membrane; lepis (G): shell. Reference to thin-shelled
eggs.
Summary
• Agents. Species of the genera Davalnes, Amoebotaenia,
Choanotaenla, Ra/ffletlna and Hymeno/epls are
significant poultry parasites (► Table 9.13). Some
Hymeno/ep/s species parasltlse rodents and are
causative agents of zoonoses (► Table 15.2).
• Life cycle, epldemlology. In a two-host cycle,
terrestrial Invertebrates (Including earthworms,
snails, slugs, and Insects) are Intermediate hosts for
cestodes of galllnaceous birds, or pigeons, and small
crustaceans (e.g. 'water fleas') for cestodes of water
fowl. The Infection occurs by Ingestion of Intermediate
hosts containing Infective larvae (cystlcercolds).
Tapeworm Infections play a role In free-ranging poultry,
but in animals maintained Indoors only If adequate
Intermediate hosts for certain cestode species are
present (e.g. so-called meal-worms, hide beetle, spider
beetle, dung beetles or houseflies).
• Cllnlcal signs, diagnosis, therapy. Mostly asymp­
tomatic Infections, rarely decreasing productivity.
Detection of tapeworms at necropsy, treatment
with prazlquantel, partly also with benzlmldazole
compounds.
The families Davaincidae, Dilepididae and Hymeno­
lcpididae arc discussed here together because they
contain various cestodc species of poultry.
Agents. A selection of species is listed in ► Table
9.13. The overview shows that in chickens and other
gallinaceous birds, small tapeworm species of a few
millimetres in length (Davainea proglottina and
Amoebotaenia wneata) occur, but also species with
a length of several centimetres (Raillietina spp.,
Choanotaenia infundibulum) ( ► Figure 9.41 ). Water
fowl is predominantly infected with species of the family
Hymenolepididae, and pigeons are hosts of species
belonging to the families Davaineidae (Davainea and
Raillietina), Hymenolepididae (Sobolevicanthus) and
Anoplocephalidae (Killigrewia).
►
9. Phylum Platyhelminthes (flatworms)

Table 9.13. Cestodes of poultry: species (selection) of the families Davaineidae, Dilepidldae and Hymenolepididae.

Family, apeclea, length (L), lntennedlate hosta (IH), paratanlc Definitive hoats and organ locallsatlon of
dlltributlon (D) hoats(PH) adult ceatodea

Family: Davaineidae
Oavainea proglortina
L: 1.5-4 mm: D: worldwide
Railfietina cestlcillus
L: 9-13 cm: D: worldwide
Raillietina ec/1/nobothrida
L: up to 25 �m: D: worldwide
Raillietina tetragona
L: 10-25 cm: D: worldwide
Railfietlna boninl
L: 6-7 cm: D: Europe, Russia, Iran
F�mlly: Dllepldldae
Clloanotaenia intundibutum
_L: up to 23 cm: D: worldwide
Amoebotaenia cuneata
L: 2-
- 4 mm:
- D: worldwide
Family: Hymenolepldldae
Drepenidotaenia
(syn. Hymenolepis) lanceolata
L.:_Ll,£..!_O 25 cm; D: worldw_�e__ PH: freshwater snails (Ly_mn
Ecllinolepis (syn. Hymeno/epis)
carioca
-L: 3-8
- cm; D: worldwide
----- -- -
Rmbriaria fasciolaris
,___ L_: u-' p_ to_ 4_ 0_ cm;-'- D
_ _: w
Gastrotaenia spp .
L: up to 13 mm; D: Europe, Asia,
North and South America
T
IH: slugs: Deroceras species and galliformes (chicken. turkey. etc.), pigeon:
others small intestine >
IH: beetles. including carabkls, dung I chicken, turkey. other galliformes; .c
a.
0
beetles, mealworms, spider and hide small Intestine TI
beetles >­
(.)
IH: ants: Tetramorium. Pflei<Jole chicken, turkey other gollilormes;
species. etc. small intestine
IH: house flloa oncl ants chicken. other gallilormes, pigeon:
smoll Intestine
I
IH: land snails and uluga I pigeons and other birds:
smoll lntastlno
H: beetles: carabids, clung boelles chicken, turkoy, other gallilormes:
etc., also house Illes, grass-hoppers small Intestine
t
H: earthworms: Elsen/a, and others chicken, other galliformes;
-- --- ---- - small Intestine
IH: small crustaceans: Cyclops, goose, duck, other waterfowl, rarely chicken;
Eucyclops among others. small intestine
_ a_ _ei_ d_a�e)�-1---------_____
IH: dung beetles (Aphodius, chicken, other galliformes;
Onthophagus) small intestine
--·- -- ------ ------>----------
IH: small crustaceans: Cyclops, goose, duck, other water birds, chicken;
_ o_ _ rl_dw
_ _ id_e___o�iap1_9_mus, etc. small intestine
IH: small crustaceans: copepods duck, swan:
gizzard, partly distal oesophagus and
glandular �omach

a b

Figure 9.41. Cestodes in the intestine of poultry: (a) Davainea proglottina (max. length 4 mm) (Graphics: IPZ, A. Seeger; after
Sprehn 1961); (b) Rai/lietina sp. (max. length 13 cm) in the intestine of chicken (Photo: P. Hilbrich; Kuhn).
 Part Ill. Parasites and parasitoses: metazoa
Life cycle. In the cycles of cestodes of poultry, various
intermediate hosts are involved, corresponding to
the food and dietary habits of the definitive hosts: in
gallinaceous birds and pigeons almost exclusively land
animals (e.g. earthworms, snails, slugs, insects) and in
aquatic birds small crustaceans ( ► Table 9.13). After
ingestion of tapeworm eggs by intermediate hosts,
cysticercoids develop within at least 3-4 weeks. Final
hosts acquire the infection by ingestion of infected
intermediate hosts. Prepatent periods of the various
species vary between 9 days and about 6 weeks.
Occurrence and epidemiology. T he important
cestode species of chicken have a wide geographic
distribution ( ► Table 9.13), but prevalences and
infection intensities are different, depending on the
rearing and habitat conditions of the hosts. In free­
range poultry, a broad spectrum of cestode species may
occur, if adequate intermediate hosts find suitable living
conditions in the habitat, such as earthworms, snails,
slugs and various species of beetles. Under housing
conditions, massive infections can occur with Rai/lietina
cesticillus, R. tetragona or Cfioanotaenia infundibulum,
if their intermediate hosts are present in large numbers,
such as mealworms, hide beetle, spider beetle, dung
beetles or houseflies. Free-ranging water fowl with
access to rivers, ponds, etc. are constantly exposed to
an infection risk, as are free-flying pigeons.
Pathogenesis and clinical signs. Generally, cestode
infections in poultry cause only minor changes in the
intestinal mucosa, and they remain asymptomatic. In
heavy infections, decline of performance and diarrhoea
may occur, for example, when chickens are infected with
D. proglottina and Rail/ietina species.
Diagnosis, treatment and control. An intravital
diagnosis with identification of genera is possible,
based on morphological features of excreted
proglottids and eggs ( ► Figure 16.18, p. 55 I). Usually,
however, the diagnosis is made at necropsy, which
enables a morphological genus- and species-specific
identification of tapeworms. Praziquantel and partly
also benzimidawle compounds are suitable for treating
chickens, pigeons and waterfowl ( ► p. 6 IO). Control
measures against intermediate hosts in the field are
not feasible, but intermediate hosts in stables can be
controlled by cleaning measures and, if necessary, by
application of insecticides against arthropods.
Selected reference
C McDougald LR (2013) Internal parasites. In: Swayne DE (ed.)
>,
CJ)
Diseases of poultry, 13th ed. Ames, IA, USA: John Wiley
0 Blackwell, pp. 1117-1146: ISBN 978-0-470-95899-5 .
0
·wco
co
0..
Family Dipylidiidae
Genus Dipylidium
Dipylidium caninum (cucumber seed
tapeworm) and related species
Disease: Dipylidiosis in carnivores. I
Di- (G): two, double; pyle (G): opening. Reference to
the two lateral genital pores.
Summary
• Agents. Dipy/ldlum caninum Is a globally widespread
and fairly common parasite of the small intestine of
dogs and cats; rarer are Dipyiidium sexcoronatum, other
D/py/ldlum species, Joyeuxiella sp. and Diplopylidium
sp.
• Life cycle. D. caninum has an Indirect life cycle with
fleas as Intermediate hosts.
• Cllnlcal signs. Mostly asymptomatic Infections, rarely
anorexia and diarrhoea, exceptionally ileus caused by
tapeworm masses.
• Diagnosis, treatment, control. 'Typical proglottids with
bilateral genital pores and egg capsules. Treatment with
prazlquantel or epslprantel, control of fleas.
• Zoonotlc Importance. Harmless Intestinal Infection in
humans, very rare.
The family Dipylidiidae includes the genera Dipylidium,
Joyeuxiella and Diplopylidium that inhabit in the adult
stage the small intestine of carnivores. The most
important species of this family is Dipylidium caninum,
a worldwide common parasite of dogs and cats.
Agents. Dipylidium caninum: Length about 13-15 cm,
rarely up to 80 cm, strobila composed of numerous,
cucumber seed-shaped proglottids ( ► Figure 9.42).
Scolex with 4 suckers and rostellum with hooks. In each
proglottid 2 sets of reproductive organs with bilateral
genital pores, located approximately in the middle of
the segment. Reticulate uterus with egg capsules (about
200x 120 µm), each containing up to 30 eggs. Eggs
spherical (30-50 µm) with thin embryophore. Parasites
of the small intestine of dogs, cats, and wild carnivores
with global distribution, rarely in humans. The genera
Joyeuxiella and Diplopylidium differ from D. caninwn,
as their egg capsules contain only I egg each, and the
two genital pores are more proximally located in the
proglottid.
Life cycle. The life cycle of D. caninum involves fleas
( Ctenocephalides felis, C. can is) as intermediate hosts
( ► Figure 9.42). In the literature a chewing louse
(Trichodectes canis) is mentioned as intermediate host
but without evidence of an epidemiological role. Gravid
proglottids leave the definitive host by active migration
., 9. Phylum Platyt1elm1nthos (flntworms)

>­
.c
a.
0

Adult tapeworm

I
(scolex and proglottid)

- - - - -(1-
Gravid
Adult -proglottid
flea

Flea larva

Flea pupa --J /

�--11(11(....---�"ill

Cystlcercold

Figure 9.42. Life cycle of O/pylidlum canlnum (Graphics: IPZ, S. Ehrat).

through the anus, or they are passed to the environment
during defoecation. Thus, the tapeworm eggs arc
accessible for flea larvae, which ingest eggs. In the body
cavity of the flea larvae, cysticercoids are beginning their
development which progresses during the life cycle of
the fleas and is completed at high ambient temperatures
(30-32 °C) when adult fleas emerge from the pupa.
At lower temperatures (20-25 °C}, the development of
cysticercoids may be delayed; it will only be completed
after the adult fleas have spent a few days on their
Occurrence and epidemiology. D. caninum has
a world-wide distribution and is a fairly common
parasite of domestic and wild carnivores, but prevalences
may vary widely in various regions. For example, in
7 European countries, an average of 2.2% of 435 cats
and 5.2% of 178 clogs harboured fleas infected with
D. caninum as determined by PCR (ranges in cats 0.7-
16.7%, in dogs 3.6-14.4%). Red foxes, raccoon dogs,
and other wild carnivores are also known to be hosts Q)
of D. rnninum (e.g. DK: prevalence 0.3% and 5% in red
·o
C

host. Under favourable conditions, the development of foxes and raccoon dogs, respectively). Joyeuxiella and '6
Q)
cysticercoids is completed in 9-19 days. The definitive Diplopylidium species are generally regarded as less 2
hosts become infected by the ingestion of infected fleas. common, but a recent necropsy study in Portugal has
co
Prepatent period 16-21 days, patency up to 3 years. revealed the following prevalences in 162 stray cats: C
·;::
Joyeuxiella pasqualei 15.4%, Diplopyldium nolleri 3.7% Q)
Trichodectes canis has been described as an intermediate and D. caninum 53.1%.
host of D. sexcoronatum. Coprophagous insects (beetles) C

are thought to act as intermediate hosts for Joyeuxiella
and Diplopylidium, and reptiles (e.g. lizards) or small
mammals may be involved in the cycle as second
intermediate (or paratenic?) hosts.
Pathogenesis and clinical signs. Dipylidium
infections lead in rare cases to slight inflammatory
changes in the small intestine and corresponding
symptoms, such as loss of appetite and diarrhoea, or,
exceptionally, to ileus due to tapeworm masses.
 Part Ill. Parasites and parasitoses: metazoa

Diagnosis. Detection of egg capsules by coproscopic Waap H, Gomes J, Nunes T (2013) Parasite communities in
examination (flotation technique) or of proglottids, stray cat populations from Lisbon, Portugal. J Helminthol
which may be discharged in large numbers to the 88: 389-395.
environment of the host. Some can adhere to the perianal
skin or the fur of the animals; they may dry and then
resemble grains of rice. Microscopic examination of Family Taeniidae
fresh(or dried - after brief soaking in water), unstained
proglottids can already reveal typical characteristics of Taenia(L): ribbon, band. Refers to the ribbon-like shape
gravid proglottids, such as the two lateral genital pores of the body.
and the egg capsules( ► Figure 16.16, p. 549). The latter
can be released by teasing the proglottids. In Dipylidium, The family Taeniidae includes the genera Taenia and
the egg capsules almost always contain several eggs; in Echinococcus, which have a 2-host life cycle. In the
Joyeuxiella and Diplopylidium species only 1 egg. A PCR adult stage, they inhabit the small intestine of humans
assay has been described for the identification of larval ( Taenia) or carnivores (Taenia and Echinococcus) and are
D. caninum in fleas. only slightly pathogenic. In contrast, the second larval
stages(metacestodes) of some species, which develop in
Therapy and control. Praziquantel and epsiprantel in mammalian animals and accidentally in humans, may
the usual therapeutic doses are highly effective against cause severe disease(echinococcosis, cysticercosis) and
Dipylidium infections in dogs and cats. Classical control death. Organs of slaughter or game animals that contain
is based on regular anti-cestode treatments on the one metacestodes are unsuitable as food.
hand, and measures against fleas on the other( ► Table
19.14, p. 600 and 19.16, p. 602). A combination of Agents. Taeniidae are a few millimetres to several
these measures is now possible by using novel drug meters long; they consist of a few to numerous
formulations, containing active substances against proglottids; the scolex bears 4 suckers and usually a
cestodes, adult fleas on the host and their larval stages rostellum, which can be equipped with two rows of large
in the environment(details ► p. 606). There is evidence and small rostellar hooks. Each proglottid contains a
from a large study in the USA that regular flea control set of male and female reproductive organs, and genital
is associated with declining prevalences of D. caninum pores are unilateral, alternating irregularly; in gravid
in dogs. proglottids uterus with tree-like branches or shaped
differently ( ► Figure 9.33). Eggs round, diameter 30-
Zoonotic importance. Harmless intestinal infections 40 µm, with oncosphere (L 1) and a thick, brownish
with D. caninum occur rarely in humans, predominantly embryophore whose main layer is composed of small
in children, by accidental swallowing of fleas containing keratin blocks ( ► Figure 9.43). Infectious larvae
cysticercoids. (L2, metacestodes) in form of cysticercus, coenurus,
strobilocercus or echinococcus ( ► Table 9.14). Within
the genus Taenia >30 species ( ► Table 9.15 and 9.16),
- Selected references r-::===::;;::;:::::::::;::. only a few species in the genus Echinococcus ( ► Table
9.18). Several species of the Taeniidae are causative
Beugnet F, Labuschagne M, Fourie J, Guillot J, Farkas R, agents of important zoonoses.
Cozma V, Halos L, Hellmann K, Knaus M, Rehbein S
(2014) Occurrence of O/py/ldlum canlnum In fleas from client-
owned cats and dogs In Europe using a new PCA detection Genus Taenia
assay. Vet Parasitol 205: 300-306.
Beugnet F, Franc M, Tielemans E (2015) Gastro-inteslinal Taenia species of man
helminthoses. In: Beugnet F, Halos L (eds.) Parasitoses &
vector borne diseases of cats. Lyon, France: Merial S.A.S.,
Q)
·u
C pp. 15-49; ISBN 978-2-9550805-0-4.
Gates MC, Nolan TJ (2014) Declines in canine endoparasite
Diseases: Taenlosls and cystlcercosis. I
'6
Q)
� prevalence associated with the introduction of commercial
heartworm and flea preventatives from 1984 to 2007. Vet Taenia saginata (beef tapeworm)
C1l Parasitol 204: 265-268.
C
·;::
Q) Rehbein S, Capari B, Duscher G, Keidane D, Kirkova Z, Taenia (L): ribbon, band; saginata (L): fattened.
Petkevicius S, Rapti D, Wagner A, Wagner T, Chester Reference to thick proglottids compared to T. solium.
C ST, Rosentel J, Tielemans E, Visser M, Winter A,
>,
0)
Kley K, Knaus M (2014) Efficacy against nematode and
0 cestode infections and safety of a novel topical fipronil, (S)­ Diseases: Taeniosis in humans, cysticercosis in
0
'iii
C1l
methoprene, eprinomectin and praziquantel combination cattle (beef measles). I
product in domestic cats under field conditions in Europe.
C1l
0.. Vet Parasitol 202: 10-17.
... 9. Phylum Platyhelminthes (flatworms)

Table 9.14. Types of infective larvae (metacestodes) of Taeniidae.

Infective larva Description

Cysticercus Fluid-filled bladder. about pea-sized or larger. with a single invaginated protoscolex ( ► Glossary.
p. 620). Wall consisting of the outer host capsule (connective tissue) and an inner layer of parasite
tissue which forms the protosco!ex. Fluid clear. contains antigens (see also cystic echlnococcus).
-�eprod�tive potentia1 : one oncosphefe =' one protoscolex ( ► Figure 9.43 - ► Figure 9.47). _
1 2

Strobilocercus Strobilocercus (syn. cysticercus) fasciolaris is the metacestode of Taenia (syn. Hydatigera)
taeniaeformis, Protoscolex connected with a 3 -20 cm long. ribbon-shaped strobila, ending In a small
bladder. In vivo enclosed in an approximately pea-sized cyst. Reproductive potential: one oncosphere
1-------- � one protoscol� ( ► Figure 9.50). _ _ _
Coenurus Fluid-filled, up to fist-sized bladder. with mulliple protoscoleces produced on Its inner wall. Wall

1 - - -------
Cystic echinococcus
-
structure and fluid as In cystlcercus. Reproductive potential: one oncosphere -• several hundred
Jprotosco�es ( ► Figure 9.48 and 9. 4 9)� _ _ _
Infective larva of Echlnococcus granutosus a.I. Fluid-filled cyst of a few millimetres up to >20 cm
-
(hydatid type) in diameter. Wall composed ol an outer host-dorlvod capsule of connoclivo tissue and Inner layers
of parasite tissue. n,ey consist of an outer. acollular laminated(" cutlcular) layer and an Inner. thin,
nucleated germinal layer. The latter forms brood capsules by asexual budding. each containing
up to 30 protoscoleces. Expansive growth by Increase In cyst size. Liquid (hydatld fluid) water-
clear, containing Inorganic substances and organic compounds (amino acids, proteins, lipids.
carbohydrates, etc.), Including parasite antigens. Reproductive potential: one oncosphere -• several
thousand protoscoleces ( ► Figure 9.52 and 9.5_4 )_.____ -
Alveolar echinococcus Conglomeration of many vesicles of variable sizes (microscopic up to approximately 3 cm in
diameter). forming an alveolar structure. The individual vesicles and the whole conglomerate are
surrounded by necrotic tissue, inflammatory reactions or dense connective tissue. Wall structure
of individual vesicles in principle as in the cystic form. Infiltrative tumour-like growth by exogenous
budding of vesicles, partly also by root -like protrusions of the germinal layer devoid of laminated layer.
Vesicles contain little liquid, but usually a gelatinous mass. Reproductive potential: one oncosphere --+
several thousand protoscoleces ( ► Figure 9.57 and 9.58).
1 Maximum number of protoscoleces, which can arise from an oncosphere in a highly susceptible intermediate host.
2 In Taenia crassiceps, the metacestode Is capable of exogenous budding thus forming multiple cysts and protoscoleces.

Summary
Agents and life cycles. Parasites of humans are Taenla
saginata, T. solium and T. sslstlca ( ► Table 9.15). Adult
Taenia species (length: a few me ters) Inhabit the small
intestine of humans. Life cycle dlheteroxenous: egg
with oncosphere __. metacestode (cystlcercus type)
in intermediate hosts --+ Infection of humans orally by
ingestion of tissue containing Infective metacestodes.
The metacestodes of T. ssglnsts and T. sol/um develop
in striated muscles of cattle or pigs, respectively, the
metacestodes of T. ssistics In the liver of pigs.
Occurrence and epidemiology. T. ssglnsts Is wide­
spread throughout the world, in Europe usually with
low prevalences in the human population. Sources of
infection for cattle are a few tapeworm carriers releasing
proglottids and eggs. Distribution of eggs occurs In
different ways (by sewage, liquid manure, defaecalion
in the environment, etc.). Eggs remain infective for at
least 1-2 months on sufficiently humid pastures. T.
solium is endemic in Asia, Sub-Saharan Africa, Central
and South America and parts of the USA. In Europe,
there is evidence of sporadic occurrence in eastern
and south-eastern countries.
• Pathogenesis, clinical signs. In humans intestinal
infection asymptomatic or with mild abdominal
disorders (taeniosis). in cattle and pigs the parenteral
..
• Diagnosis. Intestinal Infection of humans: detection of
eggs or copro-antlgen In faecal samples or of proglottids
shed with or without defaecatlon. Cystlcercosls In
groups of living cattle or pigs: detection of serum
antibodies using specific test procedures. Post mortem
diagnosis In cattle: mandatory Investigation of slaughter
cattle (Incision and adspectlon of the masticatory
muscles, heart, etc.); however, the sensitivity of this
technique Is low.
• Therapy, control. Treatment of human Taenls carriers
with a highly efficcaclous cestodiclde. Chemotherapy
of cattle Infected with cystlcercl Is not feasible.
Slaughtered cattle, heavily Infected with cysticerci, are
unsuitable for human consumption; weakly parasitised
carcasses are released for consumption after freezing.
Other measures: purification of wastewater, hygiene,
education. Overall, the available control measures are
insufficient. Cysticercosis of cattle causes significant
economic losses. Vaccination of cattle or pigs is
possible, but a commercial vaccine is not currently
available.
• Zoonotic importance. Cysticercosis in cattle is a
zoonosis of human origin with significance throughout
the world. Metacestodes of T. solium may develop
In humans and cause severe forms of T. so/ium

"Infection (cysticercosls) Is usually asymptomatic. cysticercosis Qncluding neurocystlcercosls and ocular

cystlcercosls). Imported cases of T. sol/um cysticercosls
are also diagnosed In Central Europe and In other non­
endemic regions.
 Part Ill. Parasites and parasitoses: metazoa
Table 9.15. Taenia species of humans (causative agents of zoonoses).
Species and length Distribution
Taenia saginata Worldwide
Length: up to 10 m
Taenia asiatica East and South-East Asia
Length: 4-8 m
Taenia solium Latin America, India, South small intestine
Length: 3-4 m East Asia, Sub-Saharan Africa, p: 9-10 weeks
rare in Europe2
1
The names of the metacestodes are not printed In italics as they are common names and not names of genera and species according
to the rules of the international zoological nomenclature.
2 Imported cases of human cystlcercosis In non-endemic areas (USA, Canada, Europe, Australia, etc.).
Agent. The adult stage of T. saginata lives in the small
intestine of humans and is the agent of T. saginata
taeniosis. The metacestodes, known as Cysticercus
bovis, are muscle parasites of bovids and the agents of
T. saginata-cysticercosis (short name cysticercosis) in
cattle and buffaloes.
• Adult tapeworm. Large, yellowish-white tapeworm,
length up to 10 m, small scolex (diameter about 2
mm) with 4 suckers, but without rostellum ('unarmed'
tapeworm); strobila with numerous (up to 2,000)
proglottids; gravid proglottids longer than wide (about
12-20x8-l 2 mm), genital pores in irregular sequence
on either side; uterus with 14-32 lateral branches, each
proglottid contains about I 00,000 (57,000-188,000) eggs
( ► Figure 9.43). Eggs with characteristics of the genus,
round, 30-40 µm, morphologically indistinguishable
from eggs of other Taenia species but differentiable by
DNA analyses.
• Metacestode. Cysticercus bovis, small (4-9x3-4
mm), fluid-filled bladder with an 'unarmed' protoscolex
( ► Figure 9.43 and 9.44a).
Life cycle. The life cycle of T saginata is diheteroxenous
with humans as definitive hosts and bovines (cattle,
buffalo, yak) as intermediate hosts ( ► Figure 9.43). The
tapeworm in the small intestine of humans (often only
one specimen per host) produces gravid proglottids,
which typically detach individually. They are shed into the
environment either during defaecation or independently
after their active migration through the anus. Eggs
can be released earlier in the intestine from damaged
uterine branches when gravid proglottids detach from
the strobila, and are then excreted in the faeces. In the
environment, the motile proglottids can crawl away from
the faeces and lose large amounts of eggs from ruptured
uterus branches during their migration. Finally, eggs
are also released when proglottids disintegrate in the
environment. After ingestion of eggs or egg-containing
'Site of adult parasites Intermediate hosts, names and main
in humans and site of metacestodes 1
prepatency (p)
small intestine cattle, buffalo, other Bovidae
p: 12-14 weeks Cysticercus bovis
striated muscles
small intestine pig, rarely cattle
p: 11 weeks Cysticercus viscerotropicus
liver
domestic and wild pig
Cystlcercus cellulosae
striated muscles, also subcutis, CNS, eye,
and other organs
proglottids by cattle or other bovines, the oncospheres
hatch in the small intestine from the embryophore; they
then penetrate the intestinal wall, invade lymph and
blood vessels and are transported in the bloodstream
to striated muscles, where they develop to infective
metacestodes (Cysticercus bovis) within approximately
12 weeks (10-16 weeks) p.i. Occasionally, cysticerci
are found in liver and lungs. Humans become infected
by ingestion of raw or undercooked beef containing
viable cysticerci. In the small intestine, the cysticercus
evaginates the protoscolex which attaches itself to the
mucosa of the upper small intestine and develops into
an adult tapeworm. Prepatent period about 3 months
(87-100 days); life-span of the parasite in man a few
months to decades.
Occurrence. T. saginata, the commonest taeniid
species of humans, has a worldwide distribution.
Prevalences in the population are subject to regional
variations between sporadic or low (<0.0 I to 2%: e.g.
countries In Central Europe) to high (>10%: e.g. some
African or Asian endemic areas). Based on abattoir
reports from several European countries, prevalences
of bovine cysticercosis between 0.007 and 6.8% have
been reported with large variations between countries,
regions, and abattoirs. At 6 slaughterhouses in CH,
0.58% of slaughter cattle were carriers of cysticerci
(2002-2005), however, prevalences up to 4.5% were
recorded in cows. Due to the low sensitivity of the
meat inspection techniques (see below), it has to be
assumed that the prevalence of cysticercosis in cattle is
generally underestimated. Usually, light infections with
low heard prevalences occur in cattle as a result of the
wide dispersal of T. saginata eggs and their low density
( ► Glossary, p. 620) in the environment. However,
high egg concentrations in individual farms can lead
to cysticercosis outbreaks ('cysticercosis storms') with
up to >50% infected animals.
., 9. Phylum Platyhelrn,nthes (flcJtworrns)

>,
.c
a.
0

Gravid
proglottlds

a
Cystleercl In
muscles of

I
Intermediate / Cystlcercus
rlS:'\
U§
hosts bovls
?--icoo�re

� .... '

Man as accidental
host of T. sol/um
oystlcercl

Figure 9.43. Life cycles of Taenia saginata und T. sol/um (Graphics: IPZ, S. Ehrat).

Epidemiology. The maintenance (persistence)
of the life cycle of T. saginata depends on various
epidemio logical factors that are partly responsible for
difficulties in control.
• Adult tapeworms and tapeworm carriers.
Taenia species have a high reproductive capacity,
associated with a long life-span of the intestinal stage.
to about 500,000 eggs, however, not all are mature and
infective. Frequently, the tapeworm infection in humans
remains untreated for extended periods. Therefore,
single or a few tapeworm carriers can contaminate the
environment with eggs to a significant extent.
C
• Distribution (dispersion) and survival of the >,
a,
eggs in the environment. Certain factors, which 0

A carrier of 7: saginata can release 1-15 or more gravid are difficult to control, favour the dispersion of eggs 2
"iii
proglottids per day during prolonged periods (weeks to in the environment, including the defaecation of cu
cu
months). A daily release of 5 proglottids corresponds tapeworm carriers in the environment close to cattle CL
 Part Ill. Parasites and parasitoses: metazoa
Figure 9.44. Metacestodes of Taenia saginata: (a) single Cysticercus bovis (4-9x3-4 mm) in skeletal muscle of cattle; (b) heart
muscle of cattle with numerous, predominately dead cysticerci; (c) cysticerci of Taenia solium (Cysticercus cellulosae) (-6-
15x5- 7 .5 mm), isolated from the connective tissue capsule (Photo: a IPH; b IPZ; c N. Taira et a/.).
pastures (e.g. in the vicinity of construction sites,
camp-grounds, highway rest stops or in cattle stables),
inadequate sanitary facilities (e.g. 'disposal' of sewage
from moving trains with large scattering effect, leaks in
sewers), insufficient purifkation and decontamination
of community wastewater and the use of mixtures of
domestic sewage from farms with liquid animal manure
for fertilising pastures. Another source of contamination
of grassland with T. saginata eggs can be overflow water
originating from settling basins in sewage works if it is
running inlo rivers or creeks. Furthermore, floods may
contribute to the dispersal of Taenia eggs. In a Swiss
case-control study (2008), 119 farms with confirmed
Cl)
C cysticercosis in cattle and 65 control farms were surveyed
Ti
'6 regarding infection risks. StatisticaJly substantiated risk
Cl)
� factors were inter alia parking places, railway lines, use
� of purchased roughage, and frequent leisure and public
co activities in proximity to farms attracting visitors (e.g.
C
·c on the occasion offestivaJs or visits). Jn Switzerland and
Q)
� other countries, the majority of farms are not connected
C to the sewer network. Therefore, T. saginata eggs in
> faeces of tapeworm carriers can pass into the liquid
-
0)
0 manure and thus to grassland.
0
·u;
After deposition to grassland, proglottids survive
co
a.. under favourable conditions (high humidity, moderate
temperature) for hours or days and can crawl a few
centimetres away from the site of deposition. Therefore.
a rapid dispersion of eggs occurs in the vicinity of the
deposition site. Contributing factors nre trampling of
faeces by grazing animals, inanimate factors (heavy
rains, floods, wind), but also mechanical dispersal by
insects (cspccinlly blowflies) or birds.
In the environment, 'foenla egg are highly tenacious if
there is adequate moisture and moderate temperatures.
On pastures in Central Europe, the majority survive for
1-2 months, and a few for 6-8 months. In laboratory tests,
T. sagittata eggs survived in a humid environment al
4 °C for almost a year, and at -4 °C for about 2½ months.
In liquid manure, stored under normal conditions at
~+20 °C (summer) or +3-8 °C (winter), a significant
proportion of Taenia eggs was viable after 30 and 60
days, respectively. In aerated liquid cattle manure with
temperatures of +35-40 °C 'faenia eggs die within 25
days. In grass silage most of the eggs of Taenia spp. are
inactivated at +20 °C after 30-40 days, and at + JO °C
after ~80 dars. In well-dried hay, Taenia eggs quickly
lose their viability because of their high sensitivity to
exsiccation. The pasteurisation of sewage sludge (e.g.
70 °C, 30 min) reliably kills the eggs of T. saginata and
other helminths.

• Intermediate hosts and metacestodes. In
Central Europe, cattle are the sole intermediate hosts
of T. saginata; in other regions buffaloes, yaks, and
possibly wild bovines can also play a certain role. Cattle
are infected most frequently through the oral uptake
of Taenia eggs with contaminated feed or drinking
water, rarely by contact with tapeworm carriers whose
hands are contaminated with Taenia eggs, for example
when feeding calves with milk. Prenatal infections
of calves have been described, but clear evidence is
lacking. The immune status of the cattle population
plays an important role as an epidemiological factor
(immunology, see below).
• Epidemiological basic patterns. In highly
endemic areas(e.g. countries in east Africa), the number
of tapeworm carriers is high. A significant proportion
of calves and young cattle acquires an infection with
Taenia eggs, resulting in a high infection intensity with
cysticerci. With the repeated intake of Taenia eggs,
immunity develops in the cattle population, which
protects, at least partially, against subsequent infections.
Most of the cysticerci established in cattle die after
about 9 months. In endemic areas with low T. saginata
prevalence in humans, a proportion of cattle may be
infected, but usually with only a few cysticerci. Under
these conditions, effective immunity cannot develop
in the population. Therefore, cysticercosis outbreaks
l
('cysticercosis storms') are possible when susceptible
cattle are heavily exposed, for example after massive
egg shedding by a tapeworm carrier on a farm. In such
outbreaks over 50% of cattle may be affected.
Pathogenesis and clinical signs
• Taeniosis in humans. The preferred site of T.
saginata within its host is the upper small intestine
where the scolex attaches to the mucosa. Adjustment
of the site is possible by detachment and re-attachment.
Often, the infection remains asymptomatic, but in a
proportion of persons, T. saginata may cause symptoms
(abdominal pain, nausea, hunger, weight loss, diarrhoea,
constipation), and unpleasant sensations due to active
discharge of proglottids from the anus.
• Cysticercosis in cattle. Within 2-4 weeks p.i., the
oncospheres transform to small, 1-2 mm large bladders
in the connective tissue of striated muscles, where they
are initially surrounded by a granulomatous cell wall
and later by a fibrous capsule. Gradually, they develop to
pea-sized(05.-1.0x0.5 cm), cysticerci(Cysticercus bovis)
(common name: measles), containing one 'unarmed'
protoscolex, reaching infectivity about 10 weeks p.i.
Viable cysts are oval, translucent, and filled with clear
fluid(► Table 9.14, ► Figure 9.44a). Heavy infections
with cysticerci can cause serous and cellular infiltration
of the inter-muscular and subcutaneous connective
tissue. Cysticerci are found in greatest, but fluctuating
densities in masticatory muscles, heart, diaphragm,
9. Phylum Platyhelminthes (flatworms)
tongue limbs and body musculature; if present in other
locations(e.g. oesophagus, adipose tissue, subcutaneous
tissue, liver, lung) the cyst numbers are usually low. Dead
cysticerci appear as white-yellowish or greenish foci with
a thickened fibrous capsule and caseous, purulent or
calcified content; grey-white scars of connective tissue cu
are indicative for cyst remnants(► Figure 9.44b). It is ;g
>­
..c
important to point out that the same animal can harbour a.
both living and dead cysticerci. Usually, the infection is 0
u
asymptomatic; clinical symptoms (fever, stiff gait) are
very rare and may appear only In massive infections.
Adverse effects of T. sagi11ata are mainly due to loss or
Impairment of meat from cattle infected with cysticerci.
In heavily affected farms, the losses can be substantial
(condemnation of whole carcasses of heavily infected
animals).
Immunology. The intestinal T saginata infection of
man stimulates, if at all, only a weak immunity, which
does not prevent re-infection. On the other hand, in cattle
after experimental or natural infection with relatively
small numbers ofT. saginata eggs, an effective immunity
develops against re-infection, which lasts unchallenged
for 10-12 months, and even life-long if the animals
are continuously exposed to infections with eggs. This
immunity is directed mainly against developmental
stages during their migration from the intestine to the
musculature and the early developmental stages in the
muscles. However, the immunity appears to be also
partially effective against the established cysticerci, of
which about 80% degenerate within 9 months p.i.
A protective immunological effect is predominantly
due to humoral antibodies, which are transmitted via
colostrum from immunised cows to calves. Antibody
and complement are involved in association with
cytotoxic reactions in the killing of oncospheres and
metacestodes. On the other hand, cysticerci can stay alive
for years if calves are infected during the first days of
life, presumably due to immune tolerance. Overall, these
immunological conditions are favourable for vaccination
(► p. 569).
Diagnosis
• Man. The diagnosis of intestinal T. saginata infection
of humans is based on detection of eggs and copro­
antigen in stool samples or identification of proglottids
released with or without defaecation. DNA analyses
allow a differential diagnosis of proglottids and eggs of
different Taenia species of humans(► p. 522).
• Cattle. In the EU(Directive 64/433/EEC) and also
in other countries (e.g. CH, USA) it is mandatory to
investigate all slaughtered cattle over 6 weeks of age for
cysticerci, by applying large-scale cuts through the outer
and inner chewing muscles(masseter)(2 cuts through
external, 1 cut through the internal muscles), inspection
Part Ill. Parasites and parasitoses: metazoa
and palpation of the tongue as well as visual examination
of the oesophagus, diaphragm and the heart which is
routinely opened by longitudinal cuts at slaughter. Due
to the usually low infection intensities of cattle in Central
Europe (e.g. mean infection intensity of cattle in DK <4
cysticerci per animal) and the location of cysticerci in
muscles that are not investigated in detail, the sensitivity
of the EU approved routine meat inspection is low. In
a recent study, it has been estimated to an average of
about 15% (range: 10-23%). Therefore, a significant
proportion of cattle carcasses parasitised with C. bovis
is not detected at routine meat inspection, and the meat
can thus pass via the food chain to humans. By additional
cuts through the heart muscle, the sensitivity can be
improved 2-3 fold. ELISAs, based on EIS-antigens or
synthetic peptides of T. saginata metacestodes, can detect
specific serum antibodies in naturally infected cattle
with an estimated sensitivity of 82% and a specificity of
96%, but it is currently neither applied in practice nor
commercially available. Serological tests for circulating
antigens released by viable cysticerci are only sufficiently
sensitve in cattle harbouring high cyst burdens (>50
cysts per animal).
Therapy. Praziquantel and niclosamide are used to
treat the intestinal T. saginata infection of humans.
Praziquantel in an increased dosage (SO mg/kg b.w.
p.o.) is also effective against C. bovis in cattle, but muscle
lesions persist after treatment for prolonged periods.
Therefore, and because of the high costs, this treatment
is not practical.
Control and prevention. The life cycle of T. saginata
provides several options for control and prevention with
different significance in practice.
• Detection and treatment of tapeworm carriers.
Comprehensive identification and treatment o f
tapeworm carriers is difficult and demanding, especially
in areas with low T. saginata prevalence. This measure
is therefore unsuitable for general control, but it can be
focally useful, e.g. in individual farms or communities.
• Detec tion of carriers of cystlcercl and mea­
sures for inactivation of cysticerci. The detection
of carries of cysticerci by meat Inspection remains
insufficient for di.agnostic reasons, but it can help to
reduce the infection risk for humans. According to
EU guidelines (Directive No. 854/2004 and 64/433/
EEC), meat of heavily infected cattle (> 10 cysticerci/
animal) is unfit for human consumption, that of weakly
infected cattle ( < 10 cysticerci/animal) can be released
for consumption after killing living cysticerci by freezing
(e.g. at -18 °C for 72 h or at -10 °C for at least 10 days).
In Central Europe, these measures have not led to a
decline in the prevalence of cysticercosis in cattle during
the last decades. More successful was a national control
program in Canada, which is based on mandatory
reporting, quarantine and sanitation of affected farms,
intensified meat inspection (risk-based meat inspection)
and cold treatment of animal carcases. As personal
prophylaxis, meat or minced meat intended for raw
consumption in households can be frozen at -20 °C
for 4 days.
• Wastewater treatment, other hygienic
measures and education. Repair of damaged sewers,
treatment of municipal wastewater in sewage treatment
plants, sanitation ( = decontamination) of sewage
sludge by heat treatment (pasteurisation), prohibition
of application of untreated sewage sludge to pastures,
and alternative methods of disposing sewage sludge
(e.g. incineration) contribute to reducing the infection
risk for cattle. In farms that are not connected to the
sewer, mixing of domestic wastewater with liquid animal
manure and the application to grassland should be
avoided. Education and hygiene measures are constantly
required to contain the cysticercosis problem.
• Vaccination. Vaccination of cattle with recombinant
oncosphere antigens of T. saginata induces a high level
of protection against experimental or natural challenge
infections (up to about 99%). A vaccine has been
successfully tested, but is not yet commercially available.
Taenia asiatica
Disease: Asiatics taeniosis. I
T. asiatica, closely related to T. saginata, is widespread
in East and South East Asia, and occurs there in
certain areas sympatrically with T. saginata and T.
solium. T. asiatica differs morphologically, genetically
and biologically from the other Taenia species of man.
Intermediate hosts are domestic and wild pigs, in which
infectious cysticerci do not develop in the muscles, but
in the liver (sporadically also in other visceral organs)
(hence: Cysticercus viscerotropicus). Susceptible are
also goats, monkeys and calves, but do not play an
epidemiological role. Raw or undercoocked pork liver
is the infection source for humans.
Taenia solium (pork tapeworm)
Disease of T. sol/um taenlosis in humans and
T. solium eysticercosis in pigs, other
animals and human s. IJ
Taenia (L): Ribbon, band: solium: from Arabic sos!:
chain.
Agent. With a length of 3-4 m T. solium is shorter than
T. saginata. The scolex of T. solium has four suckers

and a rostellum armed with a double row of hooks.
In gravid proglottids, the number of branches of the
uterus with 7-16 on each side is often (but not always)
smaller than that of T. saginata; a vaginal sphincter is
missing, the ovary is 3-lobed. Metacestode: Cysticercus
cellulosae, size about 6-15x5- 7.5 mm, structure similar
to C. bovis, but with 'armed' protoscolex ( ► Figure 9.43
and 9.44). Eggs are morphologically identical to those
of Taenia saginata.
Life cycle. The life cycle is similar to that of T. saginata
(► Figure 9.43), but for T. solium the pig is the natural
intermediate host, in which the metacestode (Cysticercus
cellulosae) develops in 2-3 months to maturity. In the pig,
the cysticerci are mainly located in the inter-muscular
connective tissue, in some animals also in the brain,
eye and in various internal organs. Cysticerci can also
develop in other mammalian animals (including dogs,
cats, and monkeys) and in humans (cysticercosis, see
below). The life cycle is closed when humans ingest pork
containing living cysticerci. Prepatent period 9-10 weeks.
Occurrence and epidemiology. T. solium is mainly
endemic in rural areas of Central and South America,
Sub-Saharan Africa and Asia, with sporadic foci in the
USA and parts of Europe (e.g. Portugal, Spain, south­
eastern Europe). Worldwide, the number of people
infected with C. cellulosae is estimated at 5-6 million.
There are alarming reports from many endemic areas,
e.g. from Mexico: in rural areas, up to 25% of pigs
are infected with C. cellulosae and up to 10% of the
population is affected by neurocysticercosis (see below).
In the USA, cysticercosis of man plays a role, especially
among immigrants from Latin America, but also in
North Americans; annually about 1,000 new cases were
diagnosed between 1990-2002, and 221 persons died
from the infection. Immigrated tapeworm carriers from
endemic areas can be infection sources for the local
population, as observed in the USA and other countries.
Outside the endemic areas, imported human cases of
T. solium cysticercosis have been diagnosed in many
countries. In 17 European countries, 167 human cases of
neurocysticercosis were reported between 1970 and 2013.
Pathogenesis and clinical signs. In humans, the
intestinal infection with T. solium causes n o or only
minor disturbances, similar to the infection with T.
saginata. Much more serious is cysticercosis caused by
the metacestode stage in humans and animals.
• T. solium cysticercosis in pigs and other animal
species. Pigs are often heavily infected, as they ingest
whole and often multiple, egg-containing proglottids by
coprophagy. In pigs, cysticerci are predominantly located
in muscles of the sacrum, shoulder blade, diaphragm and
tongue, less often in other muscles, visceral organs (liver,
lung, kidney) as well as the brain and eyes. Symptoms
are generally not observed, but they may occasionally
occur, such as respiratory disorders, stiff gait, difficulties
9. Phylum Platyhelminthes (flatworms)
with food intake and nervous disorders. Cerebral T.
solium cysticercosis has also been described in dogs
and cats; cysticerci with armed protoscoleces have been
found inter alia in different species of monkeys, wild
ruminants, rodents, wild carnivores, but an accurate
species identification of the parasites has not been co
"'O
performed. >,
.c
0.
• Cysticercosis in humans. People can become 0
u
infected with T. solium eggs resulting in various forms
of cysticercosis, such as cysticercosis of the CNS
0
(neurocysticercosis), the eye, muscles, and subcutaneous
tissue.
Diagnosis. Detection of intestinal 7: solium infection
of man as in 'f'. saginata. Differential diagnosis between
T. saginata and 7'. so/ium is important (based on
morphology of the proglottids, more reliable by PCR).
Regionally, T. asiatica has to be considered. Cysticercosis
in pigs can be diagnosed intra vitam in some animals
by examining the tongue for cysticerci (pea-sized
protrusions). Detection of specific antibodies in serum
samples is possible, but currently not applicable i n
practice. In meat inspection of slaughtered pigs, T. solium
cysticercosis has to be taken into account (EU Regulation
No 854/2004) (note: slaughterhouse records often do
not differentiate between T. so/ium and T. hydatigena
cysticercosis).
The diagnosis of human cysticercosis is based on the
detection of cysticerci by imaging techniques, serological .c
Cl)
......
C
detection of specific antibodies (ELISA, WB) or of
antigens and DNA in the cerebrospinal fluid.
.E
Q)
:r:
Therapy and control. Intestinal T. solium infections
in humans are treated with praziquantel or niclosamide.
Praziquantel is also efficacious against cysticercosis in
humans.
After a single treatment of pigs with oxfendazole (30
mg/kg b.w. p.o.), T. so/ium cysticerci in muscles die
within 12 weeks, but fibrous scars remain. Cysticerci
localised in the brain are not fully affected by this
therapy. The intestinal infection of humans with T.
solium can be prevented by cooking or freezing pork
(-10 °C for at least 10 days). Control measures include:
Q)
education of the population, improvement of hygiene
·o
C
and meat inspection as well as mass treatment of the ti
population in endemic regions with praziquantel (less 2
Q)
frequently with niclosamide), which is tentatively 2:-
complemented by simultaneous treatment of pigs with C'O
C
oxfendazole. Vaccination of pigs with a recombinant ·;:::
Q)
oncosphere antigen (TSOL18) induces a high degree of �
immunity. In a study in Cameroon, pigs after vaccination .S
with TSOL18 and a simultaneous single treatment with >,
Ol
oxfendazole were free of C. cellulosae (infection rate 0
of the controls 20%). This is a promising option for 'ci)
an effective control. A TSOL18 vaccine is currently
co
undergoing the process towards registration. CL
 Part Ill. Parasites and parasitoses: metazoa
Zoonotic importance. Man is the only natural
definitive host of T. saginata and T. solium, and thus a
source of infection for T. saginata cysticercosis in cattle
and T. solium cysticercosis in pigs, respectively. T. solium
eggs may lead to autoinfections of tapeworm carriers or
to infections of other people resulting in cysticercosis.
The importance of cysticercosis of humans and of 'f.
asiatica is highlighted above.
Taenia species of carnivores
Disease: Taeniosls In carnivores, cystlcercosls and
coenurosls In Intermediate or accidental
hosts. fd
Summary
• Agents. Dogs are definitive hosts for several �en/a
species, of which 7ilen/a hydatfgena, T. plslformls, T.
ovls and T. multfceps are the most Important species In
Europe and elsewtiere. T. (syn. Hydatlgera) taen/aeformls
Is the only common species In cats.
• Life cycle, epidemiology, The llfe cycle Is dlhetero­
xenous similar to ».enla species of humans (► Table
9.16). Important epidemiological factors Include: high
reproductive potential, longevity of adult parasites,
considerable tenacity of eggs In the environment and
Immunity of Intermediate hosts directed against larval
stages.
• Pathogennls, cllnlcal signs. Since Intestinal stages
are of minor pathogenlclty for carnivores, the Infections
are usually asymptomatic. Metacestodes of different
Taen/a specl11 can cause severe Illness and death In
Intermediate hosts. For example, migrating larvae of T.
hydat/Qtna (sheep, goat, pig) or T. pls/formfs (rabbit) may
C8UN llv« di..... , and cystlcercl of T. multfceps CNS
dlsordn (e.g. In lhetp 'gld', 'stagger'). Infections of
slaughtered animals with metse11todes are significant
for food hygiene.
• Dlagnosla. Intestinal Infections of carnivores are
dlagnoeed by coproscoplc detection of proglottlda,
cop,o-antlgens, and eggs. The latt« an, morphologlcally
lndlatlngulahable from Echlnococcus eggs, but can be
ldentlffed by DNA analy188.
• Therapy and control. Prazlquantel and epslprantel
are effective ceetodlcldes for treatment of carnivores
(► Table 19.14). Control: prevent 8CC888 of dogs to
Q)
C raw viscera or muscles of slaughter or wild animals;
°[)
'6 strategic antlcestodlal treatments of dogs, Including
Q) Imported dogs. Control of T. taeniaeformls In free­
ccu ranging cats with frequent anthelmlntlc treatments
(see E. multifocularls, ► p. 251).
C species (e.g. horses, primates) and omnivores (pig) are
·c:: • Zoonotlc Importance. Infections of humans with
Q)
metacestodes of different Taenla species of carnivores
j are rare(► p. 511).
C wall, enter the liver via the portal vein, and migrate
>,
-
0)
0
0 into small cysticerci (small bladders, after 12 days
·u5
cu
0.
Agents and life cycles. The domestic dog is a host
of several Taenia species, of which the most important
are listed in ► Table 9.16. In contrast, in the domestic
cat, only one species (Taenia taeniaeformis) plays a
role. Taenia infections of the red fox and regionally of
other wild carnivores are of epidemiological interest.
The identification of species is based on different
morphological features, of which the number, shape
and size of scolex hooks as well as the structure of
proglottids and reproductive organs are important.
Many Taenia species can be identified by molecular
assnys. lntraspecific genetic variations may have practical
implications (see T. multiceps).
All Tae11in species of carnivores are parasites of the small
intestine. In principle, their life cycles correspond to
Tae11ia species of humans (► Figure 9.43). A carnivore
host can be infected with several specimens of the same
'fncnia species, but mixed infections with different Taenia
species or with other genera (Dipylidium, Echinococcus)
are also quite common. The metacestodes of the different
Taenia species, developing in intermediate hosts, belong
to various morphological types (cysticercus, coenurus,
strobilocercus) (► Table 9.14).
Taenia hydatigena
In the adult stage, 1: hydatigena is a parasite of dogs and
other can ids (► Figure 9.45a). Each tapeworm produces
a daily average of 2-6 proglottids, each with ~55,000
eggs. Depending on the infection intensity, a dog can
excrete up to 50 proglottids per day, of which about
½ are released without and 1/2 with defaecation. Eggs
(about 16% of all eggs produced) are already released
in the intestine and shed in the faeces; they originate
from uterine branches ruptured during detachment of
proglottids from the strobiln. However, the majority are
passed into the environment within proglottids. Regular
shedding of proglottids and eggs can persist for a long
time, but may be discontinued for irregular periods.
Intermediate hosts may acquire the infection by uptake
of entire proglottlds thus Ingesting large quantities of
eggs all at once. However, more frequent are weaker and
repeated infections with eggs that have been released
from proglottids or from faeces and then spread in the
environment.
Intermediate hosts for 'I: hydatigena are numerous
species of herbivores, especially sheep and goats,
but also cattle and wild ruminants. Other herbivore
susceptible. In the intermediate host, the oncospheres,
which hatched from the eggs, penetrate the intestinal
through the liver parenchyma, while transforming
about 2-3 mm long, after 20-25 days 6-9 mm). About
3 weeks p.i., they reach the subserous tissue of the
liver surface, where further development takes place.
 9. Phylum Platyhelminthes (flatworms)

Table 9.16. Taenia species (selection) of carnivores.

Species and length, Definitive hosts 1 and Natural Intermediate hosts, common Names of Infection• In
distribution (D) prepatency (p) namH and predilection altea of lntermedlilte haste
metaceatodea 1,2

Taenia hydatigena dog, fox, wolf, other canids. domestic and wild ruminants, pig, etc. visceral cysticercosis ctl
Length:50-250 crn (cat) Cysticercus tenuicollis g
>,
D: worldwide -- _e_:2=_9�ee�-- in_!!ially �ver, then abdominal cavity -- - .c.
a.
Taenia pisiformis dog, fox, wolf, (cat), etc. hare, rabbit, rodents visceral cyslicercosis 0
Length:35-155 crn p: 6 weeks Cysticercus plsiforrnis
u
D:worldwlde ---
Initially liver, then abdominal cavity ----
Taenia ovis 3 dog, fox, wolf sheep. goat , muscular cysticercosis

--
Length: 60-145 crn p: 6-8 weeks Cysticercus ovls
D:worldwide
--Striated
-- musculature
- -·- -
Taenia krabbei wolf, red fox, dog roe deer, red deer, fallow deer, reindeer, muscular cysticercosis
(syn.T. cerv1) p: no data moose
Length: 200-250 cm Cystlcercus tarandi
D: norti1ern hemisphere ---- --
striated musculature - - -- --
-
Taenia multiceps3 dog, fox, wolf, other canids, sheep, goat, cattle, buffalo, yak, wild cerebral and non-cerebral
(syn. Multiceps m.) hyena ruminants coenurosls
Length: 20-120 cm p: 5-6 weeks Coenurus cerebralls
D:worldwide CNS, connective tissue
Taenia serialis3 fox, wolf, (dog, cat) hare, rabbit, (rodents) coenurosis of connective
Length: 20-72 cm p: 5-6 weeks Coenurus serialis tissue
D: worldwide subcutaneous and intermuscular tissue
Taenia crassiceps3 fox, wolf, jackal, raccoon rodents, (moles) cyslicercosis of connective
Length: 10-22 cm dog (dog, cat) Cysticercus longicollis tissue and body cavities
D:northern hemisphere p: 4-6 weeks subcutaneous tissue, body cavities
Taenia polyacantha fox, wolf, raccoon dog (dog), rodents, lagomorphs. cysticercosis of body
Length:10-14 cm other canids Cystlcercus cavities
D: northern hemisphere p: no data initially liver, then body cavities
Taenia taeniaeformis cat, lynx, other felids rodents cysticercosis of the liver
.c.
Cl)
(syn. Hydatigera t,) (mustelids) Cysticercus (Strobilocercus) fasciolaris
Length: 15-60 cm p: 5-8 weeks liver c
D: worldwide .E
Q)
Taenia martis3 mustellds, wild cat rodents cysticercosis of body I
Length: up to 20 cm p: no data cavities, rarely CNS
D: northern hemisphere
1 Intestinal infections with adult stages, rare hosts in parentheses.
2 The names of the metacestodes are not in Italics, because they are common names and not the names of genera and species.
3 See below zoonotic importance,

Other cysticerci penetrate the liver capsule and settle
subsequently in the subserous tissue of the abdominal
cavity(omentum, mesentery), more rarely of the thoracic
cavity( ► Figure 9.45b, c). Within 6-8 weeks, p.i., the
development of fertile cysticerci is completed; these
are called Cysticercus tenuicollis. They are thin· walled,
semi-transparent, large bladders(up to 8 cm long) with a
the liver surface and further development in subserous
tissues(liver, mesentery, omentum). The metacestode
('pea-sized cyst', Cysticercus pisiformis) is infective
7-8 weeks p.i. In heavy infections, the cysticerci are
aggregated into grape-like conglomerates ( ► Figure
9.46). Prepatent period 6 weeks.
Q)
·u
C

long neck, containing a protoscolex and clear fluid. After Taenia ovis and Taenia krabbei '6
Q)
ingestion of fertile cysticerci by a susceptible definitive �
host, gravid tapeworms develop within 52-66 days. T. ovis is a parasite of the dog and wild canines. The �
metacestode, Cysticercus ovis, develops in cardiac and ctl
C
·;::
Taenia pisiformis skeletal muscles of sheep and goats ( ► Figure 9.47). Q)
Prepatent period of T. ovis 6-8 weeks. T. krabbei(syn.
Parasite of dogs and other canids, rarely also of cats(e.g. Taenia cervi) is transmitted in a wild-life cycle with _s:;
0.6% of 155 cats in DE). Development in the intermediate canines (wolf, red fox, dog) as definitive hosts and >,
Ol
host(hare, rabbit) in principle as in T. hydatigena: initial Cervidae as intermediate hosts. Muscle cysticerci of 0

migration of oncospheres and young cysticerci through this species have been found in roe deer, red deer, fallow .8
·u5
the liver, after about 2 weeks p.i. beginning migration to deer, reindeer, etc.
ctl
Q_
 Part Ill. Parasites and parasitoses: metazoa

Figure 9.45. (a) Taenia hydatigena: several, adult tapeworms (length 50-250 cm) in the intestine of a dog; (b) surface of lamb
liver with migration tracks, caused by migrating, young cysticerci; (c) mature cysticerci (Cyslicercus tenulcollis) (length of the
lower cyslicercus about 4 cm, diameter 2.5 cm) (Photo: a, b: IPZ; c: IPH).

metacestodes, which can reach diameters of >5 cm

( ► Figure 9.48). The metacestode, typically containing
numerous protoscoleces, is called Coenurus cerebralis.
Previously it was anticipated that oncospheres, having
invaded other organs, usually do not survive, and that
coenuri found in subcutaneous, intermuscular tissues
or in other locations are metacestodes of T. gaigeri.
However, recent ONA analyses suggest that r multiceps
and r gaigeri arc not distinct, but variants within a single
species. Therefore, it can be assumed that cerebral and
non-cerebral coenurosis might be caused by different
strains of T. multiceps. Metacestode infections have also
been reported from accidental hosts (e.g. dog, horse,
Figure 9.46. Conglomerate of cysticerci of Taen/a plsifarmls man), but the diagnosis should be regarded with caution
(Cysticercus plsiformis) (diameter of individual vesicles 5-7 ( ► p. 511). Prepatent period 5-6 weeks.
mm) (Photo: IPH).
Q)
C Taenia crassiceps and Taenia serialis
'[j
'6
Q) Taenia multiceps (syn. Multiceps multiceps) The most important definitive hosts of these species are
L
ccu foxes. In intermediate hosts (rodents), the metacestodes
C Parasite of dogs, foxes, wolves and other canids. The of T. crassiceps inhabit body cavities, subcutaneous tissues
·c
Q) most frequent natural intermediate hosts are domestic and also the brain. The metacestodes are small bladders
� ruminants (sheep, goats, cattle, buffalo, yak), and (2-4 mm), containing one protoscolex, and are capable of
C apparently less frequently wild ruminants, such as asexual reproduction by budding, resulting in numerous
>,
0) wild sheep and goats. Oncospheres, hatched from new cysticerci (e.g. 1,800 in a naturally infected Microtus
0 ingested eggs, are transported via the portal vein and arvalis). The metacestodes of r serialis, which develop
0
·u5 the bloodstream to the brain and less frequently to the in subcutaneous and intermuscular tissues of rabbits
cu spinal cord. After migration through meninges and and hares, are translucent coenuri of variable sizes,
cu
a.. nerve tissue, they develop in about 3 months into fertile sometimes with daughter bladders, containing clusters
 9. Phylum Platyhelminthes (flatworms)

Figure 9.47. Metacestodes (cysticerci) of Taen/a ovis (Cysticercus ovis): (a) living cysticercl in the diaphragm musculature of a
sheep (cysticercus diameter 4-5 mm); (b) dead cystlcercus in the heart muscle of a sheep (Photo: IPZ).

Figure 9.48. Coenurus cerebralis (metacestode of Taenia Figure 9.49. Coenurus serialis from subcutaneous tissue
multiceps) in the brain of a sheep (Photo: IPZ, P. Deplazes). of a rabbit: opened bladder with clusters of protoscoleces
(Photo: IPZ).
-
Cl)
.c
C

ofprotoscoleces. Occasionally, metacestode infections Taenia taeniaeformis (syn. Hydatigera

occur in accidental hosts(e.g. T. crassiceps: dog: subcutis;
man: brain, eye, subcutaneous, intermuscular tissue.
T. serialis: cat: brain; monkeys: muscle; man: brain).
Prepatent periods: T. serialis 5-6 weeks, T. crassiceps 4-6
we eks(► Figure 9.49).
Taenia polyacantha
.E
a5
taeniaeformis) I
Common parasite of domestic cats, wild cat, lynx, red
fox. Intermediate hosts are mice, rats, muskrats and
other rodents; the metacestode, Strobilocercus fasciolaris
(syn. Cysticercus fasciolaris) develops in the liver of
these hosts(► Figure 9.50). Prepatent period 5-8 weeks.

Parasite of red fox (very frequent in Europe), arctic

fox, raccoon dog, and wolf, rare in dogs. In the liver
of intermediate hosts (voles, muskrats), oncospheres
transform into small cysticerci, which pass to the
peritoneal cavity, where multiple, flattened, monocephalic
Q)
larvae (3-11 mm long) with pseudo-segmentation are
·u
C

formed by exogenous budding. These stages are found 'a

non-encysted in body cavities. Q)
�

Taenia martis
c
ro
C
·;:::
Q)
Parasite ofmustelids (Martes martes) (pine marten), M.
foina(stone marten), M. putorius(European polecat) and -�
wild cat. Intermediate hosts are rodents. Occasionally, >,
0)
metacestode infections occur in accidental hosts (e.g. Figure 9.50. Metacestode of Taenia taeniaeformis. Left: 0
0
abdominal cavity in Macaca tonkeana, Lemur catta: encapsulated metacestode in the liver of a vole; right: isolated
·wro
brain and eye in man). Strobilocercus (Cysticercus) fasciolaris (length about 33 mm)
ro
(Photo: IPZ, P. Deplazes). 0....
 Part Ill. Parasites and parasitoses: metazoa

Occurrence incidence in sheep of I% in Sardinia). In Greece,

• Canids. Worldwide, Taenia infections in dogs are
common in highly variable prevalences. In Europe,
T. hydatigena, T. pisiformis and T. ovis are regarded
as the most important species but recent and reliable
prevalence data are rare. In Albania, 2.7% of 111 dogs
in suburban areas were carriers of T. hydatigena. An
indirect prevalence indicator is the infection rate of
sheep with Cysticercus tenuicollis (e.g. 29.4% of 2,000
sheep in GR). Wild canines have to be considered
as potential infection sources of domestic and wild
ruminants. In Latvia, Italy, Portugal and Spain, 8-45%
of wolves were infected with T. hydatigena. T. ovis, a
,I t
fairly common parasite in countries with large sheep
and goat populations, is rare in Central Europe, but
it sporadically causes outbreaks of cysticercosis in
sheep, which can lead to significant economic losses in
individual flocks. The main definitive host is the dog,
but patent infections have been reported in foxes and
wolves. England claims annual losses of over£ 7 million
due to the condemnation of sheep carcasses interspersed
with Cysticercus ovis (epidemiology, see below). In
Canada 0.2 to I 9% of 133 farms suffered from such
condemnations between 2009 and 2011.
The metacestode of T. multiceps, known as Coenurus
cerebralis, is the causative agent of cerebral coenurosis,
predominantly affecting sheep, and to a lesser extent
cattle, yaks and goats. This infection is endemic in parts
of Asia, northern Africa, Middle East, and Europe. In
Jordan, 3.8% of dogs were infected with T. multiceps
and 3% (n: 451) of slaughtered sheep with Coenurus
cerebralis. In Latvia, 47% of wolves (n: 34) were infected
with T. multiceps. Southern Italy (Lazio, Apulia, Sicily,
Sardinia) is one of the European endemic areas (annual
symptoms of cerebral coenurosis were observed in 20%
of 57 investigated sheep flocks. Sporadic cases of cerebral
coenurosis in cattle and sheep have been reported
from various countries. For example, in Switzerland,
an outbreak of coenurosis occurred (2003) in a dairy
sheep flock, caused by a dog imported from Italy,
infected with T. multiceps. Non-cerebral coenurosis
has been observed, for example, in 1.74% of 17,223 goats
slaughtered in Dubai (2008).
In France, a recent study (using a multiplex PCR) has
shown that dogs (n: 817) from urban and peri-urban
areas, are rarely carriers of T. crassiceps (0.61%), T.
serialis (0.24%) and T. polyacantha (0.12%). In contrast,
prevalences in wild carnivores are high, as indicated
by data from Lithuania: 26.4% of foxes (n: 269) were
infected with T. crassiceps and 61.7 with T. polyacantha.
The corresponding infection rates in raccoon dogs (n:
85) were much lower (3.5% and 5.9%, respectively).
• Cats are frequently carriers of T. taeniaeformis
(e.g. CH and DE 22-36% of 454 necropsied cats; PT
3.1% ). In Switzerland, five rodent species were infected
with metacestodes (Strobilocercus fasciolaris), especially
common voles (Microtus arvalis 12% of 250) and water
voles (Arvicola sp. 11% of 894).
Epidemiology
• T. hydatigena and T. ovis. In regulating epide­
miological processes, several key factors play a role; these
have been studied in relation to T. hydatigena, T. ovis
and Echinococcus granulosus in New Zealand and are
shown in a simplified form in ► Table 9.17. Knowledge
of these factors led to the development of a mathematical

Table 9.17. Key factors in the epidemiology of Taenla hydatlgena and T. ovls in sheep.

Epldemlologlcal llgntftoanoe

Adult parasites: A few tapeworm carriers can

• Long life-span in the final host (1-5 years) sheet numerous Taenla eggs and
• High reproductive potential (about 15,000 to 100,000 8Q. s per roglottld),_____ contaminate the environment
Eggs In the environment: Eggs can be widely distributed in the
• Areal distribution (dispersion) of eggs by infected definitive hosts and further spreading environment and form an Infection
by flies, birds, inanimate factors (rain, floods, wind), or human activities reservoir
• Trampling and spread of dog faeces by grazing animals
• Considerable tenacity of eggs in sufficient humidity (at +20 °C approximately 2 months,
at lower temperatures longer, at +38 °c only 2-1O days, overwintering possible, but
high sensitMty to exsiccation)
Metacestodes in the Intermediate host: After slaughter of infected sheep
• Numerous metacestodes, each containing one protoscolex. can develop in their organs or muscles are potential
immunologically naive animals sources of infection for definitive
• A proportion of metacestodes remains infectious for several months hosts
Host factors: Immunity of intermediate hosts plays
• In definitive hosts, natural Taenia infections stimulate only weak immune responses a role in the regulation of the parasite
against reinfection (lower susceptibility, shorter patencies, reduced reproductive population
potential)
• Intermediate hosts can rapidly develop a more or less pronounced immunity, if they are
constantly exposed to infections
♦
model of epidemiology, which was very useful in the
assessment and monitoring of strategic control measures
against Taenia species and E. granulosus.
According to recent studies in England and Canada,
domestic dogs (farm dogs, guard dogs. pet dogs,
imported dogs) infected with T. ovis are sources of
infection for sheep. The potential epidemiological role
of wild carnivores (foxes, wolves, coyotes) is unclear,
but presumably not significant. Special risk factors are
feeding of raw organs of sheep to dogs and scavenging
of dogs on dead stock.
• Other Taenia species. The epidemiology of Twmia
species with life cycles including leporidae, rodents
and other small mammals as intermediute hosts, is
characterised by a predator-prey relationship. This
applies to T. serialis, T. crassiceps and ·1: polyacantha of
foxes and T. taeniaeformis of cats.
Pathogenesis and clinical signs. Intestinal Taenia
stages in a definitive host have little pathogenicity,
however, metacestodes can cause diseases in intermediate
and accidental hosts.
• Intestinal infections in definitive hosts. In
the small intestine of definitive hosts, Taenia species
can cause tissue changes (flattening, necrobiosis and
desquamation of the epithelium, cellular infiltration
of the mucosa, thickening of villi, increased mucus
production), but these are usually mild. Therefore, most
infections are asymptomatic. In some cases diarrhoea,
dehydration, emaciation, loss of appetite, abdominal
pain and other non-specific symptoms have been
associated with Taenia infections. Rarely, infections
with many Taenia specimens lead to intestinal occlusion.
• Parenteral infection of intermediate or
accidental hosts with metacestodes. In inter­
mediate or accidental hosts, metacestodes of some
Taenia species can cause various forms of cysticercosis
or coenurosis, associated with organ changes which are
described below.
Liver lesions. The migration of a few young larvae
of T. hydatigena or T. pisiformis through the
liver parenchyma of intermediate hosts remains
asymptomatic. However, after mass uptake of
oncospheres, the migrating larvae can cause in non­
immune animals serious, sometimes lethal changes
of traumatic hepatitis, similar to acute fasciolosis
(► Figure 9.45b). Predominant in the acute phase
are blood-filled, winding migration tracks - visible
on the liver surface and on liver sections -, as well
as blood loss into the liver parenchyma and the
peritoneal cavity. In migrating tracts, the elongated,
up to 9 mm long, glassy-like whitish cysticerci are
detectable. If the animals survive this phase, the
migrating tracts are gradually repaired by granulation
and connective tissue and eventually by scarring.
9. Phylum Platyhelminthes (flatworms)
Traumatic hepatitis, caused by 7: l1ydatige11<1, occurs
mainly in lambs, kids, piglets. fawns. usually in
isolated cases, but also heaped. Metacestodes of T.
pisiformis can induce similar changes in the liver of
hares and wild or domestic rabbits. The cherry-sized
metacestodes of T. tae11iaefor111is cause liver damage
in mice, which might. if heavily infected, become ;:g
>,
easier prey for cats. Usually. mature metacestodes of ..c
a.
T l1yde1tige11<1 in body cavities do not induce clinical
u
0
symptoms.
Lesions l.n muscles and connective tissue. Muscle
lesions are associated with •1: ovis cysticercosis in
sheep or goals ( ► Figure 9.47). Predilection sites
of the meluceslode cysts ure cardiac and skeletal
muscles. After experimental infection of sheep
with large numbers of eggs, inflammatory and
degenerative muscle changes and clinical symptoms
were observed (e.g. weakness, apathy, locomotory
disorders, fever, elevated serum levels of glutamate
dehydrogcnasc). In such cuses, migrating cysticcrci
can also occur in the brain. Viable cysts are similar
to that of 1: saginata, but they contain a protoscolex
with hooks. Cysticerci of T. ovis die off relatively
early after infection, and only a few survive longer.
Therefore, often dead, caseous or calcified muscle
lesions are found at slaughter.
Metacestodes of T. multiceps, regarded as causative
agents of non-cerebral coenurosis in goats and sheep
(see above), are located between muscles (legs, back,
diaphragm, abdomen) or attached to the abdominal
serosa, but usually not in the CNS. They can grow
to a large size and may cause lesions of muscles and
connective tissue. This applies also to metacestodes
of some other Taenia species. Examples include T.
crassiceps (subcutis, dog) and T. serialis (limb,
monkey).
Lesions in the CNS. In ruminants the predilection
site of Coenurus cerebralis, the metacestode of T.
11111/ticeps, is the brain, and less frequently the spinal
cord. Parasites, having invaded other sites, usually
die off. After migration in the meninges and the
brain, the metacestodes often establish near the brain
surface and transform to bladders of considerable
size (diameter >5 cm) ( ► Figure 9.48). After a long
incubation period, pathological changes in the CNS
can lead to cerebral coenurosis, associated with
Q)
clinical signs, such as apathy, loss of appetite, ataxia, C
·c::;
blindness, staggering gait, head tilt, circular motion '6
Q)
and other symptoms (common names of the disease �
'gid' or 'stagger'). Rarely, other animal species are c
affected by cerebral infections with metacestodes al
C
(example: T. serialis, cat; unidentified coenurus: ·.::
Q)
Nubian ibex).
C
Diagnosis. In recent years, considerable progress in >-
0)
the diagnosis of Taenia infections in carnivores has been 0
0
achieved with the introduction of new methods (see also ·u5
echinococcosis, ► p. 245).
C1J
Q.
 Part Ill. Parasites and parasitoses: metazoa
• Diagnosis in definitive hosts. In the living animal,
Taenia infections can be diagnosed by finding expelled
proglottids or eggs and by detecting specific copro­
antigens or copro-DNA; post mortem, the parasites can
be easily found in the intestine.
Detection of proglottids and eggs. Gravid
proglottids of Taenia species of dogs and cats
are about 7-12x3-4.5 mm long, usually longer
than wide and macroscopically visible. However,
the identification of the Taenia species based on
proglottid morphology is not possible. During
the patent period, Taenia eggs can be detected in
faecal samples using a flotation technique (flotation
solution with density of 1.3 or higher), or on the skin
(especially at the underside of tail and in the peri­
anal region) using the adhesive tape method ( ► p.
533) (sensitivity of flotation technique 60-80%, of
adhesive tape method a little higher).
Characteristics of Taenia eggs. Spherical, about 26-
4 l x24-45 µm, thick, radially striped embryophore,
with oncosphere ( ► Figure 16.16, p. 549). Since the
eggs of Taenia and Echinococws species cannot be
distinguished morphologically, they are collectively
referred to as 'taeniid eggs' in diagnostic reports.
However, eggs of Taenia and Echinococcus species
.. , can be differentiated by DNA analyses .
'
• Detection of copro-antigen and copro-DNA.
In the intestine of infected dogs, Taenia antigens (copro­
antigens) are released, which are detectable in the faecal
fluid by ELISA already in the prepatent period and later
during patency and postpatency. After elimination of the
Taenia tapeworms by therapy, copro-antigens excretion
in faeces ends within 5 days. Such tests have been
developed for T. hydatigena and other Taenia species,
but they are only used in a few specialised laboratories.
Another diagnostic option is the examination of faecal
samples for DNA which is contained in cestodes eggs
and parasite tissue (see also echinococcosis, ► p. 245).
Therapy and control. Drugs of choice for treating
intestinal Taenia infections are the highly effective and
well-tolerated cestodicides praziquantel (dogs and cats:
5.0 mg/kg b.w. p.o. or 5.7 mg/kg b.w. s.c.; cat 8 mg/kg b.w.
spot-on) or epsiprantel (dog: 5.5 mg/kg b.w. p.o., cat: 2.75
mg/kg b.w. p.o.) ( ► Table 19.14). In some commercial
(1)
preparations, these drugs are used in combination with
·o
C
'6 nematocides ( ► Table 19.15). Nitroscanate (in dogs) and
(1)
� some benzimidazoles (fenbendazole, flubendazole) are
� alternative taeniacidal drugs. Treatment of cysticercosis/
ro
C coenurosis in intermediate hosts with benzimidazoles
·c
(1) has a poor prognosis; surgical removal of coenuri from
j sheep brain may represent an alternative in some cases.
C Christodoulopoulos G, Kassab A, Theodoropoulos G (2013)
>, Preventive measures are of paramount importance in
CJ)
0
0 the control of taeniosis in dogs. Internal organs (liver,
'cii lung, etc.) or muscles of domestic and game animals
ro
ro
should only be fed to dogs after cooking or freezing
a.. (-18 °C, 3 days), and access of dogs to slaughter offal
and dead stock should be prevented. Measures against
pasture contamination with Taenia eggs include
regular examinations and anthelmintic treatments of
dogs (farm, guard and pet dogs), and cleaning up dog
faeces from the environment. Routine treatment of
all imported dogs with a highly effective cestodicide
is recommended or compulsory (in some countries),
because such animals are often carriers of Taenia spp. or
other tapeworms. Control programs in sheep breeding
areas have included mass treatments of dogs at intervals
of 6-8 weeks. However, Taenia species are much harder
to control than Echinococcus granulosus, mainly due to
their higher reproductive rates in definitive hosts ( ► p.
236). Sheep can be successfully vaccinated against T.
multiceps, as shown in a field trial in Sardinia. Control
of T. taeniaeformis in free-ranging privately owned
cats can be achieved by monthly treatment (see E.
multilocularis, ► p. 251).
Zoonotic importance. Rarely, Taenia species of
carnivores cause disease in humans, such as metacestodes
of T. crassiceps (brain, eye, subcutaneous and
intermuscular tissue), T. serialis (brain, intermuscular
tissue), T. multiceps or T. ovis (CNS) and T. martis (CNS,
r-i-----•
eyes).
Selected references
Allepuz A, Gabriel S, Dorny P, Napp S, Jansen F, Vilar MJ,
Vives L, Picart L, Ortuno A, Gutierrez J, Casal J (2012)
Comparison of bovine cysticercosis prevalence detected
by antigen ELISA and visual Inspection In the North East of
Spain. Res Vet Sci 92: 393-395.
Abo-Shehada MN, Jebreen E, Arab B, Mukbel R, Togerson
PR (2002) Prevalence of Taenia multiceps In sheep In northern
Jordan. Prev Vet Med; 55: 201-207.
Assana E, Kyngdon CT, Gauci CG (2010) Elimination of Taenia
solium transmission to pigs In a field trial of the vaccine
TSOL18 In Cameroon. Int J Parasitol 40: 515-519.
Brunet J, Passon B, Chermette R, Regnard P, Grimm F,
Deplazes P, Ferreira X, Sabou M, Pfaff AW, Abou-Bacar
A, Candolfl E (2014) First case of peritoneal cysticercosls in
a non-human primate host (Macaca tonkeana) due to Taenia
martis. Paraslt Vectors 7: 422.
Calvo-Artavia FF, Nielsen LR, Alban L (2013) Epldemlologic
and economic evaluation of risk-based meat inspection for
bovine cystlcercosis in Danish cattle. Prev Vet Med 108:
253-261.
Craig HL, Craig PS (2005) Heimlnth parasites of wolves (Canis
lupus): a species list and an analysis of published prevalence
studies in Nearctlc and Palaearctlc populations. J Helminthol
79: 95-103.
Occurrence of non-cerebral coenurosis in sheep. J Helminthol
87: 125-127.
♦,'
oeW olf BD, Peregrine AS, Jones-Bitton A, Jansen JT,
MacTavish J, Menzies Pl (2012) Distribution of. and risk
factors associated with, sheep carcass condemnations due
to Cysticercus ovis infection on Canadian sheep fanns. Vet
Parasitol 190: 434-441.
DeWolf BD, Poljak Z, Peregrine AS, Jones-Bitton A, Jansen
JT, Menzies Pl (2013) Development of a Taenia ovis
transmission model and an assessment of control strategies.
Vet Parasite! 198: 127-135.
Eichenberger RM, Karvountzis S, Ziadinov I, Deplazes P
(2011) Severe Taenia ovis outbreak in a sheep flock in south­
west England. Vet Rec 168: 619.
Eichenberger RM, Lewis F, Gabrlil S, Dorny P, Torgerson
PR, Deplazes P (2013) Multi-test analysis and model-based
estimation of the prevalence of Taenla saginata cysticercus
infection in naturally Infected dairy cows In the absence of a
'gold standard' reference test. Int J Parasltol 43: 853-859.
Fabiani S, Bruschi F (2013) Neurocystlcercosls In Europe: still
a public health concern not only for Imported cases. Acta
Trop 128: 18-26.
Alsser A, Craig P, Ito A. 2011Cysticerosls and taenlosls: Taenia
solium, Taenia saginata and Taenia asiatlca. In: Palmer SR,
Lord Soulsby, Torgerson PR, Brown DWG (eds.): Oxford
Textbook of Zoonoses. 2nd ed, Oxford, UK: Oxford University
Press;: 625-642. ISBN 978-0-19-857002-8.
F liitsch F, Heinzmann D, Mathis A, Hertzberg H, Stephan
R, Deplazes P (2008) Case-control study to identify risk
factors for bovine cysticercosis on farms in Switzerland.
Parasitology 135: 641-646.
Lavikainen A, Haukisalml V, Lehtinen MJ, Henttonen H,
Oksanen A, Meri S (2008) A phylogeny of members of the
family based on the mitochondrial cox1 Taeniidae and nad1
genetic data. Parasitology 135: 1457-1467.
Lightowlers MW (2012) Cysticercosis and Echlnococcosis.
Curr Top Microbial lmmunol 365: 315-335.
Loos-Frank B (2000) An up-date of Verster's (1969) 'Taxonomic
revision of the genus Taenia Linnaeus' (Cestoda) in table
format. Syst Parasitol 45: 155-183.
Priemer J, Krone O, Schuster R (2002) Taenia krabbei
(Cestoda: Cyclophyllidea) In Germany and Its delimitation
from T. ovis. Zool Anz 241: 333-337.
McFadden AM, Heath DD, Morley CM, Dorny P (2011)
Investigation of an outbreak of Taenia saginata cysts
(cysticercus bovis) in dairy cattle from two farms. Vet Parasltol
176: 177-184.
Michelet L, Fleury A, Sciutto E, Kendjo E, Fragoso G, Paris
L, Bouteille B (2011) Human neurocysticercosis: comparison
of different diagnostic tests using cerebrospinal fluid. J Clin
Microbial 49: 195-200.
MurrelKD (ed.) (2005) WHO/FAO/OIE Guidelines for Surveillance,
Prevention and Control of Taeniosis/cysticercosis. Paris,
France: World Organization for Animal Health; ISBN. 92-
9044-656-0.
Nakao M, Lavikainen A, lwaki T, Haukisalmi V, Konyaev
S, Oku Y, Okamoto M, Ito A.(2013) Molecular phylogeny
of the genus Taenia (Cestoda: Taeniidae): proposals for the
resurrection of Hydatigera Lamarck, 1816 and the creation
of a new genus Versteria. Int J Parasitol 43: 427-437.
9. Phylum Platyhelminthes (flatworms)
Oryan A, Nazifl S, Sharifiyazdl H, Ahmadnla S (2010)
Pathological. molecular. and biochemical characterization
of Coenurus gaigeri in Iranian native goats. J Parasitol 96:
961-967.
Oryan A, Akbari M, Moazeni M, Amrabadi OR (2014) Cerebral
and non-cerebral coenurosis in small ruminants. Trap Biomed ro
:g
31: 1-16. >,
Scala A, Cancedda GM, Varcasia A, Liglos C, Genchl C .s:::
a.
(2007) A survey of Taenia multiceps coenurosis in Sardinian 0
sheep. Vet Parasitol 143: 294-298.
Scandrett B, Parker S, Forbes L, Gajadhar A, Dekumyoy P,
Waikagu1 J, Haines D (2009) Distribution of Taenla saglnata
cysticercl in tissues of experimentally infected cattle. Vet
Parasitol 164: 223-231.
Schuster RK, Sivakumar S, W leckowsky T (2010) Non­
corebral coem1rosls In goats. Parasltol Res 107: 721-726.
Trachsel D, Deplozee P, Mathis A (2007) Identification of
taenlld eggs In tho faeces from carnivores based on multiplex
PCR using targets in mitochondrial DNA. Parasitology 134:
911-920.
Genus Echinococcus
Disease: Intestinal and extra-Intestinal
echinococcosis. 11
£chinos (G): hedgehog, spine; k6kkos (G): berry, grain. rn
.s:::
Summary .E
Q)
• Agents. E. granulosus s.l. (worldwide) and E. I
multllocularls(northern hemisphere: North America,
Eurasia) are the most Important members of the
genus Echlnococcus. The taxon E. granulosus s.l.
comprises several species - Including one or more
strains/genotypes - that differ In host specificity,
development, morphology, geographical distribution
and other features. The status of some of these species
Is currently controversially discussed. The adult stages
of all Ech/nococcus species are only a few millimetres
long and Inhabit the small Intestine of carnivores.
• Life cycle, epidemiology. The life-cycles o f
Ech/nococcus species are Indirect a n d similar t o
that of Taenla spp., but they differ regarding final
and Intermediate host assemblages and other
characteristics.
- E. granu/osus s.l. is a term for several closely related
species(► Table 9.18). Definitive hosts are dogs,
other canids and the lion. Metacestodes develop in
internal organs of natural intermediate hosts(sheep,
other ruminants, pigs, horses, etc.) or accidental
hosts (mammals, humans) causing an infection,
called cystic echinococcosis (CE), Humans have
been found infected with almost all species of E.
granu/osus s.l., but most cases of CE are caused by
E. granu/osus s.s. (sheep strain). This species has
both wild-life and domestic cycles, the latter being
of special zoonotlc significance.
y
 Part Ill. Parasites and parasitoses: metazoa
- E. multi/ocu/srls is predominantly transmitted In
a wild-life cycle Involving wild carnivores (red fox,
arctic fox, raccoon dog, wolf, coyote) as definitive
hosts and small mammals (usually rodents) as
Intermediate hosts. In recent years, fox-rodent cycles
have been documented in urban areas of several
countries. Domestic dogs and cats may be involved
in a synanthroplc cycle, If they prey on rodents.
The metacestode stage, developing In accidental
hosts (man, pig, monkey, dog, etc.), Is the causative
agent of alveolar echinococcosls (AE}, In humans
a mostly lethal disease, If left untreated.
Distribution. Species of the E. granulosus a.I. have a
world-wide distribution or are more confined to certain
areas. E. multilocularls Is endemic In large regions of
the northern hemisphere, Including many European
countries.
• Pathogenlclty, cllnlcal slgna. The Infection of definitive
hosts with Intestinal stages of Echlnococcus species
Is harmless. Metaceatodes of species belonging to
E. granulosus s.l. are typlcally fluid-filled, large cyata
with expansive growth. They rarely induce symptoms
In natural Intermediate hosts, but may cause severe
disease In humans (CE: cystic echinococcosls of llver,
lung, bones, brain, etc.). Due to an lnflHratlve type of
growth, metacestodea of E. multilocu/arls In humans or
other accidental hosts behave like malignant tumours
and can cause severe llver disease with metastasis
formation In other organs (AE: alveolar echlnococcls).
• Diagnosis. Intestinal Infections In living definitive
hosts are diagnosed by coproscoplc detection of
Echlnococcus eggs (further characterised by ONA
analyses), and parasite antigens or DNA in faecal
samples. Occasionally, proglottlds can be found in
faecal samples. Special techniques are employed
for discovering the small parasites In the Intestine
at necropsy. For work with Infected definitive hosts,
their lntntlnes, faecal or other material, posslbly
contaminated with Echlnococcu, eggs, special safety
precautions are required, because of the Infection
risk for humane ( ► p. 534). Metecestodes In living
lntermedlate or accidental hosts (humans, monkeys,
dogl, etc.) .. ua,ally diagnosed by Imaging techniques,
In combination with the detection of 1peclflc serum
antibodlN. lmmunohlstology or DNA analyses ant uled
for the examination of blopay material.
• Thenlpy, PNVentlon and control. Prazlquantel and
epslprantel are highly effective against Immature
and matute lnteetlnal stagee of E. granulosus and E.
multilocularls (for details, see below: prevention and
control).
• Zoonotlc Importance. Due to their high pathogenic
potential, CE and AE belong to the most Important
helmlnthlc zoonoses.
C The genus Echinococcus (family Taeniidae) includes
>-
0')
several species and genotypes/strains, whose adult stages
0 are only a few millimetres long; they inhabit the small
0
·enco intestine of carnivores ( ► Table 9.18). Their significance
is attributable to the fact that most species are infectious
co
a.. to humans and can cause severe or even lethal diseases.
Furthermore, infections oflivestock with metacestodes
of E. granulosus s.l. are associated with economic losses.
Here, Echinococcus granulosus s.s. and E. multilocularis
are predominantly considered, as they are the most
important agents.
Echinococcus granulosus s.s. (dangerous dog
tapeworm, dwarf dog tapeworm) and related
species
Disease: Intestinal echinococcosls in dogs and other
carnivores and cystic echlnococcosls (CE)
in Intermediate hosts, humans and other
accidental hosts. I
Echi110s (G): hedgehog, spine; k6kkos (G): berry, grain;
gram1losus (L): grainy. According to R. Leuckart the
genus name Echinococcus refers to the hook-bearing
protoscoleces of the metacestode; the species name is
related to the granular appearance of brood capsules on
the germinal layer of the mctacestode.
Agent. E. granulosus s.s. is a 1-7 mm long tapeworm
with scolcx (4 suckers and rostellum with two rows of
hooks) and typically 3 (2-6) proglottids ( ► Figure 9.5 I
and 9.55). Important features arc the position of the
genital pore near (mostly posterior) to the middle of
the gravid proglottid, uterus with lateral sacculations,
containing about 600 eggs on average. Eggs: diameter
30-40 µm, morphologically indistinguishable from eggs
of other Echinococcus and Taenia species. Further species
of the E. granulosus group are listed in ► Table 9. I 8.
Life cycle. The most important definitive host of
all species within the E. granulosus s.l. group is the
dog; regionally, wild carnivores (Canidac, Hyaenidae)
can play a role. An exception is E. felidis with a fetid
carnivore, the lion, as definitive host (hyenas arc also
carriers of this species). Herbivorous and omnivorous
mammals, predominantly domestic animals, net as
intermediate hosts; in some areas also wild animals. as
indicated in ► Table 9. I 8 nncl ► Figure 9.53.
In the small Intestine of deflnitlve hosts, the adults of
£. grmw/0s11s s.s. live about 6 months. with only a fow
lasting almost 2 years. Eggs arc released from gravid
proglottids in the intestine and excreted in faeces, or
they arc shed within proglottids to the environment
( ► Figure 9.52). Intermediate hosts, humans and other
accidental hosts become infected by ingestion of eggs.
In the small intestine, the oncospheres hatch from the
eggs, penetrate the intestinal wall, invade blood vessels
and are transported in the bloodstream. Initially. the
oncospheres transform into small bladders, which
gradually develop to the metacestode stage mainly in
the liver, less frequently in the lungs and other organs.
., 9. Phylum Platyhelminthes ( flatworms)

Table 9.18. Echinococcus species, E. granulosus strains and genotypes (G) (also► Figure 9.53).

Species, strains and genotypes (G) Definitive hosts (DH), Intermediate (IH) and Disease in humans and
L: length1 P: typical number of accidental (AH) hosts of metacestodes predilection sites of
proglottlds, D: distribution metacestodes
--
E. granulosus s.l. L: 2-7 mm, P: 3 co
Echinococcus granulosus s.s. DH: dog, other canids (dingo, fox. jackal. etc.)
-
cystic echinococcosis (CE)
;g
>,
(sheep strain G1-G3) IH: sheep, cattle. buflalo, goat, yak, camel. liver, lung. other organs ..c
0.
D: Worldwide macropods, etc. 0
AH: man. many species of other mammals TI

Echinococcus equinus DH: dog human cases not known

(horse strain G4) IH: horse, donkey, zebra
D: Europe, North and South Africa, AH: lemur (primate)
Middle East, USA 1
Echinococcus ortleppi DH: dog cystic echlnococcosis (CE)
(cattle strain GS) IH: cattle, buffalo, sheep, goat lung, liver
D: Europe, Asia, Africa, Central and AH: man
South America
Echinococcus intermedius DH: dog cystic echlnococcosis (CE)
• camel strain G6 IH: camel, cattle, sheep, goat liver, lung
D: Africa, Asia, South America AH: man
• pig strain G7 DH: dog,
D: Focally worldwide IH: pig, wild boar, (cattle)
AH: man -.
Echinococcus canadensis2 DH: wolf, dog
(cervid strains GB, G10) IH: cervids (moose, reindeer, wapiti)
D: northern America and Eurasia AH: man
(subarctic and boreal)
Echinococcus felidis DH: lion, hyena human cases not known
D: Africa IH: warthog, presumably other wild animals
Other Echinococcus species
Echinococcus multllocularis DH: red and arctic fox, wolf, raccoon, jackal, alveolar echlnococcosls ( AE) en
L: 1.2-4.5 mm; P: 5 coyote, dog, (cat) primarily liver, secondarily other ..c:
D: northern hemisphere: Alaska,
USA, Asia, Europe (see text)
IH: rodents (common vole, water vole, muskrat) organs
and other small mammals .E
a5
AH: man, monkeys, horse, pig, dog, etc. I
Echinococcus vogeli DH: bush dog (Speothos venaticus) polycystlc echinococcosis (PE)
L: 3.9-5.6 mm; P: 3 IH: rodents (paca, agouti) liver, lung, other organs
D: Central and South America AH: man

Echinococcus oligarthrus DH: wild fellds (puma, jaguar, etc.) unlcystic echinococcosis (UE)
L: 2.2-2.9 mm; P: 3 IH: rodents (agouti, cotton rat, paca) musculature, skin, orbita, internal
D: Central and South America AH: man organs
Echinococcus shiquicus DH: Tibetan fox (Vuipes ferrilata) human cases not known
L: 1.3-1.7 mm; P: 3 IH: plka (Ochotona curzoniae)
D: Tibetan plateau
1 Usually sporadic distribution.
2 Recently, the name E. canadensis was proposed for G10 and E. borea/1s for GB. The validity of G9 has been questioned.

The metacestode stage of E. granulosus s.s. and related
species, named hydatid or hydatid cyst (hydatis, [G]:
water bladder) is typically a single- or multi-chambered
bladder filled with antigen-containing fluid. The wall of
the bladder is composed of an inner cellular germinal
layer and an outer, acellular laminated layer, surrounded
by connective tissue of host origin (► Table 9.14;
► Figure 9.52). A few months p.i., the germinal layer
produces brood capsules (diameter 250-1,500 µm), each
containing up to 30 protoscoleces. The protoscolex is
equipped with 4 suckers and a rostellum with double
row of hooks. If the thin brood capsule walls rupture,
protoscoleces are released into the hydatid fluid; they
are then components of the so-called 'hydatid sand',
together with remnants of brood capsules and calcareous
corpuscles. Cysts with mature protoscoleces are called
fertile, while the others are sterile.
Size, shape and numbers of cysts depend on their age,
organ localisation, host species, and other factors. The
cyst diameter can vary between about 1 mm and 20
cm. Large cysts (mother cysts) sometimes contain
smaller cysts (daughter cysts). Both in the natural
intermediate hosts and in humans or other accidental
Part Ill. Parasites and parasitoses: metazoa
Figure 9.51. Echinococcus granu/osus in the Intestine of a dog: (a) aspect of small intestinal mucosa with adult specimens of
E. granu/osus (length 4-6 mm); (b) histological section through the small intestine with sections of E. granu/osus. The picture
shows the deep insertion of the parasite between the villi (Photo IPZ, J. Eckert).
hosts, metacestodes of the E. granulosus group develop
predominantly in the liver and lung, less frequently in
other organs(including spleen, kidney, heart, CNS, eye,
muscle, bone) and in body cavities( ► Figure 9.54). In
slaughter animals, cysts are almost exclusively located
in organs of the abdominal and thoracic cavity. The
predilection sites of cysts may differ, depending on
the intermediate host and Echinococcus species; for
example, metacestodes of E. granu/osus s.s. develop
preferentially in the liver of sheep, but cysts of E. ortleppi
are predominantly found in the lung of cattle.
Outside of the animal body, protoscoleces in cysts
survive about 2 weeks at+ 1-10 °C and I week at +20 °C.
This is favourable for transmission. The life cycle is
closed when susceptible carnivores consume slaughter
offal, carcasses or prey, containing fertile metacestodes.
In the host's small intestine, protoscoleces develop to
sexually mature stages within a few weeks p.i. Depending
on the Echinococcus species, the prepatent period varies
between 34 and 58 days(about 5-8 weeks).
Occurrence. £. granulosus s.s. has a cosmopolitan
distribution and is particularly common in areas
with sheep and livestock practices in Eurasia, Africa,
Middle East, South America, Australia and elsewhere.
In Europe, some countries of the Mediterranean region
are especially affected(e.g. prevalence in dogs: TR up to
40%, Sardinia 16-20%; metacestode prevalences in sheep:
20-75 in IT, up to 39 in GR). In contrast, E. granu/osus
s.s. is rare in northern and Central Europe. For example,
in Germany, Austria and Switzerland dogs are only
sporadically infected, and the prevalence of metacestodes
in slaughter animals is very low. Dogs imported from
endemic areas should be regarded as potentially infected
with Echinococcus. In Central Europe, human cases
of CE are continuously diagnosed, but the majority
is imported, mainly from Mediterranean countries.
Information on the distribution of other species of the
E. granulosus group is presented in ► Table 9.18.
Epidemiology. E. gram1/osus s.l. is transmilled both
in wild-life and domestic cycles( ► Figure 9.53). The
persistence of the latter is favoured by several factors,
such as large dog and sheep populations, access of
dogs to slaughter offal or carcasses of fallen livestock,
lack of anthelminthic dog treatments, and low level
of education of the public. Therefore, domestic cycles
pose a special infection risk to humans. Natural
intermediate and accidental hosts acquire the infection
by ingestion of Echinococcus eggs via contaminated food
or drinking water. In humans, also the direct contact
with Echinococcus carriers or their faeces may result
in an infection (e.g. eggs adhering to the body surface
of dogs -+ hands -+ mouth). In a moist environment,
Echinococcus eggs remain viable a few weeks or months,
depending on the ambient temperature. In the European
climate, they can survive the winter period, but they
die quickly at dehydration and higher temperatures.
The eggs can be killed by heat(75- I 00 °C) in a few
minutes and by freezing at -80 °C within 48 h; common
chemical disinfectants are ineffective( ► p. 571 ). In the
epidemiology of E. granulosus s.s. similar key factors
play a role as in T. hydatigena/T. ovis, but there are
 9. Phylum Platyhelminthes (flatworms)

g
>,
..c
a.
0
u

Adult tapeworm

Cattle lung
with cysts
�
Gravid
proglottfd
�

Cattle as typical and sheep

as accidental intermediate hosts --(DJ
/ -?.rs
BK I�

Mar:i as accidental
Cyst with brood Diagram of cyst wall
host of metacestodes
capsules (see legend)

Figure 9.52. Life cycle of Echinococcus ortleppi with cattle as typical and sheep as occasional intermediate hosts. Insert:
Diagram of the cyst wall: 1. host tissue, 2. connective tissue and hyaline intermediate zone, 3. laminated layer of the parasite
without nuclei, 4. nucleated germinal layer of the parasite; BK: brood capsule, PS: protoscolex (Graphics: IPZ, S. Ehrat).

important differences. Thus, in sheep populations of of the individual tapeworms, the parasite is capable
highly endemic regions, an age-dependent increase of maintaining a species-sustaining biotic potential
Cl)
in prevalences of Echinococcus cysts and numbers ( ► Glossary, p. 620), because large egg numbers are C

of protoscoleces was observed, indicating that these produced in case of multiple or massive infections
·o
'6
Cl)
intermediate host populations did not develop sufficient of definitive hosts, and numerous protoscoleces are �
immunity. Naturally infected dogs are predominantly formed by asexual reproduction in metacestode cysts �
Ctl
infected with less than 100 E. granulosus specimens, within intermediate hosts. In addition, the long lifetime C
with a few harbouring higher worm burdens (up to of metacestodes in intermediate hosts plays a role. -�
100,000). Differences in the infection dose, the age of Therefore, intermediate hosts have to be included in j
the worm population and probably also the susceptibility control programs (see control). C
and immunity of the hosts are made responsible for this >,
Ol
variability (see also immunology). Pathogenesis and clinical signs. While the 0

intestinal stages of E. granulosus are barely pathogenic, ·u5

Ctl
Proglottids of E. granulosus s.s. contain an average metacestodes can cause severe organ damage.
of about 600 eggs. Despite the low egg production 0....
 Part Ill. Parasites and parasitoses: metazoa

( E granuiosus

E. ortleppi

)
( E. equinus

Figure 9.53 Species of the Echlnococcus granulosus group: life cycles and their lnfectlvlty for humans (arrows) (Graphics: IPZ,
A. Seeger; adapted from J. Eckert and R.C.A Thompson 1997). E. canadensls Includes the genotypes GB and G10: recently a
species status was proposed for these genotypes (E. canadesn/s and E. borea/1s).

• Definitive host (dog). Species of E. granu/osus
s.l. inhabit preferentially the anterior half of the small
intestine and are attached with the scolex to the mucosa
deeply inserted into the crypts of Lieberkiihn between
Q)
the villi, and cause only minor changes (flattening or
·o
C
tissue as well as reactive, partly immune-mediated
inflammatory processes are known as pathogenic
factors. Cysts can rupture spontaneously or under
external influence (e.g. by external forces) and cause
allergic reactions. Infections in cattle, sheep, pigs,

'5 damage to the epithelium, mild cellular infiltration of etc. are mostly asymptomatic and therefore remain
Q)
the mucosa, increased mucus production). Therefore, undetected in living animals. In individual cases, clinical
�
cro the infection is usually asymptomatic, even in heavy
infections ( ► Figure 9.5 I ).
symptoms have been described, e.g. in horses massively
infected with cysts: disorders of liver and lung function,
C
·;::
Q) hypergammaglobulinaemia, symptoms of chronic
• Natural intermediate hosts. The pathogenicity obstructive pulmonary disease, colic, loss of appetite,
£ of metacestodes in natural intermediate hosts depends emaciation and reduced performance ( ► Figure 9.54b).
>,
Ol
on the organ and tissue localisation of the cysts,
0 their number, size and growth rate, and also on their • Accidental hosts of metacestodes. In
·u5
interactions with adjacent structures (e.g. bile ducts, humans, cystic echinococcosis remains initially and
ro blood vessels) and tissues. Especially the expansive in a proportion of cases permanently asymptomatic
ro
CL growth of the cysts, the compression of surrounding (up to >30%), especially when only small, well
..
Figure 9.54. Metacestodes of Echlnococcus granulosus s.l.: (a) single cyst In the lung of cattle: brood capsules (arrow) are
visible through the thin cyst wall; (b) cysts (diameter up to 1 O cm) In the liver of a horse (Photos: IPZ).
encapsulated, or calcified cysts are present. Symptoms
can occur after months or years, if one or more cysts
af fect organ functions due to their size, expansive
growth and localisation. The symptoms are variable,
corresponding to different organ localisations of the
cysts; most common are liver and lung symptoms. Latent
or apparent infections with cysts of E. granulosus s.l. have
been described in several accidental animal hosts, e.g.
in monkeys, rarely in cats.
Immunology. There is evidence from endemic areas that
dogs develop a partial immunity if heavily exposed to the
infection. Indicative are higher infection prevalences and
intensities of E. granulosus in young animals compared
to older animals. After experimental infection with E.
granulosus in dogs, systemic and local(mucosa), Peyer's
plates) cellular and humoral immune responses are
detectable. However, correlations between the infection
intensity or the state of development of intestinal stages
of the parasite and the measurable immune responses
(antibodies, T-cell proliferation, cytokine production)
were not seen in previous studies. Furthermore, several
re-infection studies and vaccination experiments have
not provided clear evidence of acquired protective
immunity in the canine host.
In the serum of infected dogs, antibodies are detectable,
which are directed against antigens of oncospheres,
protoscoleces or adult stages. Antibodies against
oncospheres are formed when the latter hatch in the
dog's intestine from the egg envelopes and penetrate
the intestinal wall. The detection of specific antibodies
in dogs and other definitive hosts is diagnostically
not useful due to lack of sensitivity and specificity. In
contrast, copro-antigens produced by the intestinal
stages and excreted in the faeces are valuable diagnostic
indicators(see below).
Similar to Taenia species, natural or experimental
infections with E. granulosus eggs stimulate immune
responses in intermediate hosts. In analogy to Taenia
species it has been assumed that in highly endemic
9. Phylum Platyhelminthes (flatworms)
(1j
;g
>­
.c
0.
0
u
areas sheep populations acquire an immune status that
can significantly limit the parasite population (i.e. the
development of cysts). Some recent studies support this
assumption, but further studies are necessary.
Immunisation of sheep and cattle with a recombinant
E. granulosus antigen(Eg95) induced a protective effect
of approximately 98%(measured by reduction of cyst
numbers as compared to non-immunised controls). The
immune protection persists without re-infection for 6
months on a fairly high level (approximately 80%). In
the course of the infection, intermediate and accidental
hosts produce circulating antibodies.
Diagnosis. Diagnostic methods are similar to those
used for Taenia spp. Differential diagnosis has to consider
mixed infections with one or more cestode species
(e.g. 1'aenia and Echinococcus species). Because of the
infection risk of people during diagnostic examinations,
special safety measures are required(► p. 534).
• Detection of E. granulosus s.l. in dogs.
Proglottids are small, 0.6-3 111111 long, whitish structures,
which can be found mainly in heavily infected dogs
on the perianal skin or on the surface of deposited
faeces. Faecal samples should be suspended in water
and thoroughly examined in thin layers. However, the
diagnostic sensitivity of this procedure is very low.
Coproscopic detection of eggs by flotation or
(I)
adhesive tape techniques. Methodology and
·u
C
sensitivity: see Taenia, ► p. 522. Eggs of E. granulosus '6
s.l. are distinguishable from E. multilocularis and (I)
�
Taenia eggs by DNA analyses.
Diagnostic deworming. Previously, dogs were
c
(1j
C
treated with arecoline preparations to induce ·c
J
(I)
defaecation and expulsion of cestodes. This
procedure, called 'diagnostic deworming: can now be -�
replaced by copra-antigen or copro-DNA detection. >,
Ol
Copra-antigen and copro-DNA detection. For 0
0
principles, see Taenia, ► p. 522, and E. multilocularis, 'ui
► p. 522. Antigen detection: mean sensitivity
ctl
65-80%, but >90% in dogs infected with >100 E. CL
 Part Ill. Parasites and parasitoses: metazoa
granulosus per animal. Specificity (with respect
to protozoa, nematodes and Taenia species) high
(>95%). DNA-detection: see E. multilocularis.
Necropsy. Because of its small size(usually 1-7 mm
in length) E. granulosus can easily be overlooked
at necropsy of definitive hosts, especially in
light infections. For a reliable diagnosis, special
procedures are required, such as the stereo­
microscopic examination of parts of the small
intestine, of several smears of the intestinal mucosa
or better of the sediment obtained from the washing
fluid of the intestine( ► p. 534). For identification
and differential diagnosis of E. granulosus and E.
multilocularis ► Figure 9.55.
• Detection of E. granulosus metacestodes in
natural intermediate hosts. In a recent study with
Sardinian sheep hepatic and lung cysts(diameter~ 1-6
cm) could be detected intra vitam with high reliability
(sensitivity 89%, specificity of 76%) using modern
ultrasound technology (high resolution microconvex
transducer). False positive images were due to cysts of T.
hydatigena. Since this diagnostic procedure is practical
and as efficient as the best current serological techniques
for antibody detection it appears to be suitable for
diagnosing CE in sheep and goats.
b
Length: upto 7 mm up to 4.5 mm
Number of
progJottids: 3 (2-6) 4-5 (2-6)
Genital pore near (usually posterior) anterior to middle
(arrow): to middle
Uterus: with lateral sad<-hke
protrusions
Figure 9.55. Differential diagnosis of adult stages of (a)
Echinococcus granulosus and (b) Echinococcus multilocularis
(Graphics: IPZ).
• Examination of slaughter animals (sheep,
cattle, pigs, etc.). Inspection ofliver, lung(palpation!),
spleen, and other visceral organs. Metacestodes are
often quite striking as rounded, about I to > 10 cm large
cysts. Small and solitary cysts can easily be overlooked,
especially in the deeper parts of the lung tissue or the
liver( ► Figure 9.54a). Dead and degenerating cysts are
often difficult to distinguish from similar lesions, caused
for example by T. hydatigena metacestodes(differential
diagnosis in special cases by histological examination
or DNA analyses).
• Diagnosis of cystic echinococcosis (CE) in
accidental hosts. Depending on the host species,
imaging techniques (US, CT, X-ray) or serological
methods can be used for antibody detection in suspected
cases, such as in monkeys or horses. For diagnosis in
humans, see below.
Therapy. Only highly efficient cestodicides should
be used for chemotherapy of£. granulosus infections
in dogs, such as praziquantel (5 mg/kg b.w. p.o. or 5.7
mg/kg i.m., not s.c.) or epsiprantel(5.5 mg/kg b.w. p.o.).
For details see£. multilocularis ► p. 251. Chemotherapy
of intermediate hosts is not indicated for economic
reasons and because of the low effect of the medication.
Control and prevention. In several countries with
high prevalence of£. granu/osus s.s. in dogs and high
incidence of CE in humans (New Zealand, Cyprus,
Spain, Argentina, Chile, Uruguay and others), control
programs have been performed or initiated in recent
decades, which included the following measures, based
on specific legislation: (a) strict control of animal
slaughter and proper disposal of slaughter offal, (b)
control of the dog population(registration) and reducing
the number of stray dogs, (c) mass treatment of dogs
with praziquantel at intervals of usually 6 weeks and
(d) education of the public. Monitoring programms for
obtaining epidemiological base-line data (e.g. prevalence
of E. granulosus in dogs. sheep and humans), and
information on control progress were included. Overall,
such control programs are very costly, the process takes
in the best case 10- I5 years, but mostly much longer,
until prevalences of£. granulosus in definitive and
intermediate host populations have reached low levels
(around I%). Therefore, new control approaches are
needed. One option is the inclusion of vaccination in
control programs. Model calculations have shown that
integrated control programs which include vaccination
of sheep(see immunology) and the elimination of older
sheep (which as cysts carriers harbour the major part
of the parasite mass) could significantly reduce the
duration of eradication programs. A vaccine (EG95)
for control of cystic echinococcosis is registered in
Argentina(► p. 569).
 9. Phylum Platyhelminthes (flatworms)

In endemic areas, dog owners are strongly advised not
to feed dogs with raw offal (especially liver and lung)
from slaughter or wild animals, but to cook the organs
beforehand or to freeze them for at least 3 days at -18 °C.
This recommendation also applies to slaughter animals
without evidence of echinococcus cysts. Experience from
values(>40 cases/100,000) in other endemic areas(e.g.
regionally in South America, China).
Echinococcus multilocularis (dangerous fox
tapeworm)
Ctl

recent years shows that the import of dogs from endemic ;g

>­
areas(e.g. from Mediterranean countries) is associated Disease: Intestinal echlnococoosls In carnivores and .c:
0..
with a risk of importing E. granulosus. Therefore, it is alVeolar echlnocoooosls (AE) In humans 0
13
recommended(mandatory in some countries!) to treat and other hosts.
imported dogs with a highly effective cestodicide.

Zoonotic importance. Cystic echinococcosis(CE) Echinococcus: see E. granulosus; multilocularis: multus

in humans, caused by species of the E. granulosus group, (L): much, many; loculus(L): capsule, chamber. Refers
is characterised by the infection of internal organs to the multilocular, spongy structure of the metacestode.
(liver, lung, spleen, bone, CNS, etc.) with metacestode
cysts. The diagnosis is based on the detection of cysts Agent. The adult stage of E. multilocularis is only
using imaging methods (US, CT, MRI, chest X-ray, 2-4 mm long, it has typically 5 proglottids(2-6) and
etc.) in conjunction with serological detection of is characterised by a genital pore located anterior the
specific antibodies. The importance of CE is generally middle of the gravid proglottid and a sack-like uterus,
underestimated, partly because the infection often takes containing up to 200 eggs( ► Figure 9.55b and 9.56).
a chronic course, and fatal cases are rare. However, the Minor genetic variation exists between E. multilocularis
disease can be severe, requiring complicated surgery isolates from Europe, Asia and North America. It is
and/or prolonged chemotherapy with albendazole or assumed that variants occurring in parts of North
mebendazole, and is often associated with considerable America might be of low infectivity to humans, because
financial burdens for the individual patient or the only a few human cases have been diagnosed in that area.
community. The worldwide annual burden(costs of However, considerable numbers of human cases have
disability-adjusted life years= DALYs, and monetary been reported in previous years from Alaska.
losses) of human CE cases was estimated to be at least
US$ 193 million in 2006. According to a recent study, the Life cycle. The cycle of E. multilocularis corresponds
genotype G 1 of E. granulosus s.s. has caused worldwide to that of E. granulosus, but has special features
88% of the so far genotyped human CE cases and was (► Figure 9.57). The most important definitive hosts
often related to transmission patterns with sheep as are red and arctic foxes, but other wild carnivores(e.g.
intermediate hosts. Other species or genotypes( ► Table raccoon dog, coyote, wolf) as well as domestic dogs
9.18) can be of high importance in more restricted areas and cats can also be involved. Intermediate hosts are
such as E. intermedius in the Baltic countries and Poland. predominantly rodents(common vole, water vole, other
vole species, muskrat, marmot, beaver, lemmings, etc.).
The mean incidence of CE in countries of the Humans and various animal species, such as monkeys,
Mediterranean, one of the main endemic areas in domestic and wild pigs, horses and even dogs, can be
Europe, varies between 1 and 10 new clinical cases affected as accidental hosts, harbouring metacestodes
per 100,000 inhabitants and year, but reaches higher (► Table 9.18). Metacestodes developing in natural

Q)
T5
C:

'6
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�
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C:
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C:
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Figure 9.56. Echinococcus multilocu/aris: (a) mass infection (about 40,000 specimens) in the small intestine of a naturally infected 0
0
dog; (b) smear (native) of the intestinal mucosa with gravid E. multi/ocu/aris (length about 3 mm) and detached proglottids ·u5
(Photo: IPZ, J. Eckert).
Ctl
Q_
 Part Ill. Parasites and parasitoses: metazoa

---------------e
Rodents as
Intermediate hosts

0 -
' Gra d
progloft(cj

U @
PS protoscolex
E exogenlc prolirerallon
of new vesicles
BK brood capsule
A root-likecellular
extension of ge ,na1
� Oncosphoro layer
Metacestode conglomerate
in liver of a rodent
Mon oCC!(lontol
Diagram of o motOCOOtOdos 0 �t or m6fOOO!ito&,a

Figure 9.57. Life cycle of Echlnococcus mu/11/oculorls (Graphics: IPZ, S. Ehrot).

intermediate hosts produce protoscoleces in few months. Individual cysts corresponds in principle to that of B.
If intermediate hosts containing fertile metacestodes are grm111los11s metacestodes (Inner germinal layer, outer
OJ
eaten by a definitive host, a new tapeworm generation laminated layer). In highly susceptible intermediate
·u
C

'6 develops in the small intestine that can produce infective hosts, protoscoleces are already produced after 2-4
OJ
eggs already 26-28 days p.i. Egg shedding lasts only a few months, but in less susceptible intermediate or accidental
weeks. The majority of the worm population survives a hosts this development takes longer, and the number
C few months, but residual worm burdens can probably of protoscoleces is often reduced (in at mo t 10% of
·;::
persist for longer {6-12 months). human AE case a few protoscoleces are present). Of
j pathological significance is the fact that indh1idual cysts
.£: The metacestode of E. m11ltilowlaris, which typically can form new cysts h}' exogenous budding. Furthermore,
>,
0)
develops primarily in the liver of intermediate or cellular and root-like thin protrusions of the germinal
0 accidental hosts, has an alveolar, sponge-like structure la}'er can invade the surrounding tissue ( ► Figure
'iii and is composed of small (<I mm) up to 3 cm large 9.57). In this manner the parasite can infiltrate large
('0 cysts, surrounded by granulation or connecti,1e tissue parts of the liver or adjacl.'nt organs, thus producing
('0
0.. (► Figure 9.57 and 9.58). The wall structure of the contact metastases. B)' dispersal of constituents of

Fi gure 9.58. Metacestodes of Echinococcus mu/tilocu/aris:
(a) in human liver (largest diameter of individual cysts about 3
cm); (b) in the liver of a dog (surgical site); (c) in the liver of a
pig (Photos: a IPZ, J. Eckert; b, c: IPZ, P. Deplazes).
the metacestode(presumably tiny individual cysts or
detached cell clusters) via lymphatic and blood vessels,
distant metastases in various organs can be formed,
for example in the lungs, brain or bones. Thus, the
metacestode of E. multilocularis behaves like a malignant,
infiltrative growing tumour. In humans, the metacestode
conglomerates may proliferate to diameters up to 20 cm;
they can centrally necrotise and form a decay cavity.
Occurrence and epidemiology. E. multilocularis is
widespread in the northern hemisphere, with endemic
areas in Asia(TR, Iran, RU and neighbouring states up
to Japan) and North America (Alaska, Canada, northern
9. Phylum Platyhelminthes (flatworms)
and central United States). In Europe, regional or more
focal infections of fox populations with E. multilocularis
occur in large areas stretching from central France over
Central Europe, including the Baltic States, to eastern
Europe (BY. UA, RU) and extending southwards to
SL.HU and HR. The northern border is patchy with focl co
in DK (Jutland and around Copenhagen) and southern ;g
>,
Sweden. Some countries in western Europe are regarded .c
Q.
as E. multilocularls - free, including IE, UK, PT and 0
TI
ES as well as NO (except Svalbard Island) and Fl in >-
0
northern Europe. Main endemic areas from which most
of the human AE cases have been recored in recent years
include central and eastern Prance, southern Germany,
Switzerland, western Austria, Poland and Lithuania.
• Role of definitive hosts. In Europe, E. multilocularis
is mainly transmitted in a wildlife-cycle with the red
fox as principle definitive host. Regionally, raccoon
dogs, wolves and jackals can be involved in this cycle.
In Canada coyotes and in arctic and subarctic areas the
arctic fox can be involved as key definitive host species.
Furthermore, synanthropic cycles are known to occur
especially in Asia and Alaska with dogs as important
definitive hosts. The epidemiological significance of
various definitive host species depends on many factors,
including their susceptibility to E. multilocularis, their
population densities as well as on prevalence, infection
intensity and persistence of the parasite in population of
definitive hosts. After experimental infection, each with
20,000 E. multilocularis protoscoleces, foxes, raccoon
dogs and dogs shed on average 280,000-350,000 eggs per
animal during the infection period, but cats only 570.
Due to longer survival of E. multilocularis in dogs, the
egg production per adult stage in this host was about
5 times higher than in the fox. These data support
previous observations that cats are likely to play a minor
epidemiological role. Further definitive hosts may be
involved in other regions(► Table 9.18).
Extensive studies in recent years in various European
countries and other regions have shown that on average
<1 to >70% of red foxes are carriers of E. multilocularis.
Within an endemic zone, foci with highly differing
infection prevalences may exist. The infection intensity
is low or moderate in most foxes; however, about 10-
25% are heavily infected (over 1000 parasites per animal
with maxima at about 100,000). In some studies, higher
infection intensities have been observed in juvenile( < 1
year old) than in older foxes. According to the current
opinion, ecological factors are probably accountable for
these differences(food supply, behaviour of foxes). For
the last two decades, an increase in fox populations has
been observed in various European countries, especially
in urban areas. In several cities (e.g. Zurich, Geneva,
Stuttgart, Nancy) E. multilocularis prevalences between
17 and 40% were found in foxes. In recreation areas,
located in outskirts of the cities, 60% of the foxes and
up to 21% of the rodents were infected. These and other
findings document the existence of an urban cycle of E.
 Part Ill. Parasites and parasitoses: metazoa
multilocularis. Dogs and cats can become carriers of E.
multilocularis by consuming small mammals infected
with metacestodes, thus constituting sources of infection
for humans. In this respect, dogs are more important
than cats because the latter are less susceptible to E.
multilocularis and therefore usually harbour only a few
parasites with sparse egg production. In several cross­
sectional studies(DE, CH, LT, FR), the mean prevalences
of E. multilocularis in dogs varied between 0.13 and
0.8%, but higher prevalences of 2.8-8.1 % were found in
some countries(CH, SK and CZ), mostly in unattended
free-ranging dogs.
• Role of eggs. Foxes are spreading E. multilocularis
eggs by depositing their faeces in rural and urban areas
(roads, fields, gardens, parks, playgrounds, cemeteries,
etc.). Additional dispersion can occur by flies, vehicles
and footwear. In the environment, the eggs of E.
.. multilocularis survive for 2-3 months in Central Europe
during summer with sufficient moisture, and in the
cooler seasons up to 8 months. The eggs are sensitive
to desiccation; at +25 °C and relative humidity of 27%,
their infectivity is lost within 2 days. Amazingly high
is the resistance of E. multilocularis eggs to cold; they
are not killed by deep-freezing for several months at
-20 °C, but they do lose their infectivity at -80 °C within
48 h. Temperatures >70 °C are lethal to the eggs within
a few minutes, but a longer heat exposure of 30 min. is
recommended for disinfection of materials.
• Role of intermediate hosts and transmission
of eggs to accidental hosts. Worldwide, numerous
species of small mammals, especially rodents, have been
identified as intermediate hosts of E. multilocularis,
including the field mouse, water vole and muskrat in
Europe. Accidentally, also humans and other aberrant
hosts may acquire the infection. Different ways of
egg transmission to humans are considered, but the
significance of the different possibilities is still unknown:
(a) hand to mouth contact after contamination of
hands with E. multilocularis eggs. The contamination
can occur, for example, by touching infected definitive
hosts (dogs, killed foxes, etc.), dogs contaminated with
fox faeces or various surfaces with adhering eggs (shoes,
gardening tools etc.) or when working with soil or plants
contaminated with eggs by faeces of definitive hosts, and
(b) through the consumption of egg-contaminated
food (vegetables, windfalls, etc.) or drinking water. In
an endemic area of Switzerland, grass from meadows to
which foxes had access, was the likely source of infection
for domestic pigs and monkeys in a zoo.
Pathogenesis and clinical signs. Definitive
hosts do not show symptoms even if heavily infected
with intestinal stages (up to I 50,000 in experimentally
infected dogs).
• Alveolar echinococcosis (AE) in animals. In
Europe and other endemic areas, various species of
mammals have been described as accidental hosts of
E. multilocularis metacestodes, such as domestic and
wild pig, horse, nutria, beaver, chinchilla, species of
monkeys in captivity and dogs. Depending on the
animal species, the development of metacestodes may
proceed to different stages (some with formation of
protoscoleces), associated with symptoms and death,
for example in monkeys and dogs. In these hosts, the
liver is primarily affected. Dogs have shown enlargement
of the abdomen, ascites, hepatomegaly, weakness,
dyspnoea, hypergammaglobulinaemia and other signs.
In some dogs, tumour-like metacestode masses reached
diameters of 10-15 cm (► Figure 9.58b). AE has to
be considered as differential diagnosis in dogs with
suspected abdominal tumours. In 2 dogs, a simultaneous
infection with metacestodes of E. multilocularis in the
liver and adult stages in the intestine was observed .
Pigs represent aberrant hosts with limited parasite
development, mostly with lesions not larger than IO
mm in diameter which calcify without protoscolex
formation (more details see: diagnosis)(► Figure 9.58c).
In Switzerland, approximately 10% of 90 pigs from free­
range farms had liver changes at slaughter, caused by
E. rnultilocularis.
• AE in humans. In humans, the infection with
metacestodes is initially always asymptomatic. After a
long incubation period of 5-15 years, the infection can
cause liver symptoms resembling those of a malignant
tumour (including upper abdominal pain, jaundice,
weight loss). The AE occurs in different age groups (7
to >80 years), but is mainly diagnosed in the elderly (50-
70 years), and is characterised by a prolonged, chronic
course with a duration of some weeks to several years
after diagnosis. Since the mortality rate can reach over
94% in untreated patients, the AE is considered one of
the most dangerous parasitic diseases. Spontaneous
cure is rare.
Immunology. Partial immunity in intestinal infection
of foxes has been suggested, but it is not documented
so far. In AE of humans, immunological reactions can
inhibit the proliferation of the metacestode. Specific
antibodies against metacestode antigens have no
protective effect, but their detection is diagnostically
useful.
Diagnosis
• Definitive hosts. The intravital diagnosis of the
intestinal E. multilocularis infection in dogs and cats
by coproscopic techniques (detection of proglottids
and eggs) is of low sensitivity (see E. granulosus, ► p.
245). More efficient is the isolation of taeniid eggs by a
flotation/sieving technique and subsequent molecular
identification of species-specific Echinococcus­
DNA (PCR: sensitivity for patent infections up to

94%, specificity close to 100%). Copro-antigen tests
(ELISA) (mean sensitivity ~80%, higher in heavy
infection; specificity 70-95%) are available in specialised
laboratories. Such tests are preferably used for mass
screening in epidemiological studies or in control
programs. The detection of E. multilowlaris at necropsy
requires special methods (intestinal smear technique:
sensitivity approximatly 70-80%; sedimentation and
counting technique: sensitivity 80-90%; specificity of
both methods close to 100%).
• Man. The intravital diagnosis of AE in humans
is mainly based on the detection of metacestode
lesions with imaging methods (US, CT, MRI , etc.)
and serological antibody detection using sensitive and
specifk methods.
• Other accidental hosts. In monkeys and dogs,
the s:1me methods are used as in humans for diagnosing
AE. In pigs, the infection manifests itself in the liver as
well-demarcated white-yellowish foci (about 1-20 mm)
with a necrotic centre or an alveolar structure; in some
lesions PAS-positive components of the laminated layer
may be detectable in histological sections. These lesions
can be identified at meat inspection, but verification
by histological examination and/or DNA detection is
required.
Therapy
• Definitive hosts. Because E. multilocularis infected
dogs (or cats) represent a potential infection risk for
humans, they should be treated under veterinary
supervision as soon as possible after diagnosis. Persons
who have come into contact with the animals should
be informed. The drug of choice is praziquantel (dog
and cat: 5 mg/kg b.w. p.o. or 5.7 mg/kg i.m., not s.c.l
Cats can also be treated with 8.0 mg/kg b.w., spot-on
solution). Repetition of treatment on the following day
is recommended in order to keep the risk of a potential
residual worm burden as low as possible. When using
epsiprantel, at least one repeat treatment is essential.
The success of treatment can be evaluated by several
follow-up examinations for copra-antigen, but very
low residual infections might not be detected. Note
that none of the available drugs is ovicidal; therefore,
eggs shed after treatment of an Echinococcus carrier
are infective. Treatments must be carried out under
special precautions to avoid the dispersal of eggs and
infection risks for humans (maintenance of dogs in
boxes that are easy to clean and disinfect; safe disposal
of faeces up to 3 days after treatment; shampooing and
thorough washing of dogs after treatment to remove
any eggs potentially adhering to the fur; personnel
involved should wear mouth protection, rubber gloves
and protective clothing).
• Accidental hosts with AE. There are a few reports
showing that in dogs with AE of the liver a combination
9. Phylum Platyhelminthes (flatworms)
of surgical resection and long-term therapy with
albendazole (daily 10 mg/kg b.w., p.o.) can result in an
improvement of the clinica.l condition lasting for several
years in some of the animals. For primates the same
thcrapeutical strategics as in humans can be applied;
albcndazole in a sweet formulation (used for children)
is well accepted for example by chimpanzee or gorillas.
Control and prevention. Extensive studies have
shown that it is feasible to treat foxes for E. multilocularis
in rural and urban areas by systematic and long-term
distribution of praziquantei-containing baits, resulting
primnrily In slgnlflc:intly reduced prevalences of the
pnrnsite In fox populations and secondarily in rodents.
However, this control option is costly and is probably
more suitable for small-scale application, for example,
In urban areas with high infection risk for humans, than
for large-scale or nationwide control.
In dogs and cats that catch and eat small mammals,
infections with gravid intestinal stages can be prevented
by treatments with praziquantel at intervals of 4 weeks,
but the procedure is quite demanding and does not
exclude other sources of infection for animal owners,
for example by foxes or the neighbour's dog. For
people living in endemic areas, special prophylactic
measures are recommended, such as precautions when
handling potentially infected foxes and other final hosts,
thorough washing or better cooking of low growing
wild or cultivated plants and windfall before eating,
and washing hands after contacts with soil. People
who have had contact with proven or likely infected
definitive hosts, often deal with foxes or are exposed to
another infection risk can be examined by serological
tests for specific antibodies against E. multilocularis at
certain intervals (aim: exclusion or early detection of an
infection). However, it is not clear at what point after
infection antibodies might be detectable.
Zoonotic importance. Despite the high prevalence
of E. nwlti/ocularis in foxes, the incidence of AE of
humans is low.' In Europe, most human AE cases
are found in central and eastern France, southern
Germany, Switzerland, western Austria and in Poland
and Lithuania. In recent years, the nationwide annual
incidences of human AE in FR, DE, AT and CH ranged
between 0.03-0.3 and up to 0.74 in Lithuania but
regionally even higher incidences up to 1.4 cases per
100,000 inhabitants were recorded. It cannot be ruled
out that ecological changes for example growing fox or
coyote populations, especially in cities, and other factors
could lead to an increasing incidence in the future. In
Switzerland, the nationwide average incidence of AE was
0.1/100,000 between 1993 and 2000, but by the end of
2005 it had increased to 0.26, and persisted thereafter
until the end of 2012 at that higher level.
Even if the small number of human cases is considered,
AE is an important zoonosis, because it is principally
 Part Ill. Parasites and parasitoses: metazoa
an incurable disease whose treatment (radical surgery,
year-long or permanent chemotherapy [albendazole
or mebendazole)) is a great burden for the patient and
incurs high costs. However, adequate treatment leads
to a significant prolongation of life in a considerable
proportion of cases. In Switzerland, the costs for an AE
patient (treatment and loss of earnings) were estimated
in 2008 at an average of€ 182,000. The global annual
incidence of new cases of human AE has been estimated
at approximately 18,000 with 91% occurring in China.
Selected references
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Echinococcus granulosus sensu lato genotypes Infecting
humans - review of current knowledge. Int J Parasitol 44:
9-18.
Budke CM, Deplazes P, Torgerson PR (2006) Global
socioeconomic impact of cystic echinococcosis. Emerg
Infect Dis 12: 296-303.
Carmena D, Cardona GA (2014) Echinococcosis In wild
carnivorous species: epidemiology, genotypic diversity, and
implications for veterinary public health. Vet Parasitol 202:
69-94.
Cardona GA, Carmena D (2013) A review of the global
prevalence, molecular epidemiology and economics of
cystic echinococcosis in production animals. Vet Parasitol
192: 10-32.
Conraths FJ, Deplazes P (2015) Echinococcus multilocu/aris:
epidemiology, surveillance and state-of-the-art diagnostics
from a veterinary public health perspective. Vet Parasitol
213: 149-161.
Craig PS, Larrieu E (2006) Control of cystic echinococcosls/
hydalidosis: 1863-2002. Adv Parasltol 61: 443-508.
Craig PS, Mastin A, Van Kesteren F, Boufana B (2015)
Echlnococcus granulosus: epidemiology and state-of-the­
art of diagnostics in animals. Vet Parasltol 213: 132-148.
Craig PS, Pawlowski ZS (eds.) (2002) Cestode zoonoses:
echlnococcosls and cystlcercosls. Amsterdam, 1110
Netherlands: IOS Press; ISBN 1-58603-220-8.
Oeplazes P, Hegglin D, Gloor S, Romig T (2004) Wilderness
in the city: the urbanization of Echinococcus multilocularis.
Trends Parasitol 20: 77-84.
Deplazes P, van Knapen F, Schweiger A, Overgaauw
PAM (2011) Role of pet dogs and cats in the transmission
of helminthlc zoonoses in Europe. with a focus on
echinococcosls and toxocarosis. Vet Parasitol 182: 41-53.
Eckert J, Oeplazes P (2004) Biological, epidemiological, and
clinical aspects of echinococcosis. a zoonosis of increasing
concern. Clin Microbial Rev 17: 107-135.
Eckert J, Gemmell MA, Meslin FX, Pawlowski ZS (eds.)
(2001) WHO/OIE Manual on Echinococcosis in Humans
and Animals: a Public Health Problem of Global Concern.
Paris, France: World Organization for Animal Health; ISBN
92-9044-522-X.
Eckert J, Deplazes P, Kern P (2011) Alveolar echinococcosis
(Echinococcus multilocularis) and neotropical forms of
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Brown DWG (eds.) Oxford Textbook of Zoonoses. 2nd e d.
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978-0-19-857002-8.
Gemmell MA, Lawson JR, Roberts MG, Kerin BR, Mason
CJ (1986) Population dynamics in echinococcosis and
cysticercosis: comparison of the response of Echinococcus
granulosus, Taenia hydatigena and T. ovis to control.
Parasitology 93 (Pt 2): 357-369.
Gottsteln B, Wang J, Boubaker G, Marinova I, Spiliotis M,
MOiier N, Hemphill A (2015) Susceptibility versus resistance
In alveolar echinococcosls (larval infection with Echinococcus
multilocularls). Vet Parasitol 213: 103-109.
Hegglin D, Deplazes P (2013) Control of Echinococcus
multilocularis: strategies, feasibility and cost-benefil analyses.
Int J Parasitol 43: 327-337.
Kopel CM, Torgerson PR, Thompson RC, Deplazes P (2006)
Reproduction potential of Echinococcus multllocularls in
experimentally infected foxes, dogs, raccoon dogs and cats.
Int J Parasitol 36: 79-86.
Lightowlers MW (2012) Cysticercosis and echlnococcosis. Curr
Top Mlcroblol lmmunol 365: 315-335.
Lymbery AJ, Jenkins EJ, Schurer JM, Thompson RCA (2015)
Echinococcus canadensis, E. borealis, and E. intermedius.
What's In a name? Trends Parasitol 31: 23-29.
Mejri N, Hemphill A, Gottstein B (2010) Triggering and
modulation of the host-parasite interplay by Echinococcus
multilocularis: a review. Parasitology 137: 557-568.
Nakao M, Lavikainen A, Yanagida T, Ito A (2013) Phylogenetic
systematics of the genus Echinococcus (Cestoda: Taeniidae).
Int J Parasitol 43: 1017-1029.
Otero-Abad B, Torgerson PR (2013) A systematic review of
the epidemiology of echinococcosis in domestic and wild
animals. PLoS Negl Trop Dis 7: 02249.
Oksanen A, Lavikainen A (2015) Host ecology and
Echlnococcus canadensls transmission In the North. Vet
Patrasitol 213: 182-186.
Rausch RL ( t 995) Ufa-cycle patterns and geographic dislribution
of Echlnococcus species. In: Echlnococcus and hydatld
disease Thompson. RCA. Lymbery AJ (eds.) Wallingford,
UK: CAB International, pp. 89-134; ISBN 0-85198-910-1.
Romig T, Ebl D, Waasermann M (2015) Taxonomy and
molecular epidemiology of E. granulosus sensu lato. Vet
Parasltol 213: 76-84.
Schweiger A, Ammann RW, Candinas D, Clavien PA,
Eckert J, Gottstein B, Halkic N, Muellhaupt B, Prinz
BM, Reichen J, Tarr PE, Torgerson PR, Deplazes P
(2007) Human alveolar echinococcosls after fox population
increase, Switzerland. Emerg Infect Dis 13: 878-882.
Tsai IJ, Zarowiecki M, Holroyd N, Garciarrubio A, Sanchez­
Flores A, Brooks KL, Tracey A, Bobes RJ, Fragoso
G, Sclutto E, Aslett M, Beasley H, Bennett HM, Cai
J, Camicia F, Clark R, Cucher M, De Silva N, Day TA,
Oeplazes P, Estrada K, Fernandez C, Holland PW,
Hou J, Hu S, Huckvale T, Hung SS, Kamenetzky L,
Keane JA, Kiss F, Koziol U, Lambert 0, Liu K, Luo
X, Luo Y, Macchiaroli N, Nichol S, Paps J, Parkinson
J, Pouchkina-Stantcheva N, Riddiford N, Rosenzvlt
• 9. Phylum Platyhelminthes (flatworms)

M, Sali n as G, Wasmuth JD, Zamanian M, Zheng Y;

Ta enia solium Genome Consortium, Cai X, Sober6n
X, Olso n PD, Laclette JP, Brehm K, Berriman M (2013)
n,e genomes of four tapeworm species reveal adaptation s
to parasitism. Nature 496: 57-63.
RCA (2013) Parasite zoonoses and wildlife: One
Tho mpson
Health, spillover and human activity. Int J Parasitol 43: 1079-
1088.
n,om pson RCA, Lymbery AJ (eds.) (1995) Echinococcus and
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0-85 198-910-1.
Torgerson PR, Schweiger A, Deplazes P, Pohar M, Reichen
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978-0-19-857002-8.
T rachsel D, Deplazes P, Mathis A (2007) Identification of
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Parasitol 213: 110-120.
Cl)
..c

.E
a3
I
 10. Phylum Nematoda (syn. Nematozoa)
(threadworms or roundworms)
Nema (G): thread; zoon (G): animal, creature.
Summary
• The phylum Nematoda (threadworms or roundworms)
comprises numerous species which are free-living or
parasites of plants or animals.
• In vertebrates, nematodes Inhabit the digestive and the
respiratory tract as well as other organ systems; they
are causative agents of Important diseases In animals
and humans.
• Nematodes are elongated, spindle- or thread-like,
rarely differently shaped, unsegmented, bilaterally
symmetrical animals of very different length (millimetres
to metres).
• The body Is covered with a cuticle, the Internal organs
are located In a llquld-fllled body cavity.
• Reproduction Is usually sexual; the life cycle proceeds
from the egg via 4 larval stages (L 1-L4) to pre-adult
stages (5th stage), which attain sexual maturity and
are then called adults. This development Includes four
moultlngs, during which the cuticle detaches from the
underlying hypodermls and Is discarded.
• Parasitic nematodes develop In direct cycles (without
Intermediate host) or Indirect cycles (with Intermediate
host). The Infection of definitive hosts occurs on
different routes (perorally, percutaneously, etc., ► p.
22). In the vertebrate host, the larval stages of certain
species undertake extensive systemic migrations.
• Ari Important characteristic of several nematode species
Is their capacity for hypoblosls (• arrested development)
during the parasitic phase of development.
The phylum Nematoda comprises more than 20,000
species that are either free-living in soil, fresh and
salt water, or they live as parasites of plants, animals
and humans (at least 1/2 of all species). Part of the
nematode species have successfully adapted to life in
extreme habitats, such as the ocean floor (up to 6,600
m deep), water of hot springs (up to 53 °C), acidic
vinegar (e.g. Turbatrix aceti) and the intestinal tract of
vertebrates. Life in such diverse habitats is possible due
to special features, including the adaptation of certain
stages to anaerobic conditions, a fairly large tolerance
of temperature fluctuations, and the ability to survive
unfavourable environmental conditions in a state of
seeming lifelessness for months.
Features and characteristics of parasitic
C nematodes. The body of nematodes is usually
>,
Ol
elongated, spindle- or thread-like, from hair-thin to
0 thick as a pencil, and rarely other shapes. The body
"cii
length of adult stages usually ranges between a few
lU millimeters and a few centimeters, but it may reach I
lU
a.. m or more (e.g. females of Placentonema gigantissima
in the placenta of the sperm whale are 8.4 m long!). The
outer integument, the internal organs (digestive tract,
reproductive organs, etc.) and the liquid-filled body
cavity are the basic elements of the nematode structure
( ► Figure 10.1 ).
• Integument und musculature. The integument,
consisting of the outer acellular cuticle and the
underlying cellular hypodermis ( = epidermis), is
closely connected with an inwardly following layer of
longitudinally oriented muscle cells, each of it with an
arm-like extension to the nervous system. The cuticle
and the hydrostatic pressure of the liquid-filled body
cavity act as a so-called hydroskeleton, holding the body
shape stable and allowing a high motility. Most common
are meandering - gliding movements. The cuticle not
only covers the body surface, but also sections of the
digestive tract (buccal cavity, oesophagus, cloaca), of
reproductive organs (distal vagina, spicula pouches),
the excretory pore and sensory organs (amphids and
phasmids). The cuticle is a resilient, flexible, acellular
complex structure, composed of several layers, for
example epicuticle, outer and inner cortex, middle
flbrillar and basic layer.
The epicuticle may be covered by a surface coat, about
5- IO µm thick, also named glycocalyx, containing
glycoproteins and mucopolysaccharides which are of
special interest in terms of immune responses of the
host. The epicuticle contains glycolipids and a highly
cross-linked insoluble structural protein, the cuticulin,
which is rich in glycine, praline and hydroxyprolinc
and is resistant to collagcnase. Main components of the
inner layers arc collagcns, cross-linked by disulphide
bonds, which are degraded by collagenasc, further
proteins and polysaccharides. In Haemonchus contortus
collagen synthesis is encoded by more than 100 genes.
The life cycle of the nematodes includes 4 moultings,
during which the cuticle detaches from the underlying
hypodermis and is stripped off.
• Digestive tract. It is a straight tube consisting
of mouth opening (stoma), buccal cavity, oesophagus
( = pharynx), intestine ( = midgut), rectum and
anus ( ► Figure I 0.1 ). The mouth opening may be
surrounded by cuticular lips (labia), protuberances,
leaf crowns or other structures (sensory organs see
below). The buccal cavity may be dilated to a thick­
walled buccal capsule, equipped with tooth- or blade­
like structures. In the Secernentea the oesophagus
consists of a cuticular tube, typically with a triradiate
lumen, surrounded by muscles and supporting cells
( ► Figure I 0.2). In the oesophagus wall, there are
♦ 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)

Buccal capsule Sensory papillae

Integument �
Oesophagus
Excretory pore Nerve ring
Excretory gland Pseudocoel Cf)
.2
Coelomocyte Intestine
·;;:
Uterus
Ovary Testis
Vulva Seminal vesicle 0

Ductus
ejaculatorius

Receptaculum
seminis Splculum
Rectum Cloaca
Anus
Phasmid Bursa copulatrix
Female Male

Figure 10.1. Scheme of body structure of nematodes (Graphics: IPZ, A. Seeger; after Lee 1965).

Muscular
part

Nerve ring
Oesophagus Oesophagus Glandular
part with
Cervical Nerve ring stichocytes
papilla
Glandular
part ---,11--�"'-�
Bulbus Q)

·u
C

Intestine
Q)
�
a d i::'
b C cu
Cylindrical oesophagus Oesophagus with bulbus Muscular-glandular Trichuroid oesophagus C
·c
(Ostertagia spp., Strongylida) (Passalurus, Oxyurida) oesophagus (Spirurida) (Trichinella spp.) Q)

Figure 10.2. Oesophagus types (selection) of adult nematodes (Graphics: IPZ, A. Seeger; after a: Skrjabin 1952; b: Hartwich C
>,
1975; c, d: B.G. Chitwood and M.B. Chitwood 1950). OJ
0

·u5
cu
0...
 Part Ill. Parasites and parasitoses: metazoa
usually one dorsal and two sub-ventral mononuclear
oesophageal glands, whose secretions are released into
the oral cavity or the oesophageal lumen. The posterior
oesophagus can be expanded into a muscular swelling
(bulb) containing a valvular apparatus; such oesophagus
types act as suction pumps( ► Figure 10.2b). In some
groups of the Secernentea the oesophagus is divided into
an anterior muscular and a posterior glandular portion
(► Figure 10.2c). Larval stages of parasitic nematodes
have different oesophagus forms, which are of diagnostic
interest, mainly in strongyles ( ► Figure 10.3). In the
Trichinelloidea (class Adenophorea) the oesophagus
consists of a short anterior muscular portion, followed
by a glandular part consisting of one or two rows of
glandular cells (stichocytes) surrounding a thin lumen.
The stichocytes are individually connected with the
lumen through small ducts ( ► Figure 10.2d). The
entodermal midgut, following the oesophagus, consists
I
..
of a single layer of epithelial cells, attached to a basement
' ·,
I
membrane, with microvilli on the surface. The rectum
,",:, is a short cuticular tube with a ventral opening(anus)
(► Figure 10.1).
• Circulatory and respiratory system. Circulatory
and respiratory organs are missing; gas exchange takes
place through the integument, and the body cavity fluid
is involved in the transport of substances. The structure
of the excretory system is variable. For example, in some
nematode groups it is an H-shaped structure, consisting
of two gland cells, that are connected with two lateral
canals (embedded in the lateral hypodermis cords)
directed anteriorly and posteriorly, and a common
excretory duct with an excretory pore. The Adenophorea
have only a ventral excretory cell with an opening to the
outside. This system has secretory and osmoregulatory
functions.
Prebulbus
Q) Isthmus
C
·c3 Bulbus with valvular
'6 apparatus
Q)
�
Intestine
ro
C
·;:: a Rhabditoid oesophagus with b Rhabditoid oesophagus
Q)
prebulbus and bulbus with bulbus
C Non-parasitic, free living nematodes Strongylids, free living larva
>- 1 and 2
0')
0
0
"ui Figure 10.3. Oesophagus types (selection) of free-living stages nematode stages (Graphics: IPZ, A. Seeger; after Burger and
ro Stoye 1968).
ro
0...
• Reproductive organs and reproduction. In most
of the nematode species the sexes are separate. However,
the parasitic generation of Strongyloides consists only
of females which reproduce by parthenogenesis. The
male reproductive organs typically consist of a single
tube differentiated into testis, seminal vesicle and vas
deferens. The latter, which may be divided into an
anterior glandular and a posterior ejaculatory part, opens
into an expansion of the rectum, the cloaca( ► Figure
10.1). Accessory organs are one or two sclerotised
structures, the spicula {singular: spiculum), an unpaired
gubernaculum (acting as a guide for the spicules), in
some groups a telamon(a supporting structure), a caudal
sucker or a bursa copulatrix( ► Figure 10.4). The latter
is a saddle-shaped structure, typically consisting of three
main cuticular lobes supported by bursa! rays. The bursa
copulatri_x is used by the male to grasp the female at
the vulva region for copulation. Bursa, spicules and
gubernaculum are characteristic structures that are
especially important for the identification of genera
and species.
The female reproductive organs consist of a single(i.e.
Trichuriidae) or mostly a pair of tubes divided into the
ovary, seminal receptacle, and uterus, followed by an
unpaired vagina and the vulva. A muscular ovijector,
located between the uterus and the vagina, serves to
expel the eggs. The vagina opens mostly near the middle
of the body or anywhere between the anterior end and
the anus; in some species it is covered externally with a
cuticular vulvar flap( ► Figure 10.1). The females are
oviparous(passing unembryonated eggs), ovoviviparus
(embryonated eggs) or viviparous(shedding of larvae).
Trichinella spp. and various filarial species are examples
of viviparous nematodes. The egg shell (capsule) is
usually composed of 3-4 layers: (a) inner, thin lipid
Bulbus with
valvular apparatus
Intestine
c Filariform oesophagus
3,d stage strongyloid
larvae
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundwo rms)

- -- Spiculum pouch

-�
U)
·c
AllfmAIH-1--- Gubernaoulum Cl)

- Prebursal papilla
co
Genital conus .c
Bursa! rays: 0
Ventre-ventral ---t-.---'l
Ventro-lateral -- - -- Lateral bursa lobe
Antero-lateral ---\.,,::::;,
Media-lateral----'-<
Postero-lateral -- --�<\\-'-.\

External-dorsal ray
Dorsal bursa lobe

Figure 10.4. Bursa copulatrix of trichostrongylid male (Graphics: f PZ, M. Mathys).

layer, (b) middle, chitinous layer, partly of considerable
thickness, and (c) outer protein layer(s) ( ► Figure 10.5).
• Sensory organs and nervous system. Various
sensory organs (sensillae), mainly aggregated at the
anterior and the posterior end as well as in the genital
area, enable the perception of mechanical, thermal and
chemical signals. These organs include the amphids
(near the mouth), the phasmids (paired at the posterior
end) and various sensory papillae and sensory bristles.
The nervous system consists of a nerve ring surrounding
Major layers of egg shell
M-J----- Lipid layer (internal)
+>r-- Chitinous layer (middle)
Protein layer (external)
Zygote
includes the following stages: the egg, four larval
stages (Ll-L4), and a pre-adult 5th stage that is termed
adult stage after having attained sexual maturity. This
the pharynx ( ► Figure I 0.2a, b) from which peripheral
nerves run forward and backward with branches to
supply the organs.
• Nutrition and energy metabolism. Nematodes
incorporate food substances through the mouth and
intestine, low-molecular substances can be absorbed
through the integument. Adult nematodes meet their
energy requirements predominantly through anaerobic -Cl)
..c
C
catabolism of carbohydrates that are not metabolised to
CO2 and water. Therefore, volatile fatty acids, succinate,
.Ea5
lactate and some other substances are excreted as I
metabolic end products. Oxidative processes are missing
or play a minor role. In contrast to the adult stages, the
free-living stages usually have an aerobic metabolism
and are able to break down carbohydrates to CO2 and
water. The infective L3 of the Strongylida do not feed, but
they can survive in the environment for several months.
Life cycle. Typically, the life cycle of the nematodes

t-
Ascaris egg
development is associated with 4 moultings. During
Cl)
the moulting process (= ecdysis) new cuticular layers C
·u
Polar plug --- are formed by the hyp odermis, simultaneously the old '6
Q)
cuticle is basically detached enzymatically and finally �
discarded as so-called exuvia. After the last moulting, �
Mcr,la eel> co
cell divisions in nematodes are greatly reduced or C
·c
entirely absent, but continue in reproductive organs. Q)
In several parasitic or free-living nematodes, moulting j
between the 2nd and 3rd larval stage is incomplete, as C

the exuvia of the 2 nd larval stage is not stripped off but

-
>,
0)
Strongylid egg Trichuris egg maintained as a sheath which completely encloses the 0
0
3'd stage, which is called 'ensheathed' larva. 'in
Figure 10.5. Examples of nematode eggs and the layers of the co
co
egg shell. Note: figures not in the same scale (Graphics: IPZ). CL
 Part Ill. Parasites and parasitoses: metazoa
• Hypobiosis. Different species of nematodes can
temporarily inhibbit their development in a host by a 'rest'
of the parasitic yd, 4th or 5th stage. This phenomenon
designated as 'hypobiosis' or 'arrested development' is of
significant importance for epidemiology, pathogenesis,
diagnosis, chemotherapy, and probably also for immune
stimulation. Hypobiosis should be distinguished from
anabiosis which is a 'dormant' state occurring in free­
living yd stage larvae, i.e. during desiccation or freezing.
• Developmental pathways. The life cycles of
nematodes are diverse. Many species develop directly
(without an intermediate host), while others undergo
indirect development (including an intermediate host).
A special feature of Trichinella spp. is that the same
host acts simultaneously as final and intermediate host.
Infection of definitive hosts takes place on various
routes, e.g. perorally, percutaneously or via the placenta;
transmission may be mediated by a vector. After
infection of a host, many nematode species undertake
migrations through various organ systems to reach their
predilection sites.
Systematics. The nematodes, genetically related to the
arthropods, belong to the Ecdysozoa whose development
is characterised by moultings. The phylum Nematoda is
divided into the classes Secernentea and Adenophorea
(► Table 9.1; Anderson, 2000).
• Secernentea (Phasmidia). Oesophagus without
stichosome ( ► Figure I 0.2a-c), phasmids present, eggs
without polar plugs; usually the 3rd stages are infective
to the host. The majority of veterinary and medically
important nematode species belongs to this class.
• Adenophorea (Aphasmidia). Oesophagus
cylindrical or with stichosome ( ► Figure 10.2d); no
phasmids; eggs usually with I or 2 polar plugs; first
larval stage often with stylet in the buccal cavity, usually
infective to the host.
Selected references
Anderson RC (2000) Nematode parasites of vertebrates. Their
development and transmission. � ed. Wallingford. UK: CAB
Q)
International; ISBN 0-85199-421-0.
·o
C:
Anderson RC, Chabaud AG, Willmott S (eds.) (1974) CIH
'6
Q)
keys to the nematode parasites of vertebrates. No. t -10.
Farnham Royal, UK: Commonwealth Agricultural Bureaux.
ro
C: Boeri F, Chung JA (eds.) (2012) Nematodes. Morphology,
·.::::
Q) functions and management strategies. New York, NY, USA:
Nova Science Publishers; ISBN 978-1-61470-784-4.
C: Kennedy MW, Harnett W (eds.) (2001) ParaSJtic nematodes.
>,
0)
Wallingford, UK: CAB International; ISBN 0-85199-423-7.
0 Lee DL, Atkinson HJ (1976) Physiology of nematodes. 2nd ed.
0
·u; London, UK: The Macmillan Press Ltd.: ISBN 0 333 18600 1.
ro
ro
(L
Kohler P (2006) Stoffwechselphysiologie von Parasiten. In: Hiepe
T, Lucius R, Gottstein 8, (eds.) Allgemeine Parasitologie.
Stuttgart, Germany: Parey, pp. 189-218; ISBN 3-8304-
4101-0.
Perry RN, Wharton DA (eds.) (2011) Molecular and physiological
basis of nematode survival. Wallingford, UK: CABI
International; ISBN 978-1-84593-687-7.
10.1 Class Secernentea
10.1.1 Order Rhabditida
Rl,abdos (G): rod. Refers to the form of oesophagus.
Summary
• Agents and life cycle. Strongy/oldes is the most
Important genus of the order; different species cause
ln1estlnal diseases, especially In young animals, e.g.
Strongytoldes suls (syn. S. ransom,) in piglets. The
parasitic generation, residing In the small Intestine of
the hosts, consists only of females which produce
eggs by parthenogenesis. Eggs (or 1 st stage larvae
In S. stercora/ls) that are passed In the faeces to the
environment may develop either Into Infective 3rd
stage larvae (L3) or to a sexual generation with males
and females. The latter produce eggs that develop
Into Infective L3. In this way, multiplication of the
parasites occurs outside the host. Infective L3 from
the environment Invade hosts primarily percutaneously,
but also perorally.
• Migration in the host: After infection by skin penetration,
the parasites undergo extensive systemic migrations:
-+ subcutaneous tissue -+ bloodstream -+ lung -+ air
passages and pharynx (tracheal migration) -+ small
Intestine, where they develop Into sexually mature
females. Furthermore, the larvae may migrate through
body tissues (somatic migration) and settle In various
parts Qncludlng subcutaneous tissues, muscle, lactic
gland), where they can survive for long periods u
hypoblotlc stages. Larvae inhabiting the lactic gland
can be transmitted via the mllk from dams to new­
borns Qactogenlo transmission), aa demonstrated for
$. westerl (horse), S. pap/1/osus (ruminants), S. $Uls (pig)
and $. sterooralls (dog).
Patt,ogone•I•, ollnlcal sign,. Heavy Strongyloides
Infections �n cause diarrhoea in young animals,
delayed growth, weight loss, hypoalbumlnaemia, skin
lesions and death.
• Diagnosis, treatment, control. lntravital diagnosis
by detection of eggs (or larvae) in faeces, treatment
with (pro)benzimidazoles in high doses or macrocyclic
lactones: hygiene measures.
• Zoonotic Importance. Larvae of Strongyloides spp. are
causative agents of skin lesions (larva migrans cutanea)
in humans. S. fuellebomi and S. stercoralis establish
Intestinal infections both in animals and humans. The
latter species can cause life-threatening systemic
infections in patients with impaired immunity.
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundwo rms)
The order Rhabditida includes free-living and parasitic
species. The genus Strongyloides is predominantly of
veterinary importance, but occasionally species of
the genera Pelodera and Halicep'1alobus may cause
diseases in domestic animals. The free-living species
Caet1orl1abditis elegans, consisting of 959 cells, has
gained scientific importance in genetics as a model
animal. Since 1998, the entire genome consisting of more
than 19,000 genes has been decoded, and important
general knowledge on ageing, cell death and other
aspects could be deduced from studies of this nematode.
C.elegans is also used in many laboratories, inter alia for
the investigation of gene functions of parasitic nematode
species.
Family Strongyloididae
Genus Strongy/oides (threadworms)
■
Disease: Strongyloidosis.
Strongylos(G): round, cylindrical; -oideus (L): similar.
More than 50 Strongyloides species are known from
mammals, birds, reptiles and amphibians. In veterinary
medicine, they are of predominate interest as pathogens
in young animals (piglets, lambs, calves, foals) and
monkeys.
Agents. A special feature of the genus Strongyloides
is that the parasitic generation, residing in the small
intestine of the host, consists only of females. However,
in the environment free-living generations with males
and females may occur. Characteristics of the parasitic
females are( ► Figure 10.6): hair-thin nematodes, only
a few millimetres long, cylindrical oesophagus, vulva as
transverse slit behind the middle of the body, leading
into two uterine tubes, one directed anteriorly and the
other posteriorly. Ovaries spirally twisted or non-twisted
(in S. stercoralis). Eggs in the uterus in a row, about 40-
55x30-40 µm, oval with flattened poles, thin-shelled
with embryo.
Life cycle. The life cycle in the genus Strongyloides
is characterised by an alternation of generations
(heterogony) and includes an external (preparasitic)
and an internal (parasitic) phase ( ► Figure 10.6).
• Cycle of S. westeri, S. suis and S. papillosus.
The external development begins with shedding of
embryonated eggs in the faeces of a host ( ► Figure
10.6.) The eggs develop parthenogenetically in females
inhabiting the small intestine (up to 2,000 eggs per
female/day). In the environment at temperatures
around 20 °C and with sufficient oxygen supply, l st
larval stages(LI)(with rhabditiform oesophagus) hatch
from the eggs. Within 3-4 days they develop through two
moultings into 2nd (L2) and infective 3'd larvae (L3); the
latter have a filarifom oesophagus and are not enclosed
in a sheath(= unsheathed) (homogonic development).
Alternatively, LI may develop through several stages
and 4 moultings into a single generation of free-living
males and females (several sexual generations have been
C'O
described in S. pla11iceps) (heterogonlc development).
E
From eggs produced by this generation, only female i5
LI arise, which develop through two moultings into .0
C'O
.c
infective L3. The potential for one or the other type of a:
development has a genetic basis, but host-derived and
environmental factors determine which route will be
taken. A higher proportion of males emerge from eggs
deposited by S. rattl females inhabiting a non-immune
host, as compared to females living in an immune host,
suggesting that oogenesis is influenced by yet unknown
mechanisms in an immune host. In the environment,
a genetic switch occurs under the influence of factors
that are perceived by sensory organs(amphids) of free­
living LI. Thus, low ambient temperatures promote
the homogonic route, while higher temperatures are
favourable for a heterogonic development. L3 stages are
very sensitive to drought; in a humid environment they
usually remain viable only a few weeks, sometimes up
to 4 months. The infection of new hosts can occur on
different routes, namely percutaneously and perorally
(including lactogenic transmission).
The internal development in hosts is associated with
systemic migrations, occurring on different routes
.c
(JJ
( ► Figure 10.6):
• Tracheal (or pulmo-tracheal) route: Skin pene­
.E
tration of free-living L3(for example, at the coronary Q)
band of a calf's claw or the abdominal wall) and I
migration to the subcutis-+ migration into lymphatic
vessels or veins-+ lympho-haematogenous transport
to heart and lungs - migration of larvae from
capillaries and invasion of alveoli - migration
via the respiratory tract and pharynx to the small
intestine - through 2 moultings development
into adult females. After peroral infection, the
L3 probably penetrate the mucosa of the upper
digestive tract, and then follow the tracheal route.
The prepatent periods are short in most Strongyloides
species ( ► Table l 0.1 ).
• Somatic route: After infection, the larvae pass in
Q)
the bloodstream to the lungs and are subsequently
·o
C:
transported via the systemic blood circulation i5
Q)
to different organs (including subcutaneous fat, �
mammary gland, muscles, etc.). Furthermore, �
after skin penetration, larvae can migrate from the al
C:
·;::
subcutis directly through body tissues, thus reaching Q)
different organs. Experimental studies suggest that j
direct somatic migration plays a greater role than .£
spreading of larvae via the systemic circulation. >,
Ol
In body tissues, parasitic larvae (L3) can remain 0
0
viable in a hyp obiotic state for prolonged periods 'ci.i
(e.g. larvae of S. suis in pigs for at least 2½ years). al
al
Such 'somatic' larvae, becoming activated during 0..
 Part Ill. Parasites and parasitoses: metazo a

Adult female
Larva 3

Larva 2

� xualy mature male (ot)Ove) Larvae 2-4

an--'1 femat (l:5elo,w)

Figure 10.6. Life cycle of Strongyloldes suls (Graphics: IPZ. S. Ehrol).

the peripartal period and lactation, can migrate piglet 3 days). Therefore, it is assumed that larvae
to the mammary gland, be excreted in the milk transmitted through colostrum establish in the
and transmilled to the offspring (lactogenic small intestine without previous systemic migrntion.
transmission). Prenatal Strongyloides infections do not play a role
Q)
• Lactogenic infection: After a heavy initial infection in domestic animals.
·o
C

of a sow, lactogenic infections of piglets can take

� place until the 3 rd liller, since not all hypobiotic • Life cycle of Strongyloides stercoralis. Special
larvae are activated at once. In piglets, lactogenic features of S. stercoralis are that I.I hatch from eggs
ro infections can also occur soon after percutaneous already in the intestine and autoinfections are possible.
C
·.:::: infection of the sow, due to dissemination of larvae Autoinfections occur when part of the LI develop in
Q)
in the body. The excretion oflarvae in milk is highest the intestine into L3, which begin a systemic migration
,r; at the beginning of lactation; the duration is subject from the large or small intestine or the perianal skin and
>,
Ol to fluctuations in various animal species (callle: return then lo the intestinal tract. Some of these larvae
0 7-33 days, sheep: 7-19 days, horse: 4-47 days, pig: use the tracheal route, others apparently other pathways.
0
:!::'.
(/)
1-21 days). After lactogenic infection of new-borns, In chronically infected hosts, persistent females can
co the prepatent periods ( ► Table JO.I) are shorter cause unnoticed autoinfections for long periods ( up to
co
a.. than after percutaneous infection (calf 6, foal 8, 40 years in humans) ( ► p. 263). Females are also able
r
10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)

Table 10.1. Species (selection) of the family Strongyloididae.

Specles1 length (L) of parasitic Hosts Organ site of adult females, Stages In ftesh faeces
females, distribution (D) prepatency (day11) and size

Strongyloides papillosus 1 cattle. sheep. goat. wild small intestine eggs

L:6-Bmm ruminants. rabbit. hare prepatency:9- 14 47-60x25-30 µm ctl
D:worldwide -- - - - -- ---- u
.:;
Strongyloides westerl 1 horse and other equids small intestine eggs '6
.D
L: 8-9mm prepatency: 10-14 40-52x32-49 µm ctl
..c
D: worldwide a:
Strongyloides suis 1 pig, wild boar small intestine eggs
(syn. S. ransom,i prepatency: 6-9 45-55x28-32 µm

--
L:4.5-5.5 mm
D:worldwide - --
Strongyloides stercora/1s 1 dog, cat 2, monkeys. humans small intestine 1 91 stage larvae
L:2.0-2.8 mm prepatency: 9-19 228-353x 15 µm
D: tropics. subtropics, rarer In
temperate regl�s -- - - -- - - - -- -
Strongytoides fuellebornl Old World monkeys small lntesllne eggs

-
L: 2.9-4.2 mm (chimpanzee, baboon, oran g- prepatency: 28 50x30 µm
D: Africa, Asia utan etc.)3, humans
Strongylo/des ra tti1 wild rodents, laboratory small Intestine eggs
L: 1.7-3.4 mm rodents (experimentally) prepatency: 4- 7 42-73x21-37 µm
D:Europe, North America
Strongyloides avium 1 chicken, turkey, goose, duck, small Intestine and caeca e g gs
L: about 2.0 mm wild birds prepatency:5-6 52-56x36-40 µm
D:Asia, Europe, North America
1 Species occurring in Central Europe.
2 Further species in carnivores: Strongyloides felis in cats (regarded by some authors as synonymous with S. stercoralis) (Australia, India),
S. planiceps in dog, raccoon dog, cat, fox (Japan, Malaysia). S. tumefaciens in cat (USA).
3 S. cebus in New World monkeys, e.g. capuchin monkeys.

to interrupt egg production temporarily and resume it
later. In dogs, lactogenic transmission of S. stercoralis
larvae has been demonstrated. However, only larvae
were excreted in the colostrum if the bitch acquired a
primary infection immediately post partum.
Occurrence and epidemiology. On a global scale,
Strongyloides infections are quite frequent in domestic
ruminants, horses and pigs, especially in young animals.
Average prevalences of egg shedding in mixed age
populations are often rather low, but in groups of young
animals they may reach locally and temporarily values
around 20-90%. Depending on the region, housing
conditions and hygiene standards, pig herds may
be free of Strongyloides or infected at varying levels.
Heavy infections can cause significant losses in piglet
breeding. Recent data from DE revealed a Strongyloides
prevalence of 4% of 126 horse farms. S. stercoralis is
rather rare in dogs in Europe (e.g. IT: 0.8%), but more
frequent in tropical regions (e.g. Brazil: up to 26%).
Under certain conditions such infections may be fatal
in dogs (see below). This species can also cause illness in
monkey colonies of zoos or primate stations. In Europe,
Strongy/oides avium occurs in wild birds.
Some special features have to be considered in the
epidemiology of the Strongyloides species. The external
development is favoured by humidity and higher
temperatures (20 °C); under drought conditions the
larvae rapidly die. In the environment, additional
infectious 13 can be produced be a sexual generation.
Percutaneous infection is epidemiologically important
and is made possible by skin contact with a faecally
contaminated environment (soil, litter, stable floors, etc.).
In piglet breeding, moist areas of the stable floor under a
heat radiator provide particularly favourable conditions
for the development of S. suis and percutaneous
infection. In ruminants, horses and pigs, lactogenic
infections of new-horns play an important role and can
surpass the significance of percutaneous infections. In
all Strongyloides species, the prepatent periods are short
( ► Table 10.1), so that egg shedding in faeces begins
soon after a primary infection. Beneficial for affected
hosts is a usually rapid immune response that controls
the infection which often remains asymptomatic.
Immunology. Depending on the intensity of the
infection, an immune response occurs sooner or later
and controls the worm population, protects from disease
and is associated with a decrease in egg shedding. The
degree of acquired immunity influences the duration of
patency as well as the establishment of parasite stages
originating from new infections. In foals, the earlier
the infected animals received specific anthelmintic
treatment, which apparently impaired the development
of immunity, the earlier re-infections occurred. Studies
Part Ill. Parasites and parasitoses: metazoa
with S. stercoralis have shown that larvae are killed several
hours after penetration of immune mice by a combined
action of IgM, complement and eosinophils. Impaired
immunity, due to illness or immunosuppressive drugs
(e.g. glucocorticoids), may cause hyp erinfections with
fatal consequences (see below) in dogs and humans
infected with S. stercoralis.
Pathogenesis. Penetration of Strongyloides larvae
into the skin may cause erythema, papules, oedema,
and after repeated infections allergic dermatitis. Such
changes at the coronary band, the fetter or on other
parts of the body have been described, for example, in
calves kept loose in stables(► Figure 10.7). In the lungs,
Strongyloides larvae emigrating from blood vessels into
alveoli cause petechial haemorrhages and small foci
of inflammation. In the small intestine, Stro11gyloidc$
females establish mainly in the duodenum and anterior
ileum, where they lie in tunnel-like aisles of the epithelial
layer, especially at the base of villi and to some extent
in the intestinal glands. Parts of the parasites protrude
into the intestinal lumen. The eggs are released into the
aisles or the intestinal lumen. Due to the presence of
Strongyloides females, the epithelium is flattened and
the basement membrane bulged out into the propria,
giving the impression that the parasites lie within the
propria. In immunocompetent hosts, the parasites
do not pass through the muscularis mucosae into the
submucosa, but this is possible in S. stercoralis infected
immunodeficient hosts (see below).
Depending on the infection intensity, Strongyloides
can cause more or less pronounced catarrhal enteritis
with desquamation and destruction of villus epithelia,
partial epithelial hypertrophy, villus atrophy and cellular
infiltration of the lamina propria. The consequences of
these alterations include reduced activity of mucosa!
enzymes (alkaline phosphatase, saccharase, maltase),
malabsorption of amino acids and loss of plasma proteins
into the digestive tract. In S. stercoralis Infections of dogs,
immunosuppression can induce severe hyperinfcctions,
Figure 10. 7. Strongy/oides pap/1/osus Infection in a calf: lesions
at the coronary band and the fetter (Photo: Taira et a/.).
leading to haemorrhages and inflammatory changes of
the small and large intestines, lungs and other organs. In
such cases, large numbers of Strongyloides females and
Ll-3 were found in the intestinal mucosa. In addition,
parasite stages colonised different extraintestinal organs,
such as liver, kidney, spleen, bladder, brain, skin and
muscles.
Clinical signs. Heavy Strongyloides infections can
cause disease and death, predominantly in young
animals. Weak infections or infections of older animals
usually remain asymptomatic.
• Piglets. First symptoms occur about two weeks
after birth: diarrhoea, fatigue, unsightly skin, retarded
growth, hypoalbuminaemia and sometimes anaemia.
In heavy infections, death is possible.
• Calves, sheep and goat kids. In heavy infections
cliorrhoea, rarely fatal cuses.
• Foals. Desicles rotavirus, Clostridium perfringens
and Cryptosporidium, heavy S. wester( infections are
responsible for diarrhoea in foals. Rarely, serious clinical
conditions have been described in foals with enteritis,
hypoalbuminnemia, hypoproteinaemia, anaemia,
subcutaneous oedema, increase of peritoneal fluid and
other symptoms.
• Dogs and cats. In tropical regions, dogs and
cats are quite frequently infected with S. stercoralis,
but rarely in Europe. Occasionally, this parasite occurs
in populations of laboratory dogs or in dog breeding
stations. Severe hyperinfections with lethargy, cough,
dyspnea, enteritis and other signs have been described
in dogs under drug-induced immunosuppression.
• Monkeys. Massive S. stercoralis infections have
been reported as causes of morbidity and mortality of
monkeys in zoos. This species and S. fuelleflorni olso
occur in primate sanctunris.
Diagnosis. Patent Strongyloides infections in ruminants,
horses, pigs, etc., ore diagnosed by egg detection In fresh
faeces(flotation technique). Because LI can hatch from
eggs already a few hours after defnecalion, the Bacrmann
technique (► p. 530) should be also employed for
isolating larval stages. The use of this technique is also
indicated in cases of suspected S. stercoralis infections.
Copro-cultures or the Agar plate culture and harvesting
L3 improve the diagnostic sensitivity and provide
material for differential diagnosis of larval stages(► p.
532). As a source of error, a potential contamination of
faecal samples with free-living nematodes should be
considered. Detection of specific serum antibodies can
provide further information, for example in S. stercoralis
infections in dogs and monkeys. Several techniques
for detecting Strongyloides DNA in faecal samples are
now available. Postmortem diagnosis: smears of the
r
10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)

intestinal mucosa are examined microscopically, or the Families Rhabditidae and Cephalobidae
sediment of the intestinal washing fluid is screened with
a stereomicroscope. Accidental ecto- and endoparasites

Therapy. Treatment of intestinal Strongyloides Pelodera strongyloides (syn. Rhabditis strongyloides)

infections in ruminants, horses and pigs with (pro) (Family Rhabditidae) is a free-living nematode that lives
Ctl
benzimidazoles in increased dosages(e.g. fenbendazole in soil and decaying organic material. Rhabditiform "D

u
:;:::,
50 mg/kg b.w., p.o. against S. westeri) or macrocyclic larvae(length about 650 µm) of this species are sporadic
.D
lactones(ML)(► Table 19.2, 19.6, 19.8, 19.10, p. 579 skjn parasites in cattle, horses, dogs and rodents Ctl
..c
ff). The efficacy of benzimidazoles against S. stercoralis where they can cause dermatitis, especially on limbs, a:
in dogs is insufficient, but single doses of0.2 mg/kg or ventral body regions and perineum. Halicephalobus
0.8 mg/kg b.w., p.o. ivermectin (off label I) are highly glngivalis (syn. 1-/alicephalobus deletrix, Micronema
effective against adult and larval intestinal stages (not deletrix) (Family Cephalobidae) is also a free- living
against extraintestinal stages!). As alternatives, other nematode, occurring in soil, that causes occasional
MLs, approved for use in dogs and active against infections in vertebrates. Most commonly such cases
Strongyloides in other host animals, can be considered. have been described in horses and only rarely in humans.
Probably, the nematodes are taken up by horses with
Zoonotic importance. Infective larvae of various feed, they invade host tissues through mucosal lesions
Strongyloides species and hookworm larvae(► p. 285 ) and are subsequently spreading to various organ
of animal origin can penetrate the human skin and systems. Multiplication of the nematodes in the host is
cause clinical sings of 'larva migrans externa' ( ='larva apparently possible, as indicated by frequent occurrence
migrans cutanea' or 'creeping eruption'). Associated skin offemales(length 250-445 µm, rhabditoid oesophagus),
lesions include erythema, papules, itching and tortuous larvae (length 1 29-2 20 µm, rhabditoid oesophagus)
migration tracks, which can persist several weeks. In the and eggs (19-40x 10-17 µm). The nematodes cause
skin, larvae remain viab!e only a few weeks, and usually granulomas and degenerative changes, especially in
do not invade the body. the sinuses of the head, in CNS, kidneys, and lungs,
but also in other organs. In the kidney, pathological
Other than the zoonotic Strongyloides species, usually changes appear as greasy, up to fist-sized foci. Clinically,
restricted in their invasiveness to the human skin, central nervous disorders, recumbency, swellings in
S. stercoralis and S. fuelleborni can cause intestinal the head region, nasal discharge, bone fractures and
Cl)
infections in animals and humans. In Africa, natural other signs may appear. Diagnosis is made in living .c
transmission of S. fuelleborni from primates to humans horses by biopsy of externally accessible granulomas
has been suggested. S. stercoralis of human origin can and histological detection of parasites or post mortem
.E
<i5
establish intestinal infections in dogs after experimental by pathohistological examinations. In one case, after I
infection. However, reports of human cases of canine surgical removal of a localised granuloma, ivermectin
origin are rare. Since various genotypes of S. stercoralis in an increased dosage (3x in intervals of 2 weeks 1.2
have been identified, it is assumed that they could have mg/kg b.w. p.o.) was effective.
different host specificities, and transmission between
animal and humans might occur less frequently than
previously thought. - Selected references------•

Strongyloidosis in humans, caused by S. stercoralis, has
a global distribution and is currently regarded as an
emerging infection, especially in the subtropics and
tropics. Prevalences in humans vary between sporadic
cases(imported or autochthonous) and values over50%.
Whereas heavy acute infections may be associated with
Brigand RA, Rotman HL, Leon 0, Nolan T J, Schad GA,
Abraham D (1998) Strongyloides stercoralis host-adapted
third-stage larvae are the target of eosinophil-associated
immune-mediated killing in mice. J Parasitol 84: 440-445.
Eberhardt AG, Mayer WE, Streit A (2007) The free-living
(l)
generation of Strongyloides papillosus undergoes sexual C:

gastrointestinal, pulmonary and other clinical signs, reproduction. Int J Parasitol 37: 989-1000.
·u
u
(l)
chronic infections are often asymptomatic. However, Hasegawa H, Sato H, Fujita S, Nguema PP, Nobusue K,
�
chronic, unnoticed infections may become activated Miyagi K, Kooriyama T, Takenoshita Y, Noda S, Sato
2:­
Ctl
by immunosuppressive diseases(e.g. HIV infection) or A, Morimoto A, Ikeda Y, Nishida T (2010) Molecular C:
·.::
therapeutic measures(e.g. long-term steroid therapy), identification of the causative agent of human strongyloidiasis (l)
leading to live-threatening, uncontrolled autoinfections acquired in Tanzania: dispersal and diversity of Strongyloides
with dissemination of parasite stages to multiple organs spp. and their hosts. Parasitol Int 59: 407-413. _s;
(intestine, liver, lung, kidney, CNS etc.)('hyperinfection >,
CJ)
syndrome' and 'disseminated strongyloidosis'). 0
0
"iii
�
a..Ctl
Part Ill. Parasites and parasitoses: metazoa
Hermosilla C, Coumbe KM, Habershon-Butcher J,
Schoniger S (2011) Fatal equine meningoencephalitis in
the United Kingdom caused by the panagrolaimid nematode
Halicephalobus gingivalis: case report and review of the
literature. Equine Vet J 43: 759-763.
Labes EM, Wijayanti N, Deplazes P, Mathis A (2011) Genetic
characterization of Strongyloides spp. from captive, semi­
captive and wild Bornean orangutans (Pongo pygmaeus) In
Central and East Kalimantan, Borneo, Indonesia. Parasitology
138: 1417-1422.
Nadler SA, Carreno RA, Adams BJ, Kinde H, Baldwin JG,
Mundo-Ocampo M (2003) Molecular phylogenesls and
diagnosis of soil and clinical isolates of Halicephalobus
gingivalis (Nematoda: Cephalobina: Panagrolalmoldea), an
opportunistic pathogen of horses. Int J Parasitol 33: 1115·
1125.
Nolan TJ, Nutman TB, Schad GA (2011) Strongyloldosls. In:
Palmer SR, Lord Soulsby, Torgerson PR. Brown DWG (eds.)
Oxford textbook of zoonoses. 2nd ed. Oxford, UK: Oxlord
University Press. pp. 717-726: ISBN 978-0-19-857002·8.
Puthlyakunnon S, Boddu S, LI Y, Zhou X, Wang C, LI J,
Chen X (2014) Strongyloidiasis - an insight into Its global
prevalence and management. PloS Neg! Trop Dis 8: 83018.
Riggio F, Mannella R, Aritl G, Perrucci S (2013) Intestinal and
lung parasites in owned dogs and cats from central Italy. Vet
Parasitol 193: 78-84.
Saari SAM, Nlkander S (2006) Pelodera (syn. Rhabditis)
strongyloides as a cause of dermatitis of 11 dogs from
Finland. Acta Vet Scand 48: 18.
Schir F, Trostdorf U, Giardina F, Khleu V, Muth S, Marti H,
Vounatsou P, Odermatt P (2013) Strongyloides stercoralis:
glObaJ dislnbutlon and rlSk factors. PloS Negl Trop Dis 7:
e2288.
S treit A (2014) How to bocome a parasite without sex
chromosomoS: a hypothesis for tho evotu1ion of Strongyloides
spp. end rel8tod nomotodos. Parasitology 141: 1244-1254.
10.1.2 Order Strongylida
Strongylos(G): round.
The order Strongylida comprises 4 superfamilies of
important nematodes(► Table 9.1), which parasitise
the gastrointestinal tract, the lungs or other organs of
various domestic and wild animal species or humans. A
characteristic morphological feature of the Strongylida
is the mostly well-developed bursa copulatrix of the
males(► Figure 10.4).
- Superfamily Strongyloidea
Family Strongylidae
• Subfamilies Strongylinae, Cyathostominae
and Gyalocephalinae
Genus Strongy/us and genera of
Cyathostominae and Gyalocephalinae
(horse strongyles)
Disease: Equine strongytidosls and
cyathostominosis.
Summary
• Agents. Numerous species of the Strongylidae are
Internal parasites of equines. Further genera and
species, not considered here, are parasites of other
animal species (elephant, rhinoceros, ostrich, etc.).
Parasites of the large Intestine of equines Include
'large atrongylea' (Strongy/us vulQBrls, S. equlnus,
S. edentatut) and 'small ltrongylea', the latter with
approxlmately 80 apecl•, moat of them belonging to
the aubfamtly Cyathoetomlnat. Mixed lnfect1on1 with
lpeciN fram both groupt, ptlVioully wldtly diltrlbutld
and common, n now me In well aupervtltd horll
populations, btcaUM lhl large 1trongylt1 have bttn
latglly tllminatld by frwquent anthelmlntlc trHtment1.
• Lift oyote. HorN ltrongyltl n tranammtd In direct
cyclol. � dlYltopmtnl from egg to free-llvlng L3.
Infection per OI by lngNtlon of L3. lntemal dtvtlopmenl
of lffllll �: aft• lnfec:tlon - 111,totrople phaH
(l3 -. l.4) In wall of caecum and oolon: hypobk»la
(1.3, ,-tty l.4) may occur; p,9p11tency, depe,,dlng on
apedea, 1�3 monthl. ui,ge ltrongylel: parenteral
m6gration aftlr Infection, fo, example S. VU/Qlrll ... L4
colon wall - migratlOn In wall of arterial veuel• - to
1'001 of the anterior rneeenteric artery (there moulting
to 5111 stage) - return in artenes to the bowel wall -.
imrrugratlOfl into intestinal lumen; prepatenl period
of S. vulpa,Js 6�7 months, SYl-11 months in other
..�species
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)
•
, Occurrence and epidemiology. Worldwide distribution.
Infections of horses mostly during pasturing. In Central
Europe, main risk of Infections with large and small
atrongyles In the second half of the grazing period.
However, epidemiological conditions can vary widely,
depending on grazing management and other factors.
, Pathogeneala. Large strongyles are particularly
pathogenic, because of parenteral migration of
fuvenlles, especially S. vu/r,arls (damage to arterial
vessels). Small strongylea are leaa pathogenic, but
heavy Infections can cauae enteropathlea with protein
loaa, especially after reactivation of large numbarl of
hypoblotlc stages within a short period of time Oarvll
cyathostomlnosls). Adult stages of large and email
atrongylea play a subordinate role pathoganatlcally.
• Cllnlcal elgne. Chronic forms are most common:
lnappetence, poor condition, emaciation, Intermittent
diarrhoea, hypoalbumlnaemla, colic. Acute strongylosls
(S. vu/garfs): embolic-thrombotlc colic, lethargy, fever,
altered peritoneal fluid. Larval cyathostomlnosls: mainly
In winter and sprtng, diarrhoea with acute onset and then
persistent, anorexia, colic, fever, hypoalbumlnaemla,
hyper-�•globullnaemla, decreased albumin/globulin
ratio, oedema, and often death.
• Dlagnosla. Epldemlologlcal and clinical case
histories are diagnostically Important. Egg detection
In faeces (flotation techniques) In patent Infections.
ldentmcatlon of large and small strongyles Is possible
by differentiation of L3, obtained from copro-cultures.
Detection of Immature stages In faeces In larval
cyathostomlnosls. By counting of eggs In faecal
samples (modified McMaster technique), horses with
relevant egg shedding can be Identified.
• Therapy. Stages In the large Intestine: pyrantel,
(pro)benzlmldazoles and macrocycllc lactonee (ML),
Problem: widespread resistance of small atrongyllB
against benzlmldazoles, to a lesser extent also against
pyrantel and ML. Hypoblotlc stages of small strongylea
In the Intestinal wall and migrating stages of large
strongyles: only some anthelmlntlcs are sufficiently
effective.
• Control. Strategic treatment with anthelmlntlca and
other measures (grazing management, pasture hygiene).
Different species of the Strongylidae are the most
important internal nematode parasites of horses (=
horse strongyles) and other equines (donkey, zebra,
mule) worldwide. Other members of this family occur
in elephants, rhinoceroses, ostriches and other species.
Only strongyles of equids are considered here.
Agents. Horse strongyles are approximately 0.5-5
cm long and rather thick nematodes( ► Figure 10.8)
with the following common features: large buccal
capsule in large strongyles, smaller buccal capsule in
small strongyles, double leaf-crowns (corona radiata)
around the mouth opening( ► Figure 10.9), males with
well-developed bursa copulatrix and two long, thin
spicules. Traditionally, distinction is made between large
cu
:'Q
>,
0)
e
C
if)
Figure 10.8. Small strongyles (length about 15-20 mm) (Photo:
IPZ).
and small strongyles, whose length dimensions partly
overlap(► Table 10.2).
In this text, species of the genus Strongylus are referred to
as large strongyles, species of all other genera as small
strongyles. This grouping is not commonly used, but
from a biological point of view it makes sense, because
juvenile stages of large strongyles undertake extensive
parenteral migrations in the host, while small strongyles
pass only a histotropic phase in the intestinal wall.
Further significant differences exist between these two
groups in terms of prepatent periods, pathogenesis, drug
resistance and other aspects. Often all small strongyles
are referred to as Cyathostominae, though in a strict
sense, this term is applicable only for members of this
Cl)
..c
subfamily(► Table 10.2). c
.E
c6
:r:
Strongylus species are approximately 1-5 cm long,
about 1 mm wide and yellow-brownish nematodes
with a large, barrel-shaped mouth capsule. Species of
worldwide importance are S. vulgaris, S. equinus and S.
edentatus which are relatively easy to distinguish solely
on structures of the buccal capsules ( ► Figure 10.9).
Additional morphological features (including bursa,
spicules, etc.) and DNA characteristics can be used for
species identification.
The yellow-white or reddish species of small strongyles
are between 0.5 and 3.0 cm long with a majority of
them being smaller than large strongyles. The most
common members of this group are the Cyathostominae
(cyathostomins) with approximately 5 0 species,
whose mouth capsules are smaller and cylindrical or
rectangular, as compared to that of Strongylus species
( ► Figure 10.9). Cyathostomins regularly occur in mixed
infections of various species (>25 per animal), but the
proportions are subject to regional variations. In Central
Europe, the following species are the most common
with prevalences of75-100%: Cyathostomum catinatum,
Coronocyclus coronatus, Cylicocyclus insigne, Cylicocyclus
nassatus, Cylicostephanus calicatus, Cylicostephanus
goldi, Cylicostephanus longibursatus and Cylicostephanus
minutus (for a list of all species, see Lichtenfels et al.,
 Part Ill. Parasites and parasitoses: metazoa

Table 10.2. Strongylids of equids: selection of genera and species.

Collective names Subfamllles, genera and species, length of males (��) and females (�� ), number of
species in parentheses

Large strongyles1 Subfamily: Strongylinae

with parenteral migration Strongylus vulgaris2 , Strongylus equinus2 , Strongylus edentatus 2 , Strongylus asini
Prepatency: 6½-11 months (total 4 species) o'o': 10-35 mm,��: 13-50 mm
Small strongyles Bidentostomum (1), Craterostomum 2 (1), Oesophagodontus (1), Triodontophorus2 (7)
without parenteral migration (total 10 species) cM: 6-20 mm,��: 7-29 mm
r--- ·
Prepatency: 1½-3 months Subfamily: Cyathostominae
Cyathostomum2 (5), Caballonema (1), Coronocyclus 2 (5), Cylicocyclus2 (11),
- Cylicodontophorus 2 (2), Cylicostephanus 2 (7), Cylindropharynx (7), Petrovinema2 (2) and 5
(L_:0her g�ner� �j!�_]_1 sp�ies to�I _51 �p�les)iM°: 4-15 mm, ��: 5-22 mm
Subfamily: Gyalocephalinae
Gyalocephalus capitatus2 ( 1)
oo:7-10 mm, 'i1 'i) : 8-13 mm
1 Some authors allocate not only species ot tho genus Strongylus, but all genera or the sublomlly Strongylinae to the large strongyles.
2 Species or genera documented In Central Europe.

Double Ioli! crown Mouth oponlng Dorso! gutter with terminal

duct of oesopt1agoal gland

'I'

2 l'0lrded tNlh-lke .. teeth-Ike strucl\l'8S No teeth-like structures

llruCt\.lle at the bale
d the buCCel �
Sfn:>n01usvulgarls Strongytus equlnus Strongylus edentatus

131...c.tl oip,- _, Ol.11:.<.� c. ,ulr, WO!t lh,,n lonl: t, 81"-C,1I c...1p'lul0 cytu)(lriCol.
b:111ul fil\ttJJ'l<.I, II 1"'1111 11<,1 o,1tttr"� Ju.if •..IOM't with B. u�torn,;t k,11 crown wllh
SII\JCtl6lll lnlfmnl w1m 2a 24 IIIIITIC)flll 6 tafgo OiOmllnl!l
tdllnro,,q
QllflrOltonUn

Figure 10.9. Buccal capsules of stroogyles, semi-schematic (Graphics: IPZ, S. Ehrat).

2008). Morphological species identification is difficult
and must be left to specialised laboratories; molecular
methods are available for species identification.
Life cycle. The life cycles of strong)•les consist of an
external (preparasitic) and an internal (parasitic) phase
(► Figure 10.10).
• External (preparasitic) development. This phase
is very similar in large and small strongyles. Strongyle
carriers pass in their faeces thin-shelled eggs, usually
containing more than 8 blastomeres. In the environment,
LI develop in a short time, they hatch from the eggs, and
moult to L2. These stages ingest faecal bacteria, from
which reserve substances (mainly lipids) are formed
and deposited in intestinal cells. After further growth
• 10 Phylum Nematoda (syn. Nematozoa) (threadwOl'ms 0/' rounclworms)

Adult strongylids
(immature stages not shown)

Figure 10.10. Life cycle of Strongylus vulgarls (Graphics: IPZ, S. Ehrat).

and differentiation, an incomplete moulting occurs by
which the cuticle is separated from the hypodermis, but
is not discarded. The resulting L3 with its newly formed
cuticle remains completely enclosed by the old cuticle,
which serves as an outer protective envelope( = sheath,
exuvia) and contributes to resistance to environmental
influences. The L3 are infective stages that can survive
for weeks to months on pasture, although they do
not feed. L3 leave faecal deposits actively, or they are
disseminated passively. With sufficient moisture, L3
migrate onto plants and are thereby ingested by grazing
horses.
• Internal (parasitic) development. In the intestine
of equines, the L3 hatch from the sheath under the
influence of given physiological conditions and begin
their internal development which differs between small
and large strongyles.
Exsheathed L3(devoid of sheath= parasitic L3) of the
small strongyles invade the mucosa or submucosa of
the caecum or colon where they moult and differentiate
to L4 within 6-12 days(► Figure 10.11). These larvae
pass through a 'histotropic' phase, which usually
lasts 1-2 months, but sometimes takes much longer.
Subsequently, they return to the intestinal lumen and
Part Ill. Parasites and parasitoses: metazoa
Small strongyles
Dorsal colon
Ileum
Ventral colon
L3 L4
Enlarged detail
Development:
penetration of exsheathed larvae (L3) Into Intestinal
wall and moulting to L4
- return to Intestinal lumen, moulting to 5th stages:
hypoblosls of L3 In Intestinal wall possible
Prepatency: 1 Ya - 3 months
Figure 10.11. Internal development of Cyathostominae
(Graphics: IPZ, S. Ehrat).
develop after another moulting into sexually mature
stages (moulting to 5rh stages sometimes occurs in the
intestinal wall). The adult stages usually settle in the
ventral colon and the caecum, and partly also in the
dorsal colon. Prepatent periods vary between species
(as far as currently known) between l ½ and 3 months;
the patencies may last up to 2½ years. An important
phenomenon in the development of small strongyles is
hypobiosis (see below). Current knowledge on the life
cycles of many species of small strongyles is incomplete.
In contrast to small strongyles, juvenile stages of large
strongyles undertake extensive parenteral migrations
on different routes, after moulting to L4 has occurred
in the large intestinal wall or the liver (S. t!dentatus).
These complicated routes are depicted in ► Figure
10.12. The biological functions of these migrations are
still obscure, but their practical significance is obvious
and lies in the substantial harmful effects which can be
induced by migrating stages, depending in severity on
the various Strongylus species and other factors.
Preferred sites of adult large strongyles are the caecum
(S. vu/garis), the transition region between caecum
and colon as well as the ventral colon (S. eq1Jit1us, S.
edentatus). The prepatent periods of large strongyles
are much longer than in small strongyles and last 6½-
11 months; the patent periods of S. v1Jlgaris and S.
edentatus are reported to last 11/2 years and 10½-11
months, respectively.
Occurrence. Strongylus vulgaris, S. equinus and S.
edentatus have a cosmopolitan distribution, while S. asini
is less widespread (Africa, Asia, South America). The
first mentioned species, previously common everywhere,
have become rare in horse populations in which frequent
anthelmintic treatments have been carried out over
many years (for example: S. vulgaris was detected in
only 0.8% of 126 horse populations in Brandenburg/
Germany, 2011). If control measures are less intensive or
absent, the prevalences of Strongylus species can still be
quite high, depending also on the type of maintenance
and other factors. Small strongyles, especially species
of the subfamily Cyathoslominae, are present in almost
all horse populations, although there are significant
differences in species composition and in prevalence.
The burdens of large strongyles are generally low (a few
to several hundred specimens per animal), while those
of small strongyles are often very high (several thousand
to about 3 million specimens per animal).
Epidemiology. Precise epidemiological knowledge is
an important prerequisite for planning strategic control
programmes. In the following section, epidemiological
key factors are discussed, referring to the climatic
conditions in Central Europe.
• Infection of hosts. Horses become infected mainly
during the grazing period by ingestion of L3 with fodder
plants ( ► Figure l 0.13). Infections in stables and in pens
are possible if L3 have developed in faeces or in litter and
are taken up by the horses with food from the ground
or when they are licked off stable walls. Furthermore,
L3 may be introduced with contaminated forage (or
hay) and lead to infection of housed horses. However,
such infections in stables are of minor epidemiological
importance.
• Pasture contamination with strongyle eggs.
Pastures arc contaminated with strongylc eggs by horses
infected with mature strongyles ( ► Figure I 0.13). At
the beginning of the grazing season in spring, older
horses (e.g. mares), which had become infected in the
previous year and remained carriers of strongyles during
winter because of inadequate or lacking treatment, may
excrete eggs. In infections with cyathostomins, a positive
correlation has been found between increased egg­
shedding in spring and reactivation of hypobiotic stages
(see below). Furthermore, foals can acquire infections in
spring or later during the grazing period and excrete eggs
at the earliest I½ months p.i. (small strongyles) or 6½
months p.i. (large strongyles). Some of the eggs which
are shed to pastures in late autumn, can remain viable
until the following spring. Donkeys are susceptible to
various species of large and small strongyles, and have
to be considered as potential excretors of eggs under
conditions of mixed grazing with horses. With regard
to control it is important to note, that usually only a few
horses with medium to high eggs counts contribute the
largest share of pasture contamination.
♦ 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)
Pancreas
Figure 10.12. Internal development of various Strongylus species (Graphics: IPZ, S. Ehrat).
• Pasture contamination with infective larvae
(L3). Preparasitic L3 develop in just one week at
temperatures of 25-30 °C and sufficient moisture
fro m strongyle eggs, deposited in faeces. At lower
temperatures, this development will take longer. The
minimum temperature for the development is 10 °C,
the maximum 35 °C. At low temperatures or desiccation
development is interrupted. At 15-20 °C, the 13 live
on pasture for 1-2 months; they can survive periods
of dryness within faecal pellets at sufficient humidity
(>20%), e.g. larvae of small strongyles for 3-4 months. L3
ofbot h large and small strongyles are rather resistant to
cold and can overwinter on pastures in Central Europe.
The number of overwintering larvae is influenced by
various factors, including the degree and duration of
Strongylus vulr,arls
Development:
Penetration of L3 Into large Intestinal wall and
moulting to L4 C1l
-+ migration of L4 on or In the lntlma of arteries :g
>,
to A. mesenterlca cranlalls, moulting to 5th stages O>
e
C
from day 90 p.l.
-+ back migration In arteries to Intestine.
Pntpatency: 8� -9 months
Strongylu• equlnu•
Development:
Penetration of L3 Into large Intestinal wall, mouftlng
to L4
-+ migration of L4 through peritoneal cavity to liver,
there migration for several weeks
- migration to pancreas, moulting to 5th stagea
-+ migration to caecum.
Prepatency: 81/2 - 9 months
Strongylus edentatus
Development:
Penetration of L3 Into Intestinal wall, transport In
portal blood to liver, moulting to L4
-+ migration phase via liver ligaments and
i'etroperltoneally, moulting to 5th stages
- back migration through mesenterium to Intestine.
Perpatency: 10� - 11 months
pasture contamination in previous autumn and the
weather conditions(temperature, humidity, snow cover,
etc.). The degree of pasture contamination with 13
during the grazing period depends on the intensity of
egg excretion by parasite carriers, the grazing density,
the age groups of horses as well as the development and
survival conditions of the larvae.
• Seasonal dynamics of infective larvae.
Knowledge about seasonal dynamics of infective larvae
is important for understanding the epidemiology. This
is demonstrated here for a permanent pasture grazed
by mares and foals(► Figure 10.13).
 Part Ill. Parasites and parasitoses: metazoa
.�\9�.....................
Larvae (L3) on plants
·1ow·················•·······························
April May June July
Figure 10.13. Epidemiological scheme of horse strongylldosls. Egg-shedding by mares and foals as well as pasture contamination
with infective larvae. The diagram reflects the situation on a permanent pasture In Central Europe (Graphics: IPZ; after Urquhart
et al. 1987).
Some larvae of the overwintering population can survive
until May or early June, a smaJI proportion even longer
(12 months) under the climatic conditions of Central
Europe. Even if the density of these larvae per kg grass is
generally low, it can be sufficient for initial infections of
grazing hosts. On contaminated pastures, on which older
horses graze permanently, the larval density increases
from July/ August and remains high until the end of
the grazing period as shown schematically in ► Figure
10.13. These dynamics are subject to temperature- and
humidity-dependent fluctuations. Reasons for the rising
larval density include increasing pasture contamination
with strongyle eggs, accelerated larval development
at summer temperatures, and finally (in summer and
late summer) favourable conditions for translocation
of L3, i.e. their transition from faeces to fodder plants.
Transition occurs in an active manner, if the larvae, in
case of sufficient moisture, emigrate in a thin film of
liquid from faeces (up to about 30 cm horizontally)
and crawl onto plants (about IO cm vertically). When
exposed to dry conditions or strong sunlight, the
larvae withdraw to top layers of soil or to leaf axils.
Passively, translocation of larvae can occur in various
ways, including washing out by rain, distribution by
Q)
C dung beetles and other insects, mechanical spreading of
·c3
'6 manure, and projecting away from faecal pats by fungal
Q)
spores (see trichostrongyles ► p. 292).
�
� can cause serious disease (pathogenesis, see below).
(I:)
C • Main infection period. Data on seasonal dynamics
·c of infective larvae ( ► Figure l 0.13) show that on
Q)
permanent pastures infections of hosts are possible
.s throughout the whole grazing season, but the greatest
>­
OJ
infection risk exists in the second half of this period,
0 because in this time densities of larvae are highest on
0
·u5 fodder plants. This period of increased infection risk is
referred to here as the main infection period. However,
weather conditions may significantly modify the seasonal
-
Aug. Sept. Oct. Nov.
dynamics of L3 and consequently the main infection
period. For example, density of larvae on vegetation
may be very low in August/September after a longer dry
period during previous months. Furthermore, pasture
management and control measures can influence both
the density and dynamics of L3. On pastures grazed
throughout the year, there is a low or zero infection
risk during the winter period under normal weather
conditions.
• Hypobiosis in cyathostomins. An interesting
biological phenomenon of epidemiological and
pathogenetic significance is hypobiosis of larval
cyathostomines. After infection of a host, parasitic
L3 invade the intestinal wall and interrupt their
development for a prolonged period as L3 (length about
0.5 mm) or partially as L4. At necropsy, some of the
hypobiotic larvae are found in the intestinal lumen. Jn
horses that have spent at least one season on pasture,
hypobiotic stages arc present year-round in Central
Europe. Their share increases from July onwards and
can reach (in massive infections) 95% of the total worm
burden in winter. Reactivation of hypoblotic stages
occurs usually gradually in late winter or early spring and
results in the development of a new population of mature
stages, followed by increased egg shedding in faeces. A
synchronous reactivation of numerous hypobiotic stages
Various factors are discussed as potential causes for onset
and ending of hypobiosis of cyathostomines, including
dose of infection, number of adult worms present in the
intestine, removal of adult worms by chemotherapy,
immune status of the host, and environmental factors
(see trichostrongyles ► p. 293).
r 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)
Pathogenesis. Both groups of nematodes can develop
signi ficant adverse effects, depending on infection
intensity, immune status of the equine host, and other
factors.
t Infections with small strongyles (especially
Cyathostominae). Although the pathogenicity
of individual small strongyles is low, they can cause
significant damage in heavy infections. Pathogenetically,
the larval stages (L3 and L4) in the intestinal wall are
of special importance. In the mucosa and submucosa
the coiling larvae induce small nodules (about 0.5-5
mm in diameter), caused by accumulation of host cells.
The number of nodules can reach high densities (20-60
per cm2 mucosa). Later on, the larvae are surrounded
by fibroblasts and encapsulated by connective tissue
( ► Figure I 0.14). In the affected parts of the intestine,
a significant proliferation of goblet cells occurs. Often,
lymphocytes (T lymphocytes), macrophages, eosinophils
and plasma cells immigrate into the vicinity of worm
nodules. Further changes are small mucosa! bleedings,
extensive inflammatory infiltrations in the mucosa and
submucosa as well as oedema of the intestinal wall.
These changes are attributed to the direct action of the
parasites and the release of inflammatory mediators
from particular cells. In infected colon parts, the
concentration of cytokines (IL-4 and IL-10) are
significantly increased; the concentrations of TNF-a only
when numerous larvae emigrate from the intestinal wall.
Cytokines could inhibit pro-inflammatory reactions
or regulate immune responses that lead to increased
production of IgG 1 and IgE, mast cell activation and
increased production of mucus. Presumably, mast cells
and proteinases, produced by them, play a role in defence
mechanisms of the host. T hrough the damaged mucosa,
proteins (especially albumin), liquid and minerals
can leak into the intestinal tract. On the other hand,
harmful substances from the gut may pass to the host
body. Massive changes are especially associated with
the sudden reactivation and emigration of hypobiotic
stages from the intestinal wall. Similar changes may
occur after chemotherapy. After fenbendazole therapy
Figure 10.14. Small strongyles: (a) larval stages (length about
2-4 mm) in wall of large intestine (Photo: K. Pfister, ITPM); (b)
histological section (Photo: IPG, T. Steinbach).
T lymphocytes and eosinophils accumulated around
L4 in the submucosa, the parasites were enclosed by
granulomas, and eosinophils attached to the surface of
L4, which disintegrated.
Adult small strongyles play a minor role in pathogenesis;
although they firmly adhere with the buccal capsule to
the mucosa, they usually cause only limited and low­
grade lesions in superficial tissue layers. They feed
mainly on intestinal mucus, but some species can open
capillaries and suck blood..
• Infections with large strongyles. Nematodes of
the genus Strongyhis have a high pathogenic potential,
mainly because of parenteral migrations of their
juvenile stages (► Table 10.3). In highly susceptible
foals, primary infections with 200 L3 of S. vulgaris or
250 L3 of S. edentatus can already cause colic and/or
other symptoms.
Particularly serious are pathological changes of the
arterial vascular system, caused by S. vulgaris larvae
during their migration on or in the intima of the vessels
(thromboarteritis of submucosal arterioles and arteries,
thromboarteritis and aneurysm formation in the anterior
mesenteric artery and their branches) with resulting
changes (embolism, bowel infarction) and functional
impairment (impairment of blood circulation, colic)
(► Figures 10.15 to 10.18). Occasionally juveniles
deviate from their normal routes and migrate from the
anterior mesenteric artery in the aortic wall cranially
to the heart or caudally. Signs are typical lesions at
the aortic arch and the aortic valve or changes in the
femoral artery and other arteries; the latter may cause
intermittent claudication in hind limbs. Aberrant
juveniles, disseminated in the blood-stream to various
organs, can continue there to migrate and cause
significant alterations (e.g. in spinal cord and brain).
Juveniles of S. equinus and S. edentatus do not damage
blood vessels, but cause lesions in liver and other organs.
In S. equinus, the loss of secretory cells and fibrosis of
the pancreas are particularly noteworthy (► Table 10.3).
large intestine ef a herse (Photo. K. "l"omc-zuk)�. _____.
Part Ill. Parasites and parasitoses: metazoa

Table 10.3. Comparative overview of pathogenesis of strongylosis (also ► Figure 10.12).

Stages of parasites Strongylus vulgarls Strongylus equlnus Strongylus eclentatus

and affected organs

Larvae (3rd and 4th large intestine: haemorrhagic large intestine: as in S. vu/garis, large intestine: hardly any
stages) in intestinal foci in mucosa of caecum also subserous bleedings in changes at invasion of L3 into
wall at the beginning of and ventral colon (also ileum), ileum and large intestine intestinal wall; possibly later
systemic migration inflammatory-reactive nodules in subserous, haemorrhagic
mucosa and submucosa nodules in caecum and colon,
likely caused by inhibited larvae
Migrating stages large intestine: thromboarteritis liver: initially inflammatory foci liver: inflammatory-reactive
(4th and 5th) in various of submucous arterioles and (2-3 mm), later winding migration foci around L3, later winding
organs arteries tracts and fibrosis migration tracts
mesenteric arteries: thrombo- peritoneal cavity: peritoneal cavity: haemorrhagic
arteritis (aneurysm) of anterior granulomatous omentitls, and Inflammatory foci
' mesenteric artery and their peritonitis subserously in intestine,
branches, embolism and retroperltoneum: subserous abdominal wall and other
infarction in small and large granulomatous lnllammatory foci organs; adhesions (greater
intestine pancreas: loss of secretory omentum, parts of intestine,
abdominal ganglia: perineurltls cells, fibrosis etc.); cause: presumably allergic
----
4 th and 5th stages: retro-
reactions
Dispersal of migrating lntima lesions and thrombosis single foci In lung
larvae to various organs in aorta and other vessels (e.g. peritoneal haemorrhages and
hind limb) and heart, migration Inflammatory foci at diaphragm,
tracts In liver: encephalomyelltis, lateral abdominal wall,
etc. - -- - perlrenally, etc. -- - - ---
Migrating stages large Intestine: lesions of small large intestine: nodular Inflammatory foci (worm nodules) in wall of
(mostly L4 , also 5th arteries, localised oedema, caecum and colon
stages) on return to bleedings, nodular Inflammatory
intestinal wall foci (worm nodules) In caecum
and ventral colon
Adult stages In large small mucosa lesions at sites of parasites, some blood withdrawal by parasites.
intestine
Prepatency (months) 6½-7 8½-9 10½-11

Strongylus vulgaris: Diagram of pathogenesis

Migration of
developmental stages

Figure 10.17. Strongylus vulgar/s: aneurysm of anterior

mesenterlc artery, horse. Arrows: parasites (Photo: IPZ).

Adults of Strongylus species attach themselves to the

Figure 10.16. Strongy/us vu/garis: diagram of pathogenesis
(Graphics: IPZ; after Jacobs 1986).
mucosa of the caecum and colon, they suck a plug of
mucus into the big buccal capsule, digest this tissue and
ingest tissue components and leaking blood as food.
This results in small, superficial mucosa! erosions at the
sites of the parasites. Heavy infections can be associated
with low-grade losses of albumin and blood as well as
disorders of gut motility ( ► Figure I 0.15).
• 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)

migrating in the CNS can cause recumbency and other

CNS disorders.

Immunology. Natural infections with small strongyles

Figure 10.18. Strongylus vulgaris: Intestinal Infarction, horse
(Photo: IPZ, J. Eckert and J. Pohlenz).
Clinical signs of cyathostominosis. Various
disease forms have been described in the literature,
some of which are listed in ► Table 10.4.
Clinical signs of strongylosis. Predominantly
chronic, rarely acute form (the latter occurs mainly in
heavy primary infections of young animals, especially
with S. vulgaris).
• Chronic form. Inappetence, emaciation, rough
hair coat, partly intermittent diarrhoea, recurrent colic,
hypoalbuminaemia, hyper-�-globulinaemia, transient
neutrophilia and eosinophilia.
induce immunity that develops slowly and can - with
increasing age of the hosts - lead to reduced worm
co
burdens and egg counts, but is often weak. Therefore, :2
horses of different ages can harbour significant worm >,
0)
C
burdens despite their defence reactions. Specific serum e
antibodies are formed, which are transmitted in the first if)
5-6 weeks post-partum via colostrum from mares to
foals. After superinfection with infective larvae, adult
stages of various species of small strongyles, living in
the Intestinal lumen, may be eliminated. Young animals,
which had been kept largely free of strongyles on pasture
by anthelmlntlc treatments, proved fully susceptible after
a challenge infection with small strongyles.
Under natural infection conditions large strongyles
also induce immune responses, often with a low
protective effect. Repeated experimental infections of
foals for several weeks or months with low doses of
L3 of S. vulgaris led to a reduction in symptoms and
pathology after a test infection. Oral immunisation (2x
at an interval of 3 weeks) with irradiation-attenuated
L3 induced a protective effect of 91 % (as measured
by reduced numbers of juvenile stages in the anterior
mesenteric artery) and significantly lower clinical signs
compared to non-immunised control animals.

• Acute form. lnappetence, fever, lethargy, colic,
alterations of peritoneal fluid (darker colour, erythro­
cytes, nucleated cells, protein, lactate), elevated serum
levels of lactate, alkaline phosphatase and y-glutamate
transpeptidase, hypoalbuminaemia. Serious illnesses
can rapidly take lead to death. Stages of S. vulgaris
Diagnosis. The diagnostic procedure should always
take into account epidemiological and clinical case
histories, clinical signs and laboratory tests. Patent
infections with strongyles can be diagnosed b y egg
detection in faecal samples (flotation technique), but
further differentiation is not possible. However, the

Table 10.4. important forms of diseases caused by small strongyles, mainly by Cyathostominae (= cyathostominosis).

Form of disease Period ef disease 'Predominantly

1 Cllnlcal signs and laboratory findings1
outbreaks affected animal
groups
'

Chronic during grazing young animals clinical signs: impaired weight gain, rough coat, variable stool
cyathostominosis period (mostly to- in 1st year of life, consistency, partly light and alternating diarrhoea
wards the end) single animals or laboratory findings: usually normal, strongyle eggs in faeces
--- groups affected after the prepatent period
Chronic diarrhoea no clear mostly horses clinical signs: chronic diarrhoea lasting 1-8 weeks, partly
seasonality > 1 year old, part recurrent
of a group affected laboratory findings: partly hypoalbuminaemia, neutrophilia,
increased SAP and SFA values; in faeces none to many strongyle
eggs; in some cases, larval strongyles detectable in faeces or in
intestinal wall biopsy
Larval November to younger and older clinical signs: acute onset, then persistent diarrhoea, weight
cyathostominosis spring (early horses up to 6 loss, sometimes colic, fever, subcutaneous oedema, often lethal
(winter- summer) years, only part of course
cyathostominosis) a group affected laboratory findings: hypoalbuminaemia, hyper-[3-globulinaemia,
neutrophilia, increased SAP and SFA values, rarely anaemia.
Strongyle eggs in faeces: none to moderate numbers; larval
strongyles: quite often detectable in faeces
1 SAP: serum alkaline phosphatase: SFA: serum fructosamine.
 Part Ill. Parasites and parasitoses: metazoa

important Strongylus species and small strongyles Therapeutic doses of moxidectin or fenbendazole in
as a group can be diagnosed by differentiation of L3 increased doses, the latter repeatedly applied for several
obtained from copro-cultures( ► Figure 16.14, p. 546). days, are effective against juvenile stages of small
It is noteworthy, that at different times of the infection, strongyles in the intestinal wall( data on fenbendazole
egg shedding may be low or absent. refer to non-benzimidazole-resistant populations).
Comparative histopathological studies revealed
According to studies in Belgium including 94 horses, severe pathological changes in the intestinal wall after
diarrhoea, poor physical condition, hyp oalbuminaemia fenbendazole therapy, which have not been observed
and a decreased albumin/globulin ratio were the following moxidectin application.
most common findings associated with larval
cyathostominosis, partly also hyp er-p-globulinaemia. Control. Strategic control of horse strongyles is based
In 36% of these horses strongyle eggs were found in on the following measures: (a) pasture management,
faeces, and in 30% larval (L4) and adult nematodes. (b) pasture hygiene and( c) strategic treatment of horses
In such cases, the macroscopic detection of strongyles with anthelmintics. Biological control measures of are
in faeces is an important diagnostic tool ( ► Figure being evaluated. If possible, these measures should be
10.19). Molecular assays have been developed for specific combined with an integrated control programme, in
diagnosis of patent infections with 21 cyathostomine which other parasites are included. When planning
species. and implementing programmes, the site-specific
conditions of the horses have to be considered. In the
Serological techniques for diagnosing infections past, recommendations for a strategic, epidemiologically
with migrating stages of S. vulgaris or larval stages of based use of anthelmintics - limited to the necessary
cyathostomins have not yet been developed. At necropsy, extent - have been widely disregarded in practice, often
attention should be paid to changes in mesenteric vessels resulting in 'overtreatment' of horses and the emergence
as well as to presence of larval stages in the intestinal of drug-resistance in small strongyles. Therefore,
wall. Special techniques are available for detecting larval new approaches are being evaluated with the aim of
stages in the intestinal wall. restricting anthelmintic treatments to horses that have
been identified as significant shedders of eggs('selective
Therapy. For treatment of strongyle infections in horses treatments'). However, the long-term effects of this
(pro)benzimidazoles, pyrantel(tetra-hydropyrimidine measure have to be further evaluated. In one recent
compound) and macrocyclic lactones (ML) are used, study selective therapy was associated with increased
which in recommended therapeutic doses are highly occurrence of Strongylus vulgaris. Details ► p. 593.
effective against immature and adult stages of non­

r:-1.a:a:a---•
resistant large and small strongyles inhabiting the
intestinal lumen ( ► Table 19.10, p. 592). ML, such as Selected references
moxidectin and ivermectin are also effective against
migrating ('somatic') larval stages of Strongylus species, Andersen UV, Howe DK, Olsen SN, Nielsen MK (2013) Recent
so that these nematodes can be successfully controlled advances in diagnosing pathogenic equine gastrointestinal
by at least 2 treatments per year. Due to widespread helminths: the challenge of prepatent detection. Vet Parasitol
drug resistance of small strongyles, the efficacy of(pro-) 192: 1-9.
benzimidazoles and pyrantel against these parasites can Becher AM, Mahling M, Nielsen MK, Pfister K (2010) Selective
be reduced(► Table 17.6, p. 564). Recent studies have anthelmintic therapy of horses in the Federal states of
indicated emerging resistance to iverrnectin in some Bavaria (Germany) and Salzburg (Austria): an investigation
countries. Into strongyle egg shedding consistency. Vet Parasitol 171:
116-122.
Cwlkllnskl K, Kooyman FNJ, Van Doorn DCK, Matthews
JB, Hodgkinson JE (2012) New insights into sequence
Q)
variation In t11e IGS region of 21 cyathostomin species and
·u
C

'6 the implication for molecular Identification. Parasltol 139:

Q)
1063-1073.
�
Davidson AJ, Hodgkinson JE, Proudman CJ, Matthews
co JB (2005) CY1okine responses to Cyathostominae larvae
C
·c in the equine large intestinal wall. Res Vet Sci 78: 1 69-176.
Q)

j Du Toit N, McGorum BC, Pemberton AD, Brown J, Dacre

-� KJ (2007) The involvement of mast cells and mast cell
>, proteinases in the intestinal response to equine cyathostomin

-
Ol
0 infection. Vet lmmunol lmmunopathol 115: 35-42.
0
·1n
co Figure 10.19. Immature small strongyles on faeces of a horse
co
Cl.. (Photo: IPZ, J. Eckert).
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)
Hertz berg H, Schwarzwald cc, Grimm F, Frey CF, Gottstein
B, Gerber V (2014) [Helminth control in the adult horse: the
need for a reorientation] (in German). Schweiz Arch nerheilkd
156: 61-70.
Lichtenfels JR, Kharchenko VA, Dvojnos GM (2008) Illustrated
identification keys to strongylid parasites (Strongylidae:
Nematoda) of horses, zebras and asses (Equidae). Vet
Parasitol 156: 4-161.
Love S (2002) Parasite-associated gastrointestinal disease.
In: Mair T, Divers T, Ducharme N (eds.) Manual of equine
gastroenterology. London, UK: WB Saunders, pp. 53-61;
ISBN 0-7020-2485-4.
Nielsen MK, Baptiste KE, Tolliver SC, Collins SS, Lyons ET
(2010) Analysis of multiyear studies in horses In Kentucky
to ascertain whether counts of eggs and larvae per gram of
feces are reliable indicators of numbers of strongyles and
ascarids present. Vet Parasitol 17 4: 77 -84.
Nielsen MK, Pfister K, von Samson-Hlmmelstjerna G (2014)
Selective therapy in equine parasite control-application and
limitations. Vet Parasilol 202: 95-103.
Ogboume CP (1978) Pathgenesis of cyathostome (Trichonema)
infections of the horse. A review. CIH Miscellaneous
Publications No. 5. Farnham Royal, UK: Commonwealth
Agricultural Bureaux; ISBN 0-85198-434-7.
Ogboume CP, Duncan JL (1985) Strongylus vulgaris in the horse:
its biology and veterinary importance. 2nd ed. Miscellaneous
Publications No. 9. SI. Albans, UK: Commonwealth Institute
of Parasitology; ISBN 0-85198-547-5.
Steinbach T, Bauer C, Sasse H, Baumgartner W, Rey­
Moreno C, Hermosilla C, Damrlyasa IM, Zahner H
(2006) Small strongyle infection: Consequences of larvlcidal
treatment of horses with fenbendazole and moxldectln. Vet
Parasitol 139: 115-131.
Studzinska MB, Tomczuk K, Demkowska-Kutrzepa M,
Szczepaniak K (2012) The Strongylldae belonging to
Strongylus genus in horses from southeastern Poland.
Parasitol Res 111: 1417-1421.
Von Samson-Himmelstjerna G (2012) Anthelmintic resistance
in equine parasites - detection, potential clinical relevance
and implications for control. Vet Parasitol 185: 2-8.
Family Chabertiidae
Summary
Agent. Medium-sized strongyles that inhabit mainly the
large intestine of artiodactyls, primates, marsupials and
rodents. Of veterinary Importance are mainly Chabertla
ovina (subfamily Chabertilnae) In sheep and other
ruminants and various Oesophagostomum species
(sub-family Oesophagostomlnae) in pigs and ruminants.
• Life cycle. In both genera monoxenous, external phase
similar to strongyles. Transmission by ingestion of L3;
Internal development with hlstotropic phase in the
Intestinal wall.
• Cllnlcal signs and diagnosis. Frequently asymptomatic
Infection, In heavy Infections lnappetence, emaciation,
sllmy and partly bloody diarrhoea. Diagnosis:
Egg detection In faeces (flotation technique) with
differentiation of the L3.
• Treatment and control. See below.
Genus Chabertia
Chabertia ovina (large-mouthed bowel worm)
Disease: Chabertiosls.
Chabert, Ph.D., 1737-1814, French veterinarian and
inspector of the veterinary schools in Lyon and Alfort;
ovis(L): sheep.
Agent. Medium-sized, yellowish-white strongyles:
males 11-16 mm, females 12-20 mm long(► Figure
10.20). Large, ovoid, slightly anterior-ventrally inclined
buccaJ capsule; mouth opening surrounded by numerous
smalJ leaves; males with bursa copulatrix, long spicules
and gubernaculum. The parasite inhabits the large
intestine of domestic and wild ruminants. Eggs: thin­
shelled, oval, with blastomeres, 72-100x38-63 µm.
Life cycle. The external development follows the
strongylid type from egg to ensheathed L3. The infection
of hosts occurs by ingestion ofL3, which - after hatching
from the sheath - invade the mucosa or submucosa of
the entire small intestine(in heavy infections also large
intestine). There, they pass through a histotropic phase
of approximately one week and moult to L4, which
immediately thereafter emigrate into the intestinal
lumen. Further development to preadult stages occurs
mainly in the caecum, the adults establish in the colon.
Prepatent period 7 weeks. Patent infections with egg­
shedding usually result from weak infection doses(a
few hundred L3), whereas after high infection doses a
significant part of the worm population is eliminated
about 2 months p.i. Consequently, egg-shedding is then
reduced or omitted completely. Hypobiosis can occur
at the stage of young L4.
 Part Ill. Parasites and parasitoses: metazoa

Leaf crown­
Buccal capsule--
ubernaculu
Spicule

Nerve ring----ir­
Oesphagus-------

Bursa with
rays

a b

Figure 10.20 Chabertia ovina: (a) anterior end; (b) males, posterior end (Graphics: IPZ, A. Seeger; after Skrjabln 1952).

Occurrence and epidemiology. C. ovina is globally Genus Oesophagostomum

widespread and common in sheep, goats and less
frequently in cattle as well as wild ruminants (including Oesophagostomum spp. (nodular worms)
deer, red and fallow deer, mouflon, chamois, alpine
ibex, bison, moose). In southern Germany ( 1998)
prevalences in sheep and in goats were 98 and 84%, Disease: Oesophagostomosis. I
respectively. Infection occurs mainly on pasture. The
parasite can overwinter in the host or as infective L3
in the environment, thereby surviving periods of frost. Oesophagus (G): oesophagus; stoma (G): mouth; nodular
Under favourable conditions, ensheathed L3 develop worms: they induce the formation of nodules in the
from eggs within I week, they may remain infectious in intestinal wall.
sufficient moisture up to IO months. Development to L3
can take place at relatively low temperatures of 4-6 °C. Summary
• Agent. Up to 2.5 cm long colon parasites, in ruminants,
Pathogenesis. Important are mainly preaduJt stages
pigs, and primates.
and adult worms, most of them attach with their buccal • Life cycle and epide miology. Cycle similar to
capsules to the mucosa of the upper colon. They cause Chabertla. After Infection per os, L3 Invade the Intestinal
mucosal lesions, inflammatory reactions and small wall, Where they develop Into L4 and then return to the
haemorrhages. Larger lesions can lead to enteropathy Intestinal lumen. The hlstotroplc phase causes nodules
with protein loss (mainly albumin) into the intestinal In the Intestinal wall (hence the name).
lumen. Clinical signs have been observed in sheep that • Clinical algna, di agnosis and control. Reduced
harboured about 200-300 adult Chabertia specimens performance, colitis, diarrhoea. Diagnosis by
after experimental mono-infection. Under natural coproscoplc egg detection and differentiation of L3.
conditions, mixed infections with other gastrointestinal Therapy, with benzlmldazoles or macrocycllc lactones.
nematodes (especially with trichostrongyles) are the rule
Q)
in which Chaberlia is one of several harmful agents.
·u
C:

'6 Agent. Medium-sized, yellowish-white strongyles;

Q)
� Clinical signs. Symptoms of chabertiosis include males 6-17 mm, females 7-24 mm. Buccal capsule
� inappetence, emaciation and diarrhoea with mucous, short and broad with mouth opening directed straight
co sometimes bloody faeces. Towards the end of winter forward; leaf crowns may be present around the mouth
C:
·c
Q) reactivation of hypobiotic stages can lead to diarrhoea. wall; at the anterior end there is a cuticular cephalic
vesicle, followed by a ventral cervical groove and broad
C: Diagnosis, treatment and control. Diagnosis: cervical alae ( ► Figure 10.21 ). Males with bursa,
>,
Ol
egg detection in faeces (flotation technique) with spicules and gubernaculum. Parasites in ruminants,
0
identification of the L3 obtained from copro-cultures. pigs, monkeys and humans. Organ localisation of adults
.8 Macroscopic detection of worms at necropsy. Therapy slightly different, depending on species, predominantly
'ii)
co and control as for trichostrongyles (► p. 299) . in colon, also in caecum. Eggs: thin-shelled, oval, with
co
Q_ blastomeres, about 50-80x26-46 (0. denlatum, 0.
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)
Leaf crown
Buccal capsule Cephalic vesicle
--Transverse
Oesophagus cervical groove
Intestine Cervical papilla
Figure 10.21. Oesophagostomum dentatum: anterior end
(Graphics: IPZ, A. Seeger; after Soulsby 1982).
quadrispinulatum) or 63-100x40-64 µm (O. radiatum,
0. venu/osum).
Important species: 0esophagostomum dentatum and 0.
quadrispinulatum in pigs and wild boar; 0. venulosum,
0. radiatum and 0. columbianum in domestic and wild
ruminants. Other species in monkeys and humans (see
below). Species identification is based on morphological
criteria and can be complemented by DNA analysis.
Life cycle. The external development corresponds to
that of Chabertia, hosts become infected by ingestion of
infectious L3 (experimental percutaneous application
of L3 resulted in very weak patent infections). In the
anterior small intestine, the L3 discard the sheath, invade
in distal parts of the small intestine ( 0. columbianum,
0. radiatum 0. venulosum) or in caecum and colon (0.
dentatum, 0. quadrispinulatum) the intestinal wall to the
submucosa, where they become surrounded by cellular
granulomas. This results in formation of nodules, 1-10
mm diameter, in which moulting to L4 occurs. After a
histotropic period of at least 6-14 days, the L4 migrate
into the intestinal lumen, where further development
to preadult and adult stages takes place. The histotropic
phase of L4 can be extended to several months due to
hyp obiosis. Adult worms live in the lumen of the colon
close to the mucosa. The prepatent periods vary with
species: 0. dentatum and 0. quadrispinulatum 17-19
days, 0. venulosum and 0. radiatum 24-26 days, 0 .
columbianum 40 days. The life-span of the adult worms
is usually 2-6 months.
Occurrence an epidemiology. In European pig
herds, 0esophagostomum infections are widespread
and common; prevalences are age dependent and in
sows generally higher (up to >80%) than in fattening
pigs and piglets (<10% to about 30%). The external
development requires a minimum temperature of 10 °C
and sufficient moisture. A considerable contamination
with infective larvae can occur on pastures during the
warm season (about mid-July to September), when the
vegetation is still intact. With increasing destruction of
the vegetation by grubbing activities of the pigs, draught
or low temperatures in the cold season, the infection
risk is greatly reduced. Chickens and pigs can ingest
0esophagostomum eggs by coprophagia and excrete it
in faeces; part of these eggs develop into L3, which are
infectious for swine.
Sheep and goats are most commonly infected with 0.
venulosum and cattle with 0. radiatum. 0. columbianum co
is the most important species in small ruminants in :g
warm countries; in Central Europe, this species was >-
0)
e
C
rarely found. Nati ve wild ruminants in Europe are hosts
of 0. venulosum (roe, red and fallow deer, ibex), 0. u5
radiatum (red and fallow deer, roe deer, bison) and
0. sikae (red and fallow deer, roe deer). In southern
Germany, 0. venulosum was found in 97% of sheep
at slaughter (n=59) and in 76% of slaughtered goats
(n=25). Epidemiology is comparable with that of
trichostrongyles ( ► p. 290), but accurate information
is lacking for European conditions.
Pathogenesis. Adults of 0esophagostomum,
inhabiting the intestinal lumen, live close to the mucosa
and probably feed mainly on intestinal mucus. They may
cause subacute to chronic inflammation of the colon.
During the histotropic phase, the coiled larvae, having
invaded the mucosa, are surrounded by a structureless,
eosinophilic sheath and later by inflammatory cells.
These granulomas appear macroscopically as smalJ, a
few millimetres wide, yellowish nodules, which may
be discoloured dark by small haemorrhages ( ► Figure
10.22). In an uncomplicated course of infection, the
nodules regress rapidly. Super- or reinfections are
frequently followed by an irregular course of the
histotropic phase with enhanced inflammatory reactions
of the mucosa and delayed emigration of the larvae,
which are enclosed in part in firm nodules and sooner or
later die. Severe infections of pigs with oesophagostomes
have prolonged the excretion of Salmonella enterica
(ser. Typhimurium) in faeces, whereas low to moderate
infections had no influence.
Clinical signs. Heavy 0esophagostomum infections
can cause in piglets inappetence, weight loss and
diarrhoea, and in finishing pigs reduced weight gain
Q)
C
"<:5
:a
Q)
�
co
C
·.::::
Q)
.s
>,
0)
0
0
"cii
Figure 10.22. Oesophagostomum nodules, small intesti e,
co
cattfe (diameter 6-1 mm) (Photo: IPZ). 0...
 Part Ill. Parasites and parasitoses: metazoa
and poorer feed efficiency. In sows reduced litter sizes
and reduced milk production were observed.
In Central Europe and other regions, oesophagostomes
are regularly associated in varying proportions with
trichostrongyles in infections of ruminants and
thus etiologically involved in the disease complex of
gastrointestinal strongylidosis with inappetence, weight
loss and hyp oalbuminaemia. Additional signs, such as
muco-haemorrhagic diarrhoea and dark discoloured
faeces can be indicative for the strong involvement of
oesophagostomes (but see also Bunostomum ► p. 285).
In monkeys oesophagostomes can cause severe colon
inflammation with fatal outcome.
IL'
,f: • Parasitol Res 83: 646-654.
I
Immunology. Repeated infections of pigs with
0esophagostomum spp. may delay parasite development
and reduce egg-shedding as well as susceptibility
to homologous re- or super-infections. However,
the resulting protection is low, as indicated by high
prevalences of 0esopfiagostomum infections in older
pigs as compared to young animals. In contrast in cattle,
already a single infection with 1000 L3 of 0. rndiat11111
induces a good protective effect against superinfection,
indicated by reduced worm burden, but also by increased
nodule formation.
Diagnosis. Egg detection in faeces(flotation technique)
and identification of L3 from copra-cultures. Third stage
larvae of 0. dentatum and 0. quadrispirmlatwn can be
distinguished by DNA-analysis.
Therapy and control. In ruminants, anthelmintics
and control measures as in trichostrongyles (► p.
586 and ► Table 19.2, p. 579). Against adult
oesophagostomes in pigs various anthelmintics are
highly effective, less against immature stages( ► Table
19.8, p. 589). Resistance of 0esopl1agostomum strains of
pigs to levamisolc, pyrantel and benzimidazoles have
been detected in DK and DE. Control measures in pigs
(► p. 588).
Zoonotic importance. 0esoplwgostomwn infections
in humans are endemic in West Africa (Togo, Ghana)
and focally frequent(prevalence up to >50%); sporadic
cases are also known from other areas (Africa, Asia,
South America). The most common pathogenic
species is 0. bifurcum which occurs in various species
of monkeys. Transmission from monkey to man and
from man lo man is possible, but the importance
of animal reservoirs is now regarded as low, due to
molecular differences between parasite populations
of monkeys and humans. In stool samples from
primates, eggs of oesophagostomes and hookworms
eggs cannot be distinguished morphologically. However,
a differentiation of L3 is morphologically possible by
DNA analysis.
Selected references
Christensen CM, Barnes EH, Nansen P (1997) Experimental
Oesophagostomum dentatum infections in the pig: worm
populations at regular intervals during trickle infections with
three dose levels of larvae. Parasitology 115: 545-552.
Ghai RR, Chapman CA, Omeja PA, Davies TJ, Goldberg TL
(2014) Nodule worm infection in humans and wild primates in
Uganda: cryptic species in a newly identified region of human
transmis sion. PLoS Negl Trop Dis 8(1 ): e2641.
Joachim A, Daugschies A, Christensen CM, Bj0rn H,
Nansen P (1997) Use of random amplified polymorphic DNA­
polymerase chain reaction for the definition of genetic markers
for species and strains of porcine Oesophagostomum.
P etersen HH, Andreasen A, Kringel H, Roepstorff A,
Thamsborg SM (2014) Parasite population dynamics in
pigs infected with Trichuris suls and Oesop/Jagostomum
de11tatum. Vet Parasitol 199: 73-80.
Roepstorff A, Mejer H, Nejsum P, Thamsborg SM (2011)
Heiminth parasites in pigs: new challenges in pig production
and current research highlights. Vet Parasitol 180: 72-81.
Telvik H, Christensen CM, Nansen P (1998) Oesophagostomum
spp. in pigs: resistance 10 relnfeclion. Parasitol Res 84:
783-786.
Family Syngamidae
Syn(G): with, together;gamos(G): marriage, wedding.
Refers to females and males of Syngamus living in
permanent copulation.
Summary
• Of Interest are species of the subfamilies Syngamlnae
and Stephanurlnae.
• Syngamlnae are parasites of the respiratory tract and
cranial cavities of numerous species of birds and
mammals. Syngamus and Cyathostoma species have
a certain significance as parasites of poultry and other
birds. Transml881on by Ingestion of Infectious larvae
(L3 In the egg or free-llvlng) or with paratenlc hosts.
The parasites can cause serious respiratory problems.
• Stepha/Jun.,, QYFUS (Stephanurlnae) Is a kidney parasite
of pigs In warm countries.
• Subfamily Syngaminae (gape worms)
Di�: Syngamlnoses.
In Europe, Syngamus and Cyatfiostom" species have a
certain significance as parasites of poultry and other birds.
In tropical and subtropical areas, Mammomonogamus
species occur in ruminants: Mammomonogamus
laryngeus (syn. Syngamus /aryngeus} in the larynx
of cattle and buffalo in Asia and South America and
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)
Mammomonogamus nasico/a (syn. Syngamus nasicola) in
the nasal cavities of ruminants in Africa, South America,
the Caribbean and some other regions. In some areas,
these parasites are common: in the Philippines, 23% of
slaughter cattle were infected with M. laryngeus and
in Sri Lanka 40%; on St. Kitts (West Indies), 45% of
cats were carriers of Mammomonogamus spp. Rarely,
Mammomonogamus infections occur in humans and
cause laryngotracheal symptoms.
Genus Syngamus
Syngamus trachea (red worms, forked worms)
Agent. Syngamus trachea parasitises mainly
gallinaceous birds (chicken, turkey, pheasant, partridge,
guinea fowl), pigeons, corvids (crows, magpie, etc.),
songbirds (starlings, house sparrow and others) and
other wild birds. Three other species occur in snipes
and thrushes. Here, only S. trachea is considered. Main
features of S. trachea are: blood-red coloured, rather
large nematodes (males 2-8 mm, females 5-20 mm long),
large, cup-shaped buccal capsule with 6-11 small teeth
at the base, males with bursa and almost equally long
spicules. Males and females live in permanent copulation
forming a Y-shaped configuration (► Figure 10.23a)
(hence 'forked worm'). Eggs: oval, rather thick-shelled,
hyaline caps on either pole, with few blastomeres, 74-
125x36-55 µm (► Figure 10.23b).
Life cycle and epidemiology. Syngamus pairs
live in the trachea. Eggs produced by females pass
from the trachea into the oral cavity, from where they
are swallowed and excreted in faeces. At favourable
temperatures, infectious 13 develop within 2-4 weeks
within the egg shell.
Infection of hosts occurs (a): by ingestion of L3, either
enclosed in the egg shell or already hatched and free­
living; (b): uptake of L3 with paratenic hosts. Paratenic
hosts are earthworms, land and freshwater snails, and
various species of insects (cockroaches, flies). The
ingested larvae migrate from the intestine preferably
via the blood - in part through the body cavity - to the
lungs and then to the trachea. Prepatent period: 12-21
days. Life-span of adult parasites up to 7 months, but
usually only 1-3 months.
Syngamus infections occur in free-ranging chickens
or in zoo and pet birds; infections can be introduced
by wild birds. In pheasantries S. trachea often causes
considerable losses. Under the climatic conditions of
Central Europe, eggs of S. trachea remain viable up to
I year, hatched (13) are less resistant, but can survive
for long and hibernate in paratenic hosts.
Figure 10.23. Syngamus trachea: (a) couple; length of female
about 16 mm; the depicted specimen has lost the red colour
due to formalin fixation; (b) Syngamus egg (length about 110
µm) (Photo: IPZ).
Pathogenesis. Chicks aged 3-4 weeks and rarely
older animals in chicken farms are mostly affected
by the infection. Turkeys and pheasants are more
susceptible than chickens and are affected even as
adults. Occasionally, Syngamus infections occur in
carrier and race pigeon populations. In heavy infections
migrating larvae cause pulmonary haemorrhages and
inflammation. In the trachea, the parasites attach firmly
with the buccal capsule to the mucosa and cause small
bleedings, pinhead-sized nodules and inflammatory
responses (tracheitis and peritracheitis) with secretions
of large amounts of mucus, which obstruct the air
passage. By blood sucking (especially by females), a
mostly moderate anaemia can occur.
Clinical signs. The most striking symptom of
syngamosis is respiratory distress (dyspnoea). The
Q)
diseased animals shake heads, stretch it up and turn C:
·c3
it back, open the beak and gasp for air, often with a '6
Q)
rattling sound or sniffle. The animals become emaciated, �
anaemic and can die from the infection. �
(1j
C:
Diagnosis. Clinical symptoms are characteristic; in ·;:::
Q)
chicks one can see the blood-red nematode through j
the skin and wall of the trachea when the animals are C:
examined in front of a strong light source. The diagnosis >,
OJ
is confirmed by detection of characteristic eggs in the 0
0
....,
faeces (flotation technique) or of parasites at necropsy. ·u5
(1j
(1j
D....
Part Ill. Parasites and parasitoses: metazoa
Therapy and control. Benzimidazole derivatives
(flubendazole) are used for treatment(► Table 19.20,
p. 611). Prophylaxis(separate rearing of chickens and
other gallinaceous birds, protection from wild birds,
drainage of outside pens) is often not practical and
insufficiently effective.
Genus Cyathostoma
Cyathostoma species (caution: not Cyathostomum,
► p. 266) differ from Syngamus morphologically and by
the fact that they do not live in permanent copulation.
In Central Europe, several species are endemic, which
predominantly parasitise waterfowl(ducks, geese, swans,
gulls, etc.). Some of these species live in the trachea,
others mainly in the nasal and infraorbital sinuses.
• Subfamily Stephanurinae (kidney worms)
The subfamily Stephanurinae contains only one species,
Stephanurus dentatus. This parasite is common in pigs
in tropical and subtropical areas, but docs not occur
in Europe. The adult parasites live in cysts in renal
fat, in the renal pelvis in the wall of the ureter and the
urinary bladder. Pigs become infected by percutaneously
penetrating L3, or by ingestion of free-living infective
stages or such stages in paratenic hosts (earthworms).
This parasite can cause considerable damage. lvermectin
(0.3 mg/kg b.w.) and doramectin (0.3 mg/kg b.w.) arc
highly effective.
- Selected references
Anderson RC (2000) Nematode parasltes of vertebrates. Their
development and transmission. 2nd ed. Wallingford, UK:
CASI Publishing, CAB International; ISBN 0-85199-421 ·0.
Swayne DE (ods.) (2013) Diseases of Poultry, 13th od. Ames.
IA, USA: John W1kJy Blackwell; ISBN 978-0-470-95899-5.
Sherwin CM, Near MA, Gale E, Petek M, Stafford K, Turp
M, Coles QC (2013) Provalonco of nemotodo infoction and
faoc:al ogg counts In froo-rongo laying hons: relations to
houSlfl9 and husbandry. Br Poull Sci 64: 12·23.
- Superfamily Ancylostomatoidea
Family Ancylostomatidae (Hookworms)
Disease: Ancylostomatidosis. I
Ancylos (G}: crooked, bent; stoma (G): mouth. Refers
to the hook-shaped, dorsally bent anterior end.
Summary
• Agents. Medium-sized nematodes, 5-30 mm long with
large buccal capsule equipped with smooth-edged
or serrated cutting plates. Males with well-developed
bursa copulatrtx, spicules and gubernaculum. Species
of major veterinary Importance: Ancylostoma canlnum,
Ancy/ostoma ceylanlcum, Ancy/ostoma tubaefonne and
Unclnarla stenocephala In carnivores, Bunostomum
stenocephala and Bunostomum phlebotomum In
ruminants.
• Life cycle. External development from egg to
L3. Infection of definitive hosts: with Infectious
L3 predominantly percutaneously (Ancylostoma
and Bunostomum species) or per os (Unclnarla
stenocephala); In carnivores also Ingestion of L3 In
paratenlc hosts (rodents).
• A. c,,n/num In dogs. After percutaneous Infection,
larvae migrate via the lung-tracheal route to the small
Intestine, where adult stages develop. After oral uptake
of free-living L3, there Is a direct colonlsatlon of the
parasites In the Intestine without parenteral migration.
At both Infection routes, part of the larvae undertake a
somatic migration through the body thus passing Into
muscles and other tissues, where they can survive a
long time as hypoblotlc L3. A proportion of hypoblotlc
stages, that have been reactivated perlpartlally, or
larvae which Infected the bitch Just before or during
lactation, are transmitted via the mllk to the puppies.
Such lactogenlc Infections can occur up to the 3,a litter,
after a single Infection of the bitch.
• CyclH of other species. see below.
• Plthog1nesl1 and cllnlcal signs. Some hookworm
species (Ancyto1tom1 canlnum, A. tubaeforme,
A. ceytanlcum, Bunoatomum 1pecle1) are blood­
fNdn and therefore particularly pathogenic. Cllnlcll
manlfntatlona of lntHtlnal lnftatatlon with th111
hookworms lnoludt diantlota, lnappetence, emaciation,
lllmy Of bloody diarrhoea, anoemla, protein loaa and
Ill conaequencet.
• 0119,,0111, � and oontrol. Detection of eggs
in f-.ces (notation ttchnlque). Therapy In dogs and
cat.a, for oumple with fonbendazole, flubendaiole or
moc:rocycl� lactonea. For control, see below.
• �Uc Importance, Hookwo,m larvae can penetrate
human lkk'I and cause larva mlgrana cutanea. Rarely, A
canhum settlel in the human Intestine without reaching
sexual maturity and causes eoslnophllic enteritis. In
recent years, A ceylanlcum, a parasite of dogs and
cats, has been identified as a common Intestinal
parasite of humans In Asia.
' 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)
Agents. Hookworm species occur in carnivores, pigs,
ruminants, primates and some other groups of animals
(including elephants, giraffes, kangaroos). The adults of
most species parasitise the small intestine, exceptionally
also the bile ducts (Grammocephalus in elephants and
Monodontella in giraffes). Some species are blood­
feeders and therefore quite pathogenic. Of greatest
veterinary significance are hookworms of carnivores. In
human medicine, intestinal infections with hookworms
(Ancylostoma duodenale, Ancylostoma ceylanicum,
Ancylostoma braziliense, Necator americanus) are
predominantly a problem in subtropical and tropical
regions.
Genera Ancylostoma and Uncinaria
■
Ois&ases·: Ancylostomosls and Unclnarlosls
(hobkWortn disease) In camlvores.
Ancylos(G): crooked, bent; stoma (G): mouth; uncinatus
(L): hook-shaped.
Agents. Hookworm species of carnivores are listed
in ► Table 10.5. In Ancylostoma species the buccal
capsule is equipped with 2 serrated cutting plates, each
with 3 teeth-like structures; that of Uncinaria contains 2
smooth-edged plates(► Figure 10.24). Species diagnosis
can be based on morphological and molecular criteria.
Life cycle. Adult hookworms live in the small intestine
and attach themselves with their buccal capsule to the
mucosa. A female can produce 3,000 to 19,000 eggs
per day, which are shed in faeces. The thin-shelled and
oval eggs contain only 4-16 blastomeres immediately
after deposition by the female, but their number can
increase rapidly during the intestinal passage and in
the environment. At suitable temperatures, in the egg
a l 51 stage larva is formed, which hatches and develops
further in 5-8 days into an infectious 13, enclosed in
a sheath. This development is delayed or prevented at
Cutting plates
a Ancy/ostoma caninum b Ancylostoma tubaeforme
Figure 10.24. Anterior ends of hookworms (Graphics: IPZ, A. Seeger; after Hartwich 1994).
temperatures below 15 °C. For its external development,
A. caninum requires higher temperatures than U.
stenocephala (epidemiology, see below). In moist soil,
the L3 can remain viable for 3-4 months, but they die
rapidly under dry conditions.
co
The routes of infection and migrations in the hosts 32
are different in various hookworm species of carnivores. >-.
0)
e
C:
• U. stenocephala (in dogs, rarely in cats). The U)
infection of definitive hosts occurs predominantly
on the oral route by ingestion of infectious 13. The
larvae pass into the stomach, they discard the sheath,
and remain nearly two days in lumina of stomach and
duodenal glands. Then they settle in the small intestine,
moult twice and develop to sexual maturity. Prepatent
period 14-18 days, patency usually 4-6 months. Part of
the ingested larvae penetrate the mucosa of the upper
gastro-intestinal tract and migrate to various organs,
especialJy to muscle and adipose tissues, where they
survive for long periods as parasitic L3. Definitive hosts
can also become infected by ingestion of paratenlc
hosts(e.g. rodents), containing L3 in body tissues. The
percutaneous infection is of minor importance, since on
this route only a few parasites reach the small intestine
and develop into adult stages. There is no evidence for
prenatal or lactogenic transmission of U. stenocephala
in dogs or cats.
• Ancylostoma caninum (in dogs). The
development of A. caninum in dogs is very complex.
Both percutaneous and peroral infections with free­
living 13, and transmission of parasitic 13 with milk
(lactogenic infection) or in paratenic hosts (rodents,
etc.) are possible(► Figure 10.25).
After peroral infection, some larvae remain in the
digestive tract and develop, after a short stay in lumina
of gastric and intestinal glands, in the small intestine
by 2 moultings (14 and sth stage) to sexual maturity.
Prepatent period 15-26 days. After percutaneous
infection, the larvae of A. caninum invade within a few
Q)
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'6
Q)
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c Uncinaria stenocephala
E
"iii
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 Part Ill. Parasites and parasitoses: metazoa
Table 10.5. Hookworm species (selection).
Species, length of males (d'�) and females (��),.
distribution (D)
Ancy/ostoma caninum 1, 2
oc3':5-14 mm, <jl<;?: 15-21 mm
D: mainly subtropics and tropics, also temperate �gions _
Ancylostoma tubaeforme 1
oo: 5-12 mm, <j><j>: 5-15mm
D: worldwide
Uncinaria stenocephala 1
oo: 3-11mm, <j><jl: 4-16mm
D: temperate regions (Eurasia, Amerlc_a)
Bunostomum ph/ebotomum 1
o'J: 10-19mm, ')?9: 13-29mm
D: worldwide - -- --
II \ Bunostomum trigonocephalum 1
I oo': 11-20mm, <jl<jl: 12-29mm
D: worldwide---- -- - -
Globocepha/us /ongemucronatus 1
(syn. G. urosubulatus)
cM: 3-7mm. <jl<jl: 4-9mm
D: mainly subtropics and temperate regions (sporadic In
Central Europe)
1 Endemic species in Central Europe.
2 A. braziliense (dog and cat), southern USA, Central and South America, Africa, southern Asia; A ceylanicum (dog, cat, man), Asia, regions
of South America, Australia.
3 Prepatent periods differ, depending on modus of Infection.
minutes hair follicles and sebaceous glands and strip off
the sheath. Subsequently they proceed on the tracheal
migration route: they penetrate subcutaneous veins,
are then haematogenously transported to the lungs and
migrate via trachea and oesophagus to glandular lumina
in the stomach and small intestine, where they remain a
few days and moult to IA. Thereafter, the parasites settle
in the small intestine and develop into adults. Prepatent
period: 14-17 days In puppies, in older dogs 26 dayR.
Both after perculoneous and pcrornl infections,
part' of !'he larvae take the sornotlc migration route
through body tissues. This migration con stnrl from
the subcutis, intestine or lungs and leads through body
tissues or body cavities 10 different organs. After a few
days or weeks, the larvae invade striated muscle or fat
cells and may persist there as hypobiotic L3 for years
(encapsulation does not occur). Somatic migration
a,
C occurs predominantly in semi-immune, older dogs and
·o in pregnant bitches, whereas tracheal migration takes
'6
Q)
place in immunologically naive young animals.
�
� can occur, if larvae are reactivated in final stages of
ro
C Some of the hypobiotic L3 are reactivated in the
·.:::::
(l) final stages of pregnancy; they reach the mammary
gland, are excreted in milk and thus transmitted to
C puppies (lactogenic infe.ction). If lactating bitches
>,
0)
are percutaneously or perorally infected for the
0 first time, some larvae migrate, within 2-5 days p.i.,
0
·u; directly to the mammary gland and are then excreted
i n the milk. In infected bitches, h )'pobiotic larvae
ro
a. can be reactivated experimentall)• b)' application of
'
Hosts (selection) Predilection site of adults,
prepatency, size of eggs
canids: dog, red fox, wolf, jackal, small intestine
etc. prepatency: 14-17days 3
------ eggs: 52-79x28-58 µm
fellds: domestic cat, wild cat, etc. small intestine:
prepatency: 19-22days 3
- eggs: 45· 78x34-57µm
canids: dog, red fox, arctic fox, small intestine
wolf. raccoon dog, rarely cat and prepatency: 14-17days
-- -
ot11er fellds - - -- eggs:
bovlnae: cattle other bovines rarely,
71-92x35-58�µm
small Intestine
caprines and cervlds, rarely sheep prepatency: 52-59days
- - eggs: 75-115x40-70µm
sheep, goat, roe deer, red deer,small intestine
prepatency: 49days
Ibex, chamoix, moose, rarely cattle
-- �ggs: 66-104x33-74 µm
wild boar, domestic pig small intestine
prepatency: 26-36days
eggs: 62-75x35-41 µm
hormones (estradiol or estradiol with progesterone).
Presumably, these hormones do not influence the
hypobiotic larvae of A. caninum directly. In rats during
late pregnancy and lactation, oestrogen and prolactin
induced elevated concentrations of the endogenous
growth factor TGF-P (transforming growth fnctor-P)
in blood plasma, in mammary and uterine tissue and
in milk. Since physiological concentrations of TGF-P
stimulate hypobiotic A. cnnlnwn lnrvae in vitro, and this
stimulation can be speciflcally inhibited by anti-TGF-P
antibodies, It is assumed that this factor plays a role in
reactivallon of these lnrvae in tissue.
In milk of bitches, Ancylostoma larvae are mainly excreted
during the flrst week post-partum, but low excretion can
continue until the end of the lactation period. In puppies,
the parasites settle probably directly in the intestine
without prior parenteral migration. After a single massive
infection of a bitch, transmammary transmission of
larvae can last up to the third lactation, but in decreasing
intensities. Endogenous autoinfections of the bitch
pregnancy, undertake a migration on the tracheal route
and settle in the intestine. Prenatal infections of fetuses,
suspected in previous times, could not be confirmed.
Another mode of infection with A. canir111m is the
ingestion of parasitic L3 in paratenic hosts, primarily
rodents, in which most L3 can remain infectious in
muscles and some in brain for approximately 1 year. In
pigs, Ancylostoma larvae were found in adipose tissue.
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundwonms)
L3�
Paratenic host \
rva 2
Figure 10.25. Life cycle of Ancylostoma caninum (Graphics: IPZ, S. Ehrat).
• Ancylostoma tubaeforme (cat). Infections
of cats with A. tubaeforme can occur both orally
and percutaneously; both routes are approximately
equivalent in terms of infection success. Prepatent
period 18-28 days . Also for this species rodents can
serve as paratenic hosts. Transmammary infections
have not been observed.
Occurrence and epidemiology. U. stenocephala
occurs mainly in temperate regions of Eurasia and the
American continent. In Central Europe, it is the most
common hookworm species of the dog and red fox.
In Central European rural and urban fox populations,
U. stenocephala was found in prevalences of 60-90%.
Similar prevalences were reported from foxes and
raccoon dogs in LT. In CH an average of 7% of a dog
population (n=S0S) shed hookworm eggs. A. caninum
has its main range of distribution in warm countries,
but occurs northward as far as southern Canada, DE
and DK. In northern Central Europe, this species
appears to be rare in dogs; prevalences up to 10% were
observed in foxes. In contrast, 33% of dogs (n= 183)
:Q
>-.
O>
e
C:
U)
§ti
Adi.lit hookworms
Egg with larva 1
in IT were infected with A. caninum. A. tubaeforme
is a fairly common parasite of cats in Central Europe
(e.g. prevalence of 17% [n=l55] in eastern Germany
[Brandenburg]; average prevalence of hookworm eggs
in> 1,500 owned cats from 7 European countries 1.4%).
U. stenocepha/a infections in cats were not demonstrated
in recent studies.
Due to adaptation of U. stenocephala to temperate
climates, the eggs of this species can develop at
temperatures between 7.5 and 27 °C; in copra-cultures
at 20 °C the development of L3 takes only 4 days. In
the environment, the duration of development may
vary, depending on temperature, between one week and
several months. In the UK, part of the larval population
survived on grassland from autumn to the following year
(May/June). Puppies become infected around weaning
and shed eggs in larger quantities approximately until
the age of 6-8 months; thereafter the intensity of egg­
shedding decreases gradually. Eggs of A. caninum can
develop at 15-37 °C; the optimum range is 25-30 °C and
is thus higher than in U. stenocephala. Cold resistance
 Part Ill. Parasites and parasitoses: metazoa
of these larvae is low. Eggs of A. tubaeforme develop in
the same temperature range as in A. caninum.
Immunology. After several infections with hookworms,
domestic animals and humans develop a Th2-type
immunity, which is often poorly expressed under
natural conditions and can be under-mined by immune
evasion of the parasites, for example by excretion of
immunomodulating substances. Protective immunity in
dogs can be stimulated by irradiated (x-rays or gamma
rays) infectious larvae of A. caninum with reduced
virulence and developmental potential. On this basis,
a vaccine was developed and used successfully in the
USA (Canine Hookworm Vaccine), but was withdrawn
from the market after a short time ( 1975). The use of
recombinant secretory proteins of L3 or a haemoglobin
protease of adult parasites as antigens can induce partial
immunity in experimental animals, indicated by reduced
worm burden or egg excretion after a challenge infection.
Antibodies, directed against secretory proteins of L3 in
immunised animals, affect the systemic migration of
larvae. On the other hand, anti-haemoglobin protease
antibodies interfere with degradation of blood diet in
adult worms.
Pathogenesis. Penetration of hookworm larvae into
the skin of their natural hosts, usually does not induce
visible changes after primary infections, but reinfection
or superinfections can cause allergic reactions including
itching, reddening, urticaria and inflammation. The
lesions are usually more pronounced in non-specific
hosts than in natural hosts. Such changes, caused by A.
caninum, are predominantly observed in warm countries,
named 'moist summer eczema'. They occur in dogs
mainly in interdigital spaces, on limbs and ventral body
regions, which are most exposed to hookworm larvae.
During tracheal migration Ancylostoma larvae can cause
small haemorrhages and inflammatory changes in the
lungs, which become apparent only in heavy infections
such as cough or other pneumonic symptoms.
In the small intestine infections with U. stenoccplrala
or Ancylostoma species have different effects.
• Uncinariosis. Adult stages of U. stc11occplrala live
preferably in the distal small intestine. They attach to
Q)
the mucosa, suck a plug of tissue into the buccal capsule
·u
C
'6 and change site quite often. This results in small lesions
Q)
�
and inflammalory changes of the intestinal mucosa. In
contrast to the haematophagous Ancylostoma spp., U.
(lj
C
stenocephala feeds mainly on tissue, but also ingest small
·c amounts of blood. Infections of dogs with >80 adult U.
Q)
stenocephala are associated with loss of plasma proteins
-� via the i.nteslinal tract.
>,
0)
0 • Ancylostomosis. Preadult and adult stages
0
"in of Ancylostoma spp. attach to the intestinal mucosa
(lj
with the buccal capsule. Their sucking activities and
a.. histolytic enzymes, released by the parasites, create small
lesions, through which blood leaks and is taken up by
the parasites or gets lost in the intestinal tract of the
host. The average blood loss, caused by A. caninum, is
estimated at 50-200 µl per adult worm and day. During
feeding, A. caninum changes its site every 4-6 hours,
leaving small lesions, which usually heal within 24 hours.
Intestinal hookworm stages produce secretions in their
oesophageal glands or intestinal cells; these are then
released into their digestive tract or are partially excreted
into the host's intestinal tract. These secretions contain
molecules, which inhibit coagulation of host blood
and dissolve aggregates of platelets due to fibrinolytic
properties. The inhibition of blood coagulation allows
hookworms an efficient haematophagy. Ingested
erythrocytes are lysed by a pore-forming protein, and
the released haemoglobin is digested by the action of
a cascade of proteases. Necator americanus produces
substances that inhibit inflammatory reactions or
degrade hnmunoglobulins (IgA, lgG), thus preventing
antibody-mediated cytotoxic attacks to the parasite. An
allergic reaction of the intestinal mucosa) can lead to the
elimination of the worm burden ('self-cure').
The pathological picture of significant Uncinaria or
Ancylostoma infections is characterised by subacute to
chronic catarrhal inflammation of the intestinal mucosa
with velvety thickening, increased mucus production,
spotted or diffuse reddening and petechial bleedings at
the sites of hookworms. Heavy Ancylostoma infections
can cause haemorrhagic inflammation with bloody
intestinal contents ( ► Figure I 0.26).
Clinical signs. Intestinal hookworm infections may be
asymptomatic or symptomatic, depending on intensity
of infection and responsiveness of the hosts. Diseases
occur mainly in young animals.
• Dog. Significant intestinal burdens of U.
stenocephala lead to growth retardation, emaciation,
mucous diarrhoea, and partly also to hypoproteinaemia.
Additional signs can occur in A. caninum infections,
including anaemia (initially normocytic normochromic
and, with increasing Iron loss, hypochromic and
microcytlc), bloody diarrhoea, metabolic acidosis,
cardiac insufficiency and death.
Figure 10.26. Ancy/ostoma caninum: intestine of a heavily
infected puppy with haemorrhagic enteritis (Photo: IPZ, J.
Eckert).
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)
I Cat. Symptoms associated with intestinal A.
tubaeforme infections correspond to that of A. caninum
infections in dogs.
Natural somatic infections (larvae in extraintestinal
tissues) of older dogs or cats remain asymptomatic.
Cutaneous lesions have been highlighted above.
Diagnosis . Patent infections are diagnosed by
coproscopic egg detection in faeces(flotation technique).
In fresh faecal samples, the thin-shelled oval eggs often
contain only a few(4-16) blastomeres, but their numbers
can increase rapidly in older faeces. Although the eggs
of U. stenocephala are usually slightly larger than that
of A. caninum ( ► Figure 16.16, p. 549), a reliable
differentiation in routine diagnosis is often not possible.
This also applies to the differentiation of L3. However,
eggs of hookworm species can be differentiated by
PCR. Post mortem, the parasites are readily visible
macroscopically in the small intestine.
Therapy and control. For treatment of hookworm
infections in dogs and cats, a series of well-tolerated and
highly effective drugs from different chemical classes
are available. Examples: fenbendazole (dog and cat daily
50 mg/kg b.w. p.o. for 3 days) or flubendazole (dog
and cat 22 mg/kg b.w. p.o. for days 2-3). Newer drugs,
such as selamectin, moxidectin and emodepside, are
highly effective in a single dose; their application to
dogs and cats in spot-on formulations is convenient
in practice (► Table 19.14 and 19.15, p. 600 ff). The
latter compounds are effective against immature (L4)
and adult intestinal hookworms.
There are several options for control hookworm in
carnivores that can be combined with measures against
ascarids and some other parasites ( ► p. 605).
Genus Bunostomum
Disease: Bunostomosis in ruminants.
Bounos(G): hill; stoma (G): mouth.
Agent and life cycle. Bunostomum trigonocephalum
preferably infects sheep and goats and Bunostomum
phlebotomum mainly cattle. In addition, wild ruminants
are suitable hosts ( ► Table 10.5). The adult stages of
these species are up to 3 cm long. They have a cup­
shaped buccal capsule with 2 ventral cutting plates and
tooth-like structures at the base.
The external development corresponds to the strongylid
type; it is suspended below 15 °C, proceeds optimally at
20-30 °C, and requires high moisture. On pastures in
Central Europe, L3 remain viable for almost 2 months
during the summer period, overwintering usually does
not play a role, because of the cold sensitivity of the
larvae. The infection of the hosts takes place on pasture,
frequently in late summer and autumn, or in outside
pens and stables. In the latter, insanitary conditions
and moist deep litter favour the infection. Both peroral
and percutaneous infections of hosts are possible; the co
latter are regarded as most important. In both cases, :Q
>,
larvae undertake tracheal migration before reaching the OJ
C
definitive site in the small intestine. Prepatent period 0
about 7 weeks( ► Table 10.5).
Occurrence and epidemiology. According to older
data from Bavaria/Germany around 5% of the slaughter
sheep were infected with B. trigonocephalum. In NL 1%
of dairy cows (n= 113) were shedders of Bunostomum
eggs. In CH, multiple coproscopic examinations
identified up to 30% of 478 young cattle as shedders of
Bunostomum eggs, with the largest proportion in farms
with deep-litter husbandry.
Pathogenesis and clinical signs. Frequently,
Bunostomum burdens are low in domestic ruminants,
so that the infections remain inapparent. In significant
infections, severe forms of anaemia with protein loss
into the intestinal tract and haemorrhagic enteritis can
develop, due to continuous blood loss caused by the
hookworms. In mixed infections with other parasites
(e.g. trichostrongylids), an accumulation of pathogenic
effects occur. Clinical signs of diseased animals include
fatigue, oedema(intermandibular oedema), emaciation
and some-times bloody diarrhoea( ► Figure 10.27).
Diagnosis, treatment and control. Eggs of B.
phlebotomum in fresh faeces are morphologically
distinguishable from eggs of other gastrointestinal
strongyles( ► Figure 16.8, p. 539). This does not apply
to eggs of B. trigonocephalum. However, genus diagnosis
is possible by differentiation of free-living L3 obtained
from copro-cultures(► Figure 16.10, p. 541). Therapy
and control as in trichostrongyles ( ► p. 586).
Zoonotic importance. In humans, Ancylostoma
duodenale and Necator americanus, specialised
to primates, cause patent intestinal infections. A.
ceylanicum, a parasite of dogs and cats in tropical areas,
was previously regarded as a rare intestinal human
parasite. However, recent studies in Asia have shown
that this species is the second most common hookworm
in humans. For example in rural Cambodia, 52% of
humans, shedding hookworm eggs, were infected with
A. ceylanicum. Other than domestic carnivores, wild
canids(dingoes) can also be carriers of A. ceylanicum,
as shown in Australia. Rarely, A. caninum invades the
intestine of man without reaching patency, and causes
mild to severe forms of eosinophilic enteritis ( cases in
Australia and USA).
Infective larvae of various hookworm genera
(Ancylostoma, Uncinaria, Bunostomum) from animals
 Part Ill. Parasites and parasitoses: metazoa

a.

Figure 10.27. (a) Heavy Bunostomum infection in cattle: clinical picture. (b) small intestine from cattle with Bunostomum infection
(length of the parasites up to 30 mm) (Photo: IPZ, J. Eckert).

are considered as causative agents of larva migrans lnpankaew T, Schilr F, Dalsgaard A, Khieu V, Chlmnoi W,
cutanea (= larva migrans externa) of humans. The Chhoun C, Sok D, Marti H, Muth S, Odermatt P, Traub
most important agents are larvae of A. braziliense, RJ (2014) High Prevalence of Ancylostoma ceylanicum
A. ceylanicum and A. caninum, whereas only sparse l1ookworm infections in humans, Cambodia, 2012. Emerg
information exists on the etiological role of Uncinaria Infect Dis 20: 976-982.
and Bunostomum species. On contact with faeces or Sager H, Steiner Moret C, Grimm F, Deplazes P, Doherr
contaminated substrates (e.g. soil, sand), the larvae MG, Gottstein B (2006) Coprological study on intestinal
penetrate the skin of humans, and migrate subsequently helminths In Swiss dogs: Temporal aspects of anthelminthic
between corium and stratum granulosum. The migration treatment. Parasltol Res 98: 333-338.
tracks appear as inflammatory, itchy and painful, slightly Smout FA, T hompson RC, Skerratt LF (2013) First report
raised and usually tortuous lesions. In Central Europe, of Ancylostoma ceylanicum in wild canids. Int J Parasitol
larva migrans cutanea is most commonly observed in Parasites Wildl 13: 173-177.
tourists after seaside holidays in warm countries. Stoye M, Schmelzle HM (1986) Ober den Ausbreitungsmodus
der Larven von Ancylostoma caninum ERCOLANI 1859
(Ancylostomidae) im definitiven Wirt (Beagle). J Vet Med B
Selected references 33: 27 4-283.
Traub RJ (2013) Ancylostoma ceylanicum, a re-emerging but
Beugnet F, Bourdeau P, Chalvet-Monfray K, Cozma V, neglected parasitic zoonosls. Int J Parasitol 43: 1009-1015.
Farkas R, Gulllot J, Halos L, Joachim A, Losson B,
Mir6 G, Otranto D, Renaud M, Rlnaldl L (2014) Parasites
of domestic owned cots In Europe: co-Infestations and risk
factors. Paraslt Vectors 7: 291.
Bowman DD (2011) Zoonolic hookworm Infections. In: Palmer
SR, Lord Soulsby, Torgerson PR, Brown DWO (edB.) Oxford
textbook of zoonoses, 2nd od. Oxford, UK: Oxford University
Press, pp. 767-773: ISBN 978•0·19·857002·8.
Brutinskalte-Schmldhalter R, SarkOnas M, Malakauakaa
A, Mathia A, Torgerson PR, Deplazea P (2012) Hatrnlnths
of red foxes (Vulpes vu/pes) and raccoon dogs (f.Jyciereutos
procyonoides) In Lilhuanle. Parasitology 139: 120-127.
Q,)
C Epe C (2009) Intestinal nematodes: biology and control. Vet Chn
·u North Am Small Alllm Pract 39: 1091-1107.
ESCCAP (2010) Worm control In dogs and cats. Guideline 01.
2nd ed. Malvern, UK: European scient1fic council companion
ro animal parasites: ISBN: 978-1-907259-16·6.
C
·c Gaseer RB, Stewart LE, Speare R (1996) Genetic marl<ers
Q,)
in ribosomal DNA for hookworm identification. Acta Tropica
C 62: 15-21.
>. Geiser BB, Ising-Volmer S, Schnieder T, Stoye M (1992)
OJ
0 Umlang und Ablauf der L..arvenausscheidung m,t der Milch
·u5 bel Hundinnen nach unterschiedhch starker fnfektJon mil
Ancylostoma canmum (Ancylostomatidae). ANJe-N Parasitol
CCI
0.... 33: 142-150.
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms}
• Superfamily Trichostrongyloidea
Family Trichostrongylidae
Disease: Trichostrongylidosis.
Trichos (G}: hair; strongylos (G}; round. Refers to a
mostly hair-like body shape.
Trichostrongylidae (= trichostrongyles} are small- to
medium-sized gastrointestinal parasites of vertebrates
(except fish}. Worldwide, they are the most important
nematodes of domestic and wild ruminants, causing
significant losses due to impairment of performance and
diseases. Although belonging to the family Molineidae,
the genus Nematodirus is discussed here together with
the Trichostrongylidae, as it is closely related to this
group.
Summary
Trtchoatrongyles In cattle, sheep and goat
• Agents. In domestic ruminants, trlchostrongyles
usually occur In mixed Infections of several species.
The most common species In cattle are: Ostertag/a
ostertagi and Trlchostrongylus axe/ (abomasum) as well
as Cooper/a oncophora and Nematodlrus he/vet/anus
(small Intestine); In sheep and goats: Haemonchus
contortus, Teladorsagla clrcumclncta, Trlchostrongy/us
axe/ (abomasum) and various species of the genera
Trichostrongylus, Cooper/a and Nematodlrus (small
Intestine).
• Life cycle. Trlchostrongyles have a direct life cycle In
which infected hosts shed eggs to the environment.
First larval stages hatch from the eggs and develop to
Infectious L3. In Nematodlrus species this development
takes place within the egg shell. Definitive hosts acquire
the Infection by ingestion of L3.
• Epidemiology. Definitive hosts become predominantly
infected on pastures. In European regions of temperate
climate, the epidemiology Is seasonal and follows
an annually recurring basic pattern, which can vary
depending on several factors. The greatest Infection
risk exists in the second half of the grazing season (=
main infection period). Nematodlrus battus L3 hatch
after the eggs have been exposed to a cold period.
These larvae represent the greatest Infection risk In
spring, especially for young lambs.
• Pathogenesis and clinical signs. Particularly
pathogenic are 0. ostertagi In cattle and H. contortus
in sheep and goats; mixed infections with other
species reinforce the harmful effects. Heavy worm
burdens, especially those with dominating pathogenic
species, cause impairment of performance, to some
extent Illness with inappetence, diarrhoea, emaciation,
hypoalbuminaemia, dehydration, and in Haemonchus
Infections of small ruminants also anaemia. Diseases
occur mainly in young animals In their first grazing
season, usually In the second half of this period. In
association with the reactivation of hypoblotlc stages,
T
A
disease outbreaks can occur end of winter or In spring
In animals that have acquired heavy Infections In the
previous autumn (so-called 'winter ostertaglosis' In
cattle, haemonchosls In ewes around the lambing
period In spring). cu
• Dlegnoll9. Epidernlologlcal and clinical case histories, :Q
'5,
egg detection In faeces (flotation technique, egg counts), O>
e
C
and differentiation of L3 (obtained from coproculturee)
are basic components of the available diagnostic ti5
options. Elevated levels of serum pepelnogen are
Indicative for ostertagloels In cattle, and anaemia for
haemonchosls In small ruminants. AntlbOdy detection
In bulk milk samples can be useful for cattle herd
surveillance and epidemlolcgical studies,
• Treatment. Anthtlmlntlcs of various chemical classes
are employed for therapy agaln1t trlchostrongyles,
Including (pro)benzlmldazolea, lmldazothlazoln
(levaml10le), macrocycllc lactonee, amlnoacetonltrll8,
and splrolndolet (► Table 17.4, p. S61), Thele druge
are effective agaln1t adult and mo1tly alao agalnet
Immature non-hypobiotlc tnchoetronygles. Special dn.,g
formulations facilitate their application to groups of
herds/flocks of ruminants (e.g. spot-on application).
Drug resistance of trlchostrongyles, mainly In small
ruminants, Is a worldwide problem.
• Control. Pasture management and strategic UM of
anthelmlntlcs, based on epidemiological knowledge, are
components of control programs, which have proved
successful In practice (see below).
Trlchostrongyles In other host species
Cl)
• WIid ruminants harbour host-specific species of .c
trlchostrongyllds, but share some species with domestic c
ruminants; horH: Trlchostrongylus axel (stomach); pig: .E
a5
Hyostrongy/us rubidus (stomach), rabbit Graphldium I
strigosum and Obellscoides cuniculi (stomach),
Trichostrongylus retortaeformls (small Intestine);
poultry: Trlchostrongylus tenuls (small Intestine, caeca).
Genera Haemonchus, Ostertagia,
Teladorsagia, Trichostrongy/us, Cooperia,
Nematodirus
■ Trichostrongylids of domestic ruminants
Agents and occurrence. Trichostrongyles of
ruminants are hair-thin, sometimes also slightly thicker
nematodes of about 5-30 mm in length with a greatly
reduced buccal capsule(► Figure 10.28 and 10.29). The
males have a well-defined, three-lobed bursa copulatrix,
two spicules, in some species a gubernaculum and genital
cone(► Figure 10.4). Morphological identification of
species is mainly based on characteristics of males, but
partly also on features of females. Numerous genera and
species can also be identified using genetic markers.
Eggs: are oval, thin-shelled, with 16 or more blastomeres,
70-98x30-50 µm(► Figure 10.30, ► Figure 16.8, p. 539).
Nematodirus eggs with thicker shell and 4-8 blastomeres,
much larger {150-180x67-77 µm) ( ► Figure 16.8).
 Part Ill. Parasites and parasitoses: metazoa
Figure 10.28. Haemonchus contortus: length of females up
to 30 mm (Photo: IPZ).
• Species of trichostrongylids in Central
Europe. Domestic ruminnnts are hosts of numerous
trichostrongylid species, inhabiting the abomasum or
small intestine (partly overlapping organ localisation)
(► Table 10.6). Mixed infections with several species
are the rule, but individual species can dominate both
in numbers and pathogenic effects.
Young and older cattle are often infected with the
abomasal parasite Ostertagia ostertagi. This species is
the most important cause of parasitic gastroenteritis
(PGE), because of its considerable pathogenicity.
Young cattle are frequently co-infected with Cooperia
oncophora, a less pathogenic small intestinal parasite. In
older cattle, prevalences and infection intensities of this
species are usually lower as a result of partial immunity.
Trichostrongylus axei (abomasum) and Nematodirus
he/vetianus (small intestine) are regionally significant.
Other species play a minor role, but may contribute to
pathogenicity.
In sheep and goats ( ► Table 10.6) other species
predominate: these are the abomasal parasites
Haemonchus contortus and Te/adorsagia circumcincta,
and small intestinal parasites, such as Triclwstrongylus
spp., Cooperia curticei and Nernatodirns spp.
Trichostrongylid species differ in their host specificity
( ► Table 10.6). Under natural conditions, T. axei and
Ostertagia /eptospicu/aris infect cattle, sheep and goats. In
(1)
contrast, 0. ostertagi is limited almost entirely to cattle;
·o
C
'5 this species colonises smaJI ruminants only sparsely and
(1)
� for a short period. On the other hand, T. circumcincta is
especially adapted to small ruminants, but occasionally
ro also occurs in cattle. Some species with low host
C
·c specificity can be transmitted from ruminants to other
(1)
mammals, such as T. axei t.o equines and humans or T.
-� co/ubriformis to humans. In Europe, autochthonous wild
>- ruminants harbour both host-specific trichostrongylids
0)
0 and species of domestic ruminants( ► p. 300). Certain
0
"iii trichostrongylid species consist of genetically different
ro strains. Of great practical importance are strains with
ro
CL resistance to anthelmintics( ► p. 564).
Figure 10.29. Trlchostrongylus axe/: length about 5-6 mm
(Photo: IPZ).
• Trichostrongylid species in other regions. Many
of the species occurring in Central Europe(► Table 10.6)
are also common in other European regions and on other
continents. Further species have to be taken into account
regionally, for example Haemonchus placei, inhabiting
the abomasum of cattle (also of goats and sheep),
especially in warm countries. This species is closely
related to/-/. contortus, but proved to be morphologically,
genetically and biologically distinct. Mecistocirrus
digilatus(subfamily Haemonchinae) is a blood-feeding
abomasal parasite of cattle and buffaloes in Asia, Africa,
Latin America, and sporadically in Europe. Marsha//agia
marsha//i (subfamily Ostertagiinae), parasitising the
abomasum of sheep, goat, cattle, buffalo, camel and
wild ruminants (antelope) in subtropical and tropical
regions, occurs also in northern Europe, e.g. in reindeer
on Spitsbergen (Norwegian Svalbard Islands).
Life cycle. T he external development of tricho­
strongyles starts with egg shedding by parasite carriers.
First larval stages hatch from the eggs and develop
into infectious L3 ( ► Figure l0.30). In Ne111atodirus
species this development takes place within the egg
shell(► Figure 10.33).
Internal development ( ► Figure I 0.30) is initiated
after ingestion of infectious, ensheathed L3. Particular
signals in the rumen or abomasum stimulate the larvae
to excrete enzymes, acting on the inner side of the
sheath. For example, larvae of H. contortus excrete an
'ex-sheathing fluid' containing a metalloendopeptidase
which attacks only a small annular zone about 20 µm
distal to the anterior end of the sheath. At this zone,
the sheath is weakened, and under the influence of
intense movements of the larva, the anterior end of the
sheath detaches as a cap, so that the larva can hatch.
Thereafter, the larva is called parasitic L3. Different
types of exsheathment are known from other nematode
species ( ► p. 289).
Depending on the predilection sites of adults, the
ensheathed larvae of various trichostrongylid species
react differently to key signals. Thus, L3 of abomasal
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)

Table 10.6. Species of Trichostrongylidae and Nematodirus (selection). autochthonous in Europe. (The most important species

..,,,.,..
are marked in bold characters in the column on prevalence.)

Rredllectloh Species (prepatent period In daya of Length of Prevatence3

ilte of adults 1 selected species)
(mm)2 Cilttfe 8heep 0081
ro
Abomasum _/jaf!mon�hus cont<?_rtus (18-19) I !+l
20-30-- ++/+++ +++ --
:g
>­
I+++/++++ ((+)) - - +)
(
OJ
_ Q_stertagia ostertag� (18-21) ·- --- -8-9 - I C
( +) -
0
- �P to 10 - +/+++ )
J+
Qstertagia4 lyr<!_� _ _
Ostertagia lep!ospicularis (17) -- - 6-11
--- -+/++++ + +-
>-
!!!ladors!!Jgia6 circumclncta (16) - - 12-13 -- (+) +++/++++ ++++ -
Teladorsagia: tri'.!!:Eafa -
9-11 (+) ++/++++ ++++ --
--
-
Tricll_oslm'!_gylus axe/ (25)- 5-6 - - +/+++ ++ ++
Small intestine Trichostrongylus CC!!_l!_bri'!}rmls (1� _ 5-6 ((+)) ++/+++ - +++
!}!c0._ostrongY!_u5:. vit!!'us (18� 9) --- 5-8 ((+)) ++/+++ ++ --
Trichostrongylus capricola -
5-7 - ((+))
+
- +- +- ---
Trichostrongylus /ongispicularis 5-7 - -- - -
Cooperia curticei (14) 5-6 + +/++++--- ++
++---
Cooperia oncophora (17) 6-12 ++/+++ +
-->-
Cooper/a zurnabada6 7-9 +/++++ +
Cooper/a pectinata 7-9 +
Cooperia punctata (14) 6-7 +/++ (+)
Nematodirus helvetianus (21-26) 15-24 +/++++ (+)
Nematodirus fi/ico/lis (21) 12-20 ( +) ++/++++ ++
Nematodirus battus (15-29) 18-15 + +/++++ ++
Nematodirus spathiger (15-21) 12-20 (+) ++
1 At necropsy, specimens of the species typically inhabiting the abomasum may be found in anterior parts of the small intestine, and (more
rarely) the species from the small intestine in the abomasum.
2 For sake of clarity, only the body length of females is listed; males are a little shorter.
3 Approximate prevalences: ++++: >75%, +++: >50-75% , ++: >25-50%, +: 10-25%, (+): <10, ((+)): sporadic, empty fields: no data.
Prevalences are subject to wide variation; data predominantly from AT, CH and DE.
4 Syn.: Skrjabinagia.
5 Formerly allocated to the genus Ostertagia. T. trifurcata and Ostertag/a pinnata, both occurring in sheep and goats, are morphologically
very similar and described either as distinct species or as synonyms.
6 Alternative spelling: C. surnabada.

parasites (H. contortus, T. circumcincta, 0. ostertagi,
T. axei, etc.) discard the sheath within 12 h p.i. in the
rumen, but this is done by only a few larvae of the
species inhabiting the small intestine (T. colubriforrnis,
N. spathiger, N. battus). In the latter group exsheathment
(ecdysis) usually starts after a short stay in the abomasum.
Important key signals for abomasal parasites are the CO 2
content of the gas phase, the buffer system H2 CO/
HC03 and a pH around 6.5 to 6.9 (corresponding to
conditions in the rumen). However, for inhabitants of
the small intestine, a pH in the acidic range as well as
the action of pepsin and CO 2 (equivalent to conditions
in the abomasum) are adequate signals. Furthermore,
temperature and some other factors play a role in ecdysis.
Cooperia species, parasitic in the small intestine, behave
more like abomasal parasites with respect to ecdysis.
After ecdysis further development takes place in the
target organ in which the adults establish. Parasitic L3
preferably invade the lumina of abomasal glands (e.g. 0.
ostertagi, O. leptospicularis, T. circumcincta), the mucosa!
crypts of the abomasum (e.g. H. contortus, T. axei) or the
crypts of Lieberkilhn and glandular lumina of the small
intestine (e.g. Cooperia, Nematodirus). Usually, they do
not penetrate the epithelial layer, and only rarely some
parasites are found in the propria, especially in parts of
the mucosa with heavy inflammatory reactions (e.g. 0.
leptospicularis, Cooperia spp., Nematodirus spp.). During
the paramucosal phase, the parasitic L3 moult usually
within a few days into L4 or sometimes into preadult
sth stages (e.g. 0stertagia species, T. circumcincta).
Subsequently these stages colonise the mucus layer of
the mucosa where they undergo further development to
sexual maturity. A portion of the nematode population
may pass to hypobiosis. Basic data on the parasitic
development of some species are summarised in ► Table
10.7. Prepatent periods of the different species vary
between 2 and 4 weeks.
Epidemiology. Trichostrongyles of ruminants are
mainly transmitted during the grazing season. In regions
of temperate climate, the epidemiological course is
Part Ill. Parasites and parasitoses: metazo a

Al!)omasum

---- - - - -
\ I
\ I
\ I
\ I
\ I
'
'\ !ti!ffllfflll�I '
hlstage

1..3 and L4 In
fundlc gland

I Ecdysis of L3
I

1
ult male
(female not shown)
_____________ _

Larvae 3 on plants Larva 3

Figure 10.30. Life cycle of Ostertag/a ostertag/ (Graphics: IPZ, S. Ehrat).

characterised by a pronounced seasonal pattern, because
the external phase of parasite development is significantly
influenced by temperature and moisture. Although this
constantly recurring basic pattern is subject to variations
due to weather conditions, geographic location, altitude
of pastures and other factors (see below), it allows the
identification of periods with the greatest infection
risks (main infection periods) and the application of
measures for targeted (or 'strategic') control ( ► p. 580).
The following factors are of particular epidemiological
importance: (a) spectrum of trichostrongylid species, (b)
contamination of pastures with trichostrongyle eggs, (c)
seasonal dynamics of the larval population on pastures
and exposure of grazing animals to infections, (d)
dynamics of parasite populations in host animals and (e)
livestock husbandry ( e.g. extensive or intensive), pasture
management, animal behaviour and other factors.
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)

Table 10.7. Data on the parasitic development of some trichostrongylid and Nematodirus species.

Speeles (host animal) Daysp.l. Development end ptepatency stage of

M: moultlng, L3: panisttlc L3', lA: 4111 stage larva, hypobloala
St. 5: pntadult &Ill stage

Haemonchus contorlus (sheep) 1-8 L3 __. abomasum. crypts. �me in lumina of gastric gla�ds - L4
M__. to L4, return to mucosa surface- - -- - - --
9-11 M__. to St. 5, furth�r d�elopment ----
18 prepatency --- - -
Ostertagia ostertagi (cattle) 1-8 L3 __. abomasum, lumina of gastric glands (mostly in fundus L4
region)
M
-__. to-L4
8-15 M__. toSt. 5 In lumina of gastric glands --
>15 emergence from gaslrlc glands to mucosa surface, further
developf2:1�1.!,_ ---
18 -- prep�tency - - - - --
Trichostrongylus colubriformis
(sheep)
1-4 L3 __. small Intestine ..... Mto L4 - - L3
6-10 -
MtoSt. 5 -
15 - _ prepatency - -
Cooper/a curlicei (sheep) 1-2 L3 ..... lumen of anterior small Intestine --- L4
3-4 migration of L3 into crypts, M-, to L4
5 most of L4 free in intestinal lumen
9-10 M-, to St. 5, further development
14 prepatency
Nematodirus battus (sheep) 1-5 L3 __. small intestine, M-, to L4 7
12 nearly all parasites in St. 5
14 prepatency
1 Parasitic L3 = infectious larva after ecdysis.

Ostertagiosis and cooperiosis in cattle
In European regions of temperate climate, 0. ostertagi
and C. oncophora are the main causative agents
of parasitic gastroenteritis (PGE) in cattle. These
species occur regularly in mixed infections with other
trichostrongylid species (see below). The following text
refers mainly to the 0stertagial Cooperia complex and
an epidemiological situation that is characterised by
grazing of young cattle on lowland or mountain pastures
(► Figure 10.31 and 10.32).
• Contamination of pastures with tricho­
strongylid eggs. During indoor maintenance in
winter, some calves may pick up trichostrongyle
infections, particularly when kept loose in stables or in
outside pens. However, the resulting low egg output is
of minor importance for pasture contamination in the
following spring. Older cattle that became infected in the
previous year and remained carriers of trichostrongylids
during winter may shed only low numbers of eggs,
which nevertheless are sufficient for an initial pasture
contamination, resulting in a certain infection risk for
other animals. Shortly after turnout of cattle to pasture in
persisting pasture contamination with eggs ( ► Figure
10.3 I). If pastures are grazed simultaneously by cattle
and sheep, the latter can contribute to contaminations
with eggs of some of the species which are also infective
for cattle (e.g. T. axei). Wild ruminants do not play a
significant role in pasture contamination for several
reasons ( ► p. 300). On the other hand, the distribution
of slurry, in which 13 of 0. ostertagi and C. oncophora
can survive 2-6 months in summer and 3-5 months in
winter, may lead to an increased pasture contamination.
• Development and survival of infective larvae.
Development of the free-living Ll-3 of 0. ostertagi,
C. oncophora and 0. leptospicularis in cattle faeces is Q)
possible in a wide temperature range of 5-35 °C with C
an optimum at 23 °C. A water content of faeces of
·u
'5
Q)
about 60-70% is favourable for the development of L3, �
lower or higher values rapidly lead to decreasing rates. 2:'
al
At constant temperatures of 10, 15 or 20 °C the L3 of C
·;::
0. ostertagi and C. oncophora develop in 21, 14 and 6 Q)
days. On pastures the development can be completed at
summer temperatures already in 1-2 weeks, but it often C
takes longer, especially in early spring and autumn. >,
Ol
During winter months, the development is suspended 0

spring, most (>90%) of the immunological naive young or proceeds very slowly (about 2 months at constant ·u5
animals become infected with overwintered L3, and 5 °C). An important prerequisite for the development
al
cause - already after some weeks - a considerable, longer of the preparasitic larval stages is sufficient aeration of CL
 Part Ill. Parasites and p arasitoses: metazoa

25 ,----------------------------,
.s::.
Cl
E

i.9 20
Egg shedding of
E young animals -
� 15

Cl

t 10
� Overwintering Infective larvae on plants

········l··········· ·················· ......................................................... .

larvae
l'.'.? 5
1l
E

0
April May June July Aug. Sept. Oct. Nov.

Grazing period

Figure 10.31. Ostertagiosis/cooperiosls of cattle: scheme of the epidemiology on permanent pastures in lowlands ( Graphics: IP Z).

25.-----------------------------,

L
.QI
.s::.
.9
20 ·········· .......................................................................................

! 15 .................................................................................................

I
Egg shedding
. of
young animals "'
Relative high
10 ·pmpor11on·oI······································
overwintering
larvae
5 ........, ............................... .
Infective larvae on plants

0
April May June July Aug. Sept. Oct. Nov.

Animals on
mountainous pasture

Figure 10.32. Ostertagiosls/cooperlosls of cattle: scheme of the epidemiology on permanent pastures In mountainous regions
(Graphics: IPZ).

the manure, which is promoted by activities of dung­ • Translocation (= translation) of infective larvae.
Q)
inhabiting organisms (e.g. beetle larvae). LI and L2 With regard to the infection risk of cattle, which usually
·u
C

are very sensitive to desiccation and low temperatures,
� and do not usually survive the winter; in contrast, L3 of
c Ostertagia and Coo peria species of cattle overwinter on
(1j
C pasture in considerable numbers, even on mountainous
·c pastures up to altitudes of about 2,400 m. These stages
Q)
avoid grazing in the immediate vicinity of cow pats, the
transition (translocation) of L3 from faeces to the more
distant surrounding area and plants is epidemiologically
significant. Rainfall plays an important role, stimulating
L3 to migrate to the surface of dung pats from which they

� which do not feed and live entirely on their endogenous are splashed off by falling raindrops or washed down
C reserves have a surprisingly long life-span (over 2 years by rainwater. Active migration of L3, which is limited
>- at constant 6-7 °C). A behavioural trait of the L3 that to a few centimetres, contributes little to horizontal
-
0)
0 contributes to the persistence of larval populations in the translocation. Important is the mechanical spread of
0
·w environment is their withdrawal to a 'refugium' in the larvae-containing faecal material by animals, people
superficial soil layers of pastures under less favourable or machines. This is indicated by the fact that L3 could
(1j
conditions. regularly be detected on limbs of grazing calves. Further
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)
possibilities of horizontal spreading of L3 include the
catapulting mechanism of fungi of the genus Pilobolus
used to launching the sporangium (Dictyocaulus ► p.
305) or dissemination by insects to which larvae from
cattle faeces can attach(phoresy). Vertically, L3 migrate
within a film of moisture to pasture plants up to a few
centimetres.
t Seasonal dynamics of the larval population
on pastures and infections risks of grazing
animals. As mentioned above, infectious L3 of cattle
trichostrongyles can overwinter on pastures, the amount
of which is proportional to the degree of pasture
contamination in the previous year, but it is influenced
by climate and weather conditions. In parts of Europe,
the population of overwintered larvae in early spring
is quite large. However, the numbers of larvae decrease
sharply until May/June, and also their concentration
per kg forage drops significantly, due to intensive plant
growth in this period( ► Figure 10.31). On mountainous
pastures at higher altitudes, L3 are protected under snow
cover for longer periods, so that significant numbers can
survive until July( ► Figurel0.32). At the beginning of
the grazing season, overwintered larvae represent an
important infection source for immunologically nai've
calves and young cattle. After 2-3 weeks, these animals
shed eggs in increasing numbers, thus contaminating
pastures on their own or together with older cattle.
The degree of pasture contamination depends not
only on the number of eggs excreted, but also on the
stocking density of the pasture. The increasing pasture
contamination with eggs is followed by gradually rising
numbers of L3. Due to favourable temperatures and
humidity, an increased translocation of L3 from faeces
to pasture plants occurs from mid-July onwards, thus
leading to an increasing infection risk for grazing
animals. Infections in this period can already be so
heavy that clinical cases of ostertagiosis may occur
(summer ostertagiosis, ostertagiosis type I). From eggs,
deposited to pastures in August, L3 continue to develop,
but relatively few of them are translocated to pasture
plants in autumn. Therefore, the infection risk decreases
gradually( ► Figure 10.31 and 10.32). A portion of these
larvae survives until the following spring.
• Dynamics of the p arasite population in
host animals. Parasite populations in host animals
are subjected to their own dynamics. Initially, L3
continuously ingested by grazing hosts develop into
adults in relatively high proportions. Due to gradually
devel oping immunity, this proportion decreases
continuously and leads to a limitation of the worm
burden(immunology, see below).
It is an important phenomenon that a variable
proportion of 0. ostertagi L3 ingested by grazing
animals develop to hyp obiotic L4. In temperate parts
of Europe and northern United States, hypobiosis (=
arrested development) occurs in young cattle of the first
grazing season increasingly in late summer and autumn,
whereas in other regions with dry summers (e.g. South
America) this occurs in spring or before onset of the
dry season. Several factors are thought to play a role in
inducing hypobiosis, including genetic predisposition
of Ostertagia strains, selection of infectious larvae by ro
environmental factors and increasing immunity of cattle :g
>,
during the grazing season. 0)
e
C
Experimentally, hypobiosis of 0. ostertagi, T. if)
circumcincta and some other species can be induced
by keeping L3 at 4-6 °C for 4-8 weeks. Hypobiotic IA
of 0. ostertagi, persisting for several months in the
lumina of abomasal glands without causing significant
host reactions, continue their development into mature
stages in late winter or spring. In this way, part of the
parasite population overwinters in host animals and
causes increased egg shedding at the beginning of the
grazing season. Cattle, heavily infected with hyp obiotic
L4, can become seriously ill, due to the synchronised
reactivation of such stages in winter or in spring(winter
ostertagiosis or ostertagiosis type II). This disease is
now rare, as it can be prevented by treating cattle at the
beginning of the housing period using anthelmintics
with high efficacy against hypobiotic stages. Hypobiotic
stages are also known to occur in C. oncophora and other
trichostrongylid species ( ► Table 10.7). The factors
responsible for the reactivation of hypobiotic stages of
trichostrongyles are still unknown (hookworms, ► p.
282).
• Influence of various factors on s easonal
dynamics of larvae and infection risk. The above­
mentioned seasonal distribution patterns of larval
density with increased infection risk on permanent
pastures in lowland areas as from mid-July was first
observed in the UK and later in other countries north
of the Alps ( ► Figure 10.31.). Variations of this basic
pattern are caused by several influences, mainly the
amount of rainfall and its distribution, temperature
profile, stocking density as well as the susceptibility and
age of host animals. Thus, the increase in larval density
on pastures - normally to be expected mid or late July
- may shift over time. If a summer is unusually dry,
larger quantities of larvae are translocated to plants later
when humid weather begins. Likewise, exceptionally
Q)
mild temperatures in autumn and winter may have C
epidemiological implications. ·u
'6
Q)
�
Special conditions exist on pastures in mountainous
areas (alpine pastures). Often, cattle graze there in
c
ro
C
mixed groups, consisting of young animals in their ·.::
Q)
first grazing season and older animals. Initially in spring,
animals are grazed on pastures close to the farms at _!;;
low altitudes, later on pre-alpine pastures (-700-1,500 >-
-
0)
m above sea-level) and finally from early July to mid­ 0
0
September on mountainous pastures at high altitude 'cij
(-2,500 m) ( ► Figure 10.32). Compared to intensively ....
managed pastures in lowland areas, the contamination Cll
Cl.. I
l
'I
 Part Ill. Parasites and parasitoses: metazoa
with L3 on pastures at medium to high altitude areas is
significantly lower. The reasons for this include lower
stocking density, mixed grazing of different age groups,
combined with several changes of pastures during the
grazing season. Therefore, worm burdens acquired by
cattle under these conditions may affect the weight gain
of the animals, but rarely cause clinical disease.
Trichostrongyli dosis in sheep and goats
In Central Europe, small ruminants harbour a wide rnnge
of trichostrongylid species ( ► Table I 0.6). In lowland
areas, the spectrum of species is often dominated by
H. co1Hort11s, whereas this spcdcs and C. c11rtii'ei ore
found less frequently in sheep grnzing in rnountninous
areas. There, ·1: circ11111ci11cta nnd Nc11111tod/rus spp. often
preclominatc. possibly due to different tcmpernture
requirements for the external development of these
species. Under expcrimcntnl conditions, the optimum
ternperatures for the development of L3 nre 16 °C for
'f. circ11111ci11ctn, 24 °C for H. co11tortus and nbout 30 °C
for C. wrticci.
The epidemiological basic patterns of trichostrongylicls
of small ruminants correspond in principle to those of
trichostrongyles of cattle. However, there arc some special
features which arc presented below, using haemonchosis
and nematodirosis as examples. Furthermore, in sheep
and goat farms, the various types of husbandry and
pasture management are to be considered, as they are
epidemiologically relevant.
• Haemonchosis in sheep. Important epide­
miologic features of H. contortus are as follows:
The ability of L3 to overwinter on pasture is
significantly weaker than in Ostertagia spp., but
the parasites survive in the host as hypobiotic L4
or adults.
Increased egg shedding occurs in ewes just before
or after lambing in spring. This phenomenon,
called 'spring rise· or 'post-par turient rise', is
predominantly due lo the reactivation of hypobiotic
stages (immunology. sec below). The increased
egg shedding coincides with the beginning of the
grazing season nnd is therefore of grenl importance
for pasture contamination.
Q)
Compared 10 other species of lrlchostrongyllds, H.
·u
C
'5 co111ort11s has a very high egg production (about
Q)
5,000 eggs/female/d). Therefore, egg shedding in
faeces can reach high values already with low worm
ro burdens, especially in non-immune lambs, and
C
·c contribute to a high pasture contamination.
Q)
Significant translocation of larvae may already
.£ occur in June and shortly thereafter lead 10 first
>,
0) clinical cases in lambs. In heavily infected lambs,
0 haemonchosis may take an acute course ,(see below).
;g Populations of adult stages, established in the
ro
1/)
ro
abomasum, can be eliminated rapidly and fairly
a.. completely after a new infection with L3 by an allergic
reaction (self-cure phenomenon) (immunology, see
below).
• Nematodirosis in sheep. In contrast to the above­
mentioned trichostrongyles, infective L3 of Nematodirus
species develop within the egg shell(► Figure 10.33).
In N. battus and N. filicollis the development to L3
usually takes about 4 weeks at constant temperatures
of20-22 °C, at 15 °C around 7 weeks, but in the field
more than 2 months.
Most of the L3 stages of N. battus and N.fi/icollis that
have developed in the eggs hatch only after the eggs
have been exposed in winter to low temperatures
or frost for several weeks and subsequently to
a temperature increase to at least IO 0C. When
temperatures rapidly increase in spring, mass
hatching of larvae can occur, leading to a high
infection risk for susceptible lambs.
Development of L3 of other Nematodirus species
(N. spathigcr, N. helvetianus) takes about 3 weeks
at 21 °C; the larvae hatch from the eggs without
previous cold stimulation.
Eggs and L3 arc cold tolerant and can overwinter
in frost; their resistance to drought is considerable.
Light Nematodirus infections may occur during
winter in housed ruminants, due to consumption
of hay contaminated with L3.
The main infection period for N. battus and N.
filicollis is spring (March to May), for other species
the second half of the grazing period.
Pathogenesis. Trichostrongyles can cause
inflammatory reactions of the abomasum (abomasitis)
and the small intestine (enteritis), whose manifestations
depend on the temporal sequence of the infection, the
number of parasites and the immune status of the host
animal.
• Lesions in the abomasum. In ostcrtagiosis
of cattle, initial lesions occur in parasitised glands
(mainly in the fundic region), including dilated
lumina, hyperplasia of epithelial cells and loss of cell
differentiation, particularly of the HCl-producing
parietal cells. Gradually, mostly focal cellular infiltrates
nre formed in basal layers of the propria, consisting
of lymphocytes, mast cells, some eosinophils and
hlstiocytcs (► Figure 10.34). Such lesions occur also
In non-parasiliscd, surrounding glands. These changes
are accompanied by an upregulution of inflammatory
cytokines (I Cs 6, 17, 21 ), as well as immnosuppressive
and cytotoxic factors. Already a few days p.i., pinhead­
sized, grey-white nodules with a central navel-like
depression are visible. The nodules are slightly raised
over the mucosa! surface and are caused by dilation
of glands and cellular infiltrates. When the parasites
emerge from the glands, a significant change occurs:
Glands, abandoned by the nematodes, collapse or are
filled by inflammatory exudate, some are destroyed.
The reaction of the mucosa is dominated by heavy,
+"
10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)

co
32
>,
0)

e
C:

L3
in Ecdysis L3 dultmale �
L4
.!m� '."_'I "_"""'._nl �

·�

Figure 10.33. Life cycle of Nematod/rus spp. (Graphics: IPZ, S. Ehrat).

diffuse or focal cellular infiltrates (for composition, see

above) in the propria, and cellular infiltrates, oedema
and in some cases small haemorrhages in the submucosa (1)
(► Figure 10.35). C:
·c3
'o
(1)
Macroscopically, the mucosa appears highly inflamed :'?!
(► Figure 10.36), the folds of the abomasum are
oedematous and later thickened by connective tissue. In co
C:
·;::
this stage of the infection, part of the worm burden may (1)
be eliminated. Finally, there is a gradual regeneration of j
the mucosa, which can take several weeks or months. _!;;
Similar, but usually less pronounced lesions occur in >­
CJ)
Figure 10.34. Ostertagiosis in cattle: changes of the abomasal ostertagiosis of sheep. Information on haemonchosis 0
0
mucosa; developmental stages of 0. ostertagi in a dilated in sheep is presented in ► Table 10.8. H. contortus ·u5
fundus gland (Photo: IPZ). can cause significant blood losses which may be lethal,
co
especially in heavily infected young lambs. Cl..
 Part Ill. Parasites and parasitoses: metazoa
Figure 10.35. Ostertagiosis in cattle: marked inflammatory
alterations in fundus gland, abandoned by the parasite, and
in submucosa of the abomasum (Photo: IPZ).
• Alterations in the small intestine. Tricho­
strongyles cause subacute to chronic catarrhal
inflammation of the small intestine with slightly swollen,
spotty or diffuse erythematous mucosa, which may
also show little bleeds and tissue defects, especially in
infections with Cooperia or Nematodirus. Histological
changes includedestruction of surface epithelia at the tips
of villi, shortening of villi, degeneration of villus stroma
and cellular infiltrations as well as hyperaemia and
oedema of the propria and partially of the submucosa.
Developmental stages of C. curticei and C. p1mctata
are sometimes enclosed in mucosal nodules. A special
feature of N. battus infections is that already juvenile
stages during the prepatent period may cause illness and
death in young lambs. Alterations in the gastrointestinal
tract are partially due to immunopathological reactions
and result in pathophysiological disturbances, which are
summarised in ► Table I 0.8.
Immunology. Various breeds of sheep and cattle differ
in their defence reactions against parasites, due to their
specific genetic constitution. Based on the heritability
of resistance factors, attempts are made to breed
populations with higher resistance to trichostrongyles
(e.g. sheep with increased resistance to H. contortus or
T. colubriformis).
Generally, naturaUy acq uired immunity of ruminants
against trichostrongyles is only partially effective; it can
Q)
protect against disease and may reduce egg production
·u
C
'6 of the nematodes, but cannot fully control the worm
�
Q)
burden. If immune animals are re-infected, the immune
c
co
responses can have the following effects on the worm
C population: (a) reduced percentage of established larval
·;::
stages, (b) increasing proportion of inhibited stages,
(c) reduced growth of nematodes, (d) decreased egg
_i; production of females, (e) elimination of the existing
>, worm burden (mainly adults) and (f) persistence of a
-
CJ)
0 portion of the nematode population.
0
·en
In all trichostrongylid species (and Nematodirus)
co
0.. development and degree of immunity depend on
Figure 10.36. Ostertagiosis in cattle: abomasal mucosa of a
heifer with severe Ostertsgis infection (left), compared with a
normal mucosa (right) (Photo: IPZ).
intensity and duration of the infection, on age as well
as the genetic and general constitution of the host
animals. A consistent finding is that immune reactions
to most of the gastro-intestinal nematodes in various
host species are accompanied by a strong Th 2 response
with interleukin (IL)-4 and IL-13 as key cytokines.
Multiple potential effector responses are stimulated,
such as the infiltration of the mucosa with mast cells
(mastocytosis), intestinal goblet cell hyperplasia, higher
turnover of intestinal epithelial cells, increased mucin
production, eosinophilia, and elevated levels of specific
IgE antibodies. However, it should be noted that various
trichostrongylid species can trigger specific immune
responses, differing in important details within a very
complex regulatory network (see below). The potential
role of antibodies in protective immunity against
gastrointestinal nematodes is still unclear.
• Ostertagiosis and cooperiosis in cattle. Na'ive
young cattle show an early immunological response after
the emergence of adult worms from gastric glands. as
indicated by significant upregulation of Th I and Th2
cytokines (ILs 4, 10, 13, 18, IFN-y). However, in calves
- naturally infected during their first grazing season
- protective immunity against 0. ostertagi develops
slowly if there is sufficient antigen supply (ingestion
of L3). Beginning with their second gazing season.
animals arc usually protected against clinical disease, but
immunity provides only partial protection. Therefore.
older cattle (e.g. dairy cows) can be infected for long
periods, harbouring populations of adult and immature
stages of Ostertagia that are able lo evade the immune
responses of the host (immune evasion, ► p. 37). An
indication of effective immune defence is the partial
elimination of the adult worm population shortly after
the prepatent period (life cycle, see above).
In contrast to 0. ostertagi, immunity against C. onco plwra
develops quite rapidly within 8- JO weeks; it leads to
decreased burdens of adult nematodes, reduction of
egg excretion and to increased proportions of inhibited
L4. In calves experimentally immunised with L3 of 0.
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)

Table 10.8. Trichostrongylidosis in ruminants: selected pathophysiological features.1

Secretory disturbances of the abomaaum (Infections with o.twta,ta, �la, HHmonchu• and T. ual)
Reduced HCI secretion:
_, elevation of pH - lower activation of pepsinogen to pepsin ..... reduced denaturation of proteins·
_, colonisation of the abomasum with gram-positive and gram-negative bacteria cu
I.::'. increased gastrin s�retion :Q
>-,
Etiology: excretory/secretory products of adult trlchostrongytids inhibit HCl-seoretion of parietal cells (documented for 0. Ol
e
/eptospicularis and 0. oster1ag1); possibly also biogenic amines and prostagfandlns, produced by Infected hosts, could C
have an inhibitory effect; destruction of parietal cells, associated With massive Inflammatory lesions of the mucosa, may
-
U)
,----
- HCI secretion
contribute to reduced
Elevated gastrin secretion:
� hypergastrinaemia � Inhibited motility of the fOrestomaoh system ..... lnappetence'
Etiology: already at a slight reduction of HCl-productlon, socrefion of gastrln lncroosos. Gastrln slimulates acid production
of parietal cells and pepslnogen secretion of chief cells: fur1horrnore, gostr1n CM Influence gastrolnteslinal motility,
absorplion and epithelial proliferation

-
Elevated pepslnogen secretion:
_, hyperpepsinogenaemla -
I Etiology: parasite products· and gaslrln stimulate chief cells to Increased secretion of pepslnogen. Pepsinogen is
not activated in the abomasal lumen and passes through the mucosa to the blood clrculalion. Mucosa permeability Is
increased, probably due to the activity of mediators of lnflammalion. Inflammatory factors are upregulated In O. ostertagl
infections of cattle
Blood loss (In haemonchosla)

-+ Loss of haemoglobin and plasma protein into the gastrointestinal tract ..... anaemia, impairment of protein metabolism, energy
production and otl1er functions
Etiology: blood losses due to blood-feeding by l4, pre-adult and adult stages of H. contor1us and leaking of blood due
to mucosal lesions. Blood loss per worm per day approximately 0.05 ml; in haemonchosis of sheep with worm burdens of
>1000-2,000 per animal: daily blood loss >50-100 ml
Protein loss (In abomasal and Intestinal trlchostrongylld Infections)

Leakage of serum proteins (especially albumin) into gastrointestinal tract, and increased gastrointestinal epithelial turnover:
-+ hypoalbuminaemia
-+ reduced oncotic pressure of blood ..... oedema formation in various tissues (wall of abomasum, subcutis, intermandibular
space)
-, increased albumin synthesis in liver - later on mobilisation of protein from musculature - emaciation, reduced utilisation of
protein for growth and production of meat, milk and wool
-, alternativeutilisatio� of protein for energy generation - ----- -·-
Etiology: leakage of plasma protein, mainly albumin, through damaged abomasal and intestinal mucosa; in spite of partial
reabsorption of protein a net loss occurs, enhanced In heavy Infections by Increased loss of gastrointestinal epithelia
1-+: consequences; ': evidence, but not yet confirmed.

ostertagi or C. oncophora and subsequently exposed to ingested larvae settle in the abomasum. The self-cure
a homologous challenge infection, the worm burden phenomenon is regarded as an allergic reaction of
of Cooperia was reduced by more than 90% and of the abomasal mucosa, mainly triggered by excretory/
Ostertagia only by 20% - an indication of different secretory antigens released by Haemonchus larvae. Other
immune reactions against these two species. manifestations of immunity include the reduction of
the total worm burden, decreased egg excretion and
Q)
• Haemonchosis in sheep. Lambs and kids achieve the increased proportions of inhibited L4, as well as C
·u
adequate immune competence against H. contortus the above-described spring-rise phenomenon, which is uQ)
only at an age of about 6 months. In the time before, due to weakening of the ewes' immune system and the �
ingested larvae can establish largely unhindered in the associated reactivation of hyp obiotic larvae. �
abomasum and can lead at critical infection intensity, (1j
C
to disease and death. Immunocompetent sheep are • Trichostrongylosis in sheep. In lambs born ·c
Q)
capable of eliminating an existing adult population of in spring, immunity to T. colubriformis develops j
H. contortus rapidly after ingesting a larger amount over a course of 5-9 months, which leads to reduced C
of L3 of the same species, thus achieving protection. establishment of ingested larvae, elimination of adult >,
Ol
This reaction is referred to as 'self-cure'. Usually, only a stages and reduced egg excretion. 0
few ingested larvae succeed in establishing themselves 2
·u5
in the abomasum (self-cure and protection), but it is • Nematodirosis in cattle and sheep. Under
cu
also possible that a significant proportion of newly sufficient antigen supply, immunity in calves and sheep a..
Part Ill. Parasites and parasitoses: metazoa
is already expressed 2-3 months after primary infection,
causing a reduction in egg shedding and elimination of
adult and immature stages. Usually, such animals are
well protected against the effects of heavy Nematodirus
infections. In contrast, immunologically na'ive lambs are
highly endangered, especially by N. battus infections
in spring.
Vaccination. A vaccine against H. co11tortus in sheep,
based on partly purified native antigen, has recently
been marketed in Australia. Because this vaccine
contains 'hidden antigens' (membrane glycoprotcins
from the intestine of H. co11tort11s), the immunological
host response is not boosted by natural infections.
Therefore, repeated immunisations arc required to
achieve sufficient protection. Current research nlso deals
with the development of vaccines against Ostertaglo and
Cooperin infections in cattle (more ► p. 569).
Clinical signs. Trlchostrongylldosis In ruminants
is primarily II disease in young animals which occurs
mainly in the second hnlf of the grazing season. The
course of disease is mostly chronic rarely subacute or
acute. Common symptoms include inappetence, watery
diarrhoea without fever, poor weight gain and impaired
productivity (meat, wool, milk), in more severe cases
anorexia, emaciation, dehydration, hypoalbuminaemia
and oedema. If left untreated, the disease can be fatal
( ► Figure I 0.37). Information on ostertagiosis in cattle
is presented in ► Table 10.9. The most common form
is ostcrtagiosis type I.
In haemonchosis of sheep and goats, there is often no
diarrhoea, faeces arc rather hard and dark. In addition,
the animals show signs of progressive, chronic anaemia
and hypoalbuminacmla(general weakness, pale mucous
membranes, slight jaundice, low hacmatocrit values
and erythrocyte counts, subcutaneous oedemn, e.g.
lntcrmandlbular oedema, so-called bottle jaw). Lambs
may be already affected curly in the gruzlng season
(first half of July) by ncute or subncutc disease with fotal
outcome. Hocmonchosls In ewes ls a rclntlvcly common
form of the disease, which usually occurs after lambing.
Figure 10.37. Helfer after Its first grazing period with signs of
winter osteneglosls In spring (Photo: IPZ).
Clinically significant N. battus infections occur in lambs
(not in older sheep) and occasionally in calves a few
weeks after beginning of the grazing period and may
be fatal in lambs within a few days after appearance of
the first clinical signs. Severe Nematodirus infections
(mostly N. helvctianus) have been described in calves
as a cause of diarrhoea in the 2nd or 3rd months of the
grazing period.
Diagnosis. The intravital diagnosis of tricho­
strongylidosis is based on the epidemiological history
(e.g. grazing history), clinical symptoms and laboratory
clntn (examples ► Table I 0.9). Detection of eggs of
trichostrongyles or Nematodirus in faeces (flotation
technique) indicates an infection of host animals, but
the number of eggs per gram of faeces (EpG) does
nol necessarily correlate with infection intensity or
clinical condition. For example, high egg counts in
lambs or calves of the first grazing season are likely due
10 high worm burdens, but high burdens of pathogenic
immature stages (e.g. of H. contortus, N. battus) can be
associated with low or even no egg shedding. Because
eggs of different trichostrongylid species are very
similar, they cannot be reliably differentiated; only
the typical eggs of Ncmatodirus spp. can be identified
( ► Figure 16.8, p. 539). However, a genus diagnosis
of trichostrongyles is possible by identification of
free-living L3, obtained from copro-culture (► p.
532). Egg counts are valuable for the identification
of animals which arc predominantly responsible for
pasture contamination with eggs, and for efficacy
evaluation of anthelmintics against sensitive and
drug-resistant nematodes under field conditions(► p.
563). Furthermore, egg counts in combination with
differential counts of L3 are important methods for
studies on the course of infections in groups of animals.
In unclear clinical cases, further laboratory tests can
provide additional information, namely hacmatocrit
vnlucs and erythrocyte counts in suspected cases
of haemonchosis in small ruminants, and serum
pepslnogcn vnlues In trichostrongylidosis of the
nbomnsum, especinlly In ostcrtagiosls In cnttle (serum
pepslnogcn concentrations are Indirect indicators for
the degrt•e of damngc of the abQmasal mucosa). For
estimating the degree of anaemia in hnemonchosis
In sheep, the so-called FAMACHA• system wns
developed In South Africa. By means of a scale,
colours of conjunctiva can be classified from normal
pink to pale. With this method, 70-80% of sheep with
significant anaemia are detected, but specificity is low.
The application of this method is only useful in !locks
and regions where /-I. co11tort11s prevails.
Detection of specific antibodies ngninst 0. ostcrtagi
In serum and bulk milk samples has been used in
cow herds 10 eslimnlc the impiH.:t of worm burdens
on milk produi:tion und reproductive perfornrnnce. In
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)

Table 10.9. Ostertagiosis type I and type II in cattle.1

Ostertaglosls type I •summer ostertaglosls' Ostertaglotls type II 'winter ostertaglosls'

1-Seas_ _o_n __ ____ -; July until end� g�ing _s_e_aso

_ n
_ _____ -+-Janua ry u!2_ti l MaL _________ __,
An imal group - young animals during their first grazing period young animals after their first grazing period,
rarely cattle after several grazing periods _
Morbidity high. majority or all young animals of a herd usually only a few animals affected
more or less affected. older cattle usually
1--- --- - -- + without clinical signs ------ -
--
1-
M_or_ t_al�
ity�-- ----- _�YI� �igh in some years
-
low _ I _ _
-- - -
Lethality mostly low -- - �--- ---(titg_h ___ ____ _ ____ __ _ ___,
Clinical signs2
lnappetence + +
Diarrhoea + (profuse, without blood)
+ (profuse, occasionally intermittent)
Weight los_s _ __ _ _ a_n_d _ m_ar ked)'--- - -----1
+�(r_ a�pid
_-+-_+ __ _______ ________
-
�cc_o_si _s _ __ _ ___+__ _ ___ __ + (rare)__ -
_ __ _ ..:!' (approximately 40% of clinical case_s_,_
) - --i
Fever -
Anaemi_a _____ (ln some cases)
-+--------------------1--+...:.
__ _ _ _
Serum pepslnogen elevated mostly elevate_ d _____-
____ ___ -1
Serum albumin in severe cases decreased mostly decreased
Parasitology
Egg detection in faeces positive positive or negative
EpG low up to >1000 very low to high
Worm burden in predom inantly adults of 0. ostertagi (often in heavy infections up to >100,000 specimens
abomasum >40,000 specimens/animal) with high proportion(30-80%) of hypobiotic and
other immature stages
Pathology abomasum: typ ical nodules, inflamed mucosa, like in type I, usually less nodules, but marked
oedema of abomasal folds, pH elevated in oedema, pH often elevated(>3)
severe cases (>3)
Therapy broad-spectrum anthelmlntics effective only certain broad-spectrum anthelmintics
effective against hypobiot ic stages(► Table
19.2, p, 579)
1 Modified after Armour et al. (1973) Bovine ostertagiasls. In: Urquhart GM, Armour J (eds.) Helminth diseases of cattle, sheep and horses
in Europe. Glasgow, UK: Robert Maclehose Comp.. pp. 11-22; ISBN O 9502034 59.
2 + : usually present, : usually absent.
-
Remark: regularly, C. oncophora und some other species are involved in the infection, but detrimental effects caused by 0. ostertagi
predomi nate.

epidemiological studies, serological antibody detection
has proven to be useful.
The post mortem diagnosis of trichostrongylidosis is
based on identification of pathological lesions, detection
of parasites and quantitative assessment of the worm
burden. Macroscopically, only H. contortus is easily
(► Figure 16 .11, p. 542, ► Figure 16.12, p. 543). More
difficult is the identification of females and immature
stages.
Therapy. For the treatment of trichostrongylidosis
in diseased ruminants and for metaphylaxis, highly
Q)
effective and well-tolerated anthelmintics of different C

chemical classes are available: (pro)benzimidazoles (e.g. ·c3

detectable, but not the smaller species of other genera
(Ostertagia, Trichostrongylus, Cooperia, Nematodirus). albendazole, fenbendazole, mebendazole, oxfendazole), �
Q)

Therefore, a washing procedure has to be used, which imidazothiazoles (levamisole), macrocyclic lactones (e.g. 2:-
also allows the infection intensity to be estimated. For ivermectin, doramectin, eprinomectin, moxidectin), cu
C
·.:::::
reliable detection of hypobiotic stages in the mucosa (e.g. amino-acetonitrile derivatives (AAD) (monepantel), Q)

ostertagiosis in cattle), a special technique for recovering and spiroindoles (derquantel) ( ► Table 17.4, p. 561;
living parasites or a digestion technique is required ► Table 19.2, p. 579; ► Table 19.6, p. 585). Most of these C
(► p. 533). anthelmintics are effective against adult and immature >,
Ol
stages of trichostrongyles (some of them also against 0

Morphological identification of trichostrongylid and other nematode species and certain ectoparasites), but ·u5
Nematodirus species is relatively easy, based on typical there are differences in the degree of efficacy. Only
features of males (bursa, spicules, gubernaculum, etc.) some anthelmintics are sufficiently effective against cu
CL
Part Ill. Parasites and parasitoses: metazoa
hypobiotic stages of 0. ostertagi in cattle. When choosing
suitable anthelmintics, the potential or proven presence
of drug-resistant parasite strains has to be considered
(► p. 564). Furthermore, safety indices and mandatory
withdrawal periods for edible tissues and milk always
have to be observed.
Macrocyclic lactones are slowly eliminated from the
animal body, so that residues of the drugs persist for
some time in concentrations which can prevent the
establishment of subsequent infections. The duration
of this residual effect, which is dependent on the drug,
dosage and mode of administration, can be used in
control programmes. For example, the residual effect of
a therapeutic dose of ivermectin (s.c. application) against
0. ostertagi and C. oncopl10m lasts I week, eprinomcctin
(pour on) up to 4 weeks, doramectin (pour on) 4-5
weeks, and moxidectin (pour on) 5 weeks.
Control. In temperate Europe, control strategies
against trichostrongylids of ruminants are principally
based on the epidemiological fact that the greatest
infection risk exists in the second half of the grazing
period(see epidemiology, above). The aim of strategic
control measures is to influence the parasite populations
to an extent that disease and performance-impairing
infection are avoided but development of host immunity
is not disturbed. The following measures are available:
(a) pasture management, (b) strategic treatments
(application of anthelmintics at epidemiologically
meaningful times) and (c) a combination of these
measures (= integrated control). In recent years,
the targeted selective treatment (TST) has been
proposed as a further option. As opposed to the
usual administration of anthelmintics to all animals
of a herd or age group, TSTs include only animals
of epidemiological relevance, i.e. animals with high
egg shedding. The primary objective of this concept
is to reduce the risk of development of anthelmintic
resistance by reducing the selection pressure on the
worm population. These options arc chosen and
applied according to the type of farming nnd farm
structure. In organic farms, special guidelines for the
use of antiparasitic drugs have to be observed. More
information on the control of trichostrongylldosis In
cattle and small ruminants can be found on ► p. 576.
Trichostrongylids of wild ruminants
Roe deer, red deer, fallow deer, mouflon, chamois
and ibex are hosts of some species which also occur
in domestic ruminants, but in addition they harbour
species that are found predominantly or exclusively
in wild ruminants. The latter include 0stertagia
leptospicularis and various species of the genera
Spiculopteragia, Apteragia and Rinadia. In general,
wild ruminants play no or only a minor role in the
contamination of pastures of domestic animals with
eggs of gastrointestinal nematodes. Wild ruminants can
be severely affected by infections with trichostrongylids
alone or in combination with other factors (malnutrition,
other diseases), especially when kept in small habitats
(e.g. enclosures). In such situations, chemotherapeutic
and prophylactic measures may be indicated.
Trichostrongylids of equines and other
animal species
In horses and other equines Trichostrongylus axei
parasitises in the stomach. Significant infections occur
only on horse pastures that are contaminated to a
considerable degree with eggs of this species originating
from ruminants. Parasite transmission within a horse
population is possible, but plays a minor role. Prevalences
of ·r. axci in horses vary from < I to >50%. The life cycle
corresponds to that in ruminants; the prepatent period
in the horse is about 3 weeks. Significant infections
may cause chronic catarrhal gastritis and proliferative
inflammation with local erosions and necrotic foci,
associated with clinical signs (inappetence, diarrhoea,
emaciation). Diagnosis is made by egg detection in
faeces, combined with differentiation of L3. Adult
parasites can be detected in freshly drawn stomach
contents. Effective anthelmintics for therapy are avaiJable
( ► Table 19.10, p. 592).
Domestic pig and wild boar are hosts for Hyostrongylus
rubidus, the worldwide distributed 'red stomach worm'
(males 4-7 mm, females 5-11 mm long, reddish colour).
The direct life cycle includes the following phases: after
ingestion of infectious L3, parasitic stages colonise the
lumina of gastric glands (mostly fundic region), where
they pass through the development to 5th stages; the
adults live on the mucosa I surface. The prepatent period
is 16-22 days. Hypobiosis as L4 occurs especially in
older animals with peripartal reactivation of these stages
and subsequently increased egg shedding. Infections
occur in housed animals, but they are more frequent and
significant in free-ranging pigs. The animals can become
Infected from spring to autumn, with an Increased
Infection risk from July to October(= main infection
period). In the case of destruction of the vegetation In
outdoor pens by rooting of the pigs, the infection risk is
reduced. Prevalences of H. rubidus depend on the type of
husbandry, as shown by data from DE: in breeding sow
farms with pasture utilisation 26% of the animals were
infected, but only about I% in farms with predominant
indoor maintenance. High prevalences and infection
intensities were observed in sows in open pens with
straw bedding. The adult parasites are blood-feeders and
cause chronic catarrhalic and partly ulcerative gastritis
in heavy infections. Clinical signs, such as diarrhoea,
emaciation, anaemia, decreased milk yield and fertility
disorders occur predominantly in sows. The eggs of H.
rubidus and 0esophagostomwn spp. are very similar.
Differential diagnosis is possible by identifying the L3.
Effective anthelmintics against H. rubidus are listed in
*
I 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)
► Table 19.8, p. 589, and control options are described
on► p. 587.
Domestic rabbits are rarely, but wild rabbits and hares
frequently infected with trichostrongyles, namely
with the stomach parasites Graphidium strigosum
and Obeliscoides cuniculi, and with Trichostrongylus
retortaeformis, a parasite of the small intestine.
Pathological lesions caused by these species are similar
to that in the abomasum or small intestine, respectively,
in ruminants.
Different species of poultry (chicken, turkey, dove,
goose, duck) and wild birds (pheasant, partridge, grouse,
quail species, etc.) are hosts of Trichostro11gylus tenuis.
This species lives in caeca and the distal part of the small
intestine, develops in a direct cycle and causes only rarely
severe infections with clinical signs (fluid and partly
bloody faeces, weakness, anaemia, etc.).
Zoonotic importance. Trichostrongyles of ruminants
are transmittable to humans. Such cases are very rare
in Europe; they occur more frequently in other areas
(e.g. southern Asia, Africa, South America) with
local prevalences up to 60%. Mainly Trichostrongylus
species have been identified as pathogenic agents,
rarely H. contortus, Ostertagia spp. and Marshallagia
marshalli. Risk factors for humans include the use of
animal manure as fertiliser in vegetable cultivation
and collection or preparation of dung of ruminants
as fuel. The infections are usually asymptomatic, but
occasionally cause gastrointestinal disturbances.
• Selected references L...:=::::::::::::::::==:::1
Bassetto CC, Picharlllo ME, Newlands GF, Smith WO,
Fernandes S, Slqueira ER, Amarante AF (2014) Attempts
to vaccinate ewes and their lambs against natural Infection
with Haemonchus contortus in a tropical environment. Int J
Parasitol 44: 1049-1054.
Bennema SC, Vercruysse J, Morgan E, Stafford K, H6glund
J, Demeler J, von Samson-Himmelstjerna G, Charller
J (2010) Epidemiology and risk factors for exposure to
gastrointestinal nematodes in dairy herds in northwestern
Europe. Vet Parasitol 173: 24 7-254.
Besler RB (2012) Refugia-based strategies for sustainable worm
control: Factors affecting the acceptability to sheep and goat
owners. Vet Parasitol 186: 2-9.
Charlier J, Duchateau L, Claerbout E, Vercuysse J (2007)
Predicting milk-production responses after an autumn
treatment of pastured dairy cattle with eprinomectin. Vet
Parasitol 143: 322-328.
Charlier J, Hoglund J, von Samson-Himmelstjerna G, Dorny
P, Vercruysse J (2009) Gastrointestinal nematode infections
in adult dairy cattle: impact on production, diagnosis and
control. Vet Parasitol 164: 70-79.
Charller J, Demeler J, H6glund J, von Samson­
Himmelstjerna G, Dorny P, Vercruysse J (201O)
Ostertagia ostertagi in first-season grazing cattle in Belgium,
Germany and Sweden: general levels of Infection and related
management practices. Vet Parasltol 171: 91-98.
Claerebout E, Vercruysse J (2000) The immune response and
the evaluation of acquired immunity against gastrointestinal
nematodes in cattle: a review. Parasitology 120 (Suppl.): 25-42.
Delafosse A (2013) The association between Ostertagia ostertagi
antibodies in bulk tank milk samples and parameters linked to
cattle reproduction and mortality. Vet Parasitol 197: 212-220.
GasHr RB, Newton SE (2000) Genomic and genetic research
on bursate nematodes: significance, implications and
prospects. In! J Parasltol 30: 509-534.
Grencls R, Harnett W (2011) Survival of animal-parasitic
nematodes Inside the animal host. In: Perry RN, Wharton
DA (eds.) Molecular and physiological basis of nematode
survival. Wallingford, UK: CASI International, pp. 66-85.
ISBN 978-1-84593-687-7.
Hertzberg H, Huwyler U, Kohler L, Rehbein S, Wanner M
(2002) Kinetics of exsheathment of Infective ovine and bovine
strongylid larvae in vivo and in vitro. Parasitology 125: 65-70.
Knox MR, Besler RB, Le Jambre LF, Kaplan RM, Torres­
Acosta JF, Miller J, Sutherland I (2012) Novel approaches
for the control of helminth parasites of livestock VI: Summary
of discussions and conclusions. Vet Parasitol 186: 143-149.
Lattes S, Ferte H, Delaunay P, Depaquit J, Vassallo M, Vittier
M, Kokcha S, Coulibaly E, Marty P (2011) Trichostrongylus
colubriformis nematode infections in humans, France. Emerg
Infect Dis 17: 1301-1302.
Mlhi B, Van Meulder F, Rinaldi M, van Coppernolle S, Chiers
K, Van den Broeck W, Goddeeris B, Vercruysse J,
Claerebout E, Geldhof P (2013) Analysis of cell hyperplasia
and parietal cell dysfunction induced by Ostertagia ostertagi
Infection. Vet Res 44: 121 .
Mihl B, Van Meulder F, Vancoppernolle S, Rinaldi M, Chiers
K, Van den Broeck W, Goddeerls BM, Vercruysse J,
Claerebout E, Geldhof P (2014) Analysis of the mucosa!
Immune responses Induced by single and trickle infections
with the bovine abomasal nematode Ostertagia ostertagi.
Parasite lmmunol 36(4): 150-156.
Roeber F, Jex AR, Campbell AJ, Campbell BE, Anderson GA,
Gasser RB. 2011Evaluation and application of a molecular
method to assess the composition of strongylid nematode
populations in sheep with naturally acquired infections. Infect
Genet Evol; 11: 849-854.
Roepstorff A, Murrell KO (1997) Transmission dynamics
of helminth parasites of pigs on continuous pasture:
Oesophagostomum dentatum and Hyostrongylus rubidus.
Int J Parasitol 27: 553-562.
Smith WO, Van Wyk JA, Van Strijp MF (2001) Preliminary
observations on the potential of gut membrane proteins
of Haemonchus contortus as candidate vaccine antigens
in sheep on naturally infected pasture. Vet Parasitol 98:
285-297.
Trapani F, Paciello 0, Papparella S, Rinaldi L, Cringoli G,
Maiolino P (2013) Histopathological, histochemical and
immunohistochemical findings of the small intestine in goats
naturally infected by Trichostrongylus colubriformis. Vet
Parasitol 191: 390-393.
 Part Ill. Parasites and parasitoses: metazoa
Family Molineidae
The genus Nematodirus, belonging to this family,
is already discussed i n the previous chapter on
trichostrongyles ( ► p. 287). Moreover, 0llulanus
tricuspis is of practical importance, especially as a
stomach parasite of cats.
Genus 01/ulanus
Disease: Ollulanosis in cats and 0ther hosts.
0llula (L): diminutive of olla: pot; tri (G, L): three; cuspis
(L): point, sting. The species name refers to the pointed
posterior end of the female.
Summary
• Agent, life cycle and occurrence. 01/ulanus trlcuspls
is a tiny stomach parasite of fellds (domestic and
wild cat, lion, tiger), dogs , foxes and pigs. Life cycle
'.• unusual: females release larvae that can develop Into
mature stages In the stomach. Parasites are vomited
end ingested by a new host. In Europe, falrty common
parasite in cats, but recent data are scarce.
• Cllnlcal algns, diagnosis and therapy. Chronic
catarrhal gastritis. Detection of parasites In vomit or
gastric w ashings (not in faecesl). Therap y: off-label
treatment with fenbendazole.
Agent and life cycle. 01/ulanus tricuspis (syn. 0. suis,
0. skrjabini): Anterior end usually coiled in a spiral,
small, cup-like buccal capsule. Males: 0.7-0.8 mm long
with distinct bursa copulatrix and two spicules (46-
57 µm); females: 0.8-l.O mm, the tail ending in three
(sometimes more) conical tips ( ► Figure 10.38). In cats
and other hosts 0. tricuspis lives on the gastric mucosa
under a layer of mucus, mainly in the fundic region.
Sexually mature females contain eggs with a morula or
an embryo and also larvae that are excreted as infective
L3 (perhaps also as L2). Since these larvae are able to
reach sexual maturity within the stomach, the cycle
can be completed endogenously, resulting in increasing
parasite numbers. The prepatent period after primary
infection is 33-37 days. The infection is transmitted t.o
other hosts by vomiting of larval and adult stages and
the ingestion of the vomit by a new host. The parasites
can survive outside the host for up to 15 days.
Occurrence and epidemiology. 0. tricuspis is a
stomach parasite of domestic and wild cats and other
felids (lion, tiger, cheetah in zoos) as well as dogs, foxes
and pigs. It occurs in many European countries and
elsewhere (including North and South America, RU,
Egypt, TR, AU and New Zealand). Prevalence in free­
ranging cats in DE 12-40% and in stray cats in PT 31%;
prevalence in foxes: 7% in DE (Berlin), about 2% in
Ovary
Oesophagus
Intestine
Uterus with
eggs
��----Larva
Posterior end
with 3 tips
Figure 10.38. 01/ulanus trlcuspls, female (Graphics: IPZ, A.
Seeger; after various templates).
AT. Infection intensities vary between a few parasites
to more than 10,000 specimens per cat. 0. tricuspis has
been recorded in pigs in RU, but there are no further
reports. Usually, the parasite is transmitted from cat to
cat or from pig to pig, but transmission from pigs to cats
and vice versa has also been described.
Pathogenesis and clinical signs. The parasites
can cause chronic, catarrhal gastritis with increased
mucus production, epithelial hyperplasia, erosions,
cellular infiltrations and sclerotisation of the gastric
mucosa, ulcerative oesophagitis and possibly also
adenocarcinoma. Clinical signs are anorexia, weight loss,
recurrent vomiting, and rarely diarrhoea. Significant
changes in the gastric mucosa and corresponding clinical
symptoms have also been observed in pigs.
Diagnosis. lntravilal diagnosis in cats by examining
spontaneous or induced vomit (after application of
Rompun• 2%, 0.1 ml/kg b.w.) or of stomach content,
obtained by gastric washings or endoscopy (detection
rate 70%-98%). Coproscopic examination Is unsuitable.
Post mortem diagnosis: Microscopic examination of
smears of the gastric mucosa (fundic region), or of the
sediment of gastric mucus (previously treated with JO%
potassium hydroxide solution and centrifuged), or of
sediment of artificially digested stomach mucosa.
Therapy and control. In cats, levamisole (Ix 5
mg/kg b.w. s.c.), oxfendazole in high doses ( JO mg/
kg b.w. p.o., 2x daily for 5 d) and fenbendazole (20-
50 rng/kg/d for 3 days p.o.) have been reported to be
effective (caution: side effects of levamisole: vomiting,
salivation, restlessness, tremor, etc.). Effective prevention
measures are not known.
+"
10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)
Selected references
Bowman DD, Hendrix CM, Lindsay DS, Barr SC (2002) Feline
clinical parasitology. Ames, IA, USA: Iowa State University
Press; ISBN 0-8138-0333-0.
Cecchi R, Wills SJ, Dean R, Pearson GR (2006) Demonstration
of 01/ulanus tricuspis in the stomach of domestic cats by
biopsy. J Comp Pathol 134: 374-377.
Dennis MM, Bennett N, Ehrhart EJ (2006) Gastric
adenocarcinoma and chronic gastritis in two related Persian
cats. Vet Pathol 43: 358-362.
Schuster R, Kaufmann A, Hering S (1997) Untersuchungen
zur Endoparasitenfauna der Hauskatze in Oslbrandenburg.
Bert Munch Tierarztl Wochenschr 11 0: 48-50.
Waap H, Gomes J, Nunes T (2013) Parasite communities In
stray cat populations from Lisbon, Portugal. J Helminthol
30: 1-7.
Families Amidostomatidae and
Ornithostrongylidae
Various genera and species of the family Amidostomatidae
are gizzard parasites of birds, especially of geese,
swans and ducks, including Amidostomum anseris,
Amidostomum acutum, Epomidiostomum uncinatum
and some other species.
Genus Amidostomum
Disease: Amidostomosis,
Agent, life cycle and occurrence. A. anseris
is described here as an example: reddish-yellowish
nematodes with fairly well developed, conical buccal
capsule, with three pointed teeth at its base. Males
10-17 mm, females 12-24 mm long. Eggs with thin
to medium-thick shell, broad-elliptic with rounded
poles, 80-110xS0-82 µm, containing many blastomeres.
Occurrence: Europe, North and South America, Africa,
Asia.
A. anseris lives under the keratin layer in the gizzard of
Anseriformes. Development: egg shedding in faeces -
development to ensheathed L3 in the egg - hatching of
L3 and migration to grass - ingestion by a new host.
The larvae can float in water and percutaneously infect
goslings. Thereafter, direct colonisation of the gizzard
or after blood-lung migration. Further development
in gastric glands and definitive establishment between
keratin layer and mucosa. Prepatent period in goslings
15-18 days, in older animals up to 33 days. Older animals
are often asymptomatic parasite carriers and sources of
infection for young animals.
Pathogenesis and clinical signs. The blood-sucking
adult stages of Amidostomum and Epomidiostomum
damage the keratin layer and cause inflammatory
alterations of the gizzard wall. Clinical signs occur
predominantly in 3-8 weeks old goslings (anaemia,
plasma protein loss, retarded growth, decreased feed �
intake, diarrhoea, weakness, emaciation, death). :g
>,
0)
e
C
Diagnosis, treatment and control. fntravital
diagnosis by coproscopic detection of eggs u5
(flotation technique). Differential diagnosis: eggs of
Tric/rostro11gylus tenuis. Post mortem detection of
nematodes at necropsy. Plubendazole ( ► p. 611) is
effective against Amidostomatidae. Preventive treatment
of older geese is recommended. Litter in stables must
be kept dry and should be changed frequently. Narrow
and damp outdoor pens should be avoided, as they may
be significant infection sources.
Genus Ornithostrongylus
Ornithostrongylus quadriradiatus (family Ornitho­
strongylidae) is a parasite of pigeons and mainly inhabits
the small intestine, but also the crop and proventriculus.
Life cycle direct, infection by ingestion of L3. Prepatent
period 5-6 days.
Selected references
McDougald LR (2013) Internal parasites. In: Swayne DE (ed.)
Diseases of poultry, 13 th ed. Ames, IA, USA: Wiley-Blackwell,
pp. 1117-1146; ISBN 978-0-470-95899-5.
Kavetska KM, Kr6laczyk K, Stapf A, Grzesiak W, Kalisiliska
E, Pilarczyk B (2011) Revision of the species complex
Amidostomum acutum (Lundahl, 1848) (Nematoda:
Amldostomatldae). Parasitol Res 109: 105-117.
Family Dictyocaulidae
Genus Dictyocaulus (large lungworm)
Disease: Dictyocaulosis.
Dictyon (G): net; kaulos (G): arm, shaft.
Summary
Agents. Dictyocau/us spp. are trichostrongylid-like
nematodes up to 1 O cm long, inhabiting the lungs of
ruminants, equics and camelids. Species: D. viviparus
(cattle, other bovids and cervids), D. filaria (sheep, goat,
wild ruminants), D. arnfieldi (donkey, horse}, D. eckerti
and D. capreolus (wild ruminants}, D. cameli (camels).
T
 Part Ill. Parasites and parasitoses: metazoa

&
D/ctyocau/us vlvlparus (cattle lungworm)
• Life cycle. Infected cattle excrete In their faeces
L 1 which develop into L3 in the environment. After
ingestion by a new host, L3 pass from the small
intestine to mesenteric lymph nodes and moult to L4.
These stages migrate in lymph and blood vessels to
the lung; they break through the capillaries into the air
passages where they moult and evolve to maturity.
Females release larvated eggs from which L 1 hatch in Figure 10.39. Dictyocaulus viviparus: adult stages (in this photo
the bronchi and are transported via the trachea to the
up to 7 cm long) (Photo: IPZ).
pharynx; they are swallowed and shed In the hosts'
faeces. Prepatency: approxlmately 3 weeks, patency
usually 1 to 2 months.
• Occurrence, epldemlology. D. vfvlparus occurs world­
wide and is predominantly prevalent In high rainfall
areas of temperate zones, partlcularly In lowlands (e.g.
coastal areas In western and northern Europe) but
also in mountainous regions (e.g. Alpine area). It also
occurs In subtropical and tropical regions, typically
In highland or coastal areas with high precipitation.
In Central Europe, pastures are contaminated at the
beginning of the grazing season with L 1 originating

.
from partly Immune lungworm carriers In their 2nd or
'
later grazing periods In which lungworms have survived
the winter months. Overwintering of low numbers of L3
on pasture la possible In some regions, but Is mostly Figure 10.40. Dlctyocaulus viviparus in bronchi of cattle lung
epldemlologlcally Insignificant. Susce ptible young (Photo: IPZ).
animals usually ac quire lnltlally llght Infections without
developing significant Immunity, followed by shedding
of larvae, continuous new Infections and a gradual long with a strongly refracting ring. Males with short,
build-up of a critical level of pasture contamination rounded bursa copulatrix; bursa lobes unseptated; bursal
with Infective L3. Outbreaks of lungwom, disease may rays characteristic for the genus. Spicules are short,
occur from June until the end of the grazing period In dark-brown; gubernaculum present(► Figure 10.41}.
Central Europe. The vulva is situated almost in the middle of the body.
• Pathogeneela, cllnical algna. Bronchopneumonla,
The ovijector is structured like that in trichostrongyles.
especially In calves of the first grazing season, but
also In older animals Qncludlng cows) with Insufficient
The most important species and their hosts are listed
Immunity. Symptoms (starting already during in ► Table I 0.10. In addition, Dictyocaulus cameli is a
prepatency): dyapnoea, tachypnoea, coughing, noteworthy species in camelids.
breathing through the mouth, fever, nose discharge,
lnappetence, emaciation, and death. The severity of
the disease depends on the Intensity of Infection and
on the Immune status.
• Dlagnotla. Detection of latvae In faeoN and of specific
antibodies In milk or aerum for herd diagnosis.
• Therapy, control. Benzlmldazolea, levamlsole, and
macrocycllc lactonea. Control by oral vaccination
with a Uva vaccine or metaphylaxla with anthefmlntlca
Q.) combined with grazin g management.
C
D. fl/aria and D. amn.ldl see below. Splculum
·0
'6 ---Gubernaculum
Q.)

Several species of the genus Dictyocaulus cause lung

(0
C:
diseases in ruminants, equids, and camelids. D. viviparus
·c is of particular importance as it can cause severe illness
Q.) Bursa copulatrix
in cattle and substantial economic losses.
.£
>,
0)
Agents. Dictyocaulus species are thin, thread-like,
0 whitish, trichostrongylid-like nematodes up to JO cm
.8 long. ( ► Figures 10.39 and I 0.40). Morphological Figure 10.41. Dictyocaulus viviparus: male, posterior end
·u;
characteristics: small buccal capsule, broader than (Graphics: IPZ, A. Seeger; after Kotlan 1960).
(0
+' 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)
Table 10.10. Dictyocaulus species (selection).
Species, length of males(era') and Main hosts
females(��). distribution (D)
Dictyocaulus viviparus cattle, occasionally other
JJ: 35-43, <jl<jl: 50-80 mm bovids and cervids
D:worldwide
Dictyocau/us eckerti roe deer, red deer, fallow
a&: 30-47, <jl<jl: 34-63 mm deer, reindeer
D:Europe, Asia, North America
Dictyocaulus capreolus roe deer, elk
M: 24-62, <jl<jl: 34-81 mm
D:Sweden
Dictyocaulus fi/aria sheep, goat, also
aa: 50-80, <jl<jl: 50-100 mm mouffion, chamois, ibex
D:worldwide
Dictyocaulus amfieldl donkey, horse, mule,
M: 26-43, <jl<jl: 43-60 mm zebra
D:worldwide
Differentiation between the species can be performed
morphologically and by DNA analysis. D. eckerti (syn.
D. noerneri) differs from D. viviparus in the structure
of the buccal capsule and genetically. D. capreolus
was described in 2002 as a distinct species in roe deer
and moose (elk) in Sweden. Dictyocaulus species of
ruminants infect preferentially particular (main) hosts
but they are not strictly host-specific. For example, after
experimental infection, D. viviparus, D. eckerti and D.
ft/aria develop to patency in fallow deer, the latter species
not as good as the others. Fallow deer is more susceptible
to D. viviparus than cattle to D. eckerti. The latter species
does not infect sheep, and D. capreolus is not infective
for cattle (see epidemiology).
Dictyocau/us viviparus (cattle lungworm)
Disease: Dictyocaulosis (lungworm disease In cattle,
husk)
Agent and life cycle. The adult stages of D.
viviparus (► Table 10.10) inhabit larger bronchi and
the trachea (► Figure 10.42). The females release thin­
shelled eggs containing a first stage larva (Ll). Most
larvae hatch immediately after egg release; they are
transported upwards by the tracheal ciliated epithelium,
are swallowed and then excreted in the faeces. Some
larvae may also be expectorated by coughing. L1 in
the faeces develop to sheathed, infectious L3 in a few
days under optimal conditions (-20 °C), but it takes
1-2 weeks at a constant temperature of 8 °C (see also
epidemiology). L3 are washed off the faeces by rain,
are dispersed by mechanical destruction (trampling
down) of dung pats or are carried away by insects (e.g.
bugs). Fungi of the genus Pilobolus play an important
additional role in the dispersion ofL3 on pastures. These
fungi grow on the surface of bovine dung, forming long
Prepatenc:y, length and charactert.Uce of larvae (L1)
oregga
prepatency: 21-25 days
L1 : 316-367 µm. posterior end pointed
prepatency: 24-26 days
L1: 295-357 µm, characteristics as In D. vivlparus
prepatency: unknown
L1:Unknown
prepatency: 26-30 clays
L1: 490·520 µm, anterior end with knob-like protrusion,
Posterior end truncated
prepatency: 5-14 weeks
eggs: 74-96><46•58 µm, with larva; L1: 420-480 µm,
oosterlor end with thorn-like tip
vertical stalks each ending in a balloon-like vesicle with
a sporangium on top. Hydrostatic pressure builds up in
the vesicle which eventually bursts, and the sporangium
is launched at high speed (2-25 m/sec, corresponding
to accelerations of 20,000 to 180,000xg) and may cover
distances of up to 2 m. Lungworm larvae make use of this
discharge mechanism; they climb up on or in the stalks
to the sporangium and are spread with the launched
sporangium. Being away from the faeces, Dictyocaulus
larvae can migrate in a film of moisture to fodder plants,
en
where they usually stay closely above the ground. ..c
L3 are ingested by a new host, they hatch from the
-E
(I)
sheath, invade the intestinal wall (predominantly o f I
the small intestine) and migrate via lymph vessels t o the
mesenteric lymph nodes where they moult to L4 within
3-8 days p.i. These larvae pass through lymph and blood
vessels to the lungs where they arrive after one to two
weeks. The larvae leave tl1e capillaries, penetrate the
alveolar wall and settle in small bronchioli where they
moult to the preadult stage which migrate to the bronchi
and the trachea where they reach sexual maturity. The
prepatent period lasts 21-25 days but may be prolonged
by a hypobiotic phase (see below). The patency usually
takes only 1 to 2 months due to a rapid development of
protective immunity. Typically, the excretion of larvae
in primary infected calves increases significantly during
the first 2 weeks of patency; thereafter it ceases and ends
after 5-6 weeks. Adult worms may persist in the host
for about half a year.
Occurrence. D. viviparus has a worldwide distribution
and is predominantly prevalent in high rainfall areas of
temperate zones, particularly in lowlands (e.g. coastal
areas in western and northern Europe) but also in
mountainous regions (e.g. Alpine area). It also occurs
in subtropical and tropical areas, typically in highlands
or coastal areas with high precipitation. A recent survey
in Germany, comprising 13 of the 16 federal states and
 Part Ill. Parasites and parasitoses: metazoa

Egg with L1

sz
L4/5111 stage
Immature female (above),
male (below)
Larva 1,
unsheathed

- L2 with detached
L3 with cuticle
s1nq1e or double sheath

Figure 10.42. Life cycle of Dictyocaulus viviparus (Graphics: IPZ, S. Ehrat).

20% of all dairy farms, revealed that an average of 17.1% key factors are similar to those of trichostrongylid
of the bulk tank milk samples (n= 19,9 JO) contained infections ( ► p. 290), although some differences must
(1)
C specific antibodies against D. vivipams with a range be considered, particularly concerning the pasture
·u between 0 and 31.2% positive herds. Serological surveys contamination and the immunological effects on the
'5
(1)
� in calves of the first grazing season in the Netherlands course of the infection.
C' and in northern Germany revealed infections in 40%
co of the herds. Lungworm infections in cattle are also • Pasture contamination. The initial pasture
C
·;::
Q) observed in mountainous regions, e.g. in Europe in contamination with lungworm larvae is mediated at
j pre-alpine areas or even on pastures at higher altitudes the beginning of the grazing season by older cattle, which
C (see epidemiology). have been infected with lungworms in the previous year
>­ and remained asymptomatic parasite carriers during
Ol
0 Epidemiology. Dictyocaulosis is a typical disease the winter season, usually because they did not receive
2 of grazing cattle. Indoor infections (in pens or stables anthelmintic treatment at housing. In such animals a few
·c;;
ro aft.er feeding on contaminated green fodder) are rare adult worms may persist, but in the majority of cases
ro
a.. and mostly of minor importance. The epidemiological the parasites survive the winter season as hypobiotic
;s 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)
stages (late 4 th, early 5 th stages), which reach sexual
maturity in spring time and subsequently produce
larvae. (Hypobiosis can be experimentally induced by
keeping L3 at 4-7 °C for several weeks). In accordance
with the relative host speciflcity of the various
Dictyocaulus species (see above), wild ruminants are of
minor importance with regard to past11re contamination
with D. viviparus larvae. In areas with mild and humid
climates (e.g. in Scotland or northern Germany), part of
the larval population on pastures may survive the winter
season, however, studies in UK, Al� CH, and NL have
shown that this is of minor epidemiological importance
compared with the survival of L3 of trichostrongylids.
As in other nematodes, in D. viviparus the time required
for the development of LI into L3 is temperaturc­
dependent, but it is noteworthy that it can take place
even at low temperatures and is surprisingly rapid (at
s °C: 30 days, 10 °C: 12 days, 20 °c: 4 days). L3 of D.
viviparus are very susceptible to dryness and higher
temperatures. For example, in laboratory experiments
about 30% of larvae survived for 8 weeks in wet faeces
at 3-6 °C, but none at 23-25 °C. In dry faeces at 23-25 °C
all larvae died within a week. Freezing {minimum -8 °C}
is lethal for most of the L3 within a few days. Only
few larvae survive storage at 20 °C in anaerobic liquid
manure for 4 weeks, and the majority dies within one
week under mesophilic conditions at 35 °C. D. viviparus
and D. fl/aria larvae are killed within 12 days in silage
at 20 °C.
• Susceptible animals. All age groups of cattle
without protective immunity are susceptible to D.
viviparus. Hence, in endemic areas, predominantly
calves fall ill during their first grazing season; older
animals {including cows) may be severely affected by
dictyocaulosis if they have never acquired an infection
with D. viviparus before and were thus unable to build
up immune protection against the parasite, or if they
were immune but immunity has ceased due to a lack of
natural challenge infections. An exceptional situation
is the reinfection syndrome of cows (see below). The
infection can be introduced into lungworm-free flocks
by asymptomatic lungworm carriers excreting larvae,
e.g. by purchasing cattle or by mixing cattle from
different flocks on community pastures.
• Epidemiological time course. Although pasture
contamination by larvae excreted by infected animals
starts in spring, clinical cases usually appear between
June and the end of the grazing season (late autumn),
with m ost cases between July and September. Infections
at the beginning of the grazing period are generally
weak but they may lead to a high output of larvae as
calves are highly susceptible. Studies have shown that
weak primary infections with approximately 300 L3
may result in the release of approximately 1.5 million
LI per animal in the course of a mean patency period
of 30 days. Pasture contamination results in infections
of other animals of a herd which contribute with a
second lungworm generation to increasing densities of
infective larvae in the environment. By this time or after
development of a third or fourth generation of parasites,
the larval density on pastures may be high enough to
cause clinical disease. The early course of an infection
co
of a herd is often inconspicuous and symptoms may :g
be overlooked. Thus, the false impression of a sudden >­
CJ)
e
C
outbreak of the disease may arise.
if)
Climatic preconditions for outbreaks of dictyocaulosis
are favourable temperatures and sufficient moisture
to nllow the transition of L3 from faecal pats to forage
plants. Such conditions ore typical for humid lowland
areas. However, parasite transmission is also possible
on pre-alpine and high alpine pastures ( I ,800-2,500
m above sea level), but clinical cases are rare, due to
extensive grazing In such areas, mixed grazing of young
and older cattle, and usually low worm burdens. The
risk of morbidity in livestock may fluctuate considerably
from year to year. Particularly hazardous situations may
arise when susceptible animals are suddenly exposed to
high larval densities on pastures, e.g. when calves are
grazed in autumn on pastures which had been previously
contaminated with larvae by young cattle or when cows
are transferred from non-endemic to endemic areas.
Pathogenesis. In primary infections of young cattle
(or non-immune older animals) several phases of the
disease can be distinguished ( ► Table l 0.11 ).
Early signs of dictyocaulosis may occur during
prepatency beginning in the second week p.i. They
are caused by temporary obstructions of bronchioli by
mucus and cellular infiltrates (neutrophils, eosinophils,
macrophages) which may result in alveolar collapse. In
the following time and during patency, the presence of
adult worms in the bronchi is associated with a multitude
of alterations like increased mucus production, loss
of cilia of the bronchial epithelial cells (impaired
expectoration), hyp erplasia and damage to epithelial cells
and their replacement by undifferentiated, cubical type
2 pneumocytes, general inflammation of the bronchial
mucosa, interstitial inflammatory reactions and
proliferation of peribronchial lymph follicles. Aspiration
of eggs and L1 into the alveoles results in pneumonia
with dense inflammatory infiltrations, associated
with sometimes extended interstitial emphysema and
oedemas. Thickening of the alveolar epithelium impairs
the gas exchange. The disease may be complicated by
proliferation of pathogens already present in the lung
(Pasteurella spp., Mycoplasma spp.) or by bacterial
secondary infections, resulting in a catarrhal-purulent
bronchopneumonia of variable severity. The lung may
appear marmorated due to the close proximity of
inflamed, atelectatic and unchanged lobules ( ► Figure
10.43 and 10.44). Overexpansion and bursting of alveoles
may cause extended interstitial emphysemas, sometimes
spreading into the mediastinum or into subpleural
 Part Ill. Parasites and parasitoses: metazoa

Table 10.11. Pathogenesis and clinical signs of dictyocaulosis in cattle (after Urquhart et al. 1973).

Phase and days p.t.

Prepatency
Days 1-7 migration phase of laNae none
Days 8-21 larvae in lungs: haemorrhagia, necrosis of alveolar coughing, increased breathing rate, in heavy
walls, bronchiolitis, bronchitis infections death possible
Patency
Days 21-60 initial and progresslng bronchopneumonla, coughing, increased breathing rate, emaciation,
beginning elimination lungworms due to developing death possible
i'!'___!!lune responses
Postpatenc¥__
__ _
Days 60-90 after elimination of lung Improvement and cure or chronic coughing and
or fibrosis and alveolar unthriftlness, deal QQSSlble

Figure 10.43. D/ctyocaulus vlv/psrus: cattle lung with Figure 10.44. Dlclyocaulus vlvlpsrus: cattle lung, section with
pathological alterations, especially In distal parts of tho lungs opened bronchi (Photo: IPZ).
(Photo: IPZ).

spaces. lmmunopathological mechanisms participat.e A particular, rare type of disease, the re-infection
in these alterations (immunology, see below). syndrome, is observed in older, immune animals which
Q)
have been exposed to a sudden heavy infection. In this
·u
C

'6 During postpatency, i.e. aft.er immune-mediated partial case, many larvae reach the lungs and are eliminated by
Q)
� or complete elimination of the worms, surviving cattle the immune system. Lymphoreticular cells proliferate
c can graduaJly recover. However, symptoms may persist around dead larvae resulting in up to 5 mm large
C'O
C for several weeks since regeneration processes need lymphoid nodules and massive eosinophilic infiltrates
·.::
Q) Lime, especially after heavy infections. Heavily infected in the lung parenchyma. The reaction may be associated
� animals may also develop a chronic disease due to an with temporary coughing and tachypnoea; in affected
-� enhanced proliferation of type 2 pneumocytes causing cows, milk production may decline transiently.
>- a rubber-like consistency of affected parts of the lungs.
0)
0 This condition may predispose the animals to bacterial
0
"ui superinfections.
ro
ro
a.
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)
Immunology. Natural D. viviparus infections in cattle
induce immunity, which leads to a partial or complete
elimination of adult worms within 1-2 months p.i.
Im munity usually offers protection from the clinical
consequences of re-infections since ingested larvae are
trapped and eliminated on their way to the lungs. By
this time small numbers of larvae may induce partial
immunity that varies between individuals. Protective
effects against challenge infections can already be
observed early in the migratory phase of a primary
infection, but the full effects need a few weeks to develop.
Persistence of immunity depends on challenge infections.
Without re-infections, the protective immunity lasts for
4-6 months and disappears within approximately one
year.
Reliable levels of specific antibodies in blood serum,
bronchial liquids and milk can be detected 3-4 weeks
after primary infections. Protection against challenge
infections is partially antibody-dependent(significant
correlation with serum IgE levels) and seems to be
mediated by antibody-dependent cellular cytotoxicity
(ADCC) reactions. The mechanisms which allow to
eliminate adult worms from the respiratory tract are
unclear.
The naturally acquired immunity to D. v1v1parus
served as a model for the development of a vaccine.
G.M. Urquhart and his group at the Glasgow Veterinary
School accomplished pioneering work by developing
a vaccine in the 1960s. This vaccine (Bovilis" Dictol)
has proven its value in the control of dictyocaulosis in
several European countries and is still in use. It is a live
vaccine and contains X-ray-attenuated (400 Gray) L3
of D. viviparus ( ► p. 569).
Clinical signs. Occasional cough and slightly
increased respiratory rates may occur as first clinical
signs during the prepatent period, approximately 2
weeks p.i. at a time when larvae are not yet excreted in
the faeces. Subsequently, symptoms correspond to an
acute or gradually developing bronchopneumonia and
become more severe with frequent coughing, tachypnoea
(respiratory rate >40/min), hyp erpnoea, nasal discharge
and sometimes with fever. Lung auscultation reveals
pathological findings. Further signs are anorexia,
dehydration and weight loss. Heavily infected animals
may show the so-called 'sawbuck-like' position with
protruded head and intense mouth-breathing(► Figure
10.45). Milk production decreases in affected cows. After
onset of immune reactions and partial elimination of the
worm burden, the animals either recover or symptoms
persist due to chronic lung pathology. Fatal cases may
occur in all phases of the disease, depending on the
intensity of infection and the immune status. Symptoms
may be highly variable within a herd, with young animals
usually being most severely affected.
Fi gure 10.45. Calf with severe dyspnoea caused by
dictyocaulosls ('sawbuck-like' position) (Photo: IPZ, F.
lnderbltzln).
Diagnosis. Case history provides important
hints (grazing history, first grazing season, pasture
management). Leading symptoms of the disease are
increased respiratory rate and coughing. After onset of
patency the diagnosis can be confirmed by detection of
L1 in the faeces(► Baermann technique, p. 530). The
larvae are unsheathed and characterised by an indistinct
oesophagus, granulated midgut, and a pointed posterior
end. The larvae show a sluggish type of movement
(► Table 10.10, p. 539; ► Figure 16.8, p. 305). In
case of negative findings, tracheal exudate should be
investigated (eggs, larvae, eosinophils). Since high
individual variations in larval shedding occur within a
herd, a representative number of animals must be tested.
Specific antibodies may be detected in serum (ELISA,
immunoblotting) and milk(bulk-tank milk, ELISA) and
are indicative for D. viviparus infections acquired by the
animals within the last 3-6 months. An ELISA using
a recombinant antigen (major sperm protein, MSP)
exhibited for serum and milk samples sensitivities >99%
and specificities >97%, respectively. This test can detect
anti-MSP antibodies from the beginning of patency
(approx. 3 weeks p.i.).
Therapy. Various macrocyclic lactones (ML),
levamisole and various benzimidazole derivatives,
given in recommended doses, are highly active against
developing and adult stages of D. viviparus. Hypobiotic
stages can also be controlled with ML, such as ivermectin
Q)
and doramectin (► Table 19.2) (note: only some C
commercial products have listed hyp obiotic stages in
·o
'6
Q)
the label claim). Macrocyclic lactones show a slightly 2
longer residual effect against D. viviparus than against
trichostrongyles (► p. 300 ff).
c
co
C
·;::
Q)
Control. Various options are available:(a) vaccination,
(b) application of long-acting anthelmintics, (c) strategic _s;
application of anthelmintics, (d) grazing management,
-
>,
CJ)
( e) prevention of import of D. viviparus into lungworm­ 0
0
free herds (for detailed information see ► p. 582 ff). 'cii
co
(l_
,!
 Part Ill. Parasites and parasitoses: metazoa
Dictyocau/us filaria (large lungworm of small
ruminants)
Disease: Dictyocaulosis in small ruminants.
Agent, life cycle and epidemiology. D. Ji/aria,
the large lungworm of sheep and goats, also occurs in
some species of wild ruminants ( ► Table l 0. 10). The
life cycle of D. fl/aria corresponds in principle to that
of D. viviparus but prepatency lasts at least 26-30 days.
The patency (after a primary infection) is approximately
45 days, but under natural conditions sheep may shed
larvae for many months. Larval development (LI -.
L3) in the environment is already possible at 5 °C and
takes up to 3 weeks, but only 5 days at 20 °C. In the
Central European growing season L3 may survive on
pastures between 6 weeks and 5 months, depending on
temperature and humidity. These stages can also resist
the winter time with frequent frost periods but are not
markedly resistant to desiccation.
Infectious larvae overwintering on pasture are
apparently of minor importance for disease transmission
in spring. Pasture contamination with D.fllaria larvae
is predominantly caused by older sheep and goats
harbouring hypobiotic stages that reach sexual maturity
at the beginning of the grazing season. This mode of
pasture contamination is particularly important in warm
and dry climates with unsuitable conditions for larval
survival on pastures. The larval density on pastures
gradually builds up, usually leading to an increased
infection risk in the second half of the grazing season.
Highest worm burdens are usually found in autumn.
However, after prolonged periods of rain, heavy
infections may occur earlier in the year.
Occurrence. D. fl/aria is a cosmopolitan parasite in
sheep and goats. Prevalences in Central European sheep
flocks vary widely (up to 50%) but clinical outbreaks
are rare. The parasite is more common in regions with
warmer climates, i.e. the Mediterranean area, the Middle
East and parts of Asia. It may be a problem in camelids
(guanacos) in South America. Mouflon, chamois and
ibex are also hosts of D. fl/aria.
Q)
T5
C development of juvenile stages. According to older
'6 Pathogenesis and clinical signs. The pathology
�
Q)
of D. Ji/aria infections in sheep corresponds in principle
c:' to that of D. viviparus in cattle, although it is generally
C'O
C less intense. Usually, the infection takes a chronic
·;::
Q) course in sheep; acute infections in lambs are rare,
j with symptoms (cough, tachypnoe, etc.) occurring 2-3
-� weeks p.i. Increased osmofragility of the erythrocytes,
>, induced by hyp erventilation and hypoxaemia, may result
-ro
O>
0 in normocytic, normochromic anaemia. Goats are often
0
"in more affected by the disease than sheep.
ro
Q..
Diagnosis, therapy and control. The diagnosis
is based on detection of L1 in faeces (Baermann
technique; ► p. 530). The larvae are similar to those
of D. viviparus, but they are slightly longer (490-520
µm), have a small cuticular knob at the anterior end
and a blunt tail ( ► Figure I 6.8, p. 539). For therapy,
the same classes of anthelmintics are used as against D.
viviparus ( ► Table 19.6). Measures applied for control
of trichostrongylids are also effective against D. Ji/aria.
Oral immunisation with irradiated larvae is possible
but a cornmercial vaccine is not available.
Dictyocau/us arnfieldi
Disease: Dlctyocaulosls In equlds.
Agent and life cycle. The adult parasites inhabit the
bronchi of donkeys, horses, mules and zebras. Female
worms produce embryonated eggs from which LI
hatch either already in the lungs, in the gastrointestinal
tract or after deposition of faeces in the environment.
Under favourable conditions (20 °C), LJ develop within
5-7 days into L3 which are ingested by equids. The
larvae invade lymph vessels of the intestinal wall and
presumably migrate via the ductus thoracicus and the
right heart to the lungs, where they moult to preadult
stages 10-12 p.i. These stages settle in the bronchi and
reach sexual maturity. Prepatency periods of 5½ to 14
weeks have been reported for horse foals and of 13 weeks
for foals of donkeys. Patency periods of 6-3 l weeks were
observed in horse foals. They are strongly reduced in
adult horses, but they may last much longer in donkeys.
Occurrence and epidemiology. D. arnfieldi
is a cosmopolitan parasite of equids. The parasite is
particularly adapted to donkeys in which it regularly
develops to sexual maturity, followed by shedding of
eggs or larvae. Intensity and extensity of the infection
Increase In donkeys up to an age of approximately two
years and subsequently persists almost unchanged for
years. Horses are susceptible to D. arnJieldi up to an age
of 6-9 months and may develop patent infections. Such
infections also occur in older horses, but the majority
of infections remains impatent due to an arrested
studies, in many countries prevalences of D. arnfieldi
were very high in donkeys (45-88% in 6 European
countries), but low in horses. Consequently, persistent
infections in horse stud farms depend on donkeys as
continuous disseminators of larvae.
During the grazing season, D. arnJieldi larvae survive
only a few weeks on pasture, even under conditions of
sufficient humidity. Overwintering of larvae on pasture
is regarded as epidemiologically insignificant. Infections
in housed animals are unlikely. Considering the Central
♦ 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)
European climatic conditions, patent infections in young
donkeys may occur as early as August, but are usually
observed in autumn.
Pathogenesis and clinical signs. D. arnfieldi
infections in donkeys generally remain asymptomatic,
independently of the age of the animals. Also young
horse foals are usually not clinically affected by the
parasites. In older horses the infection may manifest
as bronchopneumonia. Chronic dry cough, dyspnoea,
anorexia, emaciation are observed; there is usually no
increase in body temperature. Eosinophilia in blood
and bronchial exudate are common. Post mortem,
worms and substantial masses of mucus are found In
bronchi and trachea; the bronchial mucosa is thickened.
Histopathologically the bronchial walls are hyperplastlc,
and peribronchial areas are infiltrated with leukocytes,
in particular with eosinophils.
Diagnosis. A history of mixed grazing of horses
and donkeys on common pastures is relevant for the
diagnosis. In case of patent infections, embryonated
eggs (74-96x46-58 µm; flotation technique) or L1 (420-
480 µm; Baermann technique) may be demonstrated in
faecal samples (both techniques should be used). The
morphology ofLl corresponds to the Dictyocaulus type,
but D. arnfieldi larvae have a characteristic spine on the
posterior end (► Figure 10.46). In case of impatent
infections, bronchoscopy and inspection of tracheal
fluid for eggs, larvae and eosinophils are recommended.
Therapy and control. Macrocyclic lactones are the
drugs of choice for therapy in horses (ivermectin: Ix
0.2 mg/kg b.w. p.o.; moxidectin lx 0.4 mg/kg b.w. p.o.)
(► Table 19.10). Donkeys can successfully be treated
with an eprinomectin pour-on product (0.5 mg/kg b.w.).
They should be treated after housing and, in case of
continued shedding of larvae, again before the grazing
season. Mixed grazing of horses and donkeys should
be avoided.
a ·;::
b Oictyocaulus eckerti. Vet Parasitol 68: 119-126.
Figure 10.46. Dictyocau/us arnfieldi: (a) Larva 1 (length 420-
480 µm); (b) Larva 1, posterior end (Photo: IPZ).
Selected references
Blenioschek S, Rehbein S, Ribbeck R (1996) Cross-infections
between fallow deer and domestic ruminants with large
lungworms (Oictyocaulus spp.). Appl Parasitol 37: 229-238.
Divina BP, H6glund J (2002) Heterologous transmission with
ct!
Oictyocaulus capreolus from roe deer (Capreolus capreo/us) :-g
>-,
to cattle (Bos laurusJ. J Helmlnthol 76: 125-130. Ol
C
Epe C, Von Samson-Hlmmelstjerna G, Schnieder T (1997) 2
Differences in a ribosomal DNA sequence of lungworm if)
species (Nematoda: Dictyocaulidae) from rallow deer, cattle,
sheep and donkeys. Res Vel Sci 62: 17-21.
Eyeker M, Kooyman FN, Ploeger HW (2001) Immunity in
calves against Dictyocaulus vtvlperus rollowing a low primary
Infection. Parasitology 123: 591-597.
Gibbons LM, H6glund J (2002) Dlctyocaulus capreolus n. sp.
(Nematoda: Trlchoslrongyloldea) rrom roe deer, Capreotus
capreolus and moose, Atces alces, in Sweden. J Helminthol
76: 119-124.
Hi>glund J (2006) Targeted selective treatment of lungworm
infection In an organic dairy herd in Sweden. Vet Parasitol
138: 318-327.
Holmgren S, Hagberg Gustavsson M, Lunden A, Wattrang
E (2014) Cytokine mRNA expression in bronchoalveolar
lavage cells during Dictyocaulus viviparous infection in calves.
Parasite lmmunol 36: 78-86.
Ploeger HW, Eysker M (2002) Protection against and
establishment of Dictyocaulus viviparus following primary
Infection at different dose levels. Vet Parasitol 106: 213-223.
Ploeger HW, Holzhauer M, Ulterwijk M, Van Engelen E
Cl)
(2014) Comparison of two serum and bulk-tank milk ELISAs .c
C
for diagnosing natural (sub)clinical Dictyocaulus viviparus
°E!
infection in dairy cows. Vet Parasitol 199: 50-58. a5
I
Rehbein S, Baggott DG, Johnson EG, Kunkle BN, Yazwinski
TA, Yoon S, Cramer LG, Soll MD (2013) Nematode burdens
of pastured cattle treated once at turnout with eprinomectin
extended-release Injection. Vet Parasitol 192: 321-331.
Schnieder T, Daugschies A (1993) Dose-dependent
pathophyslologlcal changes in cattle experimentally infected
with Dictyocaulus viviparus. J Vet Med 40: 170-180.
Schunn AM, Conraths FJ, Staubach C, Frohlich A, Forbes
A, Schnieder T, Strube C (2013) Lungworm infections
in German dairy cattle herds - seroprevalence and GIS­
supported risk factor analysis. PLoS One 5: e74429.
Strube C, Schnieder T, Von Samson-Himmelstjerna G
1!I
(2007) Differential gene expression in hybobiosis-induced ,,
Q)
and noninduced third-stage larvae of the bovine lungworm
-c3
Dictyocau/us viviparus. Int J Parasitol 37: 221-231.
Von Samson-Himmelstjerna G, Woidtke S, Epe C, Schnieder
T (1997) Species-specific polymerase chain reaction for >,
the differentiation of larvae from Dictyocaulus viviparus and ct!
C
Q)
Von Samson-Himmelstjerna G, Schnieder T (1999)
Morphology of inhibited larvae of the bovine lungworm .£
Oictyocaulus viviparus. J Helminthol 73: 79-83. >,
Veneziano V, Di Loria A, Masucci R, Di Palo R, Brianti E,
Gokbulut C (2011) Efficacy of eprinomectin pour-on against
Dictyocaulus arnfieldi infection in donkeys (Equus asinus).
·oo
ct!
Vet J 190: 414-415.
I
i.
 Part Ill. Parasites and parasitoses: metazoa
Yafetto L, Carroll L, Cui Y, Davis DJ, Fischer MW, Henterly
AC, Kessler JD, Kilroy HA, Shidler JB, Stolze-Rybczynski
JL, Sugawara Z, Money NP (2008) The fastest flights in
nature: high-speed spore discharge mechanisms among
fungi. PLoS One 3: e3237.
- Superfamily Metastrongyloidea
Family Metastrongylidae (lungworms of
porcines)
Disease: Metastrongylldosis.
Meta- (G): after; strongylos (G): round.
Summary
Agents. The family consists of the genus Meta­
strongylus, comprising 6 species of which M. aprl,
M. pudendotectus and M. salmi are most common.
Features: 2.5 cm (cM') and up to 5 cm (� �) long
nematodes, a pair of trilobed Ups around the mouth
opening. Small, trllobate bursa; filiform spicules ending
In a hook. Females are ovoviviparous. Medium-sized
eggs with thick, rough shells, containing a L1.
• Occurrence, life cycle and epidemiology. Cosmo­
politan parasites In bronchi and bronchloll of porcines,
frequent In wild boars and In outdoor-raised domestic
pigs. Heteroxenous life cycle with earthworms as
Intermediate hosts. Migration In the final host from the
Intestine via mesenterlal lymph nodes and right heart
to the lungs. Prepatency lasts 4-5 weeks, patency 6-9
months. Eggs In the environment survive for months,
larvae In earthworms for years.
• Cllnlcal algna. Newcomers may develop bronchitis
and Impaired respiration. Often the Infection remains
asymptomatic but may predispose tor bacterial and
viral affections of the lungs.
• Dlagnoala. Detection of typical eggs, but often low
egg excretion.
• Therapy. Benzlmldazoles and macrocycllc lactones are
effective. WIid boars may be treated using medicated
feed.
Agents and life cycle. Adults (see above) live in
Q)
T5
C bronchi and bronchioli. It is peculiar for Metastrongylus
'6 species that females release larvated eggs which pass via
Q)
� the trachea to the pharynx, are swallowed and excreted in
the faeces. The eggs are ingested by earthworms (Eisenia,
co Lumbricus spp. and others) in which L3 develop under
C
·c summer conditions within 1-2 weeks. After ingestion of
Q)
infected earthworms by pigs the larvae migrate from the
,£:,: intestine via mesenterial lymph nodes and right heart to
>,
OJ
the lungs and settle in the bronchi. Prepatency lasts 4-5
0 weeks. Life expectancy of adult worms is 6-9 months
'iii with decreasing egg production in the final 3-5 months.
co
co
a..
Occurrence and epidemiology. Metastrongylus
species are cosmopolitans. I n Central Europe the
occurrence is almost limited to wild boars in which
prevalences may reach 100%. Usually mixed infections
of several Metastrongylus species are found with
regionally varying prevalences. Under special conditions
(maintenance in enclosures) wild boars may be infected
with several hundred lungworms. Domestic pigs are at
risk when kept on pastures. Areas, once contaminated,
remain sources of infection for a long time: infectious
eggs survive for more than I year in soil, and earthworms
remain infected for several years.
Immu nology, pathogenesis and clinical signs.
Young ( < 1/2 year old) animals are usually more frequently
and more seriously infected than older animals. This
suggests a certain degree of immunity after exposure.
Since Metastrongylus spp. have a low pathogenicity,
wild boars may tolerate several hundred worms without
noticeable clinical symptoms. However, young animals
kept in enclosures may develop signs of verminous
bronchopneumonia, associated with nasal discharge,
cough, tachypnoea, etc. and retarded growth. Lungworm
infections can enhance the consequences of bacterial
and viral lung infections. Previous assumptions that
Metastrongylus spp. transmit viruses (swine fever virus)
and rickettsiae are unlikely.
Diagnosis. Detection of the characteristic eggs in
faeces by flotation techniques (flotation solutions with
high density). Infected animals shed relatively few eggs;
e.g. wild boars infected with >400 worms had average
epg values of 200/g faeces.
Therapy and control. Levamisole, benzimidazoles
(febantel, fenbendazole, flubendazole) and macrocyclic
lactones (ivermectin, doramectin) in recommended
doses are efficacious against Metastrongylus spp.
( ► Table I 9.8, p. 589). Wild boars in enclosures have
been successfully treated with medicated feed (30 ppm
flubendazole for 10 days or 0.5 mg ivermectin/kg b.w.).
Sustainable control of metastrongylidosis in animals
kept on pasture or in enclosures may be achieved by
chemotherapy and subsequent transition of the animals
to clean areas. Purchased animals should be treated
with an anthelmintic and kept in quarantine before
integration into the group.
Selected references
Carstensen L, Vaarst M, Roepstorff A (2002) Helminth
infections in Danish organic swine herds. Vet Parasitol 106:
253-264.
Garcia-Gonzalez AM, Perez-Martin JE, Gamito-Santos JA,
Calero-Bernal R, Alcaide Alonso M, Frontera Carrion EM
(2013) Epidemiologic study of lung parasites (Metastrongy/us
spp.) in wild boar (Sus scrota) in southwestern Spain. J Wildl
Dis 49: 157-162.
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)

Gass6 D, Rossi L, Mentaberre G, Casas E, Velarde R, Nosal

P, Serrano E, Segales J, Fernandez-Llario P, Feliu C "
• Therapy and control. Macrocycllc lactones are highly
(2014) An identification key for the five most common species
effective against Protostrongylus spp. but much less
of Metastrongylus. Parasitol Res 113: 3495-3500.
efficacious against the other genera. Benzlmidazoles
Roepstorff A, Mejer H, Nejsum P, Thamsborg SM (2011)
(feballtel, albendazole, etc.) largely reduce the excretion
Helminth parasites in pigs: new challenges in pig production of larvae In the faeces.
and current research highlights. Vet Parasitol 180: 72-81.

Agents. The members of the family Protostrongylidae

Family Protostrongylidae (small discussed here are hair-like nematodes, without buccal
lungworms) capsule, 5-6 mm long. Males with small bursa copulatrix,
2 spicules, a well-developed gubernaculum and
Protos (G): the first; strongylos(G): round. telamon exhibiting complex, species-specific structures
( ► Figure 10.47). A broad spectrum of protostrongylid
species occurs in domestic and wild ruminants, hares
Disease: Protostrongy11dosls. and rabbits ( ► Table 10.12). The following description
refers particularly to protostrongyles of sheep and goats.

The family includes 13 closely related genera with
numerous species infecting ruminants. Additionally,
5 species of the genus Protostrongylus are parasites of
Lagomorpha. They are mostly parasites of the lungs,
are widely distributed and often highly abundant.
Elaphostrongylus spp. inhabit fasciae and intramuscular
connective tissues; Parelaphostrongylus spp. invade
cerebral venous sinuses and subdural spaces of wild
ruminants. All species of the family deposit the eggs
in the lungs. Hatched L1 are passed to the pharynx,
swallowed, and excreted in the faeces. Their further
development requires terrestrial molluscs(snails, slugs)
as intermediate hosts.
Life cycle. The adults live in the lung parenchyma,
in the bronchioles and in the small and medium-sized
bronchi where eggs are deposited in which L 1 develop
quickly(► Figure 10.48). Hatched larvae pass to the
pharynx, are swallowed and excreted in the faeces. In
the environment LI penetrate the foot of coprophageous
snails or slugs and develop within approximately 2
a
(/)
.c

Genera Protostrongy/us, Muel/erius,

.E
a5
Cystocau/us and others I

Summary
• Agents. Small, hair-llke nematodes, 5 to 60 mm long,
inhabiting the lungs. Common species In sheep and goats:
Protostrongylus rufescens, P. brevlsplcu/um, Mue/lerlus
capillaris, Cystocau/us ocrestus, Neostrongylus llnearls.
• Occurrence, IHe cycle, epidemiology. Mostly cosmo­
politan parasites in the lungs of small dom estic and
wild ruminants. The life cycle Is Ind irect. Females
are ovoviviparous, L1 are shed In the faeces. These
la rvae invade slugs or snails and develop Into L3.
When intermedi te hosts containing L3 are Ingested by
definitive hosts th'3 larvae migrate via mesenterial lymph Spiculum
nodes and the right heart to the lungs. Prepatency
Gubernaculum
lasts 5-9 week ; adult worms persist for years In the
definitive host. No protective im munity to challenge
infections; intensity and extensity of infection Increase Telamon
with the age of the host.
• Pathogenesis, clinical signs. Protostrongylus spp. Bursa cop ulatrix
live in medium-sized and small bronchioles, the other
genera in nodules in the lung parenchyma. Infected
animals usually don't show clinical signs but lung
functions are generally subclinlcally affected.
• Diagnosis. Detection of the 250-450 µm long, Figure 10.47. (a) Protostrongylus raillieti: male, posterior end;
transparent L1 in faeces (Baermann technique). (b) P. rufescens: gubernaculum (Graphics: IPZ, A. Seeger;
T
after Kotlan 1960).
 Part Ill. Parasites and parasitoses: metazoa
Table 10.12. Species of protostrongylids (selection).
Hosta Species of protostrongyllda
Sheep, goat Protostrongylus rufescens, P. brev/sp/culum, Mueller/us caplllarls, Cystocaulus ocreatus, Neostrongylus linearis
Moufflon P. rufescens, M. capil/aris, C. ocreetus, N. J/nearls
Chamois P. ruplcaprae, M. cap/1/arls, M. tenulsplculatus, Splculocaulus austrlacus, N. llnearis
Ibex P. rufescens, M. cap/1/arls, M. tenulsplculatus, N. 1/nearis, S. sustriacus
Roe deer Varestrongylus (syn. Cepreocaulus) capreoll
Red, fallow deer II. (syn. Bleau/us) sagittatus
-----
Hare P. pulmonalis (syn. P. commutatus),3 taurlcus
Wild rabbit _!J. pt}!monslis (syn. P. C9_mmuta_!ys), P. '?_ry�tolagl
weeks (summer temperatures) to L3. The spectrum
of intermediate hosts is broad and includes snails (e.g.
genera He/ice/la, Zebri11a, A/Jida, Bmdy/Jae11a, Aria11ta,
Theba, etc.) or less frequently slugs (genera Arion,
Agriolimax, Deroceras). Definitive hosts acquire the
infection by ingestion of infected intermediate hosts.
Larvae are released by digestion, invade the intestinal
wall and travel to the lungs via mesenteric lymph
nodes, where they moult to L4, and to the right heart.
The L4 penetrate the alveolar walls and establish in
the respiratory part of the lungs. N. linearis has been
reported to migrate through the liver. The prepatency is
species dependent and lasts 5-9 weeks. Protostrongylids
are long-living parasites and may persist for several years.
Occurrence and epidemiology. Various proto­
strongylid species infect sheep, goats and several wild
ruminant species ( ► Table I0.12). Roe deer, red deer and
fallow deer arc hosts of other small lungworm species.
The prevalences of the various species may markedly
differ geographically; mixed Infections arc common. For
example, most studies in Europe and North Africa have
revealed protostrongylid prevalences of 50-80% in sheep.
According to a recent study In north-western Spain 98%
of sheep were infected wilh M. capillarls and only 5%
with N. lincaris. In contrast, groups of slaughter sheep In
southern Germany harboured 5 protostrongylid species.
Lambs under 6 months of age shed few if any larvae but
prevalences increase with age. In ES, for instance, I 4%
of sheep< I year old were infected with/� rrifescem, and
50% >3 years old. Thus, older animals are the major
(J)
T5
C contaminators of pastures. In older animals a seasonal
u dynamic in shedding of larvae was observed with peaks
Q)
� in spring and autumn and a largely reduced excretion
� in winter (November/December till March). It seems
cu that the increased larval shedding in spring is associated
C
·c
Q) with gestation and lactation, since it is missing in barren
j animals.
C view of the extent of the lesions and the loss offunctional
>, LI survive in faecal pellets of small ruminants for
CJ')
0 several weeks, and sometimes months. Infectious
2
'in larvae in molluscs probably survive as long as these
cu animals live and remain infectious for approximately
cu
(L
�
�
one week in dead intermediate hosts. Since many
species of intermediate hosts live in different habitats,
protostrongylid infections of sheep and goats or wild
ruminants occur in wet and dry habitats.
Immunology. Protostrongylids induce only weak
immunity in sheep which at the most may cause
trapping of some larvae in the mediastinal lymph nodes
of challenged animals. However, a protective immunity
does not develop as indicated by increasing parasite
prevalences with host age.
Pathogenesis. P. rufescens is found in medium-sized
and small bronchi, whereas C. ocreatus, M. capillaris
and N. linearis settle in the lung parenchyma (M.
capillaris predominantly in the subpleural tissue).
Small nodules ('worm nodules') and larger lesions of
multifocal bronchopneumonia are characteristic for
protostrongylid infections. Worm nodules arc 1-3 mm In
size and contain a single or a few, often immature living
or dead worms ( ► Figure I 0.49). The larger lesions
usually enclose several fertile worms. The surrounding
tissue and the alveoles arc interspersed with eggs and
free I. I. The lesions are predominantly found in the
caudal lobes of the lungs. I� rufescens associated lesions
arc found in the whole bronchial tree. In case of M.
capillaris lesions arc flat due to their rather subpleural
position ( ► Pigure 10.50). On the lung surface they
appear as solid, pulvinated, greyish to yellowish/greenish
areas which are demarcated by inflammatory infiltrates.
Histopathologically they represent extended areas of
inflammation with multiple granulornas, type II-cell
hyperplasia and rnastocytosis in the parenchyma and
broncho-alvcolar exudates in bronchioli and alveoles
(► Figure 10.51).
Clinical signs. If at all, only weak respiratory
symptoms arc apparent so that the consequences of
the infection are usually underestimated. However, in
lung parenchyma, considerable effects on gas exchange
are to be expected. Indeed, in sheep naturally infected
with protostrongylids, the respiratory rate, the CO2
partial pressure as well as the total concentrations of
CO2 and HC03 in blood were doubled, whereas the 02
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)

co
:g
>,
0)
C
e
U)

L4/5l" stage

Male (female not shown)

L3 in Inter­ Larva 1
mediate host

Intermediate host

(I)
C
·c3
=o
(I)
�
Figure 10.48. Life cycle of protostrongylids (Graphics: IPZ, S. Ehrat, modified by S. Amrein). �
(ti
C
·;::
(I)
partial pressure was reduced by half as compared with Diagnosis. Detection of Ll using the Baermann �
uninfected controls. In addition to impaired pulmonary technique. The larvae are 250-450 µm long and _\;
gas exchange, heavy infections have been associated with transparent so that oesophagus and intestine are >,
0)
decreased carcass weight. indistinct. Forms and structures of the posterior end 0
allow a differentiation of genera(► Figure 16.8, p. 539). B
"'iii
(ti
(ti
a.
 Part Ill. Parasites and parasitoses: metazoa

Figure 10.49. Muel/erius capil/aris: worm nodules, lungs, sheep Figure 10.50. Mueller/us capillaris: larger lesions, lungs, sheep
(Photo: IPZ, R. Sauerltinder). (Photo: IPZ, R. Sauerltinder).

• I
�
Selected references
i

Berrag B, Cabaret J (1996) Impaired pulmonary gas exchange

Figure 10.51. Protostrongyllds In sheep lung: histological
picture with cross-section of an adult parasite and eggs (arrows)
in alveoli (Photo: IPZ).
Therapy and control. Protostrongylus spp. respond
better to chemotherapy than the species inhabiting
the lung parenchyma. T hus, macrocyclic lactones
(ivermectin, abamectin, doramectin, moxidectin) in
recommended single doses ( ► Table 19.6) are effective
against Protostrongylus spp., whereas the efficacies
against the other genera are mostly low. Benzimidazoles
(e.g. febantel or albendazole, 5 mg/kg b.w. p.o.) reduce
temporarily larval excretion without a sustainable
effect on the adult worm population. Usually specific
Q)
treatments against protostrongylids are not performed
·o
C
in ewes naturally infected by small lung worms. Int J Parasitol
26: 1397-1400.
Berrag B, Rhalem A, Sahibi H, Dorchies P, Cabaret J
(1997) Bronchoalveolar cellular responses of goats following
infections with Muel/erius capil/aris (Protostrongylidae.
Nematoda). Vet lmmunol lmmunopathol 58: 77-88.
Braun U, Feige K, Gansohr B, Degen H, Wolff K, Gohm D,
Sydler T (2000) Protostrongyliden-Pneumonien bei Saanen­
Ziegen. Tiertlrztl Umsch 55: 338-340. 343.
Kuchboev AE, Krucken J, Ruziev BH, Von Samson­
Hlmmelstjerna G (2015) Molecular phylogeny and diagnosis
of species of the family Protostrongylidae from caprine hosts
In Uzbekistan. Parasitol Res 114: 1355-1364.
L6pez CM, Fernandez G, Cienfuegos S, Panadero R,
Vazquez L, Diaz P, Pato J, Lago N, Dacal V, Diez-Barios
P, Morrondo P (2011) Protostrongylld Infection In meat sheep
from Northwestern Spain: prevalence and risk factors. Vet
Parasltol 178: 108-114.
L6pez CM, Cienfuegos S, Decal V, Vazquez L, Panadero R,
Fernandez G, Diaz P, Lago N, Diez-Barios P, Morrondo
MP (2010) Efficacy of anthelmlnthic control programs against
natural Muellerius capillaris infection in sheep in the north­
west of Spain. Effect on blood gases and pH in venous blood
samples. Parasite 17: 167 -171.

'6 because the symptoms of the disease are inconspicuous. Manga Gonzales Y, Morrondo Pelayo P, Cordero del
Q)
Control of intermediate hosts is not feasible. Campillo M (1986) Molluscos hospedadores intermediaries
de Protostrongylidae ovinos. Leon, Spain: Universidad de
lU
C Le6n; ISBN 84-600-4546-3.
·;;::
Panayotova-Pencheva MS, Alexandrov MT (2010) Some
pathological features of lungs from domestic and wild
C: ruminants with single and mixed protostrongylid infections.
>, Vet Med Int 2010: 741062.
OJ
0

'cii
lU
lU
0..
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)
Genus Elaphostrongy/us
Efaphostrongylus cervi
Disease: Elaphostrongylosis in wild ruminants, goats
and sheep.
Elaphos (G): deer; strongylos (G): round; cervus (L.): deer.
Elaphostrongylus cervi, a parasite of the intramuscular
connective tissue, occurs in Europe, Asia and New
Zealand. It typically produces asymptomatic, patent
infections in red deer, the natural hosts, and impotent
infections with severe neurological symptoms in
aberrant hosts, such as goats and sheep.
Agent and life cycle and occurrence. In definitive
hosts the adult stages of E. cervi (cM': 29-38 mm,��:
49-58 mm) inhabit the fasciae and the intermuscular
connective tissue, primarily of the breast, thorax and
back. Unembryonated eggs released by females into
the capillaries are carried to the lungs where Ll develop
and hatch. The larvae pass via the respiratory tract to
the pharynx, they are swallowed, and excreted in the
faeces. Several snail species serve as intermediate hosts
in which L1 develop into L3. Snails containing L3 are
ingested by definitive hosts in which the larvae migrate
via the haematogenous route from the intestine to the
CNS where they develop in meninges and submeningeal
spaces into adults which migrate to their predilection
sites. The prepatent period lasts at least 3-6 months.
Occurrence and epidemiology. E. cervi infections
in red deer have been reported in several European
countries (e.g. AT, CH, CZ, DE, IT, SE) with high
prevalences (-45-70%) and less frequently in fallow
deer. Further species occurring in Europe (Scandinavia)
are E. rangifer in reindeer, and E. alces in moose.
Parelaphostrongylus tenuis infects wild ruminants in
North America. In Europe, clinical cases in goats and
sheep (see below) were observed in areas with mixed
grazing of these ruminants with red deer infected with
E. cervi (e.g. CH, IT, SE) or E. rangifer (NO).
Clinical signs and pathogenesis. E. cervi
infections in red deer, the natural hosts, are usually
asymptomatic. In contrast, infected aberrant hosts,
such as goats, sheep and other cervids, may develop
mild to severe behavioural changes (aggressivity,loss of
herd instinct), nervous disorders (ataxia, limb paresis
and paralysis), occasionally blindness, respiratory
disturbances and death. Pathological changes include
verminous pneumonia, due to the accumulation of eggs
and larvae in the lungs; severe lesions in the brain and
spinal cord are caused by migrating juvenile stages. Also
lungs, kidney and other organs may exhibit pathological
lesions. ell
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Diagnosis and therapy. The infection in natural
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hosts is diagnosed by detection of LI (Baermann 0
technique) in faeces; the larvae must be differentiated u5
from larvae of the lungworm Varestrongylus sagittatus
(morphology, DNA analysis). Case history, clinical
symptoms, examination of CSP and necropsy are the
main options for diagnosing the infection in aberrant
hosts. A group of goats with weak to moderate central
nervous symptoms was treated with an increased dose
of fenbendazole (SO mg/kg b.w. p.o.) plus ivermectin
(0.2 mg/kg b.w. s.c.) for 5 days plus antiphlogistic drugs.
Clinical improvement was observed in some animals.
Selected references
Alberti EG, Gioia G, Sironi G, Zanzani S, Riccaboni P,
Magrini M, Manfredi MT (2011) Elaphostrongylus cervi in
a population of red deer (Cervus elaphus) and evidence of
cerebrospinal nematodiasis in small ruminants in the province
of Varese, Italy. J Helminthol 85: 313-318.
Dobey CL, Grunenwald C, Newman SJ, Muller L, Gerhold
AW (2014) Retrospective study of central nervous system
lesions and association with Parelaphostrongylus species
by histology and specific nested polymerase chain reaction
in domestic camelids and wild ungulates. J Vet Diagn Invest
26: 748-754.
Handeland K, Gibbons LM, Skorplng A (2000) Experimental
Elaphostrongylus cervi infection in sheep and goats. J Comp
Pathol 123: 248-257.
Prosl H, Kutzer E (1980) Zur Pathologie des Elaphostrongylus­
belalls balm Rothirsch (Cervus elaphus hippelaphus).
Monatsh Vet Med 35: 151-153.
Pusterla N, Hertzberg H, Viglezio M, Vanzetti T, Braun
U (1998) Untersuchungen Ober das Vorkommen der
lumbalen Parese bei Ziegen und Ober das Auftreten von
Elaphostrongylus cervi bairn Rothirsch im Kanton Tessin.
Schweiz Arch Tierheilkd 140: 76-82.
Pusterla N, Caplazi P, Hertzberg H, Ehrensperger F, Braun
(I)
C
U (2001) Elaphostrongylus cervi infection in a Swiss goat.
Vet Rec 148: 382-383.
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 Part Ill. Parasites and parasitoses: metazoa
Family Crenosomatidae
Crenatus(L): serrated; soma(G): body. Refers to cuticular
annulations with small spines around the anterior end
of the parasite.
Genus Crenosoma
Crenosoma vu/pis (fox lungworm)
Disease: Crenosomosls In dogs and other canlds.
Summary
• Agent, llfe cycle and occurrence. C. vu/pis Is a
cosmopolitan lungworm of wild canlds and dogs
Inhabiting the bronchi and bronchioles. L1 are shed In
the faeces, they Invade slugs or snails as Intermediate
hosts and moult into L3. Infection of final hosts happens
by Ingestion of Infected intermediate hosts. Migration
to the lungs via the liver and the right heart. Prepatency
3 weeks; patency 10 months and more.
• Cllnlcal algna, diagnosis, therapy. Bronchitis,
perlbronchitis. Detection of L 1 in the faeces (Beermann
technique) or bronchial lavage fluid. Macrocyclic
lactones are regarded as the drugs of first choice for
chemotherapy of dogs.
Agent. Relatively small (oo:
4-8 mm,��: 12-16 mm)
nematodes in the bronchi and bronchioli. Both sexes
show at the anterior third of the body approximately
20 circular annulations with small spines of the cuticle
(resembling horsetail plants). LI measure 250-300 µm
and possess a straight, pointed tail( ► Figure 16.16,
p. 549).
Life cycle. Developing and adult C. vu/pis inhabit the
bronchi and bronchioli of definitive hosts( ► Figure
I 0.52). The females are ovoviviparous. LI are excreted
in the faeces and invade slugs and snails(genera Capaea,
Agriolimax, Arion, Succinea, etc.) and develop into
L3 within 2-3 weeks. Final hosts become infected by
ingestion of snails and slugs containing L3. The larvae
invade the intestinal wall and migrate to the lungs via
the liver and the right heart. An alternative migration
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via lymph and blood vessels without a liver passage
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'6 has been described in the literature. Prepatency lasts 3
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� weeks; adults survive for at least IO weeks.
� Africa(Malawi), IT and GR, and Trog/ostrongylus spp.
co Occurrence and epidemiology. C. vu/pis occurs in
C:
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Q) temperate regions of Europe, Asia and North America.
j Final hosts are foxes(red fox, polar fox), other wild
-� canids(raccoon dogs, wolves) and dogs. For instance,
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2-6% of dogs with respiratory symptoms in Germany
0 excreted C. vu/pis larvae, and 0.4% of a normal dog
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population. Approximately 40% of red foxes in Europe
co are infected with C. vu/pis. Closely related Crenosoma
co
CL
spp. are found in raccoons(C. goblei), badgers(C. melesi)
and mustelids(several species). A common parasite of
hedgehogs in Europe is C. striatum which is clinically
important in these animals.
Pathogenesis and clinical signs. Temporary
alterations are caused by migrating stages in the
parenchyma of liver and lungs. Preadult and adult
worms cause eosinophilic bronchiolitis and bronchitis
with a tendency to chronicity and expansion to the lung
parenchyma resulting in bronchopneumonia.
Diagnosis. Detection of Ll in the faeces with the
Baermann technique. Bronchoscopy and examination of
BAL(often eosinophilia) may be employed. Differential
diagnosis between C. vu/pis and other lung nematode
larvae has to consider the morphology of the posterior
end of the larvae( ► Figure 16.16, p. 549).
Therapy and control. Fenbendazole(SO mg/kg b.w.
p.o. on 3-14 consecutive days) is reported to be effective.
Milbemycin oxime(0.5 mg/kg b.w., single oral dose) and
topically administered moxidectin(2.5 mg/kg b.w.) have
shown high efficacy. These two drugs have also proved
highly effective when applied in combination products
( ► Table I 9.15). Prophylaxis is difficult; e.g. successfully
keeping slugs and snails away from dog kennels depends
on good construction.
Genus Trog/ostrongy/us
Disease: Troglostrongylosls in felids.
Troglodytus(G): cave-dwelling; strongylos(G): round.
Cave-dwelling refers to the first finding in the frontal
sinus of a leopard cat.
Agents and occurrence. Members of the genus
Troglostrongylus(syn. Bronchostrongylus) are parasites
of wild felids and domestic cats, with T. subcrenatus
inhabiting the trachea and bronchi and T. brevior being
localised in bronchi and bronchioli. Further species
are T. wilsoni (bronchi, lung parenchyma) and r
troglostrongylus(frontal sinuses) of wild felids. r brevior
is frequently found in European wildcats (Pelis silvestris)
and was detected in 6.5% of private cats and colonies
in Sardinia/IT. T. subcrenatus has been found in cats in
in Spain. Co-infections with Aelurostrongylus abstrusus
and T. b revior have been described in domestic cats.
The whitish adults of Troglostrongylus spp. vary in
size among species(up to 10 mm (oo)
and 24 mm
( � �)); they are wider than Aelurostrongylus abstrusus
in cats and can be differentiated by the clearly longer
spicules ( 600-700 µm compared with approximately
is;
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)
r 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)

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Figure 10.52. Life cycle of Crenosoma vu/pis (Graphics: IPZ, S. Ehrat).

200 µm in A. abstrusus) and the position of the vulva Clinical signs, diagnosis and therapy. Depending Q)

in females (it opens almost in the middle of the body on the parasite load, the clinical outcome varies from C
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in Troglostrongylus spp. whereas it is located near the asymptomatic to coughing, nasal discharge and dyspnoea.
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posterior extremity in A. abstrusus). The parasitological diagnosis is based on the coproscopic �
detection of L1 (Baermann technique) and requires a �
ctl
Life cycle and epidemiology. Slugs and snails discrimination of Troglostrongylus and Aelurostrongylus C
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serve as intermediate hosts in the indirect life cycle. larvae. Since morphological differentiation is difficult, Q)

However, paratenic hosts (amphibians, reptiles, birds, DNA analysis should be employed for species-specific
small rodents) are thought to play an important role. diagnosis. In a few cats chemotherapy with emodepside -�
L3 are reported to survive at least 4 months in mice. (3 mg/kg b.w., spot-on) or eprinomectin (0.5 mg/kg b.w., >,
OJ
Findings of T. brevior in kittens gave rise to speculation spot-on, in combination with fipronil, S-methoprene and 0
on direct infections from the queen to offspring. Details praziquantel) was efficacious against Troglostrongylus. 'ui
are not known. ctl
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 Part Ill. Parasites and parasitoses: metazoa
- Selected references======--•
Brianti E, Giannetto S, Dantas-Torres F, Otranto D (2014)
Lungworms of the genus Troglostrongylus (Strongylida:
Crenosomatidae): neglected parasites for domestic cats.
Vet Parasitol 202: 104-112.
Conboy G, Hare J, Charles S, Settje T, Heine J(2009) Efficacy
of a single topical application of advantage multi(= advocate)
topical solution (10% imidocloprid+2.5% moxidectin) In the
treatment of dogs experimentally infected with Crenosoma
vu/pis. Parasitol Res 105: 49-54.
Di Cesare A, Iorio R, Crisi P, Paoletti B, DI Costanzo R,
Dimitri CF, Traversa D (2015) Treatment of Troglostrongylus
brevior (Metastrongyloidea, Crenosomatldae) in mixed
lungworm infections using spot-on emodepslde. J Feline
Med Surg 17: 181-185.
Falsone L, Brlantl E, Gogllo G, Napoli E, Anlle S, Mallia
E, Giannelli A, Poglayen G, Giannetto s, Otranto D
(2014) The European wild cats (Fe/is sylvestris sylvestris)
as reservoir hosts of Troglostrongylus brevior (Strongyllda:
Crenosomatidae) lungworms. Vet Parasltol 205: 193-198.
Giannelli A, Passantino G, Ramos RA, Lo Presti G, Lia RP,
Briantl E, Dantas-Torres F, Papadopoulos E, Otranto D
(2014) Pathological and histological findings associated with
the feline lungworm Trog/ostrongylus brevior. Vet Parasitol
204: 416-419.
Giannelli A, Brlantl, E, Varcasla A, Tamponl C, DI Paola G,
Knaus M, Halos L, Beugnet F, Otranto D (2015) Efficacy
of Breadline® spot-on against Aelurostrongylus abstrusus
and Troglostrongylus brevior lungworms In naturally infected
cats from Italy. Vet Parasitol 209: 273-277.
Jefferiea R, Vrhovec MG, Wallner N, Catalan DR (2010)
Aelurostrongylus abstrusus and Troglostrongylus sp.
(Nematoda: Metastrongyloidae) infections in cats inhabitating
Ibiza, Spain. Vet Parasltol 173: 344-348.
Taubert A., Pantchev N, Vrhovec MG, Bauer C, Hermosilla
C (2009) Lungworm Infections l,A.nglostrongylus vasorum,
Crenosomo vu/pis, Aelurostrongylus abstrusus) In dogs and
cats In Garmany and Denmark In 2003-2007. Vet Parasltol
169: 176-180,
Traverse 0, DI Ce1■re A, Conboy a (2010) Canine and reline
cardiopulmonary parasitic namatodes In Europe: emerging
and underestimated. Paraslt Vectors 3: 62.
Traversa D, DI Ceure A, Brlentl E(2015) Lungworm Infections.
In: Beugnet F, Halos L (eds.) Parasltoses & vector borne
diseases of cats. Lyon, France: Meriaf S.A.S., pp. 95-106;
Q)
T>
C ISBN 978-2-9550805-0-4.
'6 Unte,.r S, Deplaze1 P, Arnold P, FI0cklger M, Reusch DE,
Q)
Glau, TM (2002) Spontaneous Cronosoma vu/pis infection
� antibodies. Treatment with macrocyclic lactones(single
� In 10 dogs: laboratory, radiographic and endoscopic find ings.
C1'
C Schweiz Arch Tierheilkd 144: 174-179.
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Family Angiostrongylidae
Angeion (G): vessel; strongylos (G): round.
Members of the family Angiostrongylidae are parasites
in blood vessels and lungs of carnivo res, marsup ials,
insectivores and rodents. Males with a well-developed
bursa, vulva of females in a caudal position. Indirect
life cycle with molluscs as intermediate hosts, in som e
species involvement of paratenic hosts. The genera
Angiostrongylus and Aelurostrongylus have a particularly
significant impact on animal health. Angiostrongylus
cantonensis and A. costaricensis are causative agents of
zoonoses.
Genus Angiostrongylus
Angiostrongylus vasorum (French heartworm)
Disease: Anglostrongylosis In dogs and other canids.
Summary
• Agent. Reddish nematodes, up to 25 mm long('?'?),
Inhabiting the arterla pulmonalis and the right heart of
canlds and mustelids.
• Occurrence, life cycle. Endemic in Europe(prevalence
In foxes regionally up to 50%), and certain areas In
Africa, North and South America. Eggs are swept
Into the capillaries of the lungs where L1 hatch. L1
penetrate Into the respiratory part of the lungs, are
transported to the pharynx, swallowed and excreted
to the environment. They Invade slugs and develop to
L3 which are Ingested with the Intermediate hosts by
carnivores. Migration In the final host via mesenterial
lymph nodes to the arterla pulmonalis and the right
heart. Prepatency 6-8 weeks; patency may last for
5 years.
• Pathogene■ la, cllnlcal signs. In dogs thrombosis
of the lung arteries by eggs, larvae and adults with
granuloma formation and development of nodules
and knots; haemorrhages In the alveoles by migrating
larvae. DIiatation of the right heart. disseminated
lntravaaoular coagulation. Clinical signs: coughing,
dyapnoea, subcutaneous haematomas, occasionally
central nervous disorders.
• Dlagnoala, therapy. Coproscoplc detection of L1
(8aermann technique); Irregular larval excretion.
Serological detection of circulating antigen or specific
topical application of moxldectln or mllbemycln oxlme
orally once weekly for 4 weeks) or fenbendazole for
several weeks. Supportive treatment (fluid or blood/
transfusion, antibiotics, corticosteroids, oxygen).
Agent. 14-18 mm (c3\3') or 18-24 mm (QQ) long
nematodes of reddish appearance; females with white
uterus coiled around the red, blood-filled intestine
(► Figure 10.53). Males with small bursa and 2 spicula,
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)
without gubernaculum. LI: 310-400 µm long, posterior
end with dorsal spine (► Figure 16.16). Definitive hosts
are mainly canids (fox, wolf, jackal, coyote, dog); in
Europe it has also been found in badgers (Me/es me/es)
and otters (Lutra lutra).
Life cycle. Adults inhabit the arteria pulmonalis and
the right heart. Unembryonated eggs are washed into the
lung capillaries where LI develop. Larvae penetrate the
alveoles, reach the pharynx, are swallowed and excreted
in the faeces. These larvae invade slugs in which L3
develop within 2-3 weeks at optimum temperatures.
Although numerous species of slugs, terrestrial and
aquatic snails can serve as intermediate hosts under
experimental conditions, to date only a few have been
identified as natural intermediate hosts. These include
in Central Europe the slugs Arion ater, A. ater rufus, A.
lusitanicus, A. distinctus, Limax maximus and Tandonia
sowerbyi. Common frogs (Rana temporaria) and chicken
are capable of serving both as potential intermediate and
paratenic hosts as shown by experimental infections.
Definitive hosts acquire the infection by ingesting
infected intermediate hosts and possibly also by uptake
of L3 released from living or dead slugs. Free L3 can
survive in water for 2 weeks at 20 °C and up to 8 weeks
at 4 °C. The potential role of paratenic hosts in the
transmission cycle is unclear.
In the definitive host the larvae invade the intestinal
wall and migrate to abdominal lymph nodes where they
moult into L4 which then pass to the portal circulation
and are transported via the right heart to the pulmonary
arteries. Prepatency usually lasts 6-8 weeks, patency can
persist up to 5 years.
Occurrence and epidemiology. A. vasorum occurs
in foxes, other wild can ids (wolf, jackal, coyote), dogs,
badgers, and some further animal species (e.g. the
Figure 10.53. Angiostrongy/us vasorum: adult female in arteria
pulmonalis of a dog (Photo: IPZ, N. Neff, G. Lott, K. Wolff).
Canadian lynx, free living otters). In Europe, red foxes
are regarded as natural hosts and reservoirs for infections
of domestic dogs.
The parasite is considered endemic in Europe, Africa
(Uganda), North America (Canada, USA) and South C1l
America with a genetically distinct population. In :g
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Europe, A. vasorum was previously regarded as a rare OJ
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parasite restricted to a few endemic regions (e.g. in
south-western France) and some small local foci in other if)
countries. Beginning at the end of the 1970s, a growing
number of studies document a much wider geographical
range of the parasite, including many countries in all
parts of the continent. Increasing numbers of foxes,
greater awareness, intensified studies and improved
diagnostic methods are discussed as some of the possible
reasons for the obvious geographical expansion. Reports
on prevalences of A. vasorum in European foxes range
from 5-56% and in dogs from 0.3 to 8.9%. In southern
England 16% of dogs with respiratory signs were infected
with A. vasorum.
Pathogenesis. The A. vasorum infection in dogs
may be asymptomatic or symptomatic with signs of
respiratory and cardiovascular disorders, coagulopathy,
and sometimes with neurological deficiencies. Severe
forms can be fatal. L1 perforating the alveolar walls of
infected dogs cause punctiform haemorrhages. Eggs,
larvae and adults induce thromboses of lung arteries
(► Figure 10.54). Granulomatous reactions around
these obliterations in the lung parenchyma result i n
multiple nodular foci, often o f greasy appearance,
which may reach the size of walnuts (► Figure 10.55).
Consequences of these alterations may be a dilatation of
the right heart, pulmonary congestion and ascites. Signs
of chronic infections include disseminated intravascular
coagulation with microthrombi and haemorrhagic
diatheses.
Clinical signs. The most common clinical signs in
dogs are respiratory disorders including cough and
dyspnoea, often associated with lethargy. X-ray and
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Figure 10.54. Canine angiostrongylosis: Arteria pulomanlis with
thrombus and sections of parasites (Photo: IPZ). "cii
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 Part Ill. Parasites and parasltoses: metazoa
Figure 10.55. Angiostrongylus vasorum: macroscopic lesions
In dog lung; elevated area of greasy appearance (Photo: IPZ).
CT findings often show lung alterations even in cases
with mild symptoms. Increasing dyspnoea, anaemia,
emaciation, weakening and occasionally fever may occur
in chronic stages. Simple contusions are sometimes
followed by conspicuous subcutaneous haematomas due
to coagulation disorders, but also by internal bleedings,
and shock-like reactions may occur. Rare events are
neurological disorders (amyostasia, ataxia, dizziness, and
seizures). These disorders are probably consequences
of systemic dissemination of larval stages or bleeding
into the CNS but may also be caused by cerebral hypoxia
due to chronic cardiac insufficiency. Mortality is high
in serious infections.
Diagnosis. Patent infections can be diagnosed by
detecting L1 (Baermann technique) in faeces or, with
lower sensitivity, in BAL. In differential diagnosis
Crenosoma larvae must be identified, which have a
pointed posterior end in contrast to A. vasorum larvae
( ► Figure 16.16, p. 549). Filaroides larvae usually do not
play a role ( ► p. 324). The high variability in shedding
of larvae and the necessity of fresh faecal samples for
the Baermann technique should be considered.
A highly sensitive and specific ELISA detects circulating
antigens in the blood from the beginning of patency. The
antigens may be detected throughout patent infections
and disappear within one month after successful
chemotherapy. A device for rapid clinical diagnosis is
available (IDEXX Angio Detect Test). Specific antibodies
can be detected at the end of the prepatency. They
Q)
C disappear 2 months after successful treatment. Detection
'[5 of A. vasorrm, DNA in blood is highly specific but less
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sensitive than detection of circulating antigens, and
�
� DNA detection in tracheal swabs and faeces is sporadic.
co
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Q) Treatment and control. Moxidectin (2.5 mg/kg b.w.
j spot on) and milbemycin oxime (0.5 mg/kg b.w. p.o.)
.£ are highly effective against L4 and older stages of A.
>- vasorum. Lf necessary, treatment with moxidectin should
0)
0 be repeated after 4 weeks. Milbemycin requires weekly
0
·u; oral administrations for 4 weeks. Both anthelmintics
include A. vasorum in their label claims and are available
co
CL in combination products (Advocate• and Milbemax-,
respectively). Alternatively, fenbendazole (25-50 mg/kg
b.w., p.o., daily for 3 weeks) may be used. Supportive
therapy including prophylactic antithrombotic measures,
fluid or blood transfusion, antibiotics and oxyge n are
recommended in severely affected dogs. Since a single
dose of moxidectin and milbemycin is highly active
against L4 stages of A. vasorum, these drugs have the
potential to prevent patent infections in endemic areas
if applied at monthly intervals.
Genus Aelurostrongylus
Ae/urostrongy/us abstrusus
Disease: Aelurostrongylosis in cats.
Ailouros (G): cat; strongylos (G): round.
summary
• Agent, occurrence. Nematodes, up to 14 mm in
len� ��) In the bronchloll of domestic cats and
ottier fellde; cosmopolitan; prevalence in European
'1XNnti1• 1"5096.
• Life eyole, cllnlcal 1lgn1. Excretion of L1 in faeces;
dMloprnent of L3 In snalls; oral infection of cats by
Ingestion of Infected snails or paratenic hosts. Nodules,
1•10 mm In diameter with eggs and adults in the lungs.
lnfeotlon la often asymptomatic; In heavy infections
coughing, tachypnoea, death.
• Dlagno1l1, therapy. Coproscoplc detection of L1
(Baermann technique). Treatment with moxidectin,
selamectln, emodepside or fenbendazole.
Agent and occurrence. 6 mm (oo) and 9-14 mm
( � �) long nematodes in the bronchioles and alveolar
ducts of domestic and feral cats in most parts of the
world and regionally also in lynxes. In 10 European
countries, the infection rates in cats ranged from 0.4
to 50%.
Life cycle and epidemiology. Eggs are deposited
in the lungs. Rapid development to Ll which hatch,
reach the intestinal tract via trachea and pharynx and
are excreted in the faeces ( ► Figure I 0.56). Many
genera and species of slugs and snails may serve as
intermediate hosts in which invaded Ll develop to L3.
Various animals which consume slugs and snails act as
paratenic hosts. After ingestion of infected intermediate
or paratenic hosts by cats, larvae migrate via blood and
lymph vessels to the lung and reach sexual maturity after
approximately 6 weeks.
Pathogenesis and clinical signs. Worms and
accumulated eggs in the lung are surrounded by solid
yellowish grey granulomatous nodules. Nodules reach
sizes of up to IO mm and most of them are localised
subpleurally. Lesions often coalesce. Weak infections
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L4/5•h stage
r.. ,. (female not shown)
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Intermediate host

I Larvae 2 and 3
\

Figur e 10.56. Life cycle of Ae/urostrongylus abstrusus (Graphics: IPZ, S. Ehrat).

re � ain asymp tomatic. Heavier infections are associated
with coughing, sneezing, nasal discharge, tachypnoea,
respiratory acidosis; animals become stunted and
may die.
Diagn0s1s. D
etection of the transparent, 360-400
µm long Ll in faeces by the Baermann technique or
in BAL (► Figure 16.16, p. 549). The often irregular
shedding of larvae has to be taken into account. In
differential diagnosis infections with Oslerus rostratus
and Troglostrongylus spp. should be considered. The
morphological diagnosis of larvae can be confirmed
by DNA analysis. Imaging techniques are used in the
clinical diagnosis to detect lung lesions.
Part Ill. Parasites and parasitoses: metazoa
Therapy. Fenbendazole (50 mg/kg b.w. p.o., daily for
3 consecutive days) is highly effective. This applies also
for single doses of moxidectin (1 mg/kg b.w., spot on)
and emodepside (3 mg/kg b.w., spot on). These drugs
are available as combination products (Advocate• and
Profender•, respectively).
- Selected references
Barutzki D, Schaper R (2009) Natural Infections of
Angiostrongylus vasorum and Crenosoma vu/pis in dogs In
Germany (2007-2009). Parasitol Res 105: 39-48.
Conboy GA (2011) Canine angiostrongylosis: the French
heartworm: an emerging threat In North America. Vet Parasltol
176: 382-389.
Elsheikha HM, Holmes SA, Wright I, Morgan ER, Lacher
DW (2014) Recent advances In the epidemiology, clinical and
diagnostic features, and control of canine cardlo-pulmonary
angiostrongylosls. Vet Res 45: 92.
Schnyder M, Fahrion A, Ossent P, Kohler L, Webster P,
Heine J, Deplazes P. (2009) Larvlcidal effect of lmldacloprld/
moxidectin spot-on solution in dogs experimentally Inoculated
with Angiostrongylus vasorum. Vet Parasltol 166: 326-332.
Schnyder M, Fahrion A, Rlond B, Ossent P, Webster P,
Kranjc A, Glaus T, Deplazes P (2010) Clinical, laboratory
and pathological findings In dogs experimentally Infected with
Angiostrongylus vasorum. Parasltol Res 107: 1471-1480.
Schnyder M, Di Cesare A, Basso W, Guscetti F, Riond B,
Glaus T, Crisl P, Deplazes P (2014) Clinical, laboratory
and pathological findings in cats experimentally infected with
Aelurostrongylus abstrusus. Parasitol Res 113: 1425-1433.
Schnyder M, Stabler K, Naucke T J, Lorentz S, Deplazes
P (2014) Evaluation of a rapid device for serological In-clinic
diagnosis of canine anglostrongylosis. Parasit Vectors 18: 72.
Schnyder M, Jefferies R, Schucan A, Morgan ER, Deplazes
P (2015) Comparison of coprologlcal, immunological and
molecular methods for the detection of dogs Infected with
Angiostrongylus vasorum before and after anthelmlntlc
treatment. Parasitology 142: 1270-1277,
Schnyder M, Schaper R, Bllbrough 0, Morgan ER,
Deplazes P (2013) Seroepldemlologlcal survey for canine
angiostrongylosis In dogs from Germany and the UK using
combined detection of Angiostrongylus vasorum antigen and
specific antibodies. Parasitology 140: 1442-1450.
Taubert A, Pantchev N, Vrhovec MG, Bauer C, Hermosilla
C (2009) Lungworm Infections l,,4ngiostrongy/us vasorum,
Crenosoma vu/pis, Aelurostrongy/us abstrusus) In dogs and
cats in Germany and Denmark in 2003-2007. Vet Parasitol
159: 175-180,
Traversa D, Milillo P, Di Cesare A, Lohr B, Iorio R, Pampurini
F, Schaper R, Bartolini R, Heine J (2009) Efficacy and
safety of emOdepside 2.1 %/prazlquantel 8.6% spot-on
formulation in the treatment of feline aelurostrongylosis.
Parasitol Res: 105 Suppl. 1: S83-S89.
Traversa D, DI Cesare A, Briantl E (2015) Lungworm infections.
In: Beugnet F, Halos L (eds.) Parasitoses & vector borne
diseases of cats. Lyon, France: Merla! SAS., pp. 95-106:
ISBN 978-2-9550805-0-4.
Family Filaroididae
Filum (L): thread; oideus (L): similar.
Members of the family Filaroididae are lung parasites
in canids, felids, mustelids and sea lions with peculiar
variations of the life cycles in some species. Whereas
Filaroides martis in mustelids and Os/erus rostratus in
felids are transmitted in indirect cycles with gastropods
as intermediate hosts, F. hirthi and 0. osleri in canids
have direct cycles.
Genus Filaroides
Filaroides hirthi
Disease: Fllaroldosls In dogs.
Agent and life cycle. Adults of F. hirthi are small
nematodes (o'o': 3 mm, without bursa, ��: 12 mm)
which live in the lung parenchyma. Females are
ovoviviparous. Eggs and hatched L l reach the intestinal
tract via trachea and pharynx and are excreted in the
faeces ( ► Figure 10.57). The infectious L1 are directly
ingested by a new host, but they can also be transmitted
by coprophagy or from the bitch to her puppies while
licking them. The larvae invade the intestinal wall and
migrate to the lungs via the portal or the lymphatic route.
In the lungs, the parasites pass through 4 moultings.
Prepatency approximately 5 weeks, patency several
months. L1 may persist in lymph nodes and cause
endogenous autoinfections.
Occurrence and epidemiology. F. hirthi was first
described in 1973 in laboratory beagle kennels in the
USA. Subsequently it spread widely, also to Europe,
predominantly by trading of dogs. When infected
dogs are put In a dog kennel, the infection can easily
spread unnoticed due to direct transmission and the
asymptomatic course of the infection. The parasite was
also found In privately owned dogs.
Pathogenesis and clinlcal signs. F. hirthi infections
in immunocompetent dogs are usually asymptomatic.
However, parasite-induced alterations of the lungs may
be misinterpreted, e.g. in toxicological studies. They
appear as dark to whitish foci, 0.5-20 mm in size, in
which sections of worms can be detected by histology.
Whereas living worms in the lung parenchyma do not
usually provoke tissue reactions, dead worms may induce
distinct tissue lesions. Immunocompromised hosts
develop hyperinfections with severe bronchopneumonia
and may die.
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)

L4
5"slogo
Adult worms

Excretion of
eggs with
Infective L1 larva or L 1

Infective L 1

Figure 10.57. Life cycle of Filaroides hirthl (Graphics: IPZ, S. Ehrat).

Diagnosis. Intra vitam diagnosis is difficult. Eggs and Genus Oslerus

larvae are rarely detected in faeces. Investigation of BAL
may yield better diagnostic results. X-ray examinations
can show small, solid aggregations. Biochemical and
haematological parameters are usually unchanged. Even
at necropsy it is difficult to detect the worm nodules in
the tissue of a collapsed lung. Differential diagnosis must
consider the rare species Fi/aroides mi/ksi.
Therapy and control. Fenbendazole (SO mg/kg
b.w. p.o., twice a day for 5 days) is effective; ivermectin
(increased dose of I mg/kg b.w. s.c. for 2 days) may
also be used and is usually well-tolerated by beagles.
Eradication of F. hirthi infections requires repeated
treatments.
Oslerus osleri (syn. Filaroides osier,)
Disease: Oslerosls In canlds.
Agents, life cycle, and occurrence. 0. osleri
is a cosmopolitan parasite of wild canids (e.g. foxes,
coyotes, dingoes), which occasionally infects domestic
dogs. Oslerus rostratus inhabits the lungs of cats. The
adults ofO. osleri (o'o': 6 mm,��: 12 mm long) live in
nodules in the mucosa of trachea and bronchi. Females
release larvated eggs through small openings of the
nodules to the respiratory tract. Eggs or LI are excreted
in faeces. LI are transmitted to the puppies early in their
life by the bitch, e.g. by licking or, in wild canids, by
feeding regurgitated food. The subsequent development
Part Ill. Parasites and parasitoses: metazoa
corresponds to that of F. hirthi. Prepatency lasts 5-6
weeks; adults survive for years.
Pathogenesis and clinical signs. Several parasites
are usually found together in nodules in the mucosa of
the trachea and bronchi. Nodules measure up to 10 mm
in diameter. Dogs show chronic coughing and often
impaired respiration.
Diagnosis and therapy. Detection of larvated eggs
and L1 in faeces or in BAL. Nodules can be easily
demonstrated by endoscopy. According to case reports
dogs were successfully treated with ivermectin (0.2-0.4
mg/kg b.w. s.c.) resulting in the resolution of nodules
within 2 weeks. However, relapses are common and
may require repeated applications. Benzimidazoles
(fenbendazole, oxfendazole) need to be administered
for weeks to show efficacy.
Selected references
Anderson RC (2000) Nematode parasites of vertebrates. Their
development and transmission. 2nd ed. Wallingford, UK: CAB
International: ISBN 0-85199-421-0.
Bauer C, Bahnemann R (1996) Control of Rlaroides hirthi
infections in Beagle dogs by ivermectin. Ve t Parasitol 65:
269-273.
Caro-Vadlllo A. Martinez-Mer1o E, Garcia-Real I, Femin­
Rodriguez ML, Mateo P. (2005) Verminous pneumonia
due to Alaroides hlrthl in a Scottish terrier in Spain. Vet Rec
157: 586-589.
Chaoqun Y, O'Toole D, Driscoll M, McFarland W, Fox J,
Cornish T, Jolley W. (2011) Alaroides osleri (Oslerus os/en):
two case reports and a review of canid Infections in North
Amooca. Vet Parasilol 179: 123-129.
Dunsmore JD, Spratt OM ( t 979) Tho lite history of FilarokJes
os/oo in w'�d and domasUc conids In Austrnlla. Vet Parasitol
5: 276-286.
Outerbrldge CA, Taylor SM ( 1998) Oslefl.Js oslort
tracheobronchft1s: trootmont wit/1 tvoonac1in In 4 dogs. can
Vet J 39: 238-240.
10.1.3 Order Ascaridida
Acaris (G): worm, intestinal worm.
The species of veterinary importance belong to the
superfamilies Ascaridoidea and Heterakoidea. Another
superfamily (Cosmocercoidea) is discussed in context
with the Oxyurida ( ► p. 343).
Adults of Ascaridida parasitise the intestinal tract of all
classes of vertebrates. Numerous species are important
parasites of domestic and wild animals and of humans.
Larval stages of several species are zoonotic agents.
- Superfamily Ascaridoidea (large
intestinal roundworms, ascarids)
Ascaridoidea (ascarids) are in the adult stage whitish,
spindle-shaped, medium-sized to large worms up to
40 cm long and 5 mm wide ( ► Figure 10.58). The oral
opening is mostly surrounded by 3 large lips ( ► Figure
I 0.59), the anterior end of several genera have cervical
alae ( ► Figure I 0.63, p. 332). The posterior end of the
cylindrical oesophagus may be expanded to a ventricle
(► Figure 10.63). In some genera the ventricle and/
or the intestine have formed characteristic diverticles.
Males with 2 spicules, posterior end without bursa,
sometimes with small lateral alae. Males and females
often with characteristic pre- and postanal papillae.
The life cycles of the Ascaridoidea are either direct or
indirect. Females release unsegmented, thick-shelled
eggs ( ► Figure I 0.5, p. 257).
Figure 10.58. Parascaris equorum In small Intestine of a zebra
(Photo: IPZ).
Figure 10.59. Parascaris equorum: anterior end with lips (PhOto:
IPH).
,, 10. Phylum Nematoda (syn. Nematozoa) (threadworrns or roundworms)
Family Ascarididae
• Subfamily Ascaridinae
Genus Ascaris
Ascaris suum (large roundworm of pigs)
■
Disease: Ascariosls in swine.
Ascaris (G): worm; sus (L): pig.
Ascariosis is one of the most frequent helmintic
infections of pigs with considerable economic impact.
Summary
• Agent. Nematodes of the small Intestine of domestic
pigs and wild boars, up to 30 cm In length. Females
produce numerous unsegmented eggs, which are
excreted In the faeces. An Infectious L3 develops Inside
the egg within 2 weeks to several months. Infection by
Ingestion of eggs with L3. Larvae hatch In the small
Intestine; migration via liver, lungs, alveoles, trachea,
pharynx to the small Intestine (tracheal migration route).
Prepatency 6-8 weeks.
Occurrence, epidemiology. Cosmopolitan distribution,
often with high prevalences, especially In fattening pigs.
Eggs may survive In soil of paddocks and pig slurry for
months. The development of patent worm populations
Is promoted by the ingestion of low or moderate egg
numbers, whereas high Infection doses usually lead to
rapid ellmlnatlon of larvae from the Intestine.
Immunology. Frequently development of a distinct
immunity, resulting In early trapping of larvae from
reinfections.
Pathogenesis, cllnlcal signs. Liver: 'milk spots',
whitish , temporary lesions In reaction to migrating
larvae (hepatitis lnteratltlalla parasltarla multiplex).
Lungs: haemorrhages, oedemas and transient
cellular Infiltrates. Intestine: thickening of the tunlca
muscularls, atrophy of vllll, after beginning of patency
reduced N-retentlon, Impaired fat digestion and lactose
intolerance with diarrhoea.
Diagnosis, therapy, control. Egg detection by faecal
examination (flotation techniques). All anthelmlntlcs
licensed for pigs are effective against adults; larval
stages are affected by certain benzlmldazoles and
macrocyclic lactones. Control by combining hygiene
measures with strategic treatment.
Agent. The adults of A. suum are large yellowish,
cylindrical nematodes tapering at both ends. The males
are 15-25 cm long, the females 20-35 cm, the latter with a
diameter up to 5 mm. The mouth opening is surrounded
by 3 distinct serrated lips. The posterior end of the male
is slightly bent ventrally, a bursa copulatrix is absent, but
it has groups of papillae and 2 spicules measuring 2-3
mm in length. The vulva in females is located at about
½ of the body length from the anterior end. Eggs: oval,
50-75x45-55 µm, unsegmented, thick-shelled, brownish,
sticky outer protein layer with irregular protrusions
( ► Figure 16.15, p. 547). A. s1111111 is closely related
to A. lumbricoides from humans (see below, zoonotic
importance).
Life cycle. Adult A. mum inhabit the lumen of
the small intestine, predominantly of the jejunum
( ► Figure 10.60). In the direct life cycle unsegmented
eggs are passed in the faeces to the environment where
an infectious L3 develops within the egg shell. This
development depends on temperature and takes 2-3
weeks under favourable laboratory conditions (28 °C,
high moisture, access of oxygen), but lasts much longer
in the natural environment (see below). Larvated eggs are
ingested by pigs; the larvae hatch in the small intestine,
invade veins of the caecum and proximal colon, and
reach the liver after 6-24 hours via the portal system.
From the liver they are transported via hepatic veins to
the heart and lungs where some larvae can be found as
early as 4 days p.i. There is evidence that some larvae
may enter the lymphatic system in the intestine and
migrate via the thoracic ducts to the lung. In the lung the
larvae penetrate the alveolar walls, pass into the trachea,
migrate to the pharynx, are swallowed and reach the
small intestine 8-10 days p.i. During migration (tracheal
migration route) the larvae moult into L4, and a final
moult into adults occurs at the earliest 25 days p.i. in
the intestine. The prepatent period lasts 6-8 weeks; the
U)
parasites may live for 7-10 months. Prenatal infections .c
do not occur in the life cycle of A. suum.
.E
o5
Occurrence and epidemiology. A. suum is a I
cosmopolitan, common pig parasite which may play
an important role in all types of pig husbandry (indoor,
outdoor, SPF or organic systems). Highest prevalences
are usually found in fattening pigs. For example, in one
study a prevalence increase from 10 to 33% was observed
over the course of the fattening period, although the
animals had been treated with effective anthelmintics in
the meantime. Older animals are generally less frequently
infected, though a relatively small proportion of breeding
sows may shed considerable numbers of eggs.
Factors of epidemiological importance are the high
reproductive potential of the parasites, a slow exogenous
development, the remarkable tenacity of the eggs, the
transmission modes in pig farms, and the dominant
role of immunity in regulating the worm population.
• Reproductive potential, exogenous develop­
ment, tenacity of eggs. Ascaris spp. have a high
reproductive potential, with an estimated daily
production of >200,000 eggs per female, and a
correspondingly high capacity to contaminate the
environment. Eggs embryonate slowly: the formation
of the infective L3 in the egg takes 4-8 weeks at room
temperature. The development suspends below 15 °C.
Part Ill. Parasites and parasitoses: metazoa

rJi-="
Adult worms:
female (above), male (below)

'
- - ··:. . 'i',
....
Developing eggs
Egg with
lnfaotfve L3

Figure 10.60. Life cycle of Ascaris suum (Graphics: IPZ, S. Ehrat).

Under stable conditions, eggs may reach infectivity only infected animals or indirectly by pig slurry. Keeping
after months. Under dry and sunny outdoor conditions, pigs in groups, particularly at high density, enhances
larvated A. suum eggs in pig faeces survive 2-4 weeks, the exposure. In case of young, susceptible animals
but 90% of the eggs are found vital after 8 weeks when low infection doses (in piglets approximately 50 eggs
placed in a shaded humid environment. In moist soils, per day) are sufficient to induce an intestinal. fertile
eggs may remain infectious for 5 years, but most of them worm population.
die within l year. Eggs can survive in raw pig slurry at
18 °C for approximately 3 months, and according to • Population biology. The population biology is
other sources at 25 °C even up to 8 months. Ensiling complex and basically influenced by immune reactions of
has hardly any effect on embryonated eggs. Due lo the the hosts. Worm burdens in groups of naturally infected
slow and variable larval development and their high pigs exhibit an overdispersed frequency distribution
tenacity, there is no seasonality of infection. Under stable so that, for example, approximately l 0% of the animals
conditions exposure is usually highest in autumn and carry 80% of the worms. Usually, the worm burdens are
winter. relatively low ( <40 worms per animal). Low infection
doses usually lead to larger worm burdens than high
• Transmission in pig populations. Transmission doses. In fact, after a primary infection, numerous larvae
of the infection occurs by the faeco-oral route. Eggs may be present in the small intestine 10 days p.i., but
with their sticky outer layer may adhere to the skin of a large proportion will be excreted already after 2-3
the animals, to walls and floors of stables, to equipment, weeks, resulting in a small residual population evolving
etc., thus increasing the environmental contamination. to maturity. Rather stable worm populations develop
Furthermore, they can readily be spread by people, when piglets - starting in the 1 s1 week of life - are
pigs and insects or by means of transport vehicles. continuously infected with small amounts of larvated
Pastures may be contaminated with eggs directly by eggs. In this case almost all animals will develop patent
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)

infections with relatively small numbers of adult worms

which persist in fatteners until slaughtering. Genetic
differences in susceptibility to A. suum infections exist
between various pig breeds and may play a role in
regulating worm populations.

Pathogenesis and clinical signs. First lesions

occur in the liver as a reaction to migrating larvae.
Within about a week so-called milk spots arise, initially
as small (1-2 111111) whitish, diffusely demarcated foci
which may later expand to larger lesions of> IO 111111
(hepatitis interstitialis parnsitaria multiplex) ( ► Figure
10.61 ). Milk spots are foci of granulation tissue and Figure 10.61. Ascaris suum: pig liver with 'milk spots' (Photo:
later of connective tissue formed around small necroses IPG).
of the liver parenchyma caused by migrating or dead
larvae. Furthermore, small spots of lympho-plasmatic
or lymphonodular patterns ure formed, coinciding
with healing. Reinfections induce lower numbers of
milk.spots because fewer larvae reach the liver (see below,
immunology). In the lungs haemorrhages are caused by
larvae migrating from the capillaries into the alveolar
space. Re-infections induce cellular, predominantly
eosinophilic infiltrations and local oedemas ( ► Figure
10.62). The infection of the intestine results in goblet cell
hyp erplasia, mastocytosis and eosinophilic infiltration
of the mucosa, swelling of the tunica muscularis, and
atrophy of the villi in the parasitised gut segment.

A. suum infections in pigs are usually asymptomatic.

However, the infection may be associated with
reduced food intake and stunted weight gain. Further
consequences are impairment of lactase activity in the
intestinal mucosa associated with osmotic diarrhoea
('chewing gum diarrhoea'). Health impairment and
liver condemnation at slaughter may incur considerable
economic loss, depending on the intensity of the
infection. Migrating larvae of A. suum may also affect
liver and lungs of other animals (e.g. sheep, calves) and
humans (see below, zoonotic importance).
Immunology and genetic influences. A. suum
infections stimulate specific cellular and humoral
immune ·reactions in pigs. A sequence of antibodies
(IgM, IgE, IgA, IgG) against stage-specific antigens is
induced reflecting the route of larval migration and
development. Infected animals develop a distinct Th2
type response with continuously increasing specific lgE
levels and - after re-infections - marked eosinophilia.
The Th2 dominated response suggests an important
role of humoral antibodies in protective immunity.
Consequently, lactogenously transmitted maternal
antibodies of chronically infected sows may protect
the litters from A. suum infections to a certain degree.
Immune reactions regulate both primary and challenge
A. suum infections. The expulsion of the largest
proportion of larval stages 3-4 weeks after a massive
primary infection is regarded as a self-cure reaction
on allergic basis ( ► p. 33) which - in contrast to
Figure 10.62. Ascaris suum: numerous haemorrhagic lung
lesions after heavy primary Infection (Photo: IPZ).
trichostrongylid infections - takes place independently
of a challenge infection. This reaction is associated with
eosinophilia and accumulation of intra-epithelial T cells
in the jejunum.
Pigs which are continuously exposed to Ascaris
infections under natural conditions gradually develop
a protective immunity by which many of the larvae
acquired by challenge infections are already trapped
and eliminated by ADCC reactions before they reach
the liver (prehepatic barrier), resulting in fewer milk
spots than after primary infections. Larvae which had
escaped these attacks can be subsequently decimated in
liver and lungs. This immunity depends on the presence
ofadult worms in the intestine (concomitant immunity).
Thus, chemotherapeutic elimination of adult ascarids
under natural conditions is in general rapidly followed
by a resettlement of the intestine by larvae.
 Part Ill. Parasites and parasitoses: metazoa
The infection intensity of A. suum in pigs is genetically
controlled with high heritability. QTL (quantitative trait
loci) which are associated with low susceptibility of pigs
are meanwhile known and can be used for selection in
breeding measures. Since corresponding mechanisms
seem also to act in Trichuris suis infections, synergistic
effects could contribute to the partial resistance.
Diagnosis. Patent infections can easily be diagnosed
by detection of the typical eggs (S0-70x40-60 µm)
(► Figure 16.15, p. 547) in faecal samples (flotation
techniques). However, false negative results may be
obtained when massive infections remain impatent. On
the other hand, coprophagy should be considered as a
reason for false positive results. Serological techniques
are currently not available for practical application. Milk
spots are detectable at meat inspection. Similar lesions
are caused by migrating Toxocara larvae ( ► p. 337).
Therapy and control. Levamisole, several benzimi­
dazoles and macrocyclic lactones are highly effective
against adult A. suum ( ► Table 19.8, p. 589). In addition,
macrocyclic lactones and some benzimidazoles exhibit
a variable effect against migrating larval stages. The
anthelmintics are administered predominantly orally as
feed additives, usually for several days, or parenterally.
In-feed administration over several days ensures a
more consistent drug intake, and an enhanced effect
against migrating larvae. Control campaigns have to
combine strategic treatments und hygienic measures.
The permanent maintenance of high hygiene standards
is of major importance. Control measures against Ascaris
( ► p. 587) also affect other gastrointestinal nematodes
(Oesophagostomum, Trichuris suis), depending on the
anthelmintics used.
Zoonotic Importance. A. suum of pig origin and
A. lumbricoides of human origin are morphologically
indistingui.shable, but differentiation is possible using
a combination of molecular markers. A recent study
has identified numerous hoplotypes of Ascaris worms
from various geographical regions with some of them
being more abundant in oscarids from human or
from pigs, respectively. Cross-infections of humans
with A. suum and of pigs with A. lwnbricoides are
experimentally confirmed and have revealed preferences
Q)
c. of the 'appropriate' host with regard to establishment of
n
0
the infection and development 10 patency. Molecular
� and epidemiological studies provided evidence that
� cross-transmission al o occurs under natural conditions.
nl
C Essentially, all human Ascaris infections studied so far
·;::
in Europe (DK, UK) originated from pigs.
J
C
>­
Cl
0
0
·u5
co
0..
Selected references
Betson M, Nejsum P, Bendall RP, Deb RM, Stothard JR (2014)
Molecular epidemiology of ascariasis: a global perspective
on the transmission dynamics of Ascaris in people and pigs.
J Infect Dis 210: 932-941.
Carstensen L, Vaarst M, Roepstorff A {;'r l12) Helminth infection
in Danish organic swine herds. Vet P,i·asitol 26: 253-264.
Cavallero S, Snabel V, Pacella F, Perr:me V, D'Amelio S
(2013) Phylogeographical studies oi .. 1 .=:caris spp. based on
ribosomal and mitochondrial DNA sequences. PLoS Negl
Trap Dis 7: e2170.
Dold C, Holland CV (2011) Asacris a11d ascariasis. Mirobes
Infect 13: 632-637.
Katakam KK, Roepstorff A, Popovic 0, Kyvsgaard NC,
Themsborg SM, Dalsgaard A (2013) Viability of Ascaris
suum eggs in stored raw and separated liquid slurry.
Parasitology 140: 378-384.
Mejer H, Roepstorff A (2006) Ascaris suum infection in pigs
born and raised on contaminated paddocks. Parasitology
133: 305-312.
Nejsum P, Roepstorff A, Jorgensen CB, Fredholm M, Goring
HH, Anderson TJ, Thamsborg SM (2009) High heritability
tor Ascaris and Trichuris infection levels in pigs. Heredity
102: 357-364.
Nejsum P, Thamsborg SM, Petersen HH, Kringel H,
Fredholm M, Roepstorff A (2009) Population dynamics
of Ascaris suum in trickle-infected pigs. J Parasitol 95: 1048-
1053.
Nejsum P, Betson M, Bendall RP, Thamsborg SM, Stothard
JR (2012) Assessing the zoonotic potential of Ascaris suum
and Trichuris suis: looking to the future from an analysis of
the past. J Helminthol 86: 1 48-155.
Roepstorff A, Mejer N, Nejsum P, Thamsborg SM (2011)
Helminth parasites in pigs: New challenges in pi g production
and current research highlights. Vet Parasitol 180: 72-81.
Vlamlnck J, Levecke B, Vercruysse J, Geldhof P (2014)
Advances in the diagnosis of Ascaris suum infections in
p igs and their possible applications In humans. Parasltology
141: 1904-1911.
Genus Parascarls
Parascaris equorum (ascarid or large
roundworm of horses).
Disease: Parascanosis In equines.
Par- (G): besides; ascaris (G): worm; equ14s (L): horse.
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)
Summary
• Agent, life cycle. P. equorum Is a large nematode up
to 40 cm ( c;') parasitising the small intestine of equicls.
Oral Infection with larvated (L3) eggs, tracheal migration
route. Prepatency 10-16 weeks.
, Occurrence, epidemiology. Cosmopolitan, predomi­
nantly in foals and yearlings. Infections on pasture and
in the stable. Eggs remain vital and infectious for yein.
, Clinical signs, immunology. Haemorrhagic lesions
in the liver. Sometimes coughing, nasal discharge and
fever during the lung phase. Heavy intestinal infections
may cause diarrhoea and colic; possible complk:atlona:
obstruction and perforation of the Intestine. With
increasing Immunity elimination of larvae in liver and
lungs.
• Diagnosis, therapy, control. Coproacoplcal detection
of eggs. Therapy with benzimidazoles, macrocycllc
lactones (consider drug resistant populations) or
pyrantel derivatives. Control by regular removal of
faeces and strategic treatments.
Agent and life cycle. The adults of P. equorum
are large, yellowish nematodes (oo: 15-28 cm,��:
18-40 cm long) inhabiting the small intestine. Eggs:
globular, 90-100 µm, unsegmented, thick-shelled
with brown outer protein layer ( ► Figure 16.13). The
development corresponds to that of A. suum ( ► Figure
10.60). Prepatency 10-16 weeks, patency up to 2 years
but mostly < I year. Old observations have suggested
that two Parascaris species exist, namely P. univalens
and P. equorum. These species are morphologically
indistinguishable but the former has only one germline
chromosome pair whereas the latter has two. Currently,
the validity of these observations and their potential
practical significance are being investigated. In this text
we refer only to P. equorum.
Occurrence, epidemiology. P. equorum occurs all
over the world in horses, donkeys and other equids,
mainly in foals and yearlings. In a survey (2013) in the
UK comprising about 1,221 horses, 38% of the animals
<I year, 4% of the yearlings and only up to 3% of the
older horses were shedding Parascaris eggs. Necropsics
of foals may yield sometimes several I 00 to l 000 ascarids
(► Figure 10.58).
In the environment development ofL3 in eggs occurs at
ambient temperatures > l O °C and takes approximately
2 weeks at 25 °C. The eggs are very resistant to adverse
environmental conditions and may survive on pasture up
to several years. Horses contract the infection in stables,
paddocks or on pastures, favoured b y the fact that the
sticky eggs may adhere to walls of stables,plants, etc. and
are thus easily accessible to horses. Coprophagia may also
play a role in transmission. Foals often become infected
in the first days or weeks of life and may shed eggs as
early as I 0-16 weeks after birth. The most intensive egg
excretion is observed under natural conditions in 4-5
months old foals, which in individual cases may amount
to millions of eggs per day. Thereafter, egg excretion
decreases continuously. Thus. foals are the principal
contaminators of pastures and the environment with ro
P. equorum eggs. -0
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ro
Pathogenesis, immunology, clinical signs. u
(f)
Migrating larvae induce focal liver damage with
haemorrhages and subsequent lesions which resemble
the milk spots In A. s1111m Infected pigs. The larvae
migrating from blood capillaries into the alveoles of the
lungs cause pctechial bleeding and focal oedemas. Initial
eosinophilic perlvascular and peribronchlolar infiltrates
become modified later on by Invading lymphocytes. A
proportion of the larvae is encapsulated in lhe lungs,
whereupon approximately 3 weeks after primary
infection subpleural knots of up to I cm in size develop,
which may persist for weeks and contain remnants of the
larvae. These reactions arc enhanced after re-infections.
The lung phase may be associated with coughing, nasal
discharge und fever. Heavy intestinal infections may
result in variable inappetence, progressive lethargy, colic
and diarrhoea. Affected horses show a lacklustre coat
and may lose weight. The pathogenesis presumably
corresponds to that of Ascaris infections of pigs. Known
complications of heavy worm burdens are intestinal
obstruction and perforation followed by peritonitis. Bile
-
ducts are occasionally invaded by ascarids.
(f)
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Immunology. Exposed horses develop a partial
immunity at the age of 4-6 months. Horses are obviously
.E
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not capable of eliminating juvenile ascarids from the ::r:
intestine by a self-cure reaction as is witnessed in A.
suun, infected pigs.
Diagnosis. Coproscopical detection of the eggs
(flotation techniques). Infected foals usually shed
large amounts of eggs. Sometimes preadult worms
are eliminated with faeces during prepatency. During
the lung phase bronchial mucus accumulation and
eosinophilia in mucus samples may be detected by
endoscopy.
Therapy and control. Benzimidazoles, macrocyclic Q)
lactones and pyrantel derivatives are effective against
·u
C
adults and juvenile stages in the intestine ( ► Table
19.10, p. 592). Resistance to macrocyclic lactones,
Q)
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particularly to ivermectin, is reported from Europe
-
and other regions. Regular cleaning of the stables and C
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weekly removal of the faeces from pastures combined Q)
with strategic treatment are suitable control measures Q)
(► p. 596). .£;
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 Part Ill. Parasites and parasitoses: metazoa
- Selected references
Clayton HM (1978) Ascariasis in foals. Vet Rec 10: 553-556.
Cribb NC, Cote NM, Boure LP, Peregrine AS (2006) Acute
small intestinal obstruction associated with Parascaris
equorum infection in young horses: 25 cases {1985-2004).
N Z Vet J 54: 338-343.
Jabbar A, Littlewood DT, Mohandas N, Briscoe AG, Foster
PG, Muller F, et al. (2014) The mitochondrial genome of
Parascaris univalens - implications for a 'forgotten' parasite.
Parasit Vectors 7: 428.
Lyons ET, Tolliver SC, Kuzumina TA, Collins SS (2011) Further
evaluation by field tests of the reactivity of three anthelmintics
(fenbendazole, oxbendazole, and pyrantel pamoate) against
the ascarid Parascaris equorum in horse foals on eight farms
in Central Kentucky (2009-2010). Parasitol Res 109: 1193-
1197.
Nielsen MK, Wang J, Davis R, Bellaw JL, Lyons ET, Lear TL,
Goday C (2014) Parascaris univalens - a victim of large-scale
misidentification? Parasitol Res 113: 4485-4490.
Reinemeyer CR (2009) Diagnosis and control of anthelmlntic
resistant Parascaris equorum. Parasit Vectors 2: 58.
Von Samson-Himmelstjerna G, Fritzen B, Demeler J,
Schurmann S, Rohn K, Schnieder T, Epe C (2007) Cases
of reduced cyotostomin egg reapppearance period and
failure of Parascaris equorum egg count reduction following
ivermectin treatment as well as survey on pyrantel efficacy In
German horse farms. Vet Parasitol 144: 74-80.
Genus Toxascaris
Toxascaris leonina
Disease: Toxascarlosls in dogs and cats.
Lips
Q)
C Cervical alae
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C
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C
Intestine
>,
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Toxocara cati
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Figure 10.63. Anterior ends of Toxocara and Toxascaris (Graphics: IPZ, M. Mathys).
Toxon (G): bow; ascaris (G): worm; lea (L): lion.
Agent. Adults of T. leonina with long, small cer vical
alae, oesophagus without ventricle (cf.Toxocara)
(► Figure 10.63), o'o' 4-7 cm,�� 5-12 cm long.Eggs:
see below, diag nosis.
Life cycle and epidemiology. The parasites inhabit
the small intestine of carnivores. Unsegmented eggs are
shed with the faeces and develop into L3 at temperatures
of 17-22 °C within 1 week. Infectim1 of a new host takes
place by oral ingestion of larvated ::1�g, or paratenic hosts
containing L3 (e.g. mice). After :nfection with eggs,
larvae hatch in the small intestin,:. :i1ost of them invade
the intestinal wall, moult into L4, ,: nd return to the gut
lumen where they mature into adl,lts. A few L3 start a
somatic migration in the course of which liver, lungs,
musculature and other organs are invaded. Prepatency
(after infection with larvated eggs): 7-10 weeks. After
ingestion of infected paratenic hosts a corresponding
development is observed, but the prepatency is shorter.
Occurrence. T. leonina has a worldwide distribution.
It is easily transmittable from dogs to cats and vice
versa, and can infect numerous wild felids (lion, tiger,
leopard, and cheetah) and canids (various species of
foxes, raccoon dog, wolf, jackal, dingo and others)
(e.g. up to 60% of red foxes in the region of Geneva,
Switzerland,were infected). The prevalences in dogs and
cats in Central Europe are distinctly lower than those of
Toxocara spp., e.g. 0.5 and 1.3% of dogs were infected in
southern and western parts of Switzerland, respectively;
cats in Germany were infected at a rate of 0.3%.
Pathogenesis, clinical signs. T. leonina is of low
pathogenicity,but heavy infections may cause enteritis.
Toxocara canis Toxascaris leonina
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)
Diagnosis, therapy and control. Coproscopical
detection of eggs (flotation techniques). Eggs are 76-95
µm in size, globular to elliptic, surrounded by a thick,
lightish, smooth shell. They can be easily distinguished
from Toxocara eggs ( ► Figure 16.16, p. 549). Effective
anthelmintics ( ► Table 19.14, p. 600 ff). Control
measures recommended for Toxocara spp. ( ► p. 605)
are also effective in case of T. leonina.
Genus Baylisascaris
Baylisascaris procyonis
Disease: Baylisascariosls in carnivores.
B. procyonis, a common intestinal parasite of raccoons
(Procyon lotor) and related procyonids, attains sexual
maturity also in dogs but not in cats. It occurs in North
America, Asia and focally in Europe (prevalence in
raccoons >80% in various areas of the USA; in central
Germany 71%). Definitive hosts acquire the infection
either by ingesting eggs or paratenic hosts containing
infective larvae. Humans may become infected by
accidental uptake of larvated eggs resulting in neural,
ocular, visceral or unapparent 'larva migrans' ( ► p.
337). Also other species of the genus Baylisascaris are
considered potential zoonotic agents.
Anderson RC (2000) Nematode parasites of vertebrates. 2nd
edit. Wallingford, UK: CAB International; ISBN 0-85199-
421-0.
Bauer C (2013) Baylisascariosis - infections of animals and
humans with 'unusual' roundworms. Vet Parasitol 193: 404-
412.
Ingle ME Dunbar SG, Gathany MA, Vasser MM, Bartsch
JL, Guffey KR, Knox CJ, Nolan AN, Rowlands CE, Trigg
EC (2014) Predicting Baylisascaris procyonis roundworm
prevalence, presence and abundance in raccoons (Procyon
lotor) of southwestern Ohio using landscape features. Int J
Parasitol Parasites Wild! 3: 113-117.
• Subfamily Toxocarinae
Summary
• Several Toxocsra spp. of the subfamily play an Important
role as parasites of the small Intestine of domestic
animals and as zoonotlo agents.
ro
• Agents, occurrence. Up to 19 cm long(��) common, 'O
i5
cosmopolHan nematodes of carnivores. Toxocara canls ·;;:::
ro
In dogs and other canlds, T. call (syn. T. mystax) In cats (.)
and other fellds; T. malayensls In cats In Malaysia and
China, T. vltulorum In large ruminants.
T. a.nl• ind r. 011t/
Life cycle, epldemlology. Eggs are shed with faeces
of the final hosts. Development of Infectious L3 Inside
the eggs In the environment. Final hosts can become
Infected with T. cants by several routes: (a) horlzontally
by oral Ingestion of eggs or paratenlc hosts containing
L3, (b) vertically by prenatal or lactogenlc transmission
of L3 from the bitch to the puppies. Vertical transmission
lmplles a somatic migration of the larvae or a reservoir
of hypoblotlc larvae In the bitch. In dogs, prenatal
Infections are of particular epldemlologlcal Importance.
Puppies Infected by this route may shed large amounts
of eggs already at an age of 3 weeks and heavily
contaminate the environment. T. est/ Is transmitted by
the same routes except the prenatal Infection.
Pathogenesis, cllnlcal signs. Massive Toxocara
Infections cause vomiting, gastroenterHls, diarrhoea,
retarded growth and rarely death In puppies of dogs
and cats.
1 • Dlagnosla, therapy, control. Coproscoplc detection
of eggs (flotation techniques); during prepatency
occaslonal excretion of Immature stages with the faeces.
Treatment of Intestinal Infections with benzlmidazoles,
pyrantel, macrocycllc lactones, emodepslde. Control
by strategic treaiment and hygienic measures.
• Zoonotlc Importance. Eggs containing L3 of T. canis
and T. cat/ are Infectious for many animal species (e.g.
rodents, pigs, monkeys, birds) and humans. Larvae
take a somatic migration route In these hosts and infect
various organs (lungs, liver, musculature, CNS, eyes
and others); In tissues they can persist for many years.
Several forms of larva mlgrans (unapparent, visceral,
ocular, and neural) are caused In humans.
T. vltulorum
• Occurs in cattle and buffaloes particularly in warm
climates; very rare in Central Europe. Lactogenic
Q)
transmission to calves with subsequent patent C
infections only in young animals up to 6 months. ·c3
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Genus Toxocara ro
C
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Toxocara canis
C
Disease: Toxocamsis in dO§S and otliler canids.
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Toxon (G): bow; kara (G): head; canis {L): dog.
 Part Ill. Parasites and parasitoses: metazoa
Agent. Adult T. can is: d d 10-12 cm, � � 12-18 cm long
with 3 lips, long and narrow cervical alae and oesophagus
with ventricle, male with 2 spicules( ► Figure 10.63).
Eggs: see diagnosis below.
Life cycle. Adult T. canis inhabit the small intestine
of dogs, foxes and other canids. Females release
unsegmented eggs which are passed in the faeces
(► Figure 10.64). In the environment infective L3(not
L 2!) develop in the eggs in 2 weeks at 25-30 °C or in
8 weeks at 12-18 °C. Dogs may contract the infection
by various transmission routes: (a) ingestion of eggs
or paratenic hosts containing L3, and (b) prenatal or
lactogenic transmission of L3 from the bitch to puppies.
Furthermore, nursing bitches can become infected by
ingestion of L4 or older stages excreted by heavily
infected puppies.
• t Life cycle and migration routes in definitive hosts .
In the definitive host the parasites migrate on different
routes which are partly used in parallel (tracheal or
somatic migration)( ► Figure 10.65).
• Tracheal (or lung-tracheal) migration. After oral
ingestion of larvated eggs the L3 hatch, penetrate the
intestinal wall, enter the blood stream and reach the liver
within 1-2 days p.i. Subsequently they are transported
to the lungs arriving there 3-5 days p.i. Larvae which
are trapped in the capillaries of the liver migrate in
liver parenchyma causing tissue damage (see below,
pathogenesis). In the lung the larvae invade the alveoles,
moult into L4 and migrate via trachea and pharynx to
the small intestine where they arrive approximately 10
days p.i. After a final moult they attain sexual maturity.
Prepatency lasts 30-39 days in young dogs, slightly
longer (40-56 days) in dogs over I year old. The mean
life span of the parasite is approximately 4 months.
Some of the larvae may be distributed from the lung
via the circulation to various organs(see below, somatic
migration).
The tracheal migration with subsequent sexual
maturation of the parasites in the intestine happens
predominantly in young dogs, up to an age of 3 months.
With increasing age the somatic migration predominates
Figure 10.64. Toxocara canis (length up to 15 cm) in small
intestine of a puppy (Photo: IPZ).
(see below). Whether a patent infection is built up at al l
depends on the infection dose. Experimental infections
with small amounts of larvated eggs(100 eggs/animal)
resulted in patent worm populations in young as well as
in older recipients. This was independent of whether the
dogs were immunologically na"ive or had experienced
prior prenatal or repeated postnatal T. canis infections
and whether the dogs were or were not treated during
prepatency. In contrast, high infection doses(10,000
eggs/animal) failed to produce adult worms even in
puppies. Tracheal migration occ lirS also after prenatal
and lactogenic infections(in the latter case prepatency
is 27-35 days).
• Somatic migration. The somatic route is taken
after infection of older dogs with infective eggs
(► Figure 10.65B). The L3 invade the gut wall, enter
the blood circulation and are t ransported to the lungs
where they are trapped in capillaries, penetrate their
walls and migrate through the tissue to re-enter the
blood stream which carries them to various organs
(musculature, liver, kidney and others). Approximately
I week p.i. they accumulate in striated muscles, where
they can survive for years in a hypobiotic stage.
When the larvae have settled in a female dog, there
are several options for vertical transmission(► Figure
10.65B):
Prenatal (transplacental) transmission. Hypobiotic
larvae in pregnant bitches are hormonally activated
in the last third of pregnancy starting approximately
42 days after conception (compare Ancylostoma
caninum ). Activated larvae invade the blood stream,
pass through the placenta to the fetus and infect
various organs, predominantly the liver. Also
larvae which are newly acquired by an infection
during pregnancy can infect the fetus after somatic
migration in the bitch. In puppies the cycle is
completed immediately after birth by migration of
the larvae to the intestine on the tracheal migration
route. Patency with egg shedding begins at an a ge
of 21-25 days in these puppies. Since not all of the
hypobiotic stages in the bitch are activated during
pregnancy, several of the subsequent litters may
become infected, even though the bitch has not
acquired new infections in the meantime.
Lactogenic (transmammary) transmission.
Migrating T. canis larvae can reach the mammary
glands of a bitch via the circulation or by somatic
migration and may subsequently be transmitted in
the milk to the puppies( ► Figure 10.658). Which
type of infection (prenatal or lactogenic) prevails.
depends on the time of infection of the bitch.
Prenatal infections pre-dominate after a primary
infection of a bitch before and up to the last quarter
of the pregnancy, whereas lactogenic transmission
prevails when infections occur at a later stage of the
pregnancy. Excretion of infectious L3 with the milk
r 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundw orms)
A. Tracheal migration route
Paratenic
host
L4/5th stage
Figure 10.65. Life cycle of Toxocara canis (Graphics: IPZ, S. Ehrat).
of a bitch starts a few days after birth of the puppies,
reaches a maximum in the 2nd and 3 rd week and
may last throughout the whole lactation period.
Prepatency after lactogenic transmission lasts 27-
35 days.
• Faeco-oral transmission of T. canis stages
from puppies to the bitch. Infected puppies often
excrete immature T. canis stages with the faeces. While
caring for the puppies the bitch may ingest these stages
which can settle in the intestine and develop to sexual
maturity.
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• Transmission of infective larvae in paratenic
hosts. A broad spectrum of animals (e.g. rodents,
lagomorphs, livestock, birds, amphibians, earth worms)
may accidentally ingest larvated T. canis eggs and
harbour L3 for prolonged periods. When eaten by a
definitive host these stages settle without migration in
the intestine and develop to maturity with a prepatency
of approximately 1 month(► Figure 10.65).
Occurrence and epidemiology. T. canis is found
worldwide in dogs, foxes, raccoon dogs, wolves, and
other canids. Toxocara larvae may be transmitted
from infected bitches to all of their litters. In Europe
Part Ill. Parasites and parasitoses: metazoa
approximately 20% of young dogs and 3-7% of older
dogs(>6 months) were reported to shed Toxocara eggs.
A recent study in NL revealed egg shedding in 4.6%
(n=916) of household dogs; dogs aged between 6 and
12 months had a higher prevalence (7.8%) than dogs
of 1-7 years of age (3.3%). There were no differences
in prevalences between dogs living in urban, rural or
woody environments, but kennelled and coprophagic
dogs had significantly higher prevalences than dogs
which were not kennelled or coprophagic. Coprophagy
can be an important confounding factor in diagnosis
(see below). Toxocara prevalences in European foxes
may amount to 70%.
In epidemiology, the prenatal transmission of T. canis
is of major importance while lactogenic transmission
plays a minor role because massive shedding of larvae
in the milk occurs only after a primary infection of the
bitch during pregnancy. Ingestion of infective eggs from
the environment is the main risk factor for young and
older dogs, whereas ingestion of of infected paratenic
host seems to play a minor role. An important aspect
is that older dogs after a previous intestinal infection
can also remain susceptible for reinfections resulting in
patent worm burdens.
The contamination of the environment with Toxocara
eggs is a relevant epidemiological risk factor both for
definitive hosts and humans or paratenic hosts, such as
rodents, pigs or avian species. The daily egg production
of a T. canis female is estimated at 25,000-85,000.
Infected puppies may shed enormous amounts of eggs
in their faeces(> 100,000 eggs/g), thus causing an intense
environmental contamination. In addition to the local
contamination, infected dogs and foxes contribute to
a wide dissemination of Toxocara eggs by defaecation
in rural and urban areas, including agricultural areas,
gardens, public parks, childrens' playgrounds, sandpits,
beaches, etc. Up to 60% of samples from such locations
have been found positive for Toxoxara eggs. The high
tenacity ensures a long survival of infectious eggs and
enhances their accumulation in the environment. In a
humid environment Toxocara eggs may survive from
several months up lo 4 years, they can resist cold periods,
but they are sensitive to desiccation and temperatures
above 35 °C.
The persistence of the transmission cycle of 7'.
canis is ensured by muJtiple epidemiological factors,
including the high parasite prevalences in final hosts, the
enormous fertility of the parasite, the high tenacity and
wide dispersal of eggs, several options of transmission
routes to the definitive hosts and the involvement of
paratenic hosts.
Immunology. The course of T. canis infections in
dogs is determined by various factors, including age,
infection dose, hormonal status and immunology.
In fetuses and neonates, which are immunologically
incompetent, the larval migration and settlement in
the intestine are not hampered. In puppies and young
dogs, prenatally acquired parasites persist in the intestine
depending on the worm burden. They are usually
eliminated at an age of 2-6 months in case of minor
infections whereas in severely infected animals the self­
cure usually starts by the age of 5-6 weeks. This reaction
is associated with a significant decline in synthesis of
the immunomodulating cytokine I L-10 by mononuclear
cells in response to larval excreto:-,·isecretory (ES) T.
canis antigens. Heavy experimen. 1' superinfections
(50,000-100,000 eggs) of puppie:. ·., iCh patent worm
burdens cause the expulsion of the maiority of the adult
worms within l-2 weeks. This react1\l11 is accompanied
by severe enteritis and seems to rnrrespond to self­
cure reactions known in trichost rongylid infections
(► p. 33).
Apart from the self-cure reaction, immune events in
dogs are predominantly directed against the newly
ingested larvae, whereas premature stages, which are
ingested by the bitch (see above), may settle in the
intestine without any restraint. Challenge infections
of immune dogs results in trapping and elimination
of migrating larvae predominantly in the liver and is
followed by the formation of confluent granulomas.
However, since part of the larvae may escape the reaction,
somatic stages may also accumulate in immune dogs.
Major mechanisms of immune evasion are probably the
formation of ES-antigen/antibody complexes and their
ability to continuously migrate in tissues. The persistence
of somatic larvae seems to be supported by a variety
of immunomodu!ating glycoproteins (particularly
O-glycosilated molecules) which are synthetised in
relative large amounts and are attached to the larval
surface.
Pathogenesis and clinical signs. Toxocara
infections can cause different types of disease in
definitive hosts (dog) and paratenic hosts.
• Clinical signs in dogs
Light to moderate intestinal infection in puppies
and older dogs:
• Asymptomatic infection or occasional vomiting.
diarrhoea, mucous faeces, retarded developmt.'nt
in young animals.
Heavy infections in puppies:
♦ Tissue damage caused by migrating larvae with
formation of disseminated granulomas in various
organs (liver, lungs, kidneys, heart muscle)
( ► Figure l0.66); in the eyes: granulomatous
retinitis and chorioretinitis.
• Intestinal infection ( ► Figure l0.64). Hyper­
trophy of the ti.mica muscularis, atrophy of the
villi, crypt hyperplasia. Repeated vomiting,
bloated abdomen, gastroenteritis, colic. obsti­
pation alternating with diarrhoea, unformed
mucous, partly bloody faeces, eosinophilia,
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)
anaemia, intermittent fever, alternate anorexia,
emaciation, retarded development, lacklustre,
scrubby coat, neurological disorders and rachitic
symptoms. Occasionally, perforation of the
intestine and invasion of bile ducts by worms.
Possibly fatal from the 2 nd and 3 rd week of life
onwards.
- Infection of older dogs by somatic larvae:
• Generally asymptomatic.
• Clinical signs in paratenic hosts. In the course
of the somatic migration, L3 invade various organs
(lungs, liver, skeletal muscles, CNS and others) of
paratenic hosts(e.g. rodents, birds, pigs, sheep, monkeys,
humans) and may cause certain reactions and disorders
ofvariable severity depending on the number of larvae
and the reactivity of the host. They may include inter
alia multiple haemorrhages, necroses and granulomas
in liver and lungs, often eosinophilia, formation of
specific antibodies to Toxocara antigens, tissue damage
in the CNS with meningitis, encephalitis, myelitis and
neurological symptoms, and pathological changes in
the eye (chorioretinitis, turbidity of the vitreous body,
etc.). Hypobiotic larvae in tissues, which can survive
for several years (in monkeys at least 10 years) may
become reactivated and continue to migrate. Various
forms of toxocarosis are mentioned below(see zoonotic
importance).
Diagnosis. Intestinal infections in dogs are diagnosed
by coproscopical detection of Toxocara eggs (flotation
techniques). Eggs: medium-sized, 80-94x65-83 µm,
thick-walled, spherical, greyish in colour, surface
pitted (golf ball-like), contents: dark, unsegmented,
grainy(► Figure 16.16, p. 549). The eggs can be easily
differentiated from those of T. leonina by morphological
characteristics, and from eggs of T. cati (68-85x58-75
µm) by morphometry and DNA analysis (relatively often
dogs shed T. cati eggs after coprophagia of cat faeces).
Immature and mature T. canis are often shed with the
faeces or regurgitated. Post mortem diagnosis: ascarids
in the intestine.
Therapy and control. Pyrantel derivates, (pro)
benzimidazoles, macrocyclic lactones and emodepside
are available for the treatment of adult Toxocara and
Toxascaris in dogs( ► Tables 19.14 and 19.15, p. 600 ff).
The drugs are effective and well tolerated. Anthelmintic
resistance was not observed so far. Control measures
include anthelmintic treatments of dogs 3-4 times a
year(details ► p. 605).
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Figure 10.68. Kidney lesions In an older dog, caused by larvae
of Toxocsra csnls (Photo: IPH, M. Stoye).
Zoonotlc Importance. Humans become infected by
accidental ingestion of Toxocara eggs containing the
infectious L3 (geophagia, contaminated food, hand­
mouth contact). Coats of dogs can be contaminated
with T. canis eggs, however, L3 develop very rarely in
such eggs suggesting that the infection risk for humans
from direct contact with dogs is limited. In the human
body the L3 migrate on the somatic route, invade various
organs(liver, lungs, muscles, CNS, etc.) and cause lesions
and granulomas. Rarely, adult Toxocara stages develop
in the human intestine. Toxocara infections in humans
are common worldwide. Mean seroprevalences in
healthy people in Central Europe range between 1-8%;
U)
in a recent nationwide study in AT the average rate of .c
seropositivity was 6.3%. Infants are particularly at risk.
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T. canis is one of the causative agents (see below) of I
a disease called 'larva migrans' (more precisely 'larva
migrans interna'). In humans various forms of larva
migrans can be distinguished: unapparent LM (no
symptoms, specific antibodies present), visceral LM,
neural LM and ocular LM. Clinical signs are rare
and are predominantly observed in children at an
age of 2-5 years, including eosinophilia, leukocytosis,
hepatomegaly, splenomegaly, episodes of fever, asthma
attacks, pneumonia, lymphadenopathy, urticaria, and
rarely CNS disorders. Ocular LM occurs predominantly
in adults and is often caused by a single larva. Clinical
signs are granulomatous chorioretinitis, turbidity of the
1
1,
vitreous body and even blindness.
T. canis and T. cati are considered the major agents of
LM in humans and animals but other ascarids may
also be involved, such as Ba ylisascaris procyonis from
raccoons, A. suum from pigs, and several species of the
family Anisakidae ( ► p. 339).
lI
l
Part Ill. Parasites and parasitoses: metazoa
Toxocara species in felids
Agent. Toxocara cati (syn. Toxocara mystax). Adults
show the characteristics of the genus (see T. canis);
compared to T. canis the cervical alae of T. cati are
broader and more convex giving the anterior end the
appearance of an arrow head ( ► Figure 10.63), ckS
3-7 cm, � � up to 12 cm in length. Eggs: see diagnosis.
Parasite of the small intestine of cats and wild felids
(wild cat, lynx). T. malayensis is a species found in cats
in Malaysia and China.
Life cycle. The life cycle resembles that of T. ca11is,
except that T. cati does not cause prenatal infections.
The cycle of T. cati includes the following transmission
and migration routes:
• Ingestion of eggs containing L3. Tracheal
migration of the larvae as in T. canis. Prepatency
approximately 8 weeks. Some larvae may invade
striated muscles.
• Somatic migration and lactogenic infection of
kittens. Such transmission occurs only if the queen
acquires the infection in the final phase of pregnancy,
resulting in somatic migration of the larvae and
their accumulation in the mammary glands. Larvae
may be excreted in the milk throughout the whole
lactation period.
• Transmission of L3 in paratenic hosts. Most of the
larvae ingested with paratenic hosts (rodents, birds)
pass through a histotropic phase in the wall of the
stomach and smaU intestine and return subsequently
to the intestinal lumen.
Occurrence and epidemiology. T. cati is the most
common ascarid of cats worldwide. On average 19.7% of
cats (n=l,519) from 9 European countries were copro­
positive for T. cati eggs with an inter-country range
between 6 and 34%.
Clinical signs and diagnosis. The spectrum of signs
includes respiratory disorders (cough), gastrointestinal
disturbances (catharal enteritis, mushy faec.es, vomiting,
abdominal bloating) and general symptoms (dehydration,
anaemia, scrubby coat, emaciation). In cats migrating
T. cati larvae may cause peripheral eosinophilia and
broncho-pulmonary lung lesions that can be clinically
visualised by radiography and high-resolution computed
tomography but cannot be differentiated from lesions
of Dirofilaria or Aelurostrongylus infections. Patent
infections are diagnosed by coproscopic egg detection.
Eggs of T. cati are slightly smaller (68-85x58-75 µm) than
T. canis eggs and can be differentiated by morphometry
and DNA analysis.
Therapy and control. Anthelmintics of various
chemical classes are approved for use in cats ( ► Tables
19.14 and 19.15, p. 600 ff). For control measures ► p.
605.
Toxocara vitulorum
Disease: Toxocarosis in cattle and buffaloes
Toxocara vitulorum (c3\3': 6-25 cm, '2�: 8-30 cm) is a
parasite of the small intestine of cattle, water buffaloes
and rarely of sheep. It is common in all tropical areas,
but rare in Central Europe with focal occurrence, e.g.
in zoos. After ingestion of larvated eggs the hatched
L3 invariably (independent of age and sex of the host)
migrate following the somatic route to liver and lungs,
settle in the parenchyma and undergo hypobiosis.
Larvae become activated in pregnant animals a few
days before calving and invade the udder. The majority
of them are shed with the milk in the first 2 days of
lactation; only very low numbers of larvae are found
in the milk after the 9th day. Without prior somatic
migration larvae settle in the small intestine of the calf
and develop into adults. Prepatency: 3-4 weeks, patency:
usually 5-lO weeks (occasional prenatal infections are
suspected). Heavily infected calves may suffer from
variable intestinal disorders, severe cases may be fatal.
The parasites discharge valeric acid which may cause an
obnoxious odour in the meat. Diagnosis by egg detection
in calves >3 weeks of age. Metaphylactic treatment of the
calves in the 2nd week of life against immature intestinal
parasite stages with benzimidazoles or macrocyclic
lactones. Animals imported from endemic areas should
be controlled (quarantine, serological and coproscopical
examination), and patent infections should be treated
to prevent introduction of the parasites.
Selected references
Beugnet F, Franc M, Tlelemana E (2015) Gastro-1ntestinal
helmlnthoses. In: Beugnet F, Halos L (eds.) Parasitoses &
vector borne diseases of cats. Lyon. France: Merial SAS..
pp. 15-49; ISBN 978-2-9550805·0·4.
Brunaaka M, Dubinsky P, Relterova K (1995) Toxocara canis:
ultrastructural aspects of larval moulting in the maturing eggs.
Int J Parasitol 25: 683-690.
Coatl N, Schnieder T, Epe C (2004) Vertical transmission of
Toxocara cati. Schrank 1788 (Anisakidae) in the cat. Parasitol
Res 92: 142-146.
Dillon AR, Tillson OM, Hathcock J, Brawner B, Wooldridge A.
Cattley R, Welles B, Barney S, Lee-Fowler T, Botzman L,
Sermersheim M, Garbarino R (2013) Lung histopathology,
radiography, high-resolution computed tomography, and
bronchio-alveolar lavage cytology are altered by Toxocara
cati infection in cats and is independent of development of
adult intestinal parasites. Vet Parasitol 193: 413-426.
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)
Deplaz es P, Van Knapen F, Schweiger A, Overgaauw
PAM (2011) Role of pet dogs and cats in the transmission
of helminthic zoonoses in Europe, with a focus on
echinococcosis and toxocarosis. Vet Parasitol 182: 41-53.
Fahrion AS, Staebler S, Deplazes P (2008) Patent Toxocara
canis infections in previously exposed and helminth-free dogs
after infection with low numbers of embryonated eggs. Vet
Parasltol 152: 108-115.
Fahrion AS, Schnyder M, Wichert B, Deplazes P (2011)
Toxocara eggs shed by dogs and cats and their molecular and
morphometric species-specific Identification: Is the finding
of T. cati eggs shed by dogs of epidemiological relevance?
Vet Parasitol 177: 186-189.
Nijsse R, Ploeger HW, Wagenaar JA, Mughini-Qras L (2015)
Toxocara canis In household dogs: prevalence, risk rectors
and owners' attitude towards dewormlng. Parasltol Res
114: 561-569.
Pinelli E, Herremans T, Harms MO, Hoek D, Kortbeek LM
(2011) Toxocara and Ascaris seroposllivlty among patients
suspected of visceral and ocular larva mlgrans In the
Netherlands: trends from 1998 to 2009. Eur J Clln Microblol
Infect Dis 30: 873-879.
Roberts JA (1993) Toxocara vitulorum in ruminants. Helmlnthol
Abstr 62: 151-174.
Sager H, Steiner Moret C, Grimm F, Deplazes P, Doherr
MG, Gottstein B (2006) Coprological study on intestinal
helminths in Swiss dogs: Temporal aspects of anthelminthic
treatment. Parasitol Res 98: 333-338.
Schnieder T, Laabs EM, Welz C (2011) Larval development of
Toxocara canis in dogs. Vet Parasitol 175: 193-206.
Strube C, Heuer L, Janecek E (2013) Toxocara spp. infections
in paratenic hosts. Vet Parasitol 193: 375-389.
Wolken S, Schaper A, Mencke N, Kraemer F, Schnieder T
(2009) Treatment and prevention of vertical transmission of
Toxocara cati in cats with an emodepside/prazlquantel spot­
on formulation. Parasitol Res 105 Suppl. 1: 75-81.
Family Anisakidae
•
Summary
Several species of the family are of concern with
regard to food safety and public health. Larval stages
can be transmitted to humans by raw marine fish or
i nsufficiently processed marine fish products and
may cause 'herring worm disease' with lesions in the
gastrointestinal tract and allergic reactions. Infections
can be avoided by deep-freezing of fish and other
measures.
Agents. Most anisakid species infecting humans are in
the adult stage parasites of the digestive tract of mammals
or birds: Anisakis simplex s.s. and A. physeteris(definitive
hosts [DH]: dolphins, porpoises, sperm whales),
Pse11doterranova decipie11s (syn. Phoca11ema decipiens)
(DH: seals, sea lions, walruses), Co11tracaecum oswlat11m
(DH: fur seals) and Porrocaecwn reticulatwn (birds).
Anisakis and Pseudoterranova are most frequently
involved in human infections. A. simplex s.s. is discussed
here as an example.
co
'O
Life cycle. The adult stages of A. simplex(6' J: 3-13 cm, '6
·�
� 'j): 4-20 cm) inhabit the stomach and small intestine (J
en
of whales, dolphins, porpoises, or more rarely of seals. <(
The life cycle is shown in ► Figure I 0.67. Unsegmented
eggs are discharged by the final host. In the water the egg
embryonates and develops further until containing an
ensheathed L3.(In some recent publications this stage is
regarded as L2, although it has been shown that a second
moult of the larva occurs in the egg). L3 stages, hatched
from the eggs, are ingested by small crustaceans(order
Euphausiacea), in which they detach the sheath, grow
up to a length of approximately 20 mm and become
infectious for paratenic and final hosts. Copepods
are probably paratenic hosts(► Figure 10.67). After
ingestion of infected intermediate or paratenic hosts
by fish the larvae invade their body and encyst in the
viscera, partly also in liver and muscles. Squids are also
susceptible. Larvae may accumulate in predatory fish
or squids. After ingestion of infected intermediate or
paratenic hosts by suitable definitive hosts the larvae
settle in their stomach or intestine and reach sexual
maturity after 2 moults. It is notable that the development
in the aquatic environment can take place at rather low
temperatures(about 5 °C), and free L3 may survive in
the cool sea water for up to 3 months. The development
of other anisakids resembles that of A. simplex.
Epidemiology and occurrence. Anisakis spp.
have a worldwide geographical range with species­
specific distribution areas, presumably dependent on
the migratory behaviour of their definitive hosts. A.
simplex larvae have been found in > 150 species of sea fish
and squids. In some regions the prevalences of anisakid
larvae in certain fish species are high. For example,
according to a recent study (2015) 80% of 300 beaked
redftsh (Sebastes me11telln) from fishing grounds in the
North Atlantic were infected with anisakid larvae; 63%
of the worms were found in the viscera and 37% in the
musculature.
Q)
C
·c3
Diagnosis and prophylaxis. European regulations
Q)
(EC No. 853/2004) and international CODEX standards �
(WHO, PAO, 2012) are designed to minimise the 2:-
co I
infection risk for humans caused by fish-borne C
I
anisakid nematodes. The regulations include inter alia ·c
the inspection of fresh fish for visible parasites (larvae I
measure 5-38 mm) and the transillumination offish ftlets -�
if technically feasible(► Figure 10.68). Morphological
characteristics are used for the identification of larvae,
but DNA analyses are also employed. Raw fish or fish ·u;
products which are intended for consumption by ,_
humans have to be treated by freezing (e.g. 24 h at core I'
Part Ill. Parasites and parasitoses: metazoa

Infection of man (aberrant

host)

Whales

Other fish species

as paratenic hosts
with L3

Free L3,
ensheathed

Crustaceans (Euphausiacea),
intermediate hosts with L3
Infection of man that are infective for paratenic
and definitive hosts

Marine copepods as
potential transport hosts

Figure 10.67. Life cycle of Anisakis simplex (Graphics: IPZ).

temperature of -20 °C) to kill nematode larvae. Products

classified as raw or semi-raw are for example sushi,
sashimi, 'white herring: sliced raw fish, cold (<60 •c)
smoked salmon or other marine fish, also including
herring marinated or sailed under condition s which do
not kill the nematodes. Heating(> 70 °Cat least 2 min)
or freezing in a domestic freezer (4 days) are convenient
prophylactic measures in private households.

Zoonotic importance. Humans become infecte�

with living anisakid larvae by ingestion of raw or senu­
raw sea fish or fish products(see above). In hum an hoStS
1 a' l t rac
t
Figure 10.68. Fish with anisakids larvae (length up to 20 mm; the larvae may invade the wall of the .mtest'n
larvae were isolated and placed on the musculature to make (oesophagus down to the rec t um; Pseudoterra11ova. spp.
1 e )es10
11s.
them more visible) (Photo: IPZ). particularly the stomach) and cause u1ceral ·v
v 1
A.-ter
t: an incubation period of a "1ew hour s up to se en1a
days the patients suffer severe epigastnc . pain ' nau s , e
. e rnaY
vomiting and fever. Invasion of the sm aII ·tntest tn nt'
cause stenosis and ileus. Anisakid larvae contain p
ote
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)
thermostable allergens. Repeated ingestion(also of kilJed
larvae in cooked food) may be followed by severe allergic
reactions. Particular eating habits are the reason that
90% of the human anisakidosis cases occur in Japan,
the remainder in Korea, Europe (e.g. CH, DE, ES, IT,
NL, FR) and in the USA.
Selected references
Baird FJ, Gasser RB, Jabbar A, Lopata AL (2014) Foodborne
anisakiasis and allergy. Mol Cell Probes 28: 167-174.
Klapper R, Kuhn T, Milnster J, Levsen A, Karl H, Klimpel
S (2015) Anisakid nematodes In beaked redfish (Sebastes
mentella) from three fishing grounds In the North Atlantic,
with special notes on distribution in the fish musculature.
Vet Parasitol 207: 72-80.
Klimpel S, Palm W (2011) Anisakld nematode (Ascarldoldea)
life cycles and distribution: increasing zoontotic potential In
the time of climate change? In: Mehlhorn H (ed.). Progress
in parasitology. Heidelberg, Germany: Springer-Verlag, pp.
201-222; ISBN 978-3-642-21395-3.
Sohn W-M, Chai J-Y (2011) Ansiakiosls (Anisakidiosis). In:
Palmer SR, Lord Soulsby, Torgerson PR, Brown DWG (eds.)
Oxford textbook of zoonoses. 2 nd ed. Oxford, UK: Oxford
University Press, pp. 774-775; ISBN 978-0-19-857002-8.
WHO/FAO (2012) Codex alimentarius. Code of practice for
fish and fishery products. 2 nd ed. Rome, Italy: WHO/FAO.
Available at: http://tinyurl.com/p7q7v72.
- Superfamily Heterakoidea
Heterakoidea with the families Heterakidae and
Ascaridiidae are of veterinary interest,predominantly
as intestinal parasites of poultry. Morphological
characteristics of both families are caudal alae and a
precloacal acetabulum at the posterior end of the males
(► Figure 10.69).
Family Heterakidae
Genus Heterakis
Disease: Heterakiosis in poultry.
Heteros(G): different; akis(G): tip.
Summary
· Agent. Heterakis spp. measure 1-2 cm in lengtlil; they
inhabit predominantly the caeca of birds. The most
important species is Heterakis ga/linarum in Galliformes.
Life cycle, clinical signs. Mon0xenic cyele or
development including earthworms as 1:>aratenic hosts.
Heavy infections cause typhlitis. H. ga/linafl!lm transmits
via its eggs Histomonas meleagridis, the agent of the
'blackhead disease' of turkeys.
------ Precloacal sucker
Caudal alae Cil
-0
'6
-�
0
en
<(
�Cloaca
Papillae
Figure 10.69. Helerakls: male, posterior end (Graphics: IPZ,
A. Seeger; after Hartwlch 1975).
Agent and occurrence. H. gallinarum has a
worldwide distribution and inhabits the caeca of poultry
and wild gallinaceous birds(chicken,turkey,partridge
and others),occasionally also of geese(Anseriformes).
H. isolonchae: in Europe predominantly in pheasants and
quails. H. dispar. worldwide in caeca of Anseriformes,
sometimes also Galliformes.
H. gallinarum(o'o': 6-13 mm,��: 9-15 m m long)
oesophagus with bulbus, lateral alae extend almost
along the entire length of the body. Posterior end of
males and females peaking in a smooth tip; males with
caudal alae, a precloacal sucker( ► Figure 10.69) and
two dissimilar spicules. Eggs 65-80x35-45 µm with a
dark zygote,thick-shelled, smooth surface.
Life cycle, epidemiology and occurrence. The
adults of H. gallinarum inhabit the caeca, rarely the
posterior parts of the small intestine and the large
intestine. Eggs are shed with the faeces,L3 develop in
the eggs at 25-27 °C in approximately 2 weeks; longer
periods of time are required at lower temperatures. After
oral ingestion of the eggs the larvae hatch,migrate into
the caecum and - often after a short histotropic phase
Q)
- reach sexual maturity. Prepatency lasts 24-34 days,
·u
C
depending on the host's age and species.
Q)
2
Earthworms which may survive for several years can act
as paratenic hosts. Larvated eggs are long-living; under C
·;:::
suitable conditions in the environment, they remain Q)
infective for 8-9 months and may also survive winter
seasons. H. gallinarum is of particular importance as a -�
vector of Histomonas meleagridis, although this pathogen
can be transmitted directly from bird to bird( ► p. 52).
·wcu
cu . I
I
 Part Ill. Parasites and parasitoses: metazoa
Prevalences of up to 25% were observed in DE in
chickens kept on deep litter or in free-range chickens;
chickens on organic farms in DK were infected at
75%. Infection rates of 7.5% and more were found in
commercial broiler farms in USA. H. gallinarurn is often
associated with Ascaridia galli.
Pathogenesis and clinical signs. Heavy infections
of chickens cause typhlitis with haemorrhages and
formation of nodules in the mucosa, associated with
inappetence, and diarrhoea. The disease may affect
fattening performance and egg yield. Co-infection with
H. meleagridis intensifies the clinical signs and shifts
the Th2 dominated immunological reaction, associated
with the H. gallinarum infection, to a Th 1 response. H.
isolonchae is highly pathogenic for pheasants.
Diagnosis, treatment and control. Detection of
parasites at necropsy. The eggs of Heterakis spp. and
Ascaridia galli are very similar; the former are slightly
smaller, but a reliable differential diagnosis is often not
possible. There are currently only a few anthelmintics
efficacious against H. gallinarum and licensed for use in
poultry (flubendazole and levamisole) ( ► Table 19.20,
p. 61 l ). Control of heterakidiosis is extremely difficult
I •
in free-range chickens because of the resistance of the
eggs and, above all, due to the inclusion of earthworms
as paratenic hosts in the life cycle.
Family Ascaridiidae
Genus Ascaridia
Oiaeaee: Acatd1oel8 In poultry.
.
naommon
..,.... .-....
-IIOIOUlblrdl
... Monoxenoul
............ and tloor-hulblndry
dallll-lldpe,fomwa
�inducelnlCl'OIN
Q)
·u
C
'6
Q)
�
� Agents. Members of the genus parasitise the small
co
C intestine of gallinaceous birds and pigeons. Ascaridia
·c:
Q) galli is a parasite of gallinaceous birds (chickens,
turkeys, guinea fowls, and game birds) with worldwide
-� distribution, A. dissimilis is found in turkeys in Europe
>-
0> and North America, and A. columbae is a worldwide
0
0
parasite of pigeons. The yellowish adults of A. galli
·wco are 1.4-7.5 cm (oo) and 3.3-12 cm (<j?<j?) long. The
mouth opening is surrounded by 3 lips; the oesophagus
ro
a.. is cylindrical without bulbus. The posterior end of the
male bears narrow caudal alae, a pre-cloaca! sucker and
two spicules. Eggs are ellipsoidal (77-94x43-55 µm),
unsegmented and thick-shelled with smooth surface.
They resemble Heterakis eggs but are slightly larger.
Life cycle of A. gal/i. Parasite carriers release
unembryonated eggs to the environment which develop
under favourable conditions (high humidity, oxygen) to
infectious L3 at 17 °C in approximately 3 weeks and at
23 °C in 10 days, while at 15 °C the development takes
8 weeks. In humid soil the eggs can survive up to one
year. After ingestion of infectious eggs, larvae hatch in
the small intestine and invade the intestinal wall where
they moult. In the 3 rd week p.i., some L4 return to the
intestinal lumen and reach sexual maturity 5-8 weeks p.i.
However, a considerable proportion of the larvae may
remain in the intestinal wall for prolonged periods (see
below, immunology). Ascaridia spp. show a tendency
to extra-intestinal migration and may be found in the
liver and other organs where they can persist for some
weeks, as observed in A. dissimilis and A. co/umbae.
Occurrence and epidemiology. A. galli is common
in chickens maintained in different husbandry systems.
In DK prevalences of A. galli were 64% in free-range
chickens, 42% in deep-litter system and 37% in a
backyard system. Turkeys and pigeons are frequently
infected by A. dissimilis or A. columbae, respectively.
Pathogenesis and clinical signs. In A. galli
infections of chickens epithelial and tissue damage
(destruction of glands of Lieberkiihn) start early after
infection and may, in heavy infections, eventually lead
to enteritis. Numerous adult worms can impair intestinal
functions and obstruct the intestine. Immature and adult
parasites may migrate up to the stomach and down to
the cloaca, occasionally also into the oviduct where
they may be enclosed in the egg before the egg shell is
formed, putting off egg consumers. Young animals are
predominantly affected by clinical disease. Enteritis
results in decreased food intake and reduced weight
gain. Animals may become anaemic and susceptible
to other pathogenic agents. A. dissimilis infections in
turkeys may induce necrotic lesions of the intestinal
wall, and juvenile parasites may spread into the liver,
causing multiple granulomas.
Immunology. Between and within certain chicken
breeds there are differences in the susceptibility to A.
galli-infections most likely due to innate immunity.
Chickens infected with A. galli develop a Th2 type
immune response and a certain degree of protective
immunity which may lead to a gradual elimination of
worms during the prepatent period. Recent studies have
shown that considerable numbers of larvae remain in the
intestinal wall as 'arrested' stages for prolonged periods.
This phenomenon may be due to acquired immunity
or other factors.
 10. Phylum Nematoda (syn. Nematozoa) (threadworrns or roundworms)

Diagnosis. Coproscopic detection of eggs (flotation 10.1.4 Order Oxyurida (pinworms)

techniques)(possible confusion with similarly looking
Heterakis eggs) and inspection for worms at necropsy.
Therapy and control. Anthelmintics used against
Heterakis (► Table 19.20, p. 61 I) are also efficacious
against Ascaridia spp. Con�rol is difficult due to the
longevity of the eggs, particularly under free-range
conditions. In case of indoor maintenance the litter
should be kept dry.
Selected references
Gauly M, Bauer C, Preisinger R, Erhardt G (2002) Genetic
differences of Ascaridia galli egg output in laying hens
following a single dose of infection. Vet Parasitol 103: 99-107.
Ferdushy T, Schou TW, Norup LR, Dalgaard TS, Thamsborg
SM, Nejsum P, Permin A, Juul-Madsen HR, Kyvsgaard
NC (2014) Acquisition of resistance after continuous Infection
withAscaridia galli in chickens. Parasitology 141: 1603-161 o.
Hoglund J, Jansson DS (2011) Infection dynamics of Ascaridia
galli in non-caged laying hens. Vet Parasitol 180: 267-273.
Norton RA, Hopkins BA, Skeeles JK, Beasley JN, Kreeger
JM (1992) High mortality of domestic turkeys associated
withAscaridia dissimilis. Avian Dis 36: 469-473.
Tabrat B, Jansson DS, Hoglund J (2015) Environmental
tolerance of free-living stages of the poultry roundworm
Ascaridia gafli. Vet Parasitol 209: 101-107.
Wongrak K, Das G, von Borstel UK, Gauly M (2015) Genetic
variations for worm burdens in laying hens naturally Infected
with gastro-intestinal nematodes. Br Poultry Sci 56: 15-21.
Family Oxyuridae
Oxys(G): sharp, pointed; ura(G): tail. Refers to the long
and pointed posterior end of the females.
Summary
• Agents. Plnworms live In the Intestine of many lower
and higher vertebrates. Characteristics of oxyurlds
are: conspicuous grey-white colour of the parasites;
oesophagus with distinct bulbus; females with long,
tapered tall; body length between <1 cm (oo) and 12
cm ('i? 'j?). Eggs with asymmetrical shape with or without
a polar plug. Common In horses (Oxyurls equl), rabbits
and hares (Pasalurus amblguus), laboratory rodents
(Syphac/a epp., Asplculurls tetraptera) and turtl• (not
further conalderecl In this book), rarely In sheep and
goats (Skrjab/nema ov/s).
Life cycle, epidemiology. Direct cycle, Infection by
Ingestion of eggs, each containing an Infective larva
(L3). Particularities in the blology of various species
(e.g. egg deposition In the perlanal region, partly
autolnfectlon) support the transmission and persistence
of the parasites In a host population.
Clinical signs, diagnosis, control. Most notably In
horses and small ruminants prurltus In the perlanal
region and disturbance of the animals. In rabblta.
depending on the worm burden, reduced weight galne
and emaciation. Diagnosis depending on the epecie9
by detection of eggs in the perlanal region (adhealve
tape technique), in faeces or at necropsy (rodents).
Chemotherapy with various anthelmlntlcs; control la
difficult and relies on hygiene measures.

Genus Oxyuris

Oxyurls equi (pinworm of equids)

Disease: Oxyurlosis In equlds.

Agent. Males(with one spicule) measure 0.8-1.5 cm,

females 2.5- I 2 cm, depending on the variable lengths
of the tail(► Figure 10.70). The distinct bulbus of the
oesophagus(► Figure 10.2, p. 255) is a characteristic
Q)
of pinworms. The uterus of gravid females is densely C
packed with eggs. The elongated asymmetrical eggs TS
'5
(approximately 90x40 µm), when shed by the female, Q)

contain an embryo in the gastrula stage; one pole

�
flattened with a polar plug (the hatching site of the ca
C
larva)(► Figure 16.13, p. 545). ·.:::

Life cycle. The adult worms inhabit the caecum and -�

colon of equids. Gravid females migrate to the anus, >.
Ol
crawl out, within minutes release 8,000-60,000 eggs and 0
die. The eggs are covered with a viscous fluid and stick
'in
in dusters to the skin of the perianal region. Desiccation
and shrinking of the egg clusters cause irritation of the a..ca
sensitive skin of this body region, resulting in pruritus
 Part Ill. Parasites and parasitoses: metazoa
Figure 10.70. Oxyuris equi (length of females with long tails
up to 12 cm (Photo: IPZ).
which prompts the animal to rub and strip off the eggs.
An infective L3 develops in the egg within 3-5 days. After
ingestion of the egg. the L3 hatches in the small intestine
and moults into L4 within 3-11 days. The L4 stages have
a large buccal capsule, they adhere to the mucosa in the
ventral colon or caecum and ingest mucosa! tissue and
blood. By leaving a site and re-adhering to another one
they migrate to the dorsal colon, moult to preadult stages
7-8 weeks p.i. and reach sexual maturity 12-14 weeks
p.i. Males die after copulation, and the females migrate
to the anus approximately 4½ months p.i.
Occurrence and epidemiology. Worldwide, 0.
equi infections are common in horses with prevalences
of approximately 10-40% (sometimes up to l00%) and
infection intensities up to I 0,000 specimens per animal.
All breeds and age groups of horses are susceptible to 0.
equi. There are no data available on protective Immunity
to the parasite. Eggs containing L3 arc resistant and
remain infectious for months.
Probstmayria vivipara, a small (2-4 mm). rare nematode
in the colon and caecum of equids is often assigned to
pinworms but belongs to the order Ascaridida. The
species i.s not further considered in this book.
a,
·u
C
Pathogenesis and clinical signs. The fourth stage
� of 0. equi feeds on the intestinal mucosa whereas the
adults do not attach to the intestinal wall. The main
co feature of equine oxyuriosis is the sustained pruritus
C
·;::
caused by the females in the sensitive anal region and in
� particular by the eggs while drying up. The horse rubs
C the base of its tail against any suitable object causing
>-
0> skin lesions and loss of hair on the dorsal side of the
0 tail ('rat tail'}. The animals become impaired by the
'ui permanent irritation.
co
co
a.. Diagnosis. The clinical signs should prompt an
inspection of the anal region where the cream-coloured
egg clusters, sometimes several cm long, may be found
and identified using the adhesive tape technique(► p.
533). Attempts to detect eggs by conventional faecal
examination usually fail. Adult worms may be voide d
spontaneously and found in horse droppings and the
litter.
Therapy and control. Most anthelmintics licensed for
horses are active against 0. equi ( ► Table 19.10, p. 592).
There is. however, some recent evidence of anthelmintic
resistance of 0. equi against macrocyclic lactones in
Germany. The longevity of the eggs, the widespread
contamination of stables, paddocks, etc. with eggs and
the obviously lacking immunity are factors that favour
reinfections. Feeding from the floor should be avoided.
An easy preventive measure is regular washing of the
perianal region of the horses with water containing a
detergent.
Genus Passalurus
Passalurus ambiguus (pinworm of
lagomorphs)
Disease: Passalurosis In rabbits and hares.
Passalos (G): hook; ura (G): tail; ambiguus (L):
changeable.
Agent. Whitish parasites; oo
measure 3-5 mm,��
8-12 mm. Oesophagus with typical bulbus; rear end
of female pointed. Eggs: elongated, asymmetrical,
brownish, 100x43 µm with moderately thick shell.
Life cycle. P. ambigu,u inhabits the caecum and
colon of rabbits and hares. Insemination takes place
in a traumatic manner as males perforate tht cuticle
of immature females (L4) and introduce their \pwns
into a hypodermal pocket in the vulvar region. Eggs
are released by females into the intestine of thl' host,
and L3 develop before the eggs are shed. Eggs are
excreted adhering to faecal pellets and contained in the
caecotrophe with which they are ingested ( ► Glo�i,ary,
p. 620). (Some authors reported that female P. a111big11us
deposit their eggs like females of 0. equi). The prepatency
of P. ambig1111s lasts 55-60 days.
Occurrence, epidemiology. The general distribution
area and the incidence of P. ambiguus are not sufficiently
studied. Prevalences of P. ambig11us in wild rabbits
varied between approximately 15% and 85% in several
European countries according to a recent report, and
5.8% of 274 slaughter rabbits were infected in PL.
Autoinfections by caecotrophy play an important role
and may cause heavy infections despite good hygienic
conditions, e.g. under intensive farming conditions.
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworm s)
Clinical signs, diagnosis, therapy, control.
Mainly young animals are affected by heavy infections
which may be associated with reduced fattening
performance, remarkable weight loss, diarrhoea and
tympany. Detection of eggs by faecal examination.
Benzimidazoles (medicated feed, e.g. fenbendazole 25
ppm fo r 5 days) were found to be effective.
Genus Skrjabinema
Disease: Skrjab1nemosls In ruminants,
K.l. Skrjabin (I 878-1972), Russian parasitologist.
Skrjabinema ovis (pinworm of ruminants) is a
cosmopolitan parasite of sheep and goats. The small
nematodes (oo: 4 111111, <;? <;?: 8 mm) inhabit the large
intestine. Prepatency lasts less than 30 days. Prevalences
in Europe are generally low (approximately 2%) but
individual animals may carry several thousand worms.
Eggs are fully embryonated when laid by the female
worms at the perianal region (see 0. equi). The pruritus
due to the deposited eggs is the major clinical effect
of the infection. Diagnosis can be made by using the
adhesive tape technique ( ► p. 533). The thin-shelled,
slightly asymmetrical eggs measure 60-30 µm. The
common benzimidazoles and macrocyclic lactones are
effective against S. ovis.
Genus Enterobius
Enterobius vermicularis (pinworm of primates)
E. vermicularis, maximum length 12 mm, is a common
human parasite throughout the world, particularly in
children between 5 and 9 years old. E. vermicularis
or closely related species may also cause problems
in monkey and ape populations (breeding stations,
orphanages, laboratories).
Genera Syphacia and Aspiculuris (pinworms
of rodents)
Agents and development. Oxyurids may represent
a severe problem in laboratory animal colonies (rats,
mice, hamsters, and others). Several species are involved:
Syphacia obvelata, S. muris and Aspiculuris tetraptera,
which all live in the caecum and colon but differ
biologically. Gravid females of the Syphacia species
migrate through the anal opening and deposit at the
perianal region infectious eggs or eggs which become
infectious within a few hours. Transmission happens by
oral infection with eggs and by retrofection, caused b y
larvae that hatch at the perianal region and migrate back
into the rectum. In case of A. tetraptera eggs are released
by the females into the intestinal lumen and shed in the
faeces. Infectivity is reached after 5-7 days. Infection
occurs by coprophagia or ingestion of contaminated
feed. Prepatency lasts 9 days and 24 days in Sypliacia
spp. and A. tetraptera, respectively. Infections are usually
asymptomatic but they may alter specific parameters,
for instance the blood picture.
Diagnosis and control. The parasites are usually co
"O
detected at necropsy, A. tetraptera also by faecal ·c
:::,
examination (flotation techniques) and the more >,
X
sensitive molecular techniques, which can also be used 0
for detecting eggs in the environment (cages, suction
holes of ventilation systems, equipment, etc.). Control is
difficult. According to one study a rodent population was
free of worms after 4 treatment cycles with ivermectin
(daily doses 2.9-4 mg/kg b.w. p.o. for 4 days; drug­
free intervals of 3 days; note: off-label use with higher
doses than the generally recommended). Amongst
macrocyclic lactones ivermectin and doramectin seem
to be more effective against S. obvelc,ta than moxidectin.
Jvermectin may also be administered via drinking water.
Alternatively, instead of direct drug administration,
spraying cages twice with a 0.1% ivermectin solution
at fortnightly intervals was successful in one case. Mice
were cured by application of tlubendazole-medicated
feed (ISO ppm for 10 days).
- Selected references
Cirak VY, Hermosilla C, Bauer C (1996) Study on the
gastrointestinal parasite fauna of ponies in northern Germany.
Appl Parasitol; 37: 239-244.
Dole VS, Zalas A, Kyricopoulos-Cleasby DM, Banu LA,
Waterman LL, Sanders K, Henderson KS (2011)
Comparison of traditional and PCR methods during screening
for and confirmation of Aspiculuris tetraptera in a mouse
facility. J Am Assoc Lab Anim Sci 50: 904-909.
Frank R, Kuhn T, Mehlhorn H, Rueckert S, Pham D, Klimpel
S (2013) Parasites of wild rabbits (Oryctolagus cuniculus) from
an urban area in Germany, in relation to worldwide results.
Parasltol Res 112: 4255-4266.
Hickman D, Swan M, Hartman GP (2008) A cost-effective and
efficacious method for pinworm treatment of large colonies
of mice. Lab Anim 37: 308-312.
Lytvynets A, Langrova I, Lachout J, Vadlejch J (2013)
Detection of pinworm eggs in the dust of laboratory animals
Q)
breeding facility, in the cages and on the hands of the C
technician. Lab Anim 47: 71-73.
·u
'6
Pritchett KR, Johnston NA (2002) A review of treatments for
Q)
�
the eradication of pinworm infections from laboratory rodent 2:'
colonies. Contemp Top Lab Anim Sci 41: 36-46. ct!
C
·c
Szkucik K, Pyz-tukasik R, Szczepaniak KO, Paszkiewicz W Q)
(2014) Occurrence of gastrointestinal parasites in slaughter j
rabbits. Parasitol Res 113: 59-64. C
Wolf D, Hermosilla C, Taubert A (2014) Oxyuris equi: lack of >,
0)
efficacy in treatment with macrocyclic lactones. Vet Parasitol 0
0
.......
201: 163-168. ·en
ct!
ct!
CL
I ,
Part Ill. Parasites and parasitoses: metazoa
10.1.5 Order Spirurida
Spira (G): turn, winding; ura (G): tail. Refers to the
coiled posterior end of males.
Spirurida are found in vertebrates in the intestinal tract,
often in its wall, in other tissues, in serosal cavities
and in the orbita. The oesophagus is divided into an
anterior muscular and a posterior glandular portion
(► Figure 10.2, p. 255; ► Figure 10.71). The posterior
end of the males is spirally coiled and may carry lateral
alae and papillae. The spicules are unequal in size and
shape (► Figure 10.72). Females are ovoviviparous or
Iarviparous. The life cycle is indirect, depending on
terrestrial or aquatic arthropods as intermediate hosts.
The order contains the 2 suborders Camallanina and
Spirurina.
- Suborder Camallanina
Camallanina use copepods as intermediate hosts and
inhabit predominantly (superfarnily Callamanoidea) the
intestine of fish. They are currently oflittle importance
in the European fresh water fish industry. Members of
a further superfamily Dracunculoidea also occur in
vertebrates and inhabit tissues and body cavities. One
species is Dracunculus medinensis, the so-called 'Guinea
Figure 10.71. Habronema spp. oesophagus, anterior muscular
portion (Photo: IPG).
I 0.5-2 cm long and thin nematodes which inhabit the
'
I io
Figure 10.72. Habronema spp. Male posterior (Photo: IPG).
worm: that was widely distributed in some subtropical
and tropical areas, is currently found only in a few
African countries. The females inhabit the subcutaneous
tissue and reach a length of 80 cm. Fish parasites of
local importance in Europe are Philometroides cyprini
in carps and Anguillicola spp. in eels. They have been
introduced from Asia.
- Suborder Spirurina
The suborder comprises several superfamilies of
veterinary interest ( ► Table 10.13) including the super­
family Filarioidea which is outlined in an other section
(► p. 353).
- Superfamily Thelazioidea
Family Thelaziidae
Genus Thelazia
Disease: Thelaziosis (eyeworm disease). I
Thele (G): tit, teat. Unclear origin of the name; refers
probably to papillae of the parasite.
S mmary
• Agent. Approximately 1-2 cm long nematodes; Inhabit
the conjunctlval pouches and the lacrimal ducts. Various
species In Europe In cattle, horse, dog and cat.
• Life cycle, occurrence, epidemiology. Females are
viviparous. Muscld flies or fruit flies are Intermediate
hosts and Ingest L1 with conjunctiva! fluid; infectious
L3 are transmitted to new hosts. Prepatency: 3-6
weeks. Common In Europe in cattle, horses and dogs.
Transmission occurs particularly in summer at high fly
densities.
• Pathogenesis and cllnlcal signs. Clinical signs are rare
and are usually limited to heavier Infections: follicular
conjunctivitis, lacrlmatlon, In severe cases degenerative
alterations of the cornea.
• Therapy and control. Systemic or local treatment with
macrocyclic lactones; fly control.
• Zoonotlc Importance. Human cases are rare but
Increasing numbers are observed In Asia.
Agents. Thelazia spp. are milky- or yellowish-white,
conjunctiva! pouches and the ducts of orbital glands.
Ll measure 180-220 µm. Species in Europe: I rfrodesi,
T. gulosa and T. skrjabini in cattle, T. callipaeda in dogs,
foxes and wolves and cats, 1: lacrymalis in horses.
Life cycle. Female worms release LI or embryonated,
thin-shelled eggs. The hatched LI are taken up with
conjunctiva! fluid by various local fly species. In the
vectors L3 develop within 4 weeks and are transmitted
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)

Table 10.13. Genera and species (selection) of the suborder Spirurina (except superfamily Filariodea).

Superfamlly; family Genus Definitive hosts Predilection site of adults Intermediate hOsts
In definitive hosts
Gnathostomatoidea -
Gnathostomatidaer alhosloma1

-r
rcarnivores I (1) Cyclop� spp .. (2)�
1c�ts in stomachwall
L -- reptiles, etc. _
_
Physalopteroldea - -
Physalopteridae Physaloptera r:�ivores, --,st�ch - beetles, locusts,
ents --- -- cockroaches
Thelazloidea
Thelaziidae · mammals, birds conjunctival sac, lacrimal duc muscid flies, frLJ_it fli�
t I 1
Thelazia
Oxyspirura birds conjunct�al sac _ �9C__!<roaches
Rlctularioidea
Rictulariidae Pterygodermatites monkeys stomach, intestine cockroaches, European
earwig
Spiruroidea
Gongytonematidae mammals, birds oesoehagu� beetles, cockroaches
---
Gongylonema
Spiruridae carnivores, etc. stomach beetles. cock�aches
- _
Protosplrura, Spirura ---
Spirocercidae Spirocerca carnivores walls of oesophagus, stomach beetles, cockroaches
and aorta -
1•· Ascarops, pigs stomach beetles
Physocephalus,
Simondsia
Habronematoidea
Habronematidae Habronema, Oraschia equids stomach and stomachwall muscid flies
(skin)2
Tetrameridae Tetrameres birds proventriculus (glands) beetles, locusts.
cockroaches
Acuarioidea
Acuariidae Cheilospirura, birds giuardwall beetles, terrestrial
Dispharynx isopods
Echinuria water birds proventriculus, wall of small Oaphnia spp. and other
intestine small crustaceans
1 Dependent on the species, also other final hosts and only one intermediate host (Cyclops spp.).
2 When larvae are deposited in skin lesions.

to new hosts during feeding of the flies on conjunctiva!
fluid. In Europe, Thelazia spp. of cattle are transmitted
by Musca domestica, M. larvipara and Musca spp. Fruit
flies (Phortica variegata) are intermediate hosts of T.
cal/ipaeda. Prepatency lasts 3-6 weeks, adult worms
persist for a year and longer.
Occurrence and epidemiology. Thelazia spp. are
common in Europe. They were found, for example,
in 10-15% (DE), 4% (UK) and 53.5% (IT) of cattle
(dominating species: T rhodesi) and in 3% (SE), 10% (FR)
and up to 40% {IT) of horses (data are highly variable
depending on region and season). Autochthonous
infections of cattle and horses have been known in
Europe for a long time. According to data from England
prevalences in cattle are decreasing, probably due to
the broad use of macrocyclic lactones as anthelmintics.
T. cal/ipaeda in carnivores, initially predominantely
dis tributed in the Far East, was only observed in recent
years in autochthonous infections in southern Europe
(IT) (prevalences 30-40% in dogs) but is meanwhile
also found in southern Switzerland (prevalence 5.3%),
France, southern Germany (single case), later on the
Iberian Peninsula and in several Balkan countries. T.
callipaeda has a broad host spectrum and is also found in
cats (overall prevalence in Switzerland 0.8%, prevalence
in cats with ocular illness 9.2%), wild carnivores (e.g.
fox, wolf, beech marten), in hares (prevalence in Italy
23%) and in humans. Phortica spp. flies as intermediate
hosts are also endemic north of the Alps.
The/azia infections of cattle in Central Europe occur
predominantly during periods of high fly densities from
May to October. In tropical regions they are observed
throughout the year. Transmission of T callipaeda in
endemic areas of southern Italy peaks between July
and September.
Horses and cattle up to an age of 3-4 years are more
frequently infected than older animals. In contrast, dogs
older than 3 years, particularly of large breeds, are more
commonly infected by T. callipaeda than younger dogs.
Part Ill. Parasites and parasitoses: metazoa
Pathogenesis and clinical signs. The parasites are
found in the conjunctiva] pouches under the nictating
membrane and in the glandular ducts ( ► Figure 10.73
and 10.74). Bovine infections are often asymptomatic
(95% of infected cattle in Great Britain were free of
clinical signs). Follicular conjunctivitis and enhanced
lacrimation may occur in infections with > 10 adult
worms. However, in heavy infections also keratitis, even
ulcers of the cornea and uveitis are observed. Similar
signs to those in cattle develop in infected horses, dogs
and cats. The clinical picture is sometimes complicated
by bacterial superinfections.
Diagnosis. Adults may be found in the conjunctival
pouch after lifting the nictating membrane. Flushing
the conjunctiva! sack and the lacrimal ducts after local
anaesthesia allows for the isolation of various stages. LI
may be detected in the sediment of the flushing fluid.
Therapy and control. A single treatment with
ivermectin (0.5 mg/kg b.w., spot on) or doramectin (0.2
mg/kg b.w. s.c.) was highly effective against Thclazia in
cattle. Dogs were successfully treated with rnoxidectin
(2.5 mg/kg b.w., spot on) or milbemycin (0.5 mg/kg
b.w., orally, twice with one week in between). Also,
Figure 10.73. ThelBZis Iser/malls In
the eye of a h orse (length
of the worms approximately 10 mm) (Ph ot o: IPZ).
Figure 10.74. Adult The/az/a ca/lipaeda in the eye of a dog
(Photo: IPZ, F. Malacrida).
local application to the eye of moxidectin ( 1-2 drops of
a 1% solution) was effective. Cats were cured in 73% of
the cases by milbemycin (2.0 mg/kg b.w., orally, twice
with one week in between). Monthly application of
milbemycin to dogs reduced the prevalence by 90%.
Zoonotic importance. Human infections with r.
callipaeda, T. californensis or T. rhodesi are known from
several geographical areas, including Europe. Increasing
incidences are reported from Asia and may also be
expected in Europe due to the endemic occurrence of
T. callipaeda in southern Europe.
Selected references
Glangaspero A, Lia R,Vovlas N, OtrantoD(1999) Occurre nce
of Thelazia tacrlmalis (Nematoda: Spirurida: Thelaziidae) in
native horses in Italy. Parassitologia 41: 545-548.
GlangasperoA,OtrantoD,VovlasN,PucclnlV(2000)The/azia
gutosa Ralllet & Henry, 1910 and T/Jelazia skrjabini Erschow,
1928 Infecti on in southern Europe (Italy). Parasite 7: 327-329.
Hodzlc A, Latofa MS, Annoscia G,Alic A, Beck R, Lia RP,
Dantas-TorresF,OtrantoD(2014)The spread of zoonotic
metaziB calli()Beda in the Balkan area. Parasit Vectors 7: 352.
Mala C, Catarlno AL, Almeida B, Ramos C, Campino L,
Cardoso L (2014) Emergence of T/Jelazia cal/ipaeda In dogs
and cats from eastern central Portugal. Transbound Emerg
Dis,. DOI: http://dx.doi.org/10.1111/tbed12284.
Motta B, Nageli F, Nageli C, Solari-Basano �. Schiess! B,
Deplazes P, Schnyder M(2014) Epidemiology of the eye
worm T/Jelazia callipaeda in cats from southern Switzerland.
Vet Parasitol 203: 287-293.
Motta B, Schnyder M, Basano FS, Nagell F, Nageli C,
Schiess! B, Mallia E, Lia RP, Dantas-Torres F, 0tranto
D (2012) Therapeutic efficacy of milbemycine/pra ziquantel
oral formulation (Milbemax®) against Tt1elazia callipaeda
in naturally infected dogs and cats. Parasit Vectors 5: 85.
Otranto D, Tarsitano E, TraversaD,Deluca F, Giangaspero
A (2003) Molecular epidemiological survey on the vectors
of T/Jetazia gulosa, T/Jelazla rllodesi and T/Jelazia skrjabini
(Splrurida: Thelazildae). Parasitology 127: 365-373.
Otranto D, Dantes-Torres F, Mir6 G (2015) Thelaz1osis. In:
Baugnet F, Halos L (eds.) Parasltoses & vector borne diseases
of cats. Lyon, France: Merla! S.A.S., pp. 109- 1 t 2; ISBN
978-2-9550805-0-4.
Shen J, Gasser RB, Chu D, Wang Z, Yuan X, Cantacessl C,
Otranto D (2006) Human thelazlosls: a neglected parasitic
disease of the eye. J Parasitol 92: 872-875.
 10. Phylum Nematoda (syn. Nematozoa) (threadworrns or roundworms)
f
f
• Superfamily Spiruroidea
f sonography. Milbemycin treatment (0.5 mg/kg b.w. p.o.),
Species of this superfamily are predominantly found in
the upper digestive tract of mammals and birds. The life
cycle is indirect with arthropods as intermediate hosts
(► Table 10.13).
Family Spirocercidae
Genus Spirocerca
Spirocerca lupi
Disease: Spirocercosis In canids and fellds..
Agent and life cycle. S. lupi is a reddish, compact,
relatively large parasite (oo: 3-4 cm, ��:up to 8 cm).
Eggs are elongated with parallel sides, thick-shelled,
small (35xl5 µm), containing Ll. Adults are parasites
ofdomestic dogs, wild canids and occasionally cats (see
below). In dogs they are commonly located in tumour­
like lesions in the walls of oesophagus, stomach and dorsal
aorta. Eggs, containing Ll, are released through small
openings in a milky fluid to the lumen of the digestive
tract and are passed to the environment with faeces or
vomit. Coprophagous beetles act as intermediate hosts
in which L3 develop. After ingestion of infected beetles
by a definitive host, the larva is released in the stomach,
invades arteries of the stomach wall, migrates within 3
weeks up to the thoracic part of the aorta and settles
in the wall of the vessel. After 3 months and the final
moultings the parasites cross over to the neighbouring
oesophagus and establish in the submucosa. They induce
tissue reactions resulting in the formation of knots up
to the size of a golf ball. Each knot contains usually
several worms in a greasy, crumbly mass. Prepatency
lasts 5-6 months. Lizards, birds and rodents may serve
as paratenic hosts.
Occurrence. S. lupi is common in dogs, wild carnivores
(fox, jackal, wolf, etc.) and occasionally in cats in all
tropical and subtropical areas. It was occasionally found
in foxes in southern Switzerland. T he prevalences in
dogs in some areas reach 60-80%. Horses and ruminants
are incidentally infected. Another species, S. arctica,
occurs in canids in north-eastern Europe.
Clinical signs, diagnosis and therapy. Scars, left
in the aorta by S. lupi, predispose to aneurysms. Knots in
the oesophagus impair swallowing and induce vomiting.
Anaemia may develop due to blood loss in the knots.
The formation of osteo- and fibrosarcomas is favoured
by the infection. Eggs are demonstrated by faecal
examination (flotation techniques, flotation solution
with high specific gravity). Otherwise sedimentation and
SAFC techniques yield satisfactory results. Alterations
of the oesophagus can be detected by endoscopy and
started 28 days after experimental infection and repeated
in 4 weeks intervals, prevented the establishment
of parasites. A similar efficacy was observed after
repeated spot-on applications of a formulation of 10%
imidacloprid and 2.5% moxidectin (► Table 19.14, co
-0
p. 600). Treatment of diseased dogs with doramectin ·;::
2
(0.2 mg/kg b.w. p.o., three times at 2 weeks intervals (if 0..
U)
necessary repeated with increased dose of 0.5 mg/kg)
resulted in clinical cure and resorption of the worms,
provided the disease had not progressed too far.
Selected references
AI-Sabr MN, Hansen MS, Chrlel M, Holm E, Larsen G,
Enemark HL (2014) Genetically distinct Isolates of Spirocerca
sp. from a naturally Infected red fox (Vu/pas vu/pas) from
Denmark. Vet Paras/to/ 205: 389-396.
Austin CM, Kopk DJ, Crafford D, Schaper R (2013) The
efficacy of topically applied lmldacloprld 10% moxidectin
2.5% formulation (Advocate®, Advantage® Multi, Bayer)
against immature and adult Splrocarca lupi worms of
experimentally infected dogs. Parasitol Res 121 Suppl 1 :
91-108.
Fisher MM, Morgan JP, Krecek RC, Kelly PJ (2009)
Radiography for the diagnosis of spirocercosis in apparently
healthy dogs, St. Kitts, West Indies. Vet Parasite/ 160:
337-339.
en
Kok DJ, Schenker R, Archer NJ, Horak IG, Swart P (2011) The ..c
efficacy of milbemycin oxime against pre-adult Spirocerca lupi
°E
in experimentally infected dogs. Vet Parasitol 177: 111-118. -a;
:r:
Pazzi P, Goddard A, Kristensen AT, Dvir E (2014) Evaluation
of haemostatic abnormalities in canine spirocercosis and
its association with systemic inflammation. J Vet Intern Med
28: 21-29.
Vas E, Kelmer G, Shipov A, Ben-Oz J, Segev G (2013)
Successful transendoscopic oesophageal mass ablation
in two dogs with Spirocerca tupi associated oesophageal
sarcoma. J Small Anim Pract 54: 495-498.
- Superfamily Habronematoidea
Members of the superfamily are listed in ► Table 10.13.
Family Habronematidae
Habronema: Habros (G): tender; nema (G): thread.
Draschia: Richard von Drasche (1850-1923), Austrian
geoscientist, described 1883 nematodes from the
collection of the 'Zoologisches Hofcabinet' in Vienna.
 Part Ill. Parasites and paras1toses: metazoa
Genera Habronema and Draschia (stomach
worms of equids)
Disease: Habronematidosis in equids.
Summary
• Agents and life cycle. Habronema muscae, H.
microstoma (syn. H. majus) and Draschla megastoma
are globally distributed parasites of horses and other
equids. The adult nematodes (7-25 mm long) live In
the stomach of equlds. Females release thin-shelled
eggs containing a larva (Habrcnema spp.) or free L1
(D. megastoma) which are shed In the hosts' faeces.
Maggots of flies Ingest eggs or L1 which develop Into
l.3. These are transmitted to new hosts when the flies
are feeding on the llps, the nostrils or on akin lesions
of a definitive host. Swallowed larvae Invade the
stomach wall (D. megastoma) or attach to the mucosa
(Habronema spp.), causing stomach habronematldosls.
Prepatency: 2 months. Larvae deposited by the flies In
skin lesions do not develop further but cause cutaneous
habronematldosls (summer sore). A rare form of the
dlteaee II pulmonal habronemoala.
• Occurrence, epldemlology. Habronematldosls of
equlds occurs In Eurasia, Africa, the Americas and
Aultralla. Several species of flies act as Intermediate
hoetl; transml11lon depends on their densities and
actMIIN.
• PathogenHle, cllnlcal signs. Gastric habro­
nematldoal1: chronic catarrhal gastritis (Habronema
epp.) or noclulel In the stomach wall (D. megastoma),
mo9lly without clinical symptoms In spite of
convnon distinct pathological alterations. Cutaneous
hlbronematldOll1: ekln lesions which may persist
throughout the whole growing season. Predilection
..._ n extrwnltlN, per1orbltal area, In male animals
the ou1lr genitalia. Without re-Infections spontaneous
twnnQ It the beginning of the winter season. Pulmonal
hlbn>nlmolll: multiple nocluln containing larvae.
, T'ller8pv and control. Macrocycllc lactones are
efflctlvt agalnlt gutrlc stages ( ► Table 19.10) and
cure cut1n10U1 leelona within 2-8 wNka. Fly control
• 1 prophylactic measure.
Agents and life cycle. The adult stages of Habronema
spp. and D. megastoma measure 7-16 mm (c)'o') and 10-
Q)
25 mm (2�) in length. Habronema spp. live enclosed in
·o
C
'6 mucus on the stomach mucosa whereas D. megastoma
Q)
inhabits nodules in the stomach wall. The females release
LI (D. megastoma) or eggs with larvae (Habronema spp.)
<U which are excreted with the hosts' faeces ( ► Figure
C
·.:: J0.75). The life cycle i s indirect with flies serving
� as intermediate hosts. Musca domestica is the main
C intermediate host for H. muscae and D. megastoma,
>- and Stomoxys ca/citrans for H. microstoma. Maggots
0>
0 of flies living in manure ingest eggs or LI. During the
0
'fl,
metamorphosis of the flies to adults the LI develop into
L3. Flies hatched from the pupa contain infectious L3
<U
0..
which migrate to the head of the insect. When infected
muscids feed on ocular and nasal discharges on a host,
the larvae migrate through the proboscis to the lips
or nostrils, are swallowed and establish in or on the
stomach wall. Occasionally, they may migrate from
the nostrils into the lung, but a haematogenous way of
migration - possibly starting in the stomach - is also
discussed. Since S. calcitrans does not feed in the head
area of equids but on the extremities and the underbelly,
infections with H. microstoma might take place as a
result of the accidental ingestion of living or dead
infected flies. Prepatency lasts approximately 2 months.
Occurrence and epidemiology. Habronematidosis
occurs in Eurasia, Africa, the Americas and Australia.
The species with the widest distribution is H. muscae.
A recent study in Bavaria/Germany revealed that
20.5% of 400 abattoir horses were infected with adult
H. microstoma and 26.5% with H. muscae. These
prevalences were higher than in most other European
countries. In the Bavarian study infection intensities
were generally low (on average 84 H. microstoma and
118 H. muscae per animal), but a few animals had worm
burdens up to approximately 3,500. D. microstoma has
apparently not been recorded in Europe for a long time.
Transmission of habronematids depends on the presence
and activity of adult flies. In Central Europe, it is likely
that the main transmission occurs in summer and fall.
In other regions, other fly species than those mentioned
above can also be involved as intermediate hosts.
Pathogenesis and clinical signs
• Gastric habronematidosis. Habronema spp. cause
a chronic catarrhal gastritis associated with enhanced
mucus secretion and occasionally ulcerations. D.
megastoma invades preferentially the fundus region
of the stomach wall and induces the development of
granulomatous nodules. Confluence of several nod ules
may result in tumour-like alterations of the size of a
chicken egg, with a necrotic, caseous content and usually
several openings to the gastric lumen. In spite of distinct
pathological alterations clinical signs are usually lacking.
• Cutaneous habronematldosis. Flies with licking·
sucking mouthparts also feed on skin le sions and on
ocular discharges. On such occasions infective larvae of
habronematids leave the proboscis and invade the tissue
where they may survive for several weeks. Characteristic
alterations develop in response to the migrating larvae.
Predilection sites are the extremities, the periorbital
area, and the outer genitalia of male equids. Initially,
small inflammatory lesions may increase rapidly in size.
They are often very itchy and show a brownish surface,
sometimes raised more than 1 cm above the skin surface.
If untreated, the lesions persist throughout the whole
summer season but usually heal spontaneously with the
beginning of the winter.
+"
10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)

.,,,,,,,.- --...
L3 transmitted to wounds

( •
I ,, ,
I

eloprnent of
Its in stomach

I L3 transmitted by

I
flies to nose and
mouth (possibly
ingestion of flies

I
with L3)

I
-it� Maggot
Egg with
L1

Fly imago

I
Development of
L1 to L3 In stages

\.:'"'"' Fly�pa

Q)
Figure 10.75. Life cycle of Habronema spp. (Graphics: IPZ, S. Ehrat).
·u
C

i5
Q)
�
• Other forms of the disease. L3 may also migrate examination of the washing fluid is another diagnostic �
C'O
to the lungs or other body regions (peritoneal cavity, option. On the other hand, attempts to detect parasite C
·;:::
CNS) and induce granulomas. stages in biopsies of the gastric mucosa after pepsin-HCI Q)
digestion often fail. The diagnosis ofthe cutaneous form
Diagnosis. Routine coproscopy does not usually is usually based on the clinical picture, considering the C

detect eggs or larvae ofhabronematids. Techniques for seasonality oflong persisting lesions. A xenodiagnostic >- �
Ol �
detecting Habronema DNA are highly sensitive and method with detection of habronematid larvae in flies 0 I

allow the discrimination of species. Gastric lavage with has been successfully used for epidemiological studies. :§
'cii II
C'O
C'O
Cl..
 Part Ill. Parasites and parasitoses: metazoa
Therapy and control. Macrocyclic lactones
(ivermectin, moxidectin) in recommended doses are
effective against adult habronematids (► Table 19.10,
p. 592). Ivermectin improves the clinical picture of
cutaneous habronematidosis in most cases within 1
week and facilitates healing within 2-6 weeks. When
required, treatment has to be repeated. Fly control is
important as a preventive measure.
Selected references
Klei T R, Rehbein S, Visser M, Langholff WK, Chapman MR,
French DD, Hanson P (2001) Re-evaluation of ivermectin
efficacy against equine gastrointestinal parasites. Vet Parasitol
98: 315-320.
Rehbein S, Visser M, Winter R (2013) Prevalence, intensity and
seasonality of gastrointestinal parasites in abattoir horses in
Germany. Parasitol Res 112: 407-413.
Schuster AK, Sivakumar S (2013) A xenodiagnoslic method
using Musca domestica for the diagnosis of gastric
habronemosis and examining the anthelmintic efficacy of
moxidectin. Vet Parasitol 197: 176-181,
Schuster AK, Sivakumar S, Kinne J, Bablker H, Traversa D,
Buzzell GR (2010) Cutaneous and pulmonal habronemosis
transmitted by Musca domestica in a stable in the United
Arab Emirates. Vet Parasitol 174: 170-174.
Traversa D, Iorio R, Petrlzzi L, De Amicis I, Brandt S, Means
A, et al. (2007) Molecular diagnosis of squid summer sores.
Vet Parasitol 150: 116-121.
- Superfamily Filarioidea
Filum (L): thread; oideus (L): similar. Thread-like
nematodes.
The superfamily contains the families Filariidae and
Onchocercidae. Their members are called here in a
simplifying way 'filariae'. Pilarlae parasitise vertebrates
except fish, particularly in tropical and subtropical areas.
In definitive hosts, they inhabit connective tissue and
tendons, body cavities as well as blood and lymph vessels
(► Table 10.14). In tropical and subtropical regions
Dirofilaria fmmitls (in Europe, the Americas, Africa,
Asia and Australia) and D. repe11s (in Asia, Africa, and
Q)
C Europe) are of special veterinary lmportance as they
·0
'5 cause the heart-worm disease and the subcutaneous
Q)
dirofllariosis in dogs and cats. In subtropical and tropical
regions, filariae infecting humans belong to the most
co important pathogens. WHO (2014) estimates that 120
C
·c millions humans are infected with W11cl1ereria and
Q)
Brugia, the agents oflymphatic filariosis, and 26 million
.£ with Onchocerca volv1Jl11s which causes onchocerciosis
> and blindness ('river blindness'), the latter affecting
0)
0 approximately 265,000 people.
0
·u5
co
co
a..
Adult filariae (macrofilariae) are mostly very thin
nematodes with body length of females between a
few millimetres and more than 80 cm; the males are
much smaller. The small mouth opening is usually
surrounded by papillae, and the cylindrical oesophagus
is divided into an anterior muscular and a posterior
glandular portion (► Figure l 0.2, p. 255 ). Males without
bursa copulatrix, the posterior end is spirally coiled,
the spicules are dissimilar both in length and shape.
The vulva in females is located near the anterior end;
they are viviparous or ovoviviparous (shedding of LI
[microfilariae] or eggs with developed larvae).
Microfilariae are slender first larval stages approximately
200-350 �tm long ( ► Figure 10.82, p. 362). In several
filarial genera the microfLlariae are enclosed in a sheath
and are called 'ensheathed' ( ► Table 10.14). This
sheath is a remnant of the membrane, surrounding the
fertilised oocyte, which undergoes profound structural
changes during embryonic development. It results in
the formation of an elongated, elastic sheath which is
reinforced by proteins released by uterine cells of the
adult female. The permeability of the sheath is limited
to molecules <70 kDa, thus preventing access of host
antibodies to the larva. Since the sheath surface is an
area of interaction between the parasite and the host's
immune system, its surface molecules play a crucial
role in immune evasion strategies of the filarial species
which produce ensheathed microfilariae.
In definitive hosts, the microfilariae invade various
tissues (e.g. skin) as well as blood vessels and the
lymphatic system. In some filarial species (or strains)
inhabiting the lymphatic system, the appearance of their
microfilariae in the peripheral blood exhibits a marked
periodicity, with maximum densities of microfilarine
either at day time or at night. Typical for non-periodic
patterns is that microfilariae are constantl y present
in peripheral blood. These patterns appear to bl' well
aligned to the phases of feeding activity of the arthropod
intermediate hosts.
The life cycles of filarinc arc indirect nnd dl'pend on
haematophagous arthropods ns Intermediate hosts, in
which microfilariac, acquired from an infected definitive
host, develop into infectious L3.
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)

Tabl e 10.14. Genera (selection) of Filarioidea (also ► Table 10.17).

F.amlly, genus Important Geographlcal Locallsatlon In definitive hoat Sheath bf lntermlldlate

hosts distribution mlcrofllarlae hosts
Adults Mlcrofllarlae

Filariidae --
Parafilaria bovids, Europe, Asia, subcutaneous skin lesions -(absent) Muscidae
equids Africa connective
-- -
tissue
-- - -- -- -- -- ---·-
Stephanofilaria bovids cosmopolitan subcutaneous skin lesions + (present) Muscidae
--- connective tissue
- -- - - - - ---�--- -·
Onchocercldae
Setaria 1 ungulates cosmopolitan body cavities blood + Culicidae,
-------- Muscldae
Dirofilaria2 carnivores North & South subcutaneous blood - Culicidae
America, Asia, connective tissue,
Australia, Africa, blood vessels,
Europe heart -- 1--
-- ----
Loa2 humans Africa subcutaneous blood + Tabanidae
·---- ----- -
connective tissue --- - ---
-
Acanthocheilonema 3 canlds, cosmopolitan subcutaneous blood Ticks, fleas, lice.
rodents -- ----
connective tissue - --- -- - keds
-----
Wucheroria3 humans - tropics _ .!}'.mphatlc �y�em blood
- +
-- -- -- r-· --
Culicldae
Brugia3 humans, tropics lymphatic system blood + Cullcldae
monkeys,
carnivores
Dipatalonema3 canids (sub· )tropics subcutaneous blood - Hard ticks,
connective tissue Ceratopogonidae
Elaeophora 3 ungulates cosmopolitan blood vessels skin - Tabanidae
Mansone//a3 humans South America, subcutaneous blood (skin) - Ceratopogonidae
Africa connective tissue
(body cavities)

Onchocerca3 ungulates cosmopolitan connective tissue skin - Simuliidae.

Ceratopogonidae

Onchocerca3 dog, cat southern and subconjunctlval skin Simuliidae

Central Europe, nodules
USA - -- -- ----- -·------
Onchocerca4 humans Africa, Central & subcutaneous skin - Simuliidae
South America connective tissue

1 Subfamily Setariinae.
2 Subfamily Dirofilariinae.
3 Subfamily Onchocercinae.
4 Onchocerca volvulus.

(1)
Family Filariidae Summary T5
C

• Agent and Ufa cycle. P. bovlcola (length of !j!!j! up to

'6
Genus Parafilaria
(1)

6.5 cm) Is the causative agent of a disease in cattle

and buffaloes, characterised by the appearance of C'
cO
Para (G): beside. The genus Parafilaria was established cutaneous bleeding spots. The parasites Inhabit C
·;::
'beside' a previously common genus Filaria. subcutaneous nodules which open to the surface and (1)

release a haemorrhagic exudate containing larvated

Parafilaria bovicola eggs or free L 1 (microfllariae) produced by mature _£;
females. Flies (in Europe Musca autumns/is) ingest L1 >,
Ol
which develop into L3. These larvae are transmitted by 0
0
Disease: Bovine parafilariosis. infected flies to a new host when they feed on mucosa!
"iii
surfaces or wounds. Within a prepatency of 6-7 months cO
the larvae migrate to various locations of the body.
'Y
i....
Part Ill. Parasites and parasitoses: metazoa
A BU, RO, SE, BE, IT, possibly DE and AT). Further cases
• Occurrence, epidemiology, clinical signs. P. bovicola
has been recorded from countries in Asia, Africa,
South America, Europe and from Canada. Starting 4-5
months p.i. On Europe beginning of December), small,
subcutaneous nodules develop in various locations of
the skin (neck, withers, thorax, back, lumbar region)
followed by the appearance of bleeding spots which
contain gravid females. Pathological changes may
extend to undertying muscles and cause economic
loss to the meat Industry.
• Therapy and control. Preventive treatment of non­
lactating cattle with injectable ivermectln 10 weeks
before slaughtering, and fly control.
Agent. Adults of P. bovicola (do': 3-3.5 cm, 9':?. 5-6.5
cm) with short elliptic or cuticular ridges on the cuticle
of anterior end. The vulva in females is located besides
the mouth opening. Eggs: thin-shelled, 50x28 µm;
microftlariae: 185-205 µm in length, unsheathed.
Life cy cle. The adult parasites live in cattle and
buffaloes in subcutaneous and intermusculnr tissue.
They induce the formation of subdermal nodules which
open to the skin surface 7-9 months p.i. and which
release a haemorrhagic exudate(► Figure 10.76).
The exudate contains larvated eggs (► Figure 10.77)
and free microfilariae, produced by mature females.
When feeding on the exudate, flies (in Europe Musca
autumnalis, the face fly) ingest these stages which
develop into infective L3 in approximately 2 weeks.
Infected flies transmit the larvae via the proboscis to
mucosa! surfaces or wounds of a new host. From the site
of entry the larvae migrate to the subcutaneous tissues
of various sites(neck, withers, thorax, and back) and
develop into adults in approximately 61/2 months. The
parasites usually survive less than I year.
Occurrence and epidemiology. P. bovicola has been
recorded in countries in Asia, Africa, South America,
Europe and in Canada. Recent reports suggest that the
Figure 10.76. Parafi/arla bovlcola: skin lesions in cattle (Photo:
Torgerson et al. 1998).
parasite is endemic in several European countries(FR,
were reported in IR and NL. However, it is not always
clear whether cases are autochthonous or imported.
In 1980, 10% of beef cattle in SE showed muscle lesions
due to the infection. Meanwhile, the situation in SE has
improved: seroprevalence in 1990 had dropped to <3%
although the infection has spread geographically. The
disease shows a distinct seasonality, with skin lesions
usua.lly appearing between December and July(northern
hemisphere) or between June and January(southern
hemisphere)(see also below pathogenesis).
Pathogenesis and clinical signs. Early lesions,
caused by the larvae ore small, yellowish, oedematous foci
in the subcutnneous tissue. Later on, larger subcutaneous
lesions, 10-15 cm in diameter, sometimes confluent
and palpable, are found predominantly on the dorsal
parts of the body(neck, withers, thorax, back, lumbar
region). These lesions, containing filarial stages of 3-4
cm in length, are infiltrated with blood, enriched with
eosinophils and may extend to the underlying muscles.
Beginning in winter (January, February), dense, painless
nodules develop in the skin (2-4 cm in diameter and 5-10
mm in height) which persist until July. Finally, 'bleeding
points' occur at which a haemorrhagic exudate with
larvnted eggs and microfilariae is discharged through a
small opening(► Figure I 0.76). Exudation stops after
1-2 days and the nodules disappear within a few days;
they may, however, recur. The general condition of the
animals is not affected but the damage to the underlying
muscles is of economic importance. Heavy infections of
beef cattle may mean a loss of 10 kg per animal.
Immunology. Observations from endemic areas in
South Africa showed markedly reduced infection rates
already in animals of the second grazing season when
compared with those of the first season, suggesting early
development of protective immunity. Protection seems
to be stronger in female cattle than in males.
Figure 10.77. Egg of Parafilaria (about 25x45 µm) (Photo: IPG).
 10. Phylum Nematoda (syn. Nemalozoa) (threadworms or roundworms)

Diagnosis. The clinical picture and the seasonality IT and ES, but is lacking in Central Europe. The parasite
of the lesions are suggestive for parafilariosis. Eggs and does not develop in M11sca domestica.
microfilariae can be demonstrated in haemolysed, fresh
exudate (addition of a few drops of 3% acetic acid). Dried Occurrence and epidemiology. P. multipapillosa is
blood samples are unsuitable. Serodiagnostic tests were common in wide areas of Africa, Asia, South America,
developed and validated in Scandinavia. Indicative levels and in southern and eastern parts of Europe. Sporadic
of specific antibodies can be detected approximately 3 occurrence has been reported from AT (Burgenland).
months p.i. The fact that the parasite never spread in Central Europe
although it was repealedly introduced in infected horses,
Therapy and control. Treatment with macrocyclic e.g. from Russia, may be explained by the particular,
lactones (e.g. ivermectin 0.2 mg/kg b.w., s.c.) 10 weeks regionally limited spectrum of intermediate hosts.
before slaughtering kills the parasites and is usually In endemic regions, the frequency and intensity of
followed by regression of the pathological alterations of infection increases in equids up to an age of 6-8 years,
the musculature. Efficient fly control was more effective independently of the sex of the animals.
than chemotherapeutic measures in reducing P. bovicola
prevalences in South Africa. Animals imported from Pathogenesis and clinical signs. During the warm
endemic regions should be treated with macrocyclic season, in Europe predominantly during July and August,
lactones to prevent importation of the parasite. infected equids develop within days subcutaneous, dense
nodules of 1-5 cm in diameter which are painless but
Parafilaria multipapi/losa obviously itching. Predilection sites are shoulders,
withers and the lateral chest. Sometimes the picture is
similar to urticaria. The nodules brake open, releasing
Disease: Parafilariosis in equines (summer bleeding). through small openings (~1.5 mm) a haemorrhagic
exudate containing eggs and microfilariae ( ► Figure
10.78). Warm weather and sunshine seem to stimulate
Summary the bleeding which continues for minutes or hours.
Thereafter, the nodules regress within 3-4 days. Small
• Agent and life cycle. Adult nematodes (!? � up to 7 cm
hairless, depigmented sites mark the previous lesions.
long) are located In subcutaneous lesions and nodules
Swellings and bleedings may occur evenly distributed
of shoulder, neck, withers, lateral chest, etc. of equids.
Nodules break open for a short time with bleeding, and
throughout the whole summer. Relapses may occur
females release larvated eggs into a haemorrhagic over a period of 4 years, independently of reinfections.
exudate which attracts flies. Eggs or L 1 present in the
exudate are ingested by flies and develop into L3 which
are transmitted to a new definitive host.
• Occurrence, epldemlology, cllnlcal signs. Common
in Africa, Asia, South America, southern and eastern
Europe, sporadic occurrence in Central Europe in
imported animals. Nodules bleed for a short time
(hours) at high environmental temperature (in Europe
July/August) and heal superficially within a few days.
Annual recurrences are possible.
Diagnosis and therapy. Clinical signs of 'summer
bleeding' are pathognomonlc. The detection of eggs
or L1 succeeds in the best case only In fresh exudate.
A single treatment with iverrnectin leads to remission
of the nodules.

Q)

·u
C

Agent and life cy cle. The adults of P. multipapillosa '5

Q)
are up to 3 cm long, the females up to 7 cm. Thin-shelled �
eggs (25x50 µm) with larva. Microfilariae unsheathed, �
(1j
160-190 µm in length. The indirect life cycle corresponds C
·;;::
in principle to that of P. bovicola, with a prepatency of
9- I 3 months. Females survive in the subcutaneous or
intermuscular connective tissue for at least 2-3 years. -�
The spectrum of intermediate hosts is only incompletely >,
Ol
known. Formation of L3 is reported in Haematobia 0
0
atripalpis (syn.: Haemotobosca atripalpis), a biting fly on Figure 10.78. Parafilaria multipapillosa infection in a donkey: 'iii
pastures occurring in south-eastern and eastern Europe, (a) bleeding skin lesion (arrow); (b) magnification of a bleeding
wound (Photo: IPZ, J. Eckert).
Part Ill. Parasites and parasitoses: metazoa
Nodules may be followed by scars which may lead to
pressure marks under saddle and harness.
Diagnosis. Diagnosis is based on clinical symptoms
and the detection of eggs and larvae in the exudate.
Therapy and control. Single dose application of
ivermectin (0.2 mg/kg b.w. s.c.) results in remission of
nodules, prevents bleeding and the formation of new
nodules. In non-endemic areas no further measures are
required. In endemic areas flies should be controlled.
Treatment with ivermectin in periods before clinical
signs occur may be a useful preventive measure.
Genus Stephanofilaria
Disease: Stephanofilarlosls in cattle and buffaloes
(Europe: summer lesions of cattle),
Steplranos (G}: wreath, rim. Refers to a circumornl
denticulated rim.
Summary
• Aaent. lh cycle. Small nematodea (�� up to 1 cm
long) Inhabiting tht aubcutll of cattle and buffaloes
with lndnct llfe cycle In which fllea (Muscldae) act
• lntermedlatt holtl. Pfll)atency at leaat 5 months,
edub p,oblbly IUrvlYe for yeara.
• C>oolrNnoe, ollnloal llgne. Bovine stephanofllartal
dlrtMlllll ha bNr'I oblerved In Alla, Australla, North
111d SouU, Amlftol and Europe (DE, FR, suspected
with the MCOnd grazing season
lun,pNn oondlttona cattle develop
lellarll on tht undM'btlly, acrotum and
•� iif� If 11ft unnattd, pnlat the whole
""""1-iiiDn. Llllonl on tht udder may hamper
,... 11".1.d-- oontlmlnatlon of the mllk,
1'NlniMt. 'ftlamlntwllh macrocycllo lactontl l'IIUltl
" ....■Ion d the akin llllonl within 2-3 WNkl but
dott not� rlllpeN In tht followtng year.
Agent. Members of the genus Steplumofllaria arc small
nematodes (. <? up lo I cm long) inhabiting the subcutis,
predominantly of cattle and buffaloes. The oral opening
is surrounded by a protruding denticulated rim, males
with unequal spicules. Eggs: thin-shelled, approximately
30x60 µm, microfilariae relatively short (SO- I SO µm),
ensheathed (see below).
Several Stephn11ofllnria species have been described in
cattle and buffaloes, including S. stilesi (North America,
Australia, Russian part of Asia). S. assnmensis (India,
southern Russia) and S. dedoesi (Indonesia). Other
species infect pigs, rhinoceroses or hippopotamuses.
Little information exists regarding Stephanofilaria
spp. occurring in Europe and some other regions (e.g.
South America). The morphology of a Stephanofllaria
sp. found in France resembled S. stilesi but a conclusive
species identification was not possible.
Life cycle. The adult parasites live in subdermal
cysts and cause locally restricted exudative dermatitis.
Females release microfilariae which can be found in the
exudate and the surrounding skin. Intermediate hosts
are muscid flies, for example the horn fly Haematobia
irritans for S. stilesi in the USA and Australia. The same
species was suspected as vector in France. After uptake
of LI from the dermal exudate, infectious L3 develop
in the fly within 2-3 weeks and are transmitted to new
flnul hosts via the proboscis. The larvae invade the host
thrnugh Oy bile lesions or small wounds in the skin and
rench scxunl mnturity nfter 2 moults. Prcpatency is not
exucl'ly known but probably lasts longer than S months.
Since the olterntions recur annually, ii is suggested that
nduh worms survive for several years.
Occurrence and epidemiology. Slephanofllariosis is
n local and seasonal disease of call le observed previously
in DE, FR. There is, however, no recent information. The
disease has been observed in male and female cattle in
which clinical signs appeared at the earliest in the second
grazing period. Usually, only some of the animals in a
particular herd ( I 0-30%) arc affected and may show
annual relapses.
Pathogenesis and clinical signs. Clinical signs
usually appear in cattle in their second grazing season
and also in older animals in the following years. Starting
2-4 weeks after turnout to pasture, animals show pea­
sized, exudative efflorescences. Predilection sites arc
the underbelly caudal of the sternum, stifle fold, udder,
particularly the teats, and the scrotal area. Within
2-5 days a clearly demarcated excoriation develops,
measuring 5-6 cm in diameter(► Figure 10.79). The
lesions exudate, especially on hot and humid days, while
they dry up with formation of cracked crusts during
cooler weather lasting for several days. Although the
wounds nre 1101 closed under scarring, some rcsululion
lakes places in cooler weather in Seplemher/Oclobl•r,
but new eruptions may occur In the following gruzing
period. This alternation between eruptions and recovery
Is a characteristic of all slephanofllarioscs. The cxuclnting
Figure 10.79. Stephanofilaria spp.: 'summer lesions' on udder
of cattle (Photo: H. Zahner).
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)
lesions itch and are permanently frequented by insects
so that the animals are continuously annoyed. If the teats
of cows are affected, milking may be difficult, and the
milk may become contaminated with blood and exudate.
In male animals orchitis was observed associated with
skin lesions on the scrotum. Other species of the genus
Stepha11ofilaria cause wounds on other body regions.
Diagnosis. Diagnosis is based on clinical signs and the
detection of parasite stages in skin biopsies. Attempts
to demonstrate eggs and microfilariae in exudates
usually fail.
Therapy and control. Symptomatic treatment is not
usually successful. After application of ivermectin (0.2
mg/kg b.w. s.c.) skin lesions usually resolve within 2-3
weeks (in cows pour-on application of eprinomectin and
moxidectin may be tried in order to avoid withdrawal
periods for milk delivery; ► Table 19.2, p. 579). Since
all these drugs are ineffective against adults they cannot
prevent relapses.
• Selected references m::==:===i===::a
Bech-Nielsen S, Sjogren U, Lundquist H (1982) Parafilaria
bovicola (Tubangui, 1934) in cattle: epizootiology - disease
occurrence. Am J Vet Res 43: 945-947.
Caron Y, Groignet S, Losson BJ, Saegerman C (2013)
Three cases of Parafilaria bovicola infection in Belgium, and
a few recent epidemiological observations on this emergent
disease. Vet Rec 172: 129.
Dirksen G (1959) Stephanofilarien als Ursache der
'Sommerwunden' des Rindes in den nordwestdeutschen
Weidegebieten. Disch Tierilrztl Wochenschr 66: 85-88.
GaluppiR, Militerno G, Bassi P, Nanni A, Testonl S, Tamplerl
MP, Gentile A (2012) Evidence for bovine parafilariosis In
Italy: first isolation of Parafilaria bovicola (Tubangui, 1834) from
autochthonous cattle. Vet Parasitol 184: 88-91.
Gibbons LM, Zakrisson G, Uggla A (2000) Redescrlptlon of
Parafilaria bovicola Tubangui, 1934 (Nematoda: Filarioldea)
from Swedish cattle. Acta Vet Scand 41: 85-91 .
Hamel D, Axt H, Pfister K (2010) First report on Parafilaria
bovicola (Nematoda: Filaroidea) in Germany. Res Vet Sci
89: 209-211.
Johnson SJ (1987) Stephanofilariasis - a review. Helminthol
Abstr (Series A) 56: 287-299.
Maloufi F (1995) Equine parafilariosis in Iran. Vet Parasitol 56:
189-197.
Swan GE, Soll MD, Gross SJ (1991) Efficacy of ivermectin
against Parafilaria bovicola and lesion resolution in cattle.
Vet Parasitol 40: 267-272.
Torgerson PR, Doherty ML, Healy A M (1998) Bovine
haemorrhagic parafilariosis in an imported charolais bull.
Irish Vet J 51: 27-29.
Watrelot-Vlrieux D, Pin D (2006) Chronic eosinophilic dermatitis
in the scrotal area associated with stephanofilariasis
infestation of charolais bull in France. J Vet Med B Infect Dis
Vet Public Heatth 53: 150-152.
Family Onchocercidae
Ogkos (G): hook, bending; cercos (G): tail. Refers to
the bent posterior end of the microfilariae of some
Onclroccrca species.
The family contains 8 subfamilies with more than 70
genera which occur in reptiles, amphibians, birds and
mamrm.11s. Morphologically, the Onchocercidae differ
from Filariidae inter alia in the position of the vulva
of the females which is located in the anterior half of
the body behind the nerve ring. In definitive hosts
Onchocercidae inhabit connective tissue, body cavities
or blood and lymph vessels. From the predilection site
of the females, microfilariae disseminate in the host
organism and are found in the skin or in the blood
from where they are taken up by haematophageous
arthropods that act as intermediate hosts ( ► Table
10.14, p. 353).
With the exception of a few species (e.g. Acantho­
cheilonema viteae) Onchocercidae contain intracellular
rickettsia-like microorganisms of the genus Wolbachia,
which are also common in arthropods. They are passed
vertically to the next generation and are regarded as
essential endosymbionts. When dogs infected with
-
en
.c
D. immitis are treated with the antibiotic doxycycline
-E
(I)
(which is active against Wolbachia), parasite embryo­ :r:
genesis, production of microfilariae, and long-term
survival of adult stages are inhibited (see therapy
below). Furthermore, the microorganisms play a role
in immunological interactions of the host with the
nematodes.
The most important genera of the family in mammals
are listed in ► Table 10.14. Here we discuss a selected
group of relevant species.
Genus Dirofilaria
(I)
Dirus (L): cruel, horrible;filum (L): thread.
·u
C
(I)
Dirofilaria species are parasites of dogs, other canids, and �
cats. D. immitis inhabits the arteria pulmonalis and the 2:-
-
co I
i
heart, and it is the agent of cardiovascular dirofilariosis, C
·;::
whereas D. repens causes cutaneous infections.
I
� /1
,£;
·u5
co I
I!
co
Part Ill. Parasites and parasitoses: metazoa

Dirofilaria immitis (heartworm)

Disease: Cardiovascular dirofilariosis in dogs, other
canids and cats (heartworm disease}. I may be poor. Furthermore, thrombosis prophylaxis and
Summary
• Agent. Adults of o. immltfs are thin and longworms (9 9
up to 30 an) inhabiting the arterla pulrnonalls and the
right heart of carnivores, especlally canlda; unsheathed
mlcrofilarlae In the blood.
• Occunnce, life cycle, e pidemiology. Common In
wann climates, lncrNtlngty spreading to tempnte
1'9giona. In nllffllc '9Q1ons d the USA and IOUthem
Europe local pr'l'1lllencea In dogs over 50'6. lnchct llf9
cyclewfthCulcldll(nul1IIIOUlapeclel)IS�
holta, which Ingest mlaoft1arlH dlrtng blood flldlng
and tranemlt L3 to MW holtl. PMdultl Httlt after
a p proximately 3 montha In the arterta pulmonalls
and heart. Prlpatancy at leut 6 montha but highly
varlabll. Mlcrotllaranla l'IIChee a plateau after 9-1 O
p.L; 3CM09fl oflnflcted dogs rtn1U1 or become
Mfillfwftl,._,__mto11r1In lpb of pnlatlng adults. In catl
llllil'!llllllllfliWM appwln the blood In approxlmately 5096
llgrll. Often asymptomatic,
'tlrtlllln the U1Q1 and other
l'lyplrttllllon , hypertrophy of
cues decompensatlon
Oldemu, ucltes; often
ecnmas. Clinical
� frequent vomiting.
Vina cava and the right
J,y aggregated wonns and
(¥11,a CIYI syndrome). The
Vll1lbll.
mbaflatll In blood samples;
of other, largely
--- Dlllollor1 of specfflc
.. blood with oommen::lal teet
antibody detection 11 of
.... butnot lndogl.
...
• Therapy and prophylaxis. Melarsomine, an arsenical
compound, is an effective adulticide, but tolerability
other adjunct therapy are advisable. An alternative is a
combination therapy with doxycycline and a macrocyclic
lactone. Surgical removal of adult parasites is especiall y
indicated in cases of vena cava syndrome. Effective
prophylaxis is possible by application of macrocyclic
lactones during the mosquito season. Drug resistance
of D. immltis (see below).
• Zoonotlc Importance. D. immitis and more frequently
D. rapens can be transmitted to humans, Infecting
predominantly lungs or subcutis, respectively.
Agent. Adults of D. immitis are thread-like, approxi­
mately l mm thick nematodes with body lengths of
12-18 cm in males and 25-30 cm in females. Six small
papillae surround the mouth opening. The spirally coiled
posterior end of the male bears 2x 5 pre-anal and 2x 6
post-anal papillae. Spicules measure 180-300 µm and
300-375 µm. The posterior end of the female is blunted.
The vulva is located approximately 3 mm behind the
anterior end. The unsheathed microfilariae measure
around 300 µm after formalin fixation in the Knott
test ( ► Table I 0.15). Generally, length measurements
may differ widely depending on the method of staining
and fixation.
Life cycle. D. immitis inhabits the arteria pulmonalis
and the right heart of carnivores, predominantly of
dogs and other canids (► Figure 10.80). Unsheathed
microfilariae, released by females into the blood, are
ingested by blood-sucking mosquitoes which act as
intermediate hosts. The density of microfilnria e in
the peripheral blood varies in the course of the day.
Microfilaraemia is highest in late afternoon and l'tirly
evening in accordance with the highest activity of the
intermediate hosts nnd decreases subsequrntly by 80-
95%, where upon the microfilariae accumulate in tht•
capillaries of parenchymntous orgnns, mainly in the
lung. Thi periodicity is probably regulated by chungcs

..........
Table 10.15. Characteristics of (unsheathed) microfilariae in blood of dogs. 1

,..... �,._,. Aoantltoohellonemr

rec,ondltum
Dlpeta'°11emr
dracuncuJokM

Mean length ± standard 1301.8±6.3 369.4:tl0.8 264.8±5.5 259.4:t6.7

devlatioo4 (µm) -

-
�-
�
Antenor end
Posteno, end
conical
Strrughl
blunt
hook- shaped
. straight, in 30-40%
blunt conical
straight
-i
I
-- 8XCf8l0f'Y and anal . anal porus. partially I
1
hook-shaped
l..ocatlOll Of aad
•·

c1Jffuse
t anal porus. excretory
phosphatase actMty porus also lflne< body ' porus (ringlike) and
coo)plex I
i n-between
1
Ensheathea � crly in Bruga infecuons w1 Asia.
2 Pr&..,ous name of the genus [}peta/onema.
3 Syn. Acant�.
◄ Meastlernents a�er lixatlOO 111 Knon test.
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)

Uptake of
microf1larlae in blood
Transmission of L3 by mosquito
by mosquito

''
'
/
/
L \
I I
I I
I Adult worms In
,. blood vessel

Mosquito (Culicldae)

Larva 3

So-called sausage form (I)

·u
C

Larva 2
2
�
Fig ure 10.80. Life cycle of Dirofilaria immitis (Graphics: IPZ, S. Ehrat). C1l
C
·c

in the partial pressure of oxygen in the blood that occur and invades the definitive host through the wound, -�
during the course of the day. The microfilariae develop generated by the blood-feeding mosquito. The larva >,

into infectious L3 in the mosquito depending on the
environmental temperature. This development takes
approximately 2 weeks at 26 °C and subsides below
14 °C. The infectious larva migrates to the proboscis
moults into L4 in the subcutaneous tissue within 1-2
weeks, migrates between muscle fibres, and after a last "iii
moult penetrates the wall of a vein and arrives in the
C1l
arteria pulmonalis or the right heart 70-110 days p.i.

11
Part Ill. Parasites and parasitoses: metazoa

At that time it has grown up to a length of 2-3 cm. The spectrum of intermediate hosts is broad and
The parasites reach sexual maturity at the earliest 180 comprises practically all genera of Culicidae; >60
days p.i. but usually need a longer time. Thereafter, the species of mosquitoes have been described as more or
females release microfilariae. Microfilariaemia increases less competent vectors. Cu/ex pipiens, Aedes vexans,
until 9-10 months p.i. but subsequently levels off to Ae. punctor, Ae. albopictus, Ae. caspius and Anopheles
a plateau-like course which may be maintained for a maculipennis are species whose vector capacity in
long time. However, in 30-50% of infected dogs the European countries is documented ( ► p. 459).
density of microfilariae in the blood drops down to
levels below the detection limit. It cannot be predicted The environmental temperature is a crucial epide­
when this happens, but it starts after development of a miological factor. The Heartworm Development Unit
stage-specific immunity targeted at microfilariae. The (HDU), a commonly used indicator in the USA, was
adult worms may persist and survive up to 7 years. introduced to estimate how many generations of L3
may develop in the regional mosquito population
Cats are less susceptible to D. immitis than dogs (when within 1 year. Eight to ten generations may occur in the
applying the same infection doses, dogs may harbour highly endemic region of the Po river valley. However,
8-10 times more adult fllariae than cats). In endemic autochthonous infections are still realistic in areas where
areas prevalences in cats are distinctly lower than in only 2 generations can develop, as demonstrated in the
dogs. Only approximately 50% of infected cats become north-eastern part of France. According to the HDU,
microfi!araemic, and parasitaemia is usually low and the Rhine valley in Germany allows the development of
lasts only for 1-3 months. Survival time in cats is 4 generations of L3, i.e. imported cases could initiate an
generally limited to less than 2 years. autochthonous D. immitis cycle in this area. It should
be noted that D. immitis and D. repens coexist in many
Occurrence and epidemiology. D. immitis is European endemic regions.
endemic in most tropical and subtropical regions
(the Americas, Africa, Europe, Asia and Australia) Pathogenesis. Predilection sites of adult D. immitis
and seems to spread increasingly to temperate areas. are the arteria pulmonalis and the right heart ( ► Figure
Thus, originating from the south-eastern coastal states I 0.81). Clinical symptoms during prepatency and early
of the USA, the infection extended in recent decades patency are usually limited to massive infections when
across the American continent up to Canada. Endemic the parasites impede the functions of the cardiac valves.
regions comprise southern Europe (PT, ES, southern Patent infections may remain asymptomatic or become
FR, IT, GR, HR, BA, HU, TR, RU) with some northern symptomatic due to primary vascular and pulmonary
extensions (up to SK, CZ, VA). The regional prevalences lesions and subsequent effects to the right heart. With
depend on the respective climatic conditions and the the arrival of the parasites in the pulmonary arteries,
vector densities. In northern Italy (Po river valley), first lesions include damage to the endothelium leading
prevalences in dogs mount to 50-80%, in cats to 24%; progressively to obliterative endarteritis, intravaSCltlar
lower prevalences are found in central and southern Italy. villus formation and thromboembolism. The damaging
In France, mostly the Mediterranean coast is affected, effects of the worms are predominantly attributed to
but autochthonous infections happen even in northern their antigenic products and substances from Wolbac/1i11
regions. In the southern provinces of Spain prevalences (see above). Furthermore, immune complexes, formed
of 10-40% have been recorded. The situation is similar in a situation of antigen excess, might also be involved
in the eastern Mediterranean areas. High prevalences as they show high affinity to endothelia. Increasing
are found on Mallorca (>30%) and Gran Canaria (60%). stenosis of lung arteries and an evolving pneumonia
Sporadic autochthonous infections arc also known from with oedema and inflammatory processes lead to
the south of Switzerland. Cases observed in DE and AT
to date were probably imported. Imported infections
concern dogs after short-term stays in endemic areas
(according to a study 12.6% of dogs which developed a
right heart disease after travelling to endemic areas were
infected with D. immitis) and animals imported from
endemic regions, often stray dogs. Patent D. immitis
infections are also known in dingoes, coyotes, red and
grey foxes, wolves, lions, polecats and ferrets. From an
epidemiological point of view, cats play a minor role
since microfilariaemia is low and of short duration.
Sea lions, seals and black bears have been found to be
infected.
Figure 10.81. Dirofilaria immitis in arteria pulmonalls of a dog
(Photo: G. Hutchinson).
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)
pulmonary hypertension and eventually to hypertrophy
of the right heart. In chronic cases, decompensation
and dilatation of the right heart result in chronic
passive congestion with liver enlargement, oedemas
and ascites. Glomerulonephritis due to immune
complexes originating from continuously released
parasite antigens represents a frequent complication of
the disease. Infected dogs often develop an eczematous
dermatitis, probably due to the kidney disorders. Ectopic
localisations (brain, eye, etc.) of heartworms rarely occur
and may cause related pathologies.
Clinical signs. Dirofilariosis in dogs may remain
asymptomatic for months or years, depending on the
worm burden and other factors. Clinical signs develop
gradually, often beginning with chronic cough, later
on associated with dyspnoea, frequent regurgitation,
lethargy and loss of condition. Further signs of the
progressing disease include tachycardia, tachypnoea
and the vena cava (or caval) syndrome, the latter
predominantly occurring in small dogs. The term
denotes a partial obstruction of the vena cava and the
right cardiac chamber with functional impairment
of the cardiac valves by aggregates of adult worms
displaced from the pulmonary artery. This is an acute
life-threatening disease with shock-like symptoms,
often associated with intravascular haemolysis and
dark, brownish urine. When a right cardiac failure
develops, intraperitoneal fluid accumulation and
swelling of the limbs may follow. Acute attacks with
severe dyspnoea and haemoptysis may occur, caused
by sudden thromboembolism.
The clinical picture in cats is very variable. The infection
often takes an asymptomatic course or clinical signs are
less pronounced because usually only a few worms are
present and microfilaraemia is low or absent. However,
there are reports on sudden deaths after occlusion of
blood vessels when worms were swept off their sites.
Immunology. D. irnrnitis infections in dogs are
immunologically characterised by (a) a suppression
of T cell reactivity, beginning with the onset of
parasitaemia, (b) a temporary, selective (antigen
specific) deficit of circulating antibodies to microfilarial
antigens, (c) a stage-specific immunity and (d) severe
immunopathological consequences.
T cells of infected dogs show poor reactivity to mitogens
and fail to proliferate in response to D. irnrnitis antigens.
Reaction patterns to fi larial antigens on the cytokine
level are complicated. They do not match with a
classical Thl/Th2 paradigm but rather represent a
mixed type. IL-10, which impairs the synthesis of Th 1
associated cytokines, is only produced by lymphocytes
of parasitaemic dogs. Humoral responses are dominated
by the synthesis of IgG 1 antibodies, which may be
associated with a Th2 type reaction as is postulated
for other filarial infections. Usually an inverse relation
exists between microfilariae density and antibody levels
but it is not clear whether this is caused by specific
immune suppression or by antibody consumption
due to high antigen levels in parasitaemic animals.
In particular microfilaraemic hosts lack antibodies
to surface components of microfilariae, but in sera
of amicrofilaraemic dogs such antibodies are present
which agglutinate microfilariae in vitro and eliminate
them in vivo by ADCC reactions. It is a strictly stage
specific immunity since the adult worms may persist
in amicrofilaraemic dogs for long time. Corresponding
situations are known from filarial infections in other
host species.
Protective immunity to challenge infections can be
experimentally induced in dogs by the application of
X-ray attenuated LJ. It seems to be mediated by antigens
which arc synthetiscd during the moulting phase from
L3 to L4. In contrast, naturally infected dogs are only
partly protected against challenge infections. However,
this limited immunity seems to be at least sufficient to
keep the worm burden at a moderate level. Dogs living
in highly endemic areas rarely harbour more than 10-20
adult D. immitis.
Immunopathological processes of the disease are
primarily influenced by high levels of circulating immune
complexes and their consequences: endothelial damage,
vasculitis and perivascular infiltrations in the lungs and
glomerulonephritis. There is evidence that antigenic
components of Wolbachia play an immunopathological
role.
Diagnosis in dogs. The clinical picture in consideration
of an anamnestic report (stay in endemic area) may
justify a tentative diagnosis. Imaging techniques may
visualise alterations of the heart and vessels. Often
diffuse shadows in the lungs are observed by X-ray.
The parasites can be demonstrated by sonography.
Auscultation, US examination and ECG are helpful
in advanced infections. Proteinuria as an indicator of
glomerulonephritis is a frequent sign. Eosinophilia can
only be detected in I 0-20% of the patients. Microfilariae
in the blood are found in only 50-70% of the cases,
although sometimes >100 microfilariae/mm3 blood
can be observed in positive dogs in the early evening.
Q)
·o
C
The etiologic diagnosis in dogs is predominantly based '6
on the detection of microfilariae in blood (rarely also �
Q)
in the urine) and of circulating antigens. In both cases >,
reliable results can be obtained only beginning 5-6 (Cl
C
months p.i. However, the antigen assay is the more ·c
Q)
reliable test.
-�
• Detection of circulating antigens. The assays >,
0) I
determine circulating excretory-secretory antigens 0
of adult female D. irnrnitis by monoclonal antibodies. ·u5
11
Several commercial test kits are available. They detect
(Cl
infections with at least one sexually mature female
Part Ill. Parasites and parasitoses: metazoa

worm, react also in amicrofilaraemic dogs and are highly

specific for D. immitis (cross-reactions in infections
with D. repens and A. vasorum can almost completely
be excluded). A positive correlation is usually observed
between antigen levels and worm counts. In case of
small numbers of worms and in dogs which had
been chemoprophylactically treated with macrocyclic
lactones, the sensitivity of the tests can be reduced.

• Detection of microfilariae. Amongst other

procedures the Knott's method was proven successful in
detecting microfilariae in the blood ( ► p. 526). It allows
a concentration of the microfilariae after haemolysis of
the blood, the fixation of the larvae with formaldehyde
and specific staining. It is necessary to exclude infections
with non-pathogenic or only weakly pathogenic fllarial
species which also release unsheathed microftlariae into
the blood (D. repens, Aca11tlwchcilonema reconditwn,
Dipetalonema dracunculoides) and which may coexist
with D. immitis in particular geographical areas(► Table
10.16). Theoretically, Dimfilaria microfilnriae can be
classified by their size (► Table 10.15), however, the
measurements are strongly influenced by the ftxation
technique employed. Histochemical investigations,
localising the activities of acid phosphatases in the
larvae, facilitate the differentiation of D. immitis and
D. repens (► Figure 10.82). By applying the filter
technique (► p. 526) for the examination of a blood
sample, microfilariae adhering to the filter can be
directly stained. Alternatively, DNA analyses may be
used for species differentiation.
• Specific antibody detection. Specific antibody
detection is of little value in the diagnosis of D. immitis
Figure 10.82. Localisation of acid phosphatase activity in
mlcrofilarlae (arrows): Dirofilarla repens (top), Dirofilaria immitis
(bottom) (► Table 10.15) (Photo: IPZ, P. Deplazes).
in dogs. In fact, humoral antibody concentrations usually
rise beginning approximately 3 months p.i., but the levels
fluctuate substantially in the course of the infection and
decrease to unreliable concentrations 9-10 months p.i.
Parasitaemia and antibody levels are often invers ely
related. Circulating antibodies persist for at least 6
months after effective chemotherapy.
Diagnosis in cats. The diagnosis is difficult. The
animals often remain amicrofilaraemic, and a ntigen
assays may fail to detect the usually weak infections.
Imaging techniques may be helpful to demonstrate the
parasites. In contrast to dogs, antibody assays may be
useful, in particular if specific, recombinant antigens
are employed.

......
Table 10.16. Fllarlal species of carnivores to be considered In differential diagnosis of suspected Dirofi/aria immitis infections.

Qeographlcal Deflnltlveho1ta(O)and Predlleotlon llt• Pathology

dlltrlbution vecto,. (V)

- Adults Mlcrofllarlae

J
Dlrof,tn11n ,upHns 1 Europe, Africo, D: dog, cot, wild carnivores subcutis skin, blood mostly opatt1ogenic,
I Asia V: Culicldae rarely pruritus. eczema
Acant11ocl101Ionema Europe, North D: dog, wild canlds subculls, blood apathogenic
recond,tum2 and South V: fleas (Ctenocephalldes body cavities,
I

-
Amenca, Asia, spp.), llce internal
Australia or�ans
�
Oipetalonema I Europe, Asia, , D: dog, fox, hyena peritoneal blood apathogenic
(Acanthoc/1eilonema)
dracunculo,des
1- -
Africa

1
: V: hard ticks (Rhipicepha/us cavity
sanguineus)
Carcopithlfitaria b8inae, I southern and - D: dog
- --
subcutis skin
-
apathogenic
-I
C. grassi, etc. eastern Europe, V: hard ticks (Rhipicephalus
I Africa, South sanguineus)
America
1 Common species: regional prevalences ot 30-40%.
2 Previous species name: Dpe
i talonema recond,tum; prevalences usually <2%.
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)
Therapy. Treatment of dogs with patent infections is
still problematic. Possible options are chemotherapy
and surgical interventions.
• Chemotherapy. Melarsomine (Immiticide•),
an arsenical compound, is the only available drug
with high activity against adult stages of D. immitis
(macrofilariae). According to the American Heartworm
Society(AHS, 2014), melarsomine therapy of dogs with
asymptomatic infection or mild symptoms is usually
well tolerated if exercise of the animals is restricted.
Symptomatic cases may require pre-treatment measures,
such as administration of glucocorticosteroids,
diuretics, vasodilators, fluid therapy, etc.(aspirin is not
recommended). Exercise restriction is essential during
therapy and the recovery period. The AHS recommends
administration of doxycycline at 10 mg/kg p.o. twice
daily for 4 weeks before melarsomine therapy. The
latter is based on a three-dose protocol (injection of
melarsomine at 2.5 mg/kg b.w., i. m., followed at least
l month later by 2 injections of the same dose 24 h
apart) together with adjunct measures. If melarsomine
therapy is not possible, the AHS recommends a therapy
with doxycycline/macrocyclic lactone. Italian studies
have shown that such a therapy is highly effective
against macrofilariae( ~75%) and microfilariae(100%)
(doxycycline 10 mg/kg b.w., p.o. daily for 30 days, and
ivermectin-pyrantel pamoate (6 µg/kg+ 5 mg/kg p.o.]
once every 15 days for 6 months; the pyrantel component
isnot essential). Another option, recommended by AHS,
is an intervention to eliminate microfilariae before
melarsomine treatment by monthly application of
macrocyclic lactones(ML) as indicated for prevention
(► p. 695). Independently of a therapy against adults,
microfilariae can be eliminated by ML alone or in
combination with doxycycline. In view of the complex
therapeutic problems and development of resistance
to ML, specialists should be consulted. The AHS has
published guidelines for the 'Prevention, diagnosis
and management of heartworm (Dirofilaria immitis)
infection in dogs' to which the reader is referred(http://
www.heartwormsociety.org/).
• Surgical measures. Surgical extraction of adult
worms is especially indicated in cases of the caval
syndrome. Damaging the parasites bears the risk of
shock reactions induced by released allergens.
• Treatment of cats. The question of whether infected
cats should be treated at all is in dispute. Melarsomine
in higher doses seems to be toxic to cats. Usually the
infection is self-terminating. In cases of lung affections
due to the infection, prednisolone is administered in low
doses. In cases of venous obturations(cava syndrome),
immediate surgical measures are indicated.
Prophylaxis. An effective and safe prophylaxis against
D. immitis and D. repens (see below) is possible using
various products containing ML (► p. 605). In the
USA evidence has accumulated on D. immitis resistance
to ML which might also evolve in the future in other
endemic regions. Therefore, several preventive measures
are recommended internationally to minimise the risk
of drug resistance development(for further details see
specialised literature).
co
"O
Dirofilaria repe11s is the agent of cutaneous dirofilariosis. ·;::
::,
\....
The adult stages live in subcutaneous tissues of dogs, cats 0.
and wild carnivores; microf11ariae(unsheathed) appear in Cl)
skin and blood( ► Table I 0.16). In the indirect life cycle
the parasite is transmitted by mosquitoes(Culicidae). The
parasite occurs in Europe, Asia and Africa. In Europe, D.
repe11s has a distribution partially overlapping that of D.
immitis. It is pnrticulnrly noteworthy that D. repens has
expanded In recent years from southern to central and
northern European countries. The infection is mostly
nsyrnptomatic, rnrely symptomatic with formation of
nodules, prurllus and eczema. Mlcrofilariae have to be
considered in differential diagnosis.
Zoonotic importance. Infectious larvae of D. repens
and occasionally D. immitis can be transmitted to humans
by infected mosquitoes. Immature stages of D. immitis
settle in the lungs and cause inflammatory infiltrates
of 1-4 cm in size which are often misinterpreted as
tumours. Juvenile stages of D. repens cause nodular
lesions in subcutaneous tissues(often head, also limbs
and other body parts). In the period between 2000 and
2011 at least 940 cases of subcutaneous dirofilariosis
were reported from 12 European countries, most of them
from Russia and Italy, and only 21 cases of pulmonary
dirofilariosis, from 6 countries. According to a recent
report 1,465 human D. repens cases were registered
in the Ukraine between 1996 and 2012 with regional
incidence rates between 0.07 and 9.8 per 100,000 people.
Genus Setaria
Most of the Setaria species have a cosmopolitan
distribution. Adults are thin and long nematodes(��
up to 15 cm) inhabiting the peritoneal cavity of ungulates
( ► Table I 0.14, p. 353). Microfilariae are ensheathed and
invade the blood circulation. Culicidae are intermediate
hosts and vectors.
Q)
S. equi inhabits the peritoneal cavity, sometimes also the C
·c:;
scrotum of equids, whereas S. multipapillosa lives in the '6
peritoneal cavity of cattle and wild ruminants(roe deer, �
Q)
red deer, antelopes, giraffes). S. digitata is found in the
peritoneal cavities of cattle and buffaloes. Several other co
C
species(S. marshalli, S. cervi and others) infect particular ·;::
ruminants in different geographical regions. Adult j
Set aria spp. are usually of little pathogenicity. However, C
as described especially for S. digitata, larval stages may >,
Ol
invade the CNS of aberrant hosts (horses, goats, etc.) 0
and cause focal encephalomyelitis with cerebral and ·u5
neuronal deficiencies, sometimes also death. co
co
0..
 Part Ill. Parasites and parasitoses: metazoa

Genus Onchocerca
Disease: Onchocercosis
Summary
Agents. More than 25 species are known as parasites of
equids, even-toed ungulates or man(0. volvulus). Most
species are large(��: >80 cm long) nematodes which
Inhabit the subcutaneous tissue, tendons and tendlnous
ligaments. Unsheathed mlcrofllarlae In the skin.
• Occurrence, llfe cycle. Onchocerca spp. are
cosmopolitan or restricted to certain areas (► Tabla
10.14). Depending on the species, Slmullldae or
Ceratopogonldae serve as Intermediate host!I, Infections
are usually asymptomatic; occasionally fistulas In the
llgamentum nuchae or lameness due to damage to the
suspensory ligaments are observed In Infected horses.
Treatment of Infected horses with macrocycllc lactones
may cause side effects (Inflammatory skin reactions)
due to the mlcrofllarlcldal activity of the drugs. When
Indicated (fistulas) surgical treatment, otherwise no
therapy required. In dogs and cats ocular disease Is
caused by 0. lupl.
Agents. Selected Onc/,ocerca spp. of bovids, equids and
carnivores are listed in ► Table 10.14. The validity of
some species is discussed.
Onchocerca spp. in equids and bovines
Life cycle. The females of Onchocera spp. are curled
up in the tissue and release unsheathed microfilariae
which accumulate in the skin of more or less defined
body regions which are independent of the locations
of the adults. Depending on the Onchocerca species
the microfilariae are taken up by Simuliidae or
Ceratopogonidae with a blood meal(► Figure 10.83).
The body regions where the microfilariae accumulate in
the skin correspond to the predilection siles of the vector
species. The larvae develop into L3 and are transmitted
to new hosts via the mouthparts of the insects. The
migration routes of the larvae to their final location
and details of the development are not exactly known.
The femaJes establish permanently at a particular site
whereas the males migrate in the host's body searching
for females which pass through severaJ reproduction
cycles per year. Prepatency lasts for at least 7 months.
The adult worms are long-living, surviving possibly
>20 years.
Occurrence and epidemiology. Information on
the geographical distribution of some Onchocerca spp.
is given in ► Table I 0.17. In Switzerland approximately
50% of pastured older cows were infected with 0.
gutturosa, as shown by the detection of microfilariae
in the skin. Microf11ariae of Onchoccrca spp. were also
found in 37% of skin samples from cattle in Finland.
The long-living adults represent an almost inexhaustible
reservoir of microfilariae. Transmission depends on the
seasonal availability of the vectors; in tropical areas ii
occurs throughout the year.
Pathogenesis and clinical signs. The adult
parasites are usually of low pathogenicity. They live in
canals or knots of ligaments and tendons or in knots
in the skin and hypodermis, enclosed by connective
tissue. Occasionally, horses develop fistulas originating
from the ligamentum nuchae ('fistulous withers') or
knotty, pressure-sensitive alteration of the suspensory
ligaments and flexor tendons of the lower limb. In cattle
infected with 0. gibsoni, inflammatory lesions of muscles
neighbouring the worms were described. In horses
dermatitis in response to Onchocerca microfilariac
are reported. Anthelmintic treatment of horses with
macrocyclic lactones may cause inflammalory reactions
in skin regions where microfilariae are killed by the
drug. Such reactions are often observed along the linca
alba. Since microfilariae of Onclwcercn spp. invade
the cornea and other parts of the eye, a relationship
was suggested between 0. cervicalis inft"ctions and

Table 10.17. Onchocerca species In domestic animals (selection).

.,... LooaU..Uon In hott lnwm,edlate hotte

·o 0. gutturosa cattle. buffalo nuchal ligament and ligaments in Simuliidae worldwide

distal limbs I
� 0. 1/enalis
---- . cattle
7
I gastrosplenic ligament
•
I Simuliidae worldwide 7
c
'
0. gibsoni cat1le ' �ubcutis. intermuscular connective I Ceratopogonidae Asia, Australia, soun1ern
tissue Africa
(tl
·.:
o. �h�ngi cattle �ubder�al nodules - ] Simuliidae Africa
0. /upi dog, cat subconj�nctival nodules -, presu�ably Europe, Turkey, Iran. North

7
-� 1 Simuliidae Africa, USA
0. cervicalis and --- -- -j---
equids -
I nuchal ligament Ceratopogonidae worldwide
0 1
sesamoidean ligaments. I eastern and southern
0. reticulata
·v, tendons of distal limbs Europe
., 10. Phylum Nematoda (syn. Nemalozoa) (threadworms or roundworms)
Adult parasites in
nuchal ligament
Infection with L3
by blood-feeding
black fly
Black fly
L3
L2
Figure 10.83. Life cycle of Onchocerca gutturosa (Graphics: IPZ, S. Ehrat).
equine recurrent uveitis. Such relationships could not
be confirmed. However, dying microfilariae (e.g. after
macrocyclic lactone therapy) are suspected to induce
keratoconjunctivitis and other damage to the eye
(microfilariae of 0. volvulus are the causative agents of
the so-called river blindness of man).
Immunology. Detailed data are available for 0. ochengi
infections of cattle and human 0. volvulus infections.
They show a continuous increase in specific humoral and
cellular immune reactions until the end of prepatency.
A subsequent distinct suppression of unspecific and
specific immunity is interpreted as a requirement for the
persistence of parasites. Nevertheless, a certain degree
of immunity seems to limit the establishment of worms
of su perinfections.
Miorofilariae in skin of
umbilical region
Diagnosis. Microfilariae migrate out of bioptic skin
samples into saline. For the test skin bioptates of a size
of 6-10 mm are minced with scissors and incubated for
6-12 h in 0.9% NaCl solution at 20-30 °C. After removal
of the skin remnants and centrifugation (10 min, 800xg),
the larvae can be found in the sediment.
Therapy and control. There are at present no
compounds available which affect adult Onchocerca spp.
Fistulous withers in horses are surgically treated, assisted
by antibiotics (it is speculated that some bacterial species
are involved in the generation of the disease). Onchocerca
dermatitis in horses is treated with macrocyclic lactones
(e.g. moxidectin 0.3-0.5 mg/kg p.o.); in case of adverse
side effects glucocorticoids are administered.
11
Part Ill. Parasites and parasitoses: metazoa

Onchocerca lupi in carnivores treatment), topical antibiotics and systemic prednisolone

0. lupi, an almost unnoticed species since its first
description in 1967, is now increasingly diagnosed
as an ocular parasite of dogs in southern and Central
Europe (e.g. PT, GR, HU, DE), and in the USA. This
parasite infects also cats and is occasionally transmitted
to humans. The adult nematodes (males approximately
5 cm long, estimates of female length at least 16-17 cm)
live in nodules in the conjunctiva and connective tissue
of the sclera. In dogs, microfilariae (unsheathed, mean
length 110 µm) are predominantly found in the skin of
the nose, ears or forehead and less frequently in other
parts of the skin (e.g. inter-scapular, back, thorax, and
limb). Simuliidae are regarded as putative intermediate
hosts and vectors. In areas of GR and PT where O. lupi
cases have been observed, microfilariae were found in
8% of 107 dogs. Clinical signs of the infection in dogs
include periorbital swelling, lacrimation, photophobia,
conjunctivitis, blepharitis, corneal ulcers, conjunctiva!
nodules, possibly blindness and general discomfort.
Diagnosis is based on clinical signs in conjunction
with the detection of microfilariae isolated from
0.9% sa.line solution in which skin snips (4-5 mm in
diameter) were soaked. 0. lupi microfilariae must be
differentiated from those of other filarial nematodes
(Cercopithifilaria). Small, ( 1-3 mm) mineralised, hyper­
echogenic structures can be detected by US examination
in peri-orbital tissues of dogs. In single cases, surgical
removal of parasite nodules followed by administration
of melarsomine (2.5 mg/kg i.m., daily for two days),
ivermectin (50 µg/kg s.c., one month after the initial
has prevented recurrence of nodules for up to more than
one year of follow-up.
Zoonotic importance. Some human cases of ocular
0. lupi infections, recently diagnosed in Turkey, Iran,
Tunisia, Albania, Russia and Germany, and the finding
of the parasite in the spinal canal of a child in the USA
explain why this zoonosis deserves further attention.
Only a few human cases, caused by other animal-derived
Onchocera species, have been reported, most of them
associated with the infection of subcutaneous tissue in
various body parts.
Onchocercidae in birds
Approximately 150 species of Onchocercidae infect
birds. In contrast to filariae in mammals they are not
strictly host specific. Intermediate hosts are chewing
lice (Amblycera, Ischnocera) and mosquitoes (Culicidae
and Ceratopogonidae), dependent on the filarial species
(► Table 10.18). Filariae are rare in poultry in Europe
but are common in exotic birds. Depending on the
parasite species they may cause endothelial lesions,
stenoses of blood and lymph vessels, thrombosis,
myocardial damage or lameness in cases where the
connective tissue around joints is infected.
Little is communicated concerning therapy and c ontrol
of filarial infections of birds.

Table 10.18. Frequent fllarial genera (famil y Onchocercidae ) in birds.

..,...,
a... (number of Location In definitive host Mlcrofllarlae
-----..-----�----� hoats
Length4 Sheath Location
Intermediate

Pelocilus 1 ( 16 )

I-
connoctivo tlssuo around tendons shOrt to +5 skin chewing lice

� 18182- (7)
I and joints
; body cavit1os
, medium length
i medium lengtl, blood I Cuhck1mi
. _J
CsrdKJfilantP (12)
. bocty cavities : long
\- blood f Culic1clae
-1
I
Chandlerella2 (26)

I
-
connective tissues around blood long blood Ceratopog idae I
I
t
I �
• vessels, partiall y 1n CNS
I
! �
Splendldofilana2 (31) connective tissue around l()lnts and short I- blood \ Ceratopogonidae
subcutaneously. walls of at1enes,
myocard1Um
Eufilana 3 I 15) subcutaneous connective tissue short blood Ceratopogonidae
Eulimdana3 (-;.11) subcutaneous and othef short l .., skin chewing lice
connective bssue I
chewi lice
-

'um, walls of blood vessels I long

-➔-- -

Satt:ooama3(2 m 1+ blood
1
Stbfanw!y D mfllarnnae: single genus with representallves ,n birds and mammals.
t

2 Subfamily Spiend.dolila111nae.
3 Sublam1/y Leffldaninae.
4 Short:< 120 µm ; medrurn length: 120-200 µn: k)ng: >200 µm.
5 Sheath ttght-fitong.
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)
Selected references
Bourguinat C, Keller K, Bhan A, Peregrine A, Geary T,
Pritchard R (2011) Macrocyclic lactone resistance in
Oirofilaria immitis. Vet Parasitol 181: 388-392.
Bowman DD (2012) Heartworms, macrocyclic lactones. and
the specter of resistance to prevention in the United States.
Parasit Vectors 5: 138.
Cortes HC, Cardoso L, Giannelli A, Latrofa MS, Dantes­
Torres F, Otranto D (2014) Diversity of Cercopithifilaria
species in dogs from Portugal. Parasit Vectors 7: 261.
Franchini D, Giannelli A, DI Paola G, Cortes H, Cardoso L,
Lia RP, Campbell BE, Dantes-Torres F, Lenoci D, AHad
EA, Ricciardi M, Valastro C, Cavaliere L, Di Bello A,
Otranto D (2014) Image diagnosis ot zoonotlc onchocercosls
by Onchocerca lupi. Vet Parasltol 203: 91-95.
Genchi C, Bowman D, Drake J (2014) Canine heartworrn
disease (Oirofilaria immitis) In Western Europe: survey of
veterinary awareness and perceptions. Parasit Vectors 7: 206.
Genchi C, Genchi M, Petry G, Kruedewagen EM, Schaper
R (2013) Evaluation of the efficacy of irnidacloprid 10%/
moxidectin 2.5% (Advocate®, Advantage® Multi.Bayer) for
the prevention of Dirofilaria repens infection in dogs. Parasitol
Res 112, Suppl. 1: 81-89.
Grandi G, Quintavatla C, Mavropoulou A, Genchi M, Gnudi
G, Bertoni G, Kramer L (2010) A combination of doxycycline
and ivermectin is adulticidal in dogs with naturally acquired
heartworm disease (Oirofilaria immitis). Vet Parasitol 169:
347-351,
Hassan HK, Bolcen S, Kubofclk J, Nutman TB, Eberhard
ML, Middleton K, Wekesa JW, Ruedas G, Nelson KJ,
Dubielzig R, De Lombaert M, Silverman B, Schorling
JJ, Adler PH, Unnasch T R, Beeler ES (2015) Isolation of
Onchocerca lupi in dogs and black flies, California, USA.
Emerg Infect Dis 21: 789-796.
Kramer L, Genchi C (2014) Where are we with Wolbach/a and
doxycycline: an in-depth review of the current state of our
knowledge. Vet Parasitol 206: 1-4.
Kramer L, Grandi G, Passeri B, Gianelli P, Genchi
M, Dzimianski MT, Supakorndej P, Mansour AM,
Supakorndej N, McCall SD, McCall JW (2011) Evaluation
of lung pathology in Oirofilaria immitis-experlmentally infected
dogs treated with doxycyline or a combination of doxycyllne
and ivermectin before administration of melarsornlne
dihydrochloride. Vet Parasitol 176: 357-360.
Magnis J, Lorentz S, Guardone L, Grimm F, Magi M,
Naucke T J, Deplazes P (2013) Morphometric analyses
of canine blood microfilariae isolated by the Knott's test
enables Dirofilaria immitis and 0. repens species-specific
andAcanthocheilonema (syn. Oipetalonema) genus-specific
diagnosis. Parasite Vector 6: 48.
Mavropoulou A, Gnudi G, Grandi G, Voita A, Kramer LH,
Quintavalla C (2014) Clinical assessment of post-adulticide
complications in Dirofilaria immitis-naturally infected dogs
treated with doxycycline and iverrnectin. Vet Parasitol 205:
211-255.
McCall JW, Arther R, Davis W, Settje T (2014) Safety and
efficacy of 10% imidacloprid+2.5% moxidectin for the
treatment of Oirofilaria immitis circulating mlcrofilariae in
experimentally infected dogs. Vet Parasitol 206: 86-92.
Moran CT, James ER ( 1987) Equine ocular pathology ascribed
to Onchocerca cervicalis infection: a re-examination. Trap
Med Parasit 38: 287-288.
Mutafchiev Y, Dantes-Torres F, Giannelli A, Abramo F,
Papadopoulos E, Cardoso L, Cortes H, Otranto D (2013)
Redescription of Onchocerca /up/ (Spirurida:Onchocercidae)
with histopathological observations. Parasit Vectors 6: 309.
Otranto D, Giannelli A, Scotty Trumble N, Chavkin M ,
Kennard G, Latrofa MS, Bowman DD, Dantes-Torres F,
Eberhard ML (2015) Clinical case presentation and a review
of the literature of canine onchocercosis by Onchocerca lupi
In the United States. Parasit Vectors 8: 89.
Otranto D, Dantes-Torres F, Giannelli A, Letrofa MS,
Papadopoulos E, Cardoso L, Cortes H (2013) Zoonotic
Onchocerca /up! Infection In dogs, Greece and Portugal,
2011-2012. Emerg Infect Dis 19: 2000-2003.
Otranto D, Dantes-Torres F, Giannelli A, Abramo F, lgnjatovic
Cupina A, Petric D, Cardoso L, Mutafchiev Y, Cortes
H (2013) Cutaneous distribution and circadian rhythmof
Onchocerca /up/ microfilariae in dogs. PLoS Negl Trap Dis
7: e2585.
Pantchev N, Etzold M, Daugschles A, Dyachenko V (2011)
Diagnosis of imported canine filarial infections in Germany
2008-2010. Parasitol Res 109: 61-76.
Satamatln RV, Pavllkovska T M, Sagach OS, Nikolayenko
SM, Kornyushin W, Kharchenko VO, Masny A, Cielecka
D, Konleczna-Satamatln J, Conn DB, Golab E (2013)
Human dirofilariasis due to Dirofilaria repens in Ukraine, an
emergent zoonosis: epidemiological report of 1465 cases.
Acta Parasitol 58: 592-598.
Sim6n F, Siles-Lucas M, Morch6n R, Gonzalez-Miguel J,
Mellado I, Carret6n E, Montoya-Alonso JA (2012) Human
and animal dirofilariasis: the emergence of a zoonotic mosaic.
Clin Microblol Rev 25: 507-544.
Sollsmaa M, Laaksonen S, Nylund M, Pitkanen E, Airakorpi
R, Oksanen A (2008) Filarioid nematodes in cattle, sheep
and horses In Finland. Acta Vet Scand 50: 20.
Sniter T, Szeli Z (2008) Onchocercosis: A newly recognized
disease in dogs. Vet Parasitol 151: 1-13.
·u
C
co
·;::
C 'I
"iii
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I I
Part Ill. Parasites and parasitoses: metazoa
10.2 Class Adenophorea
(Aphasmidia)
10.2.1 Order Enoplida
Members of the class Adenophorea (Aphasmidia) are
important parasites of the gastrointestinal tract or
other organ systems of animals and humans; some are
zoonotic agents. Characteristically they lack phasmids
(pairs of sensory organs) at the posterior end of the
body. Eggs usually with two polar plugs. Trichinelloidea
with trichuroid oesophagus (muscular anterior part
and a posterior part, consisting of stichocytes};
Dioctophymatoidea with cylindrical oesophagus
( ► Figure I 0.2, p. 255). The first stage larva (Ll) is
infectious to a new host.
- Superfamily Trichinelloidea
Family Trichuridae
• Subfamily Trichurinae
Genus Trichuris (whipworm)
Disease: Trichuriosis. II
Tl1rix (G): hair; 11ra (G.): tail.
Trichuris spp. exhibit a whip-like shape with an anterior
slender and a posterior stout part. Since formerly the
anterior part was supposed to be the hind part, the
name Triclturis = 'hair-tail' was created. The correct
name of the genus would be 'Tric/10cephalus' [kephale
(G): head]; this name is used in the literature but is not
officially accepted.
� Whlp-Ulw nematodN, 3-8 cm In length,
111� thin lnta1or po,tlon and stout
IINIV ,-t. MIia with one IJ)lculum. Parult11
t· le■otffllfflffllla(e.g. ruminants, pigs,
..... manlrlrtl, lunlna).
Malt. MWU � with egg lheddlng to
.._. � L1 d9velop Inside
---• ' Illd br I rww hall Hlltotropic
��•--·•--·f aw W. ..alenwlt In CMCUffl
...�_..P11; PPqtl walka and longer.
........... Common In ruminants,
- ....... llow dMelopmant of L1 In the
__.It on .,._, lunldlly. Eggs can
11'111 19 n,-. allnlclll--.
�W,_.lnherwtronnw,t.
Low worm tudenl are
...., lnlectiol• may Impair performance
-(T.--, Md ca.- hwnonhagic inflarrmation
•af ...... irdu&w I, dogs (r .upls).
Diagnosis. Coproscopic detection of the typical,
lemon-shaped eggs.
Therapy and control. Various benzimidazoles and
macrocyciic lactones are effective; in dogs also
emodepside, oxantel and combination products
(► Table 19.13 and 19.14). Hygiene measures must
consider the longevity of larvated eggs.
Zoonotic importance. Occasionally transmissio n ol
T. vu/pis and T. suis to humans.
Agents. Parasites of the large intestine of mammals,
including man. Numerous species are known (selection):
Trichuris ovis, T. globulosa, T. sk1jabini (domestic and
wild ruminants), T. suis (domestic pig, wild boar), T
vu/pis (dog, fox, other canids), T. leporis (rabbit, hare),
1'. tric'1fura (humans, other primates), T. serrata, I
campanula, T. felis (all very rare in cats); no sp ecies
known in equlds.
Whipworms measure 3-8 cm in length and are
characterised by the whip-like shape, with a thin, long,
anterior part (approximately 2/3 of the body length)
and a thicker posterior portion(► Figure 10.84).The
posterior end of the male is coiled and contains one
spicule with a sheath, armed with fine cuticular spines.
Eggs are lemon-like, brownish, with two polar plugs.
They are released unsegmented to the environment
(► Figure 10.85). Egg sizes vary with the species, e.g.
T. suis: 47-71x27-34 µm, T. vu/pis: 70-8Sx36-40 µm, I
trichiura: 50-56x2 l-25 µm.
Life cycle. The cycle of T. suis is described here as an
example. This species inhabits the caecum and colon of
pigs ( ► Figure 10.85). The females produce numerous
eggs (T. trichiura: up to approximately 14,000-20,000
per female and day) which are voided unsegmented
in host faeces. In a humid environment an infectious
LI de velops inside the egg within 5 weeks (25 °C)
or within 3½ months at lower temperatures (20 °C).
L_ Anterior body
a
Posterior body
Figure 10.84. (a) Trichuris female; (b) Trichuris ovis: male,
posterior end (Graphics: IPZ, A. Seeger; after Skrjabin 1954).
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)

Cil
:g
a.
0
cij

Adult stage

Figure 10.85. Life cycle of Trichuris suis (Graphics: IPZ, S. Ehrat).

Q)

·o
C

After ingestion by a definitive host the LI ( -200 µm in Other Trichuris species have similar cycles, e.g. T. '6
length) hatch from the eggs in the distal part of the small vu/pis with a prepatency of9-10 weeks. However, dogs Q)
�
intestine or in the caecum and colon, invade the mucosa obviously do not regulate the whipworm population i::'
of the large intestine and moult to L2 around day 10 p.i. by early worm expulsion like pigs do. Rather, a chronic Cil
C
·;;::
Subsequently, these stages migrate back to the surface stage with persisting worm burdens develops in dogs Q)
of the mucosa where they establish under the epithelial similar to T. trichiura infections in humans. Worms may j
layer, pass through 3 further moults and protrude their survive in the dog for up to 16 weeks. C

posterior end into the gut lumen. Prepatency 6-7 weeks.

-
>,
Ol
Most of the worms are expulsed during early patency Epidemiology and occurrence. Trichuris eggs 0
0
(8-13 weeks p.i.) due to immune reactions. Thus, in the are sensitive to desiccation and depend on a moist ·cn
cu

I
majority of the animals only a small worm population environment for development. Moist and shady outside l.....
cu
persists (see immunology below). 0...

I
I
 Part Ill. Parasites and parasitoses: metazoa

pens with natural flooring and wet places on pastures Immunology. Trichuris spp. are potent inducers ofTh2
provide favourable conditions for egg development and reactions. For instance, secretory-excretory proteins of
infection of hosts. adult T. suis stimulate in vitro the synthesis of IL-6 and
IL-10 in enterocytes, i.e. immunomodulators which
• T. suis. During the European growing season, the strongly enhance Th2 dominated immune reactions.
development of Ll in T. suis eggs takes 2-3 months and Primary and challenge infections of pigs with T. suis
often even longer(> 1 year). During the winter months are immunologically controlled. In primary infections
with low temperatures the development subsides. the majority of young worms are usually eliminated in
Eggs may survive in moist soil for >6 years, however, the 9th week p.i., so that a small remaining population
the majority dies off within 1-11/1 years as shown in usually persists in the host. The intensity of this reaction
DK. Continuous use of paddocks may result in heavy is strictly genetically controlled in a complicated manner.
contamination with Triclwris eggs and clinically relevant Studies in a mouse model showed that the expulsion
infections in pigs. In stables, the conditions(moisture, of 'f: nrnris depends on the I L-l 3-induced expression
temperature) for larval development are basically of a mucin, Muc5ac, in the intestinal mucosa which is
suitable, but the long developmental time is a limiting usually expressed only in nonintestinal mucosa! tissues.
factor. Thus, in northern Europea.n countries, T. suis The mechanism whereby this mucin induces the worm
infections are relatively rare in housed pigs (intensive expulsion is not yet clarified. However, the observation
husbandry), but more frequent in free-range or organic that the expression of the Muc5ac genes is upregulated in
systems. For instance, 9 out of 10 outdoor (organic) T. suis infected pigs suggests a host species independent,
farms were positive for T. suis in DK and 37% in the NL. Th2-associatecl, comprehensive mechanism.
Highest prevalences are usually observed in younger
pigs (8-36 weeks of age). Primary infections with T. suis induce a strong protective
immunity in pigs. Experimental studies showed
• Trichuris in ruminants. Trichuris infections are protection against challenge infections up to 95%.
common in ruminants. For example, 50-70% of slaughter The immune mechanisms are not yet clear, but ADCC
sheep were infected (T. globulosa, T. ovis, T. skrjabini) reactions( ► p. 27 and p. 32) may possibly reduce the
in Germany, and 44% of calves in Swiss mother cow numbers of worms during the histotropic phase in the
husbandries shed Trichuris eggs. intestinal wall.

• Trichuris in dogs. Patent T. vu/pis infections are
found in dogs older than 9 weeks. Prevalences vary
between l % and 30%, depending on the area and the
type of dog maintenance. High prevalences arc often
found in dog shelters.
Pathogenesis. Whipworrns are nnchored in the
mucosa with their thin anterior end which usually
lies in epithelial tunnels in or just below the epithelial
layer, sometimes also in the propria (but worms do not
penetrate the muscularis mucosac). Heavier infections
induce subacute catarrhal inflammations, and massive
infections (>200 worms) cause haemorrhagic alterations
of the caecum, partly also the colon, particularly in young
dogs. The resulting anaemia and hypoalbuminaemia are
enhanced by additional direct withdrawal of blood by the
parasites: whipworms feed on mucosa! cells and blood
Q)
(approximately 5 µJ per worm and day). T. suis infections,
·u
C
Clinical signs. In pigs, experimentally induced mass
infections with T. suis (>6,000 specimens per pig)
caused watery-bloody diarrhoea, hypoalbuminaemia
and retarded development. Natural Trid11.1ris infections
of pigs and ruminants often remain asymptomatic but
may nevertheless stiU be economically relevant. Clinical
or even fatal trichuriosis have been observed in wild
ruminants (e.g. moose), maintained in padch:ks. In
dogs, heavy naturally acquired '/: vu/pis infections can
cause catarrhal or haemorrhagic colitis, associah:d with
diarrhoea, anaemia, anorexia, stunting and emaciation.
Diagnosis. Coproscopic detection of the typical eggs
using flotation techniques(flotation solution with high
specific gravity� 1.3!). Adult Trichuris stages arc easily
detectable at necropsy.
Therapy and control. Penbendazole, flubendazole,

'6 either alone or in mixed infections with Ascaris suum milbemycin, moxidectin, emodepside, oxantel. and
�
Q)
or Oesoplwgostonwm spp., may affect feed utilisation, some combination products are highly effective
� weight gain and meat quality. Simultaneous infections against Tric/wris in dogs( ► Table 19.14 and 19.15).
ro of germ-free pigs with T. suis and Campylobacter jejimi Faeces should be frequently and thoroughly removed,
C
·c:: caused enhanced pathological alterations and clinical particularly in kennels, to reduce floor contamination
Q)

j symptoms when compared with infections with the with eggs. Trichuris infections in pigs may be treated
_!; single agents only. Helminth infections may inhibit Th l with flubendazole, febantel and fenbendazole( ► Table
>
0)
reactions and thereby affect the efficacy of vaccinations l 9.8). lvermectin and doramectin given in usual doses
0 against bacteria and viruses as demonstrated in A. suum­ are not sufficiently effective against T. suis. Control
0
·en infected pigs after vaccination against Mycoplasma measures in pigs ► p. 588. Chemotherapy against
hyopneumoniae. Trichuris spp. in ruminants is generally not necessary.
ro
Cl. Some anthelmintics used against trichostrongyles are
,., 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)
also efficacious against ruminant Trichuris spp. ( ► Table
19.2).
Zoonotic importance. T. trichiura of man and T.
suis of pigs are morphologically very similar but can
be differentiated genetically. Although both species
can mutually be transmitted experimentally, reports on
documented natural transmission of T. suis to humans
are very rare. More cases of human infections with
T. vu/pis were observed(some recently confirmed by
molecular methods).
In recent years, the oral administration of T. suis eggs,
containing infective larvae, has induced disease remission
in some human patients suffering from Morbus Crohn or
ulcerative colitis. These diseases are generally associated
with Th 1 and Th 1 7 immune responses, whereas intestinal
helminth infections stimulate Th2 dominated immune
reactions. Obviously, a short-term establishment of
larval T. suis stages in the intestine of patients (the
parasites do not usually reach maturity) can mediate a
Th 2 dominated reaction and suppress damaging effects
of an overwhelming Th I response. It has been shown that
excretory/secretory products of T. suis larvae suppress
pro-inflammatory cytokine production, whereas the
production of T h2-inducing cytokines is stimulated.
Currently, this therapy and the underlying mechanisms
are being further evaluated.
• Subfamily Capillariinae
Summary
• Agents. Numerous species belong to the genus
Cap/Ilaria (synonyms ► Table 10.19 and 10.20), which
has been divided Into several genera (see below).
Capillaria spp. are 70-80 mm long and hair-thin, there
Is little difference In diameter between the anterior
and posterior part of the body; the former Is occupied
by the trichurold oesophagus. They are parasites of
the intestinal tract, urinary bladder and other organs
of vertebrates and of particular Importance In poultry
and carnivores.
• Life cycle. Poultry: some species develop mono­
xenously (C. contorts, C. obsignata, C. anatis), others
heteroxenously with earthworms as intermediate hosts.
The adults inhaoit the intestinal tract (from oesophagus
to the large intestine). Mammals: C. plica (parasite In
the urine bladder of dog, fox, and cat) and C. putorii
(in stomach and small intestine of cat, polecat and
others) have indirect cycles, depending on earthworms
as intermediate hosts. The cycle of C. aerophila (in
the lungs of dog, cat, fox, and hedgehog) is thought
to be direct, but the involvement of earthworms as
intermediate or paratenic hosts cannot be excluded.
The same applies to C. boehmi which inhabits the nasal
passages and sinuses of wild and domestic canids.
• Epidemiology, occurrence. C. obsignata is most
common in intensive husbandry of poultry. Dogs and
cats are infrequently infected with Cap/Ilaria spp.,
' however, infections should not be disregarded.
A
• Pathogenesis, cllnlcal signs. Cap/Ilaria spp. usually
cause catarrhal Inflammation of mucosal tissues.
Symptoms depend on the worm burden and the organ
Infected.
• Diagnosis. Detection of eggs in urine (C. piles),
tracheal or nasal mucus (C. serophlls, C. boehmf), or
(1j
:g
faeces (other species). Parasite detection at necropsy Q_
0
(particularly in poultry). C
w
• Therapy. Umited options (see below)
• Zoonotlc Importance. Human infections with C.
hepatics, C. serophlls or C. boehml are rare. More
important Is C. ph/1/pp/nensls, causing a fish-borne
zoonosls In South-East Asia.
Genus Capil/aria (capillary worms)
Disease: Caplllarlosls.
Capillus(L): hair.
Cap ii/aria spp. infect internal organs of vertebrates (fish,
amphibians, reptiles, birds, mammals). Infections of
poultry and carnivores are of particular veterinary
importance.
Agents. In many attempts to reclassify the taxonomy
of the numerous Capillaria species {-300), several
en
new genera were established. Some of the well-known .c
species(e.g. Capillaria caudinjlata) have been assigned
to genera unfamiliar to most readers(e.g. Aonchotheca
.E
Q)
I
caudinflata). For reasons of simplicity we retain the
name Capillaria in this textbook, but mention other
genus names as synonyms(► Tables 10.19 and 10.20}.
Capillaria spp. are 70-80 mm long and hair-thin with
little difference in diameter between the anterior and
posterior part of the body; the former is occupied by
the trichuroid oesophagus(► Figure 10.86). Males
are usually equipped with one long spicule and may
bear special structures at the posterior end; the vulva
of females may be covered by a vulva! flap. Eggs:
► diagnosis and ► Figure 10.87.
Q)
Capillaria species of poultry and other birds
·u
C
'o
Agents and life cycle. Poultry and other birds Q)
�
can harbour a variety of Capillaria spp. which inhabit
different sections of the gastrointestinal tract(► Table (1j
C
·;::
10.19). C. contorta, C. obsignata, and C. anseris are Q)
transmitted in a direct cycle, whereas the other species
depend on earthworms as intermediate hosts(genera .!;;
Allolobophora, Eisenia, Lumbricus). Eggs produced by >.
Ol
Capillaria females are non-embryonated and shed in host 0
0
faeces. Under the condition of sufficient moisture and ·u5
suitable temperatures(20-24 °C) L1 develop in the eggs
within 1-2 weeks. In the case of monoxenous species, the
I I
Part Ill. Parasites and parasitoses: metazoa

Table 10.19. Capillaria species (selection) of poultry and other birds.

Speciee, length of males1 (��) and Hosts (selection) and predilection Life cycle (intermediate host in
femal.ee (��), distribution (D) sites (Pl of adults
1 parenthesis) and prepatency in days

Capil/aria annu/ata chicken, turkey, other gallinaceous birds, I indirect (earthworms)

(syn. Eucoleus annulatus) also duck prepatency: 16-26
,
o :11-20,C.''J?:up to 35mm P: oesophagus, crop,rarely beak cavity
D: Euro�e, North and South America,Asia
Capil/aria contorts
---
goose, duck other species of water
- -,__ _____________
direct
(syn. Eucoteus contortus) birds. gallinaceous birds, passerine birds J prepatency: 45-54
"•: 7-12. •��: 11 -20 mm P: oesophagus, crop, rarely beak cavity
D:worldwide
Capillaria bursata cl1icktln, turl-.oy, pheasanl, also duck 1 Indirect (earthworms)
(syn. Aonchotheca bursata) P: small inIost1ne 1 prepatency: 20-25
o&: 15-18, ;�: 28-35 mm
D: worldwide
Capil/aria caudinflata chicken, turkey, ot11er gollinaceous birds . ! Indirect (earthworms)
(syn. Aonchotheca caudinflata) pigeon. also gooso, duck,passer ine prepalency: 22-24
03:8-11, ) 1':15-20mm birds
-------
0

D: worldwide P: small inlestine

Capil/aria obsignata chicken. turkey, ot11er golllnaceous birds, direct
(syn. Baruscap1/18na obsignnta. Capillar,a pIgoon. also goose. duck. passenne I prepatency: 20-26
columbae) birds
,!,!: 7-12, ·;'�: 9-15 mm P: small intestine
D: worldwide
Capil/aria anatis goose, duck. wild Anseriformes, also direct
(syn. Gaptllaria retusa, Thominx anatis) gallinaceous birds, pigeons,etc. prepatency: 28
110:
�dwlde
1
7- 3,,.
�: 8-18 mm P: caeca, rarely small intestine

1 Measurement records higt1ty variable ,n hterature.

Epidemiology and occurrence. Capillaria eggs

are fairly resistant to environmental influences. For
Anterior
end
instance, they survive temperature fluctuations from
-7 °C to + 12 °C for 2 weeks. Earthworms live several
years. Therefore, outside pens of poultry may remain
contaminated for a long time. In addition, parasites may
be introduced by wild birds.

Due to the direct life cycle, only C. obsignata plays a role

Figure 10.86. Caplllaria obsignata: male (Graphics: IPZ, A.
Seeger; after Skrjabin 1954).
hosts get infected by ingestion of larvated eggs. Adults
develop in the intestine after 4 moults. In C. obsignata
prepatency lasts 3-7 weeks and patency approximately
2 months(► Table 10.19). In heteroxenous species
larvated eggs are ingested by earthworms, where the
LI hatch, invade the tissues and reach infectivity for
the final hosts within 2-4 weeks. Prepatency lasts 2-4
weeks in these species.
in indoor husbandry of poultry. The other pccies are
predominantly found in free-range chicken , wild birds
but also in ducks and geese. Studies in DK in free-range
chickens revealed prevalences of 54% ( C. obsig11at11),
32% (C. anatis) and 1.5% (C. caudinflata). Chickens kepi
indoors on deep litter harboured exclusively C. ol,sig11i1ta
(prevalence: 52%). Also pigeons, water fowl and aviary
birds are commonly infected with Capillaria spp.
Pathogenesis, clinical signs. Capillaria spp.
invade the superficial layers of the intestinal muco sa
(epithelium, propria) and cause local defects of the
epithelium, inflammatory infiltrations of the propria
mucosae, also haemorrhages in case of heavy infections.
Chronic infections may be associated with fibrotic
alterations of the wall of the small intestine. In heavy
infections there may be losses of plasma proteins into
the bowel, anaemia, disorders of intestinal resorption.
dysentery, reduced egg yields, emaciation, and even
death.
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)

Table 10.20. Capillaria species(selection) of mammalian animals and humans.

Species, length1 of males (�cS) Hosts (ielectloh) encl . Ute cycle (ll'ltettnedlate hOsts In parentheses),
and females (!j?!j?), distribution (D) predllectlon sltel (P) of •duita prepatency In days, cllnlcal sign§ (C), eggs and
egg detection

Cap/Ilaria bovis cattle, sheep, wild ruminants direct

cM: 12-17, ?.?.: 20-27 mm
D: Europe, Russia, North America
Capillaria longipes
oo: 11-13, ?.?.: 20 mm
D: probably as in C. bovis
Capillaria putorii2
(syn. C. mustelorum,
Aonchotheca putori1)
M: 6.0-8.5, ?.'i': 9-13 mm
D: Europe, Russia, North America
Capillaria aerophila
(syn. Eucoleus aerophilus)
oo: 16-18, ?.?.: 18-20 mm
D:woridwide
Capillaria boehml
(syn. Eucoleus boehm1)
oo: 15-25, ?. <jl: 30-40 mm
D: North America, Europe
(temperate regions)
Capillaria plica 3
(syn. Pearsonema plica)
oo: 13-30, <jl(j?: 30-60 mm
D: worldwide
Cap/Ilaria hepatica
(syn. Ca/odium hepaticum,
Hepaticola hepatica)
oo: 24-37, <jl<jl: 53-78 mm
D:worldwide
1 Measurement records highly variable in the literature.
2 Morphologically highly variable and not distinguishable from Capillaria mustelorum (from mustelids) and C. erinacei(from
hedgehogs).
3 Capillaria feliscati (syn. Pearsonema feliscat1) was described from urinary bladder of cats but species Identity is doubtful.
P: small intestine
sheep
P: small intestine
mustelids. raccoon, cat
P: stomach, small intestine
red fox, dog, cat, badger.
marten, hedgehog, racoon dog,
rarely man
P: trachea, bronchi, nasal and
frontal cavities
red fox, wolf, dog
P: nasal and frontal cavities
red fox, polar fox, dog, wolf,
raccoon dog, cat, mustelids
P: urinary bladder(rarely ureter,
renal pelvis)
rodents, lagomorphs(rabbit,
hare), more rarely other
mammals(hedgehog, horse,
dog, cat), humans
P: liver
prepatency: no data cu
C: mostly asymptomatic infection :-g
eggs 47-49x24-28µm, in faeces
a.
0
C
direct w
prepatency: no data
C: mostly asymptomatic infection
eggs: 45-50x22-25µm, in faeces
direct and indirect(earthworms)
prepatency: 26-32
C: gastrointestinal symptoms, vomiting
eggs: 54-66><21-26µm, in faeces
direct, presumably also indirect(earthworms)
prepatency: 25-40
C: bronchitis, tracheitls, cough, nasal discharge
eggs: 62-73><35•40 µm, surface with network of
branching ridges( ► C. boehm�; In faeces and tracheal
---
mucus
direct or indirect (not documented)
prepatency: unknown
C: rhinitis, sneezing, nasal discharge, hypo- or anosmia
eggs: 50-60x30-35µm, surface with tiny pits
(► C. aerophila); In faeces and nasal mucus
indirect(earthworms)
prepatency: 58-63
C: cystitis, urinary incontinence, dysuria, haematuria,
fever( ► Figure 10.88)
eggs: 55-67x26-29 µm, in urine
direct. egg deposition in liver parenchyma, and no egg
shedding to the environment
C: liver lesions, icterus, apathy, anorexia, vomiting, etc.
eggs: 56-62><28-32µm, in liver tissue
-

Diagnosis. Diagnosis in poultry is usually performed Capillaria species in mammals

by necropsy and morphological characterisation of the
parasites (► Figure 10.87 ). Eggs can be detected in
faeces. Capillaria eggs resemble those of Trichuris spp.
but are more barrel-shaped with almost parallel sides
and less prominent bipolar plugs; they measure 48-
54x25-27 µm to 60-62x24-27 µm, depending on the
species(► Figure 10.87 and ► Figure 16.18, p. 551).
Therapy and control. The control of Capillaria
infections in poultry flocks is based on periodic
diagnostic measures and strategic anthelmintic treatment
(flubendazole, levamisole) ( ► Table 19.20). Hygienic
measures should protect from parasite introduction by
wild birds and include renewal of deep litter.
Disease: Caplllarlosis. II
Agents and occurrence. Selected Capillaria species
of mammals are listed in ► Table 10.20. The species
parasitising the small intestine of ruminants are of
minor importance, the infection is usually weak and
asymptomatic. Capillaria spp. in carnivores are more
relevant. C. putorii was found in 2.7% of stray cats in
Germany. The parasite occurs also in foxes and raccoon
dogs, for instance in LT with prevalences of 29 and
51%, respectively. In several European countries,
prevalences of C. aerophila in cats varied between 0.2
and 17% and amounted to 72% in foxes in Germany. The
species is only occasionally found in dogs. C. plica is a
Part Ill. Parasites and parasitoses: metazoa

0
a Male, posterior end; b Female, vulva c Mala, posterior and; d Female, vulva e Egg from
spiculum sheath region spiculum shortened region C. caudinflata
shortened

Figure 10.87. (a, b) Capillaria obsignata; (c-e) C. caudinflata (Graphics: IPZ, A. Seeger; after Skrjabln 1954).

common parasite in foxes with worldwide distribution

and prevalences in European countries (CH, DE, DK,
HU, LT. NL and NO) between 23 and 93%. C. feliscati
(syn. Pearsonema feliscati, its validity is doubtful) was
described in 1-2 .7% of stray cats in Germany.

C. boel1mi is reported in dogs in Europe and North

America, prevalences in foxes from IT, NO, DE and
HU varied between 8-3 1%. C. l1epatica, parasitises
the liver mainly of rodents occasionally this species is
also observed in carnivores. Hedgehogs are commonly
infected by C. erinacei (gastrointestinal tract) and C.
aeropfiila (respiratory tract).

Life cycle and epidemiology. Mammals get infected

by the ingestion of larvated eggs or earthworms as
intermediate hosts which contain infectious LI ( ► Table
I0.20). Juvenile stages of species with extralntestinal
location (lungs, urine bladder, and liver) probably
migrate to the target organs via blood and lymph vessels.
A special situation exists with C. hepatlca which infects
the liver parenchyma of rodents and occasiona.lly of
carnivores. The females migrate to the liver and deposit
the eggs into the parenchyma where they are enclosed
by granulomas. The eggs are liberated only after the
death of the host by maceration of the organ or when
the host is ingested by a carnivorous animal which later
spreads the eggs with its faeces; the eggs embryonate in
the environment.
Clinical signs, diagnosis. Clinical signs and
diagnostic hints are summarised in ► Table 10.20. C.
plica infections in dogs may be asymptomatic or cause
cystitis associated with uriesthesis, dysuria, haematuria,
and sometimes with bacterial superinfections.
Obstructions of the urethra or the ureter and renal
failures are reported as consequences ( ► Figure I0.88).
Figure 10.88. Cap/Ilaria pl/ca: histological section of urinary
bladder wall with sections of the parasites and severe lesions
of the mucosa (Photo: IPZ).
X-ray and US investigations of the urinary bladder and
analyses of the urine may provide helpful diagnostic
hints. Eggs can be demonstrated in the urine sediment
and worms may be shown by cystoscopy.
Therapy, control. Broadline", a combination formu·
lation with a registered indication against other parasites
in carnivores, has shown high efficacy against C. plica
and C. aerophila in cats when topically applied in a
single dose of0.1 2 ml/kg b.w. (delivering 10 mg fipro nil
+ 12 mg (S)-methoprene + 0.5 mg eprinomectin +IO
mg praziquantel). Eprinomectin (macrocyclic lactone)
is the key component active against Capi/laria spp.
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)
Chemotherapy ofcapillariosis of the urinary bladder in
dogs is difficult as repeated treatments with fenbendazole
(SO mg/kg b.w. p.o., for 10 days) or ivermectin (0.2 mg/
kg b.w. s.c.) may not be successful. Another option is
Jevamisole (7.5 mg/kg b.w. s.c., on 2 consecutive days,
off-label use). Advocate•, a spot-on combination
formulation with moxidectin and imidacloprid, has
shown high efficacy against C. boehmi in dogs when
administered in its registered indication against other
parasites, while milbemycin oxime was effective in a
dose of 2 mg/kg b. w. p.o.
Zoonotic importance. Human infections with C.
aerophila, C. hepatica or C. boehmi are documented
in the literature, but they are rare. C. philippinensis is
an important zoonotic parasite in Asia often causing
severe intestinal ill ness in humans. The life cycle
involves piscivorous birds as definitive hosts and fish
as intermediate hosts.
• Subfamily Trichosomoidinae
Genus Anatrichosoma
■
Disease: Anatrlchosomosis in monkeys and
other hosts.
Several Anatrichosoma species are parasites of primates,
carnivores, rodents and marsupials. In monkeys (Asia,
Africa), A. cutaneum or other species inhabit the
subcutaneous tissue, the nasal mucosa or some other
locations. A. buccalis occurs in the buccal mucosa of
opossums. Sporadic Anatrichosoma infections have been
found in dogs and cats with eggs in micro-abscesses
in the dorsal skin or in detritus in cases with otitis
externa. A few human cases with skin alterations or
lesions of the buccal mucosa were diagnosed in Asia
and the USA, respectively. Anatrichosoma females are
approximately 20 mm long, the eggs are of the Trichuris
type (52-70x37-42 µm) with thick shells, 2 polar plugs,
containing an embryo when shed. It is assumed that eggs
are released together with epithelial cells or exudate and
are immediately infective.
i.========
• Selected references
Barus V, Sergejeva TP (1989, 1990) Capillariids parasitic in
birds in the Palaearctic region. (1-4). Acta Sci Nat Brno 23(3):
1-50; 23(6): 1-47; 24(13): 1-53; 24(12): 1-48.
Basso W, Spanhauer Z, Arnold S, Deplazes P (2014) Capillana
plica (syn. Pearsonema plica) infection in a dog with chronic
pollakiuria: challenges in the diagnosis and treatment.
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Bork-Mimm S, Rinder H (2011) High prevalence of Capillaria
plica infections in red foxes (Vulpes vulpes) in Southern
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Eberhard ML, Hellsteln JW, Lanzell E A (2014) Zoonolic
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:g
Ebner F, Hepworth MR, Rausch S, Janek K, Nlewienda A, a.
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KOhl A, Henkleln P, Lucius R, Hamelmann E, Hartmann C
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Guardone L, Deplazes P, Macchlonl F, Magi, M, Mathis
A (20·13) Ribosomal and mitochondrial DNA analysis of
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Haanaln SZ, Evans CM, Roy M, Gallagher AL, Klndrachuk
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Hiemstra IH, Klaver EJ, Vrijland K, Kringel H, Andreasen
A, Bouma G, Kraal G, Van Die I, Den Haan JM (2014)
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Cl)
Magi M, Guardone L, Prati MC, Mignone W, Macchloni F .c
c
(2014) Extraintestinal nematodes of the red fox Vulpes vulpes
in north-west Italy. J Helminthol 11: 1-6.
.E
<D
Nejsum P, Thamsborg SM, Petersen HH, Kringel H , I
Fredholm M, Roepstorff A (2009) Population dynamics
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Nejsum P, Betson M, Bendall RP, Thamsborg SM, Stothard
JR (2012) Assessing the zoonotic potential of Ascaris suum
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the past. J Helmlnthol 86: 148-55.
Nlthlkathkul C, Salchua P, Royal L, Cross JH (2011)
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978-0-19-857002-8. I,
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Traversa D, Di Cesare A, Brianti E (2015) Lungworm infections.
In: Beugnet F, Halos L (eds.). Parasitoses & vector-borne
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-
Veronesi F, Morganti G, Di Cesare A, Schaper R, Traversa
·;::
D (2014) A pilot trial evaluating the efficacy of a 10%
imidacloprid/2.5% moxidectin spot-on formulation in the
treatment of natural nasal capillariosis in dogs. Vet Parasitol .�
-
200: 133-138.
"iii
 Part Ill. Parasites and parasitoses: metazoa

Family Trichinellidae Trichinella spp. are the agents of trichinello sis

(colloquially named trichinosis). Numerous mammalian
Genus Trichine/la species and humans are hosts for several Trichinella
species, some species parasitise birds and reptiles. A
special feature of Trichinella spp. is that they use the same
Disease: Trichinellosis. host organism as the definitive and the intermediate
host. Adult worms inhabit the intestine where females
release larvae which subsequently infect striated muscles
Thrix (G): hair; -el/a (L): diminutive. Trichinella: 'small cells where they survive for years. Trichinellosis is a
hair: worldwide zoonosis, associated with a low incidence
of human cases on the one side and high costs for
Summary prevention programmes on the other. The annual costs
• for testing pigs for trichinellosis in lhe EU are estimated
• Currently, 9 1l1chmeiM species and Nveral at € 220 to 570 million.
�are known which Pl('liltlN mammals, birds
or niptllea. Seven of thtN ipecles are Infective for
humans, whereas two epeckil hive not been found In Agents. Trichinella is the sole genus of the family
hodi (T. ilmbibwensll, T. patagonltnsla). The Trichinellidae. Up to 1972, only one species, T. spiralis,
IPICIII oocu. In Oll'tiln geographical .,..., was known. Meanwhile, 8 further species and additional
1l1chlnelll ,pnJI, which NII I wider distribution, genotypes were identified ( ► Table 10.21). The females
Ing '9glona In Europe, Alla, and the Amerlcu of 'I: spira/is measure 3-4 mm in length and are 60-70 µm
IQ'!portlrltepeclealn Europe thick; males are 1-1.8 mm long, without spicule, at the
-Adult 111ch/neUa -­ posterior end equipped with a pair of lateral appendages
by a trlchurold serving as aid for copulation. A prominent character
Larval Stagll In the of larvae and adults is the trichuroid oesophagus with
lated or non-
stichocytes ( ► Figure I 0.89). The infective muscle
the aame lndMclual larvae of the various species measure 600-1,300 µm
host. Adult worms in length. Except for T. pseudospiralis, T. papuae and
fwnales release L1 T. zimbabwensis, the intracellular muscle larvae are
Ind lymph vessels and enclosed in a capsule ( ► Table 10.2 I). The adults of
which they can survive the various species and genotypes of the genus cannot
by lngeltlon of larvae be differentiated morphologically. Differentiation is
possible by DNA analyses and by considering biological
l9glonl, 7Hch/ne/la differences of the muscle larvae (e.g. infectivity for
, cyclee, but T. pigs and other host species, resistance to freezing
In aynanthroplc temperatures) and adults.
. The concomitant
wlcllftand domNtlc
of raw Life cycle. The development of T. spiralis is described
- Important here as an example ( ► Figure 10.90). Under natural and
experimental conditions, this species is infective to> 130
funlnl .. fllltlVlly ,.,., species of mammals and to humans. The infection of a
pnonl .. oftln ln¥olvld carnivorous or omnivorous host occurs by ingestion of
.... ormeatormllt striated musculature containing encapsulated infectious
ltll _,. IIMOI, larvae (LI). The larvae are released in the gastrointestinal
Hurlwll ffllY dlvllop tract and settle in epithelial cells of the small intestine,
...... (Jncludlng the predominantly at the bases of the villi. The epithelial cells
1H 11nc.11on1 ..
are transformed to syncytial layers, which are invaded
Q.)
by the 1,300 µm long larvae. They moult four times
·u
C
poet morwm detection of
'6 clglltlor, IC00Rlng ID offldll and develop into adults within 24-36 hours. Female
Q.)
start to release LI (length 130 µm) 5-6 days p.i. Each
lndlclted In ....... female worm produces 200-1,500 larvae in the course of
co BJ and national P9glllationa a maximum life span of 4-6 weeks (the males die after
C
·c copulation). The larvae invade the lamina propria, and
Q.) --- and meat Intended for
of food aafety (deep migrate within 5-7 days via the haemolymphatic system
.£: l'Mllt), contlOI of rodents In to the skeletal muscles or organs (occasionally also to
>, Ml'llllmlltnnn of 'lHdllnela-frN' farma. the liquor cerebrospinalis and the mother's milk). Those
Ol
0 human Infections reaching unsuitable tissues (myocardium, brain, liver,
--101n- thin In the pat. eye, etc.) die and may induce heavy local inflammatory
'iii
co reactions. Larvae which invade muscle cells (several cm
a..
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundwo rms)

Table 10.21. Species and genotypes of the genus Trichinella.

Species and genotypes (T) 1 Epldemlologlcal cycles and hosts (selection) General distribution; occurrence In
of THchlnells Europe (examples)2

1. Species with encapsulated rnuscl�arvae (encapsul�ed clade). Hosts: mammals -- -

Trichinella spiralis (T1)
Trichinella britovi (T3)
Trichinella nativa (T2)
Trichine/la murrelli (T5)
- co�ga!!_i:nu_stellds!.. �orse,_9og, gat, man
Trichinelta netsoni (T7)
Trichina/la patagoniensis
2. Species with non-encapsulated muscle larvae (non-encapsulated clade). Hosts: mammals, birds and reptiles
Trichina/la pseudospiralis
(T4)
Tn'chinella papuae (T10)
Trichinella zimbabwensis
(T11)
1 Genotypes: T6 (USA. Canada, related to T. nativa), TB (from wild carnivores, South Africa, Namibia, related to T. britov1), T9 (from wild
carnivores, Japan).
2 Details: http://www.iss.it/siteffrlchinella/scrlpts/ .
cycle predominantly synanthropic, also in wildlife General: eastern Asia, Europe, Egypt,
cycle USA, Mexico, South America. Hawaii,
domestic pig, wild boar, horse. dog, cat, red fox. New Zealand
raccoon dog, bear. rat, man Europe: ES, DE, IE, Fl, EE, LT, LV, PL.
HA.
- -BG, AO
AS,
wildlife cycle General: temperate zones: Eurasia,
red fox, raccoon dog, wolf, jackal, wild cat, lynx. north-western Africa. south-western Asia
brown bear, badger, marten, common otter. Europe: many countries from ES to AU
domestic pig, wild boar, horse, man and from-----
NO to IT and BG
wildlife cycle General: Arctic and subarctic regions in
polar bear, walrus, other seals, brown and black North America and Eurasia
bear, wolf, polar lox, red lox, raccoon dog, lynx, Europe: NO, SE, Fl, AU, EE, LT. LV, PL,
wild cat, tiger, mustellds, wild boar, domestic pig, DE, FA
dog, cat, man -- - -- - -
wlldllle cycle General: southern Canada, USA
red lox, raccoon, coyote, bobcat, black bear, Europe: -
-- - -- - - --
wildlife cycle General: Sub-Saharan Africa
jackal, hyena, lion, leopard, genel, serval, big-eared Europe: -
fox, bush pig, wart hog, man
wildlife cycle General: Argentina
cougar, no human cases reported Europe: -
wildlife cycle General: cosmopolitan
red fox, raccoon dog, lynx, badger, raccoon, wild Europe: IE, FA, DK, SE, Fl, EE, LT, DE,
boar, domestic pig, cat, rat, bird species (crows, AT, IT, SK, HU, BG, AU
hawks, falcons, eagles, owls, vultures, etc.),
(/)
marsupials, man ..c:
wildlife cycle
wild pig, domestic pig, saltwater crocodile, man
General: Asia (Papua-New Guinea,
Thailand) .E
Q)
Europe: - I
cycle In crocodile farms and wildlife cycle General: Africa (Ethiopia, Zimbabwe,
NIie crocodile, Nile monitor, lion Mozambique, South Africa)
no human cases reported Europe: -

Oesophag us,
glandular part --�
with stichocytes

Male: posterior end with

Mouth opening ___/ l eaf-like copulatory appendi­
ces

Posterior end

Figure 10.89. Trichinel/a spiralis: male (Graphics: IPZ, A. Seeger; after Skrjabin 1954).
 Part Ill. Parasites and parasitoses: rnetazoa

Development in intestine

A
I
L1 in blood
circulation

..r,., C)�
::"'\.

0 ,-, r: v

--&�
Development In musculature }

(D

u
C:

'6 L 1 migrating to the

(D
musculature
�
� L 1 invading a
co muscle cell
C:
.::
(D

j Figure 10.90. Life cycle of Trichina/la spiralis (Graphics: IPZ, S. Ehrat).

C:
>­
Ol
0 in length with diameters up to 130 µm) transform these grow rapidly, coil up until the 3 rd week p.i. and reach
B cells into 'nurse cells: which provide nutrition for the infectivity already 17-21 days p.i. Approximately 7 days
-en
co larva and clear waste products (see below pathogenesis) . p.i., the infected muscle cell begins to encapsulate the
co
a.. The larvae, which initially lie longitudinally in the cell, larva (rarely several larvae) within the cell membrane by
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)
producing various types of collagen. After 4-6 weeks the
entire process is finished, and the larvae are enclosed by
an oval, lemon-shaped capsule. Capsules of T. spiralis in
pig musculature measure 300-700x200-300 µm. Around
5-6 weeks p.i., granulation tissue and fat cells accumulate
at the polar ends, and the capsule gradually calcifies
(in pigs and humans beginning about 5 months p.i.).
Encapsulated larvae may survive for a very long time, for
instance 40 years in man and 11 years in pig. The cycle
is completed after ingestion of the larvae by a new host.
The development of the other species and genotypes in
principle corresponds to that of T. spiralis, yet 3 species
lack the formation of a capsule around muscle larvae
(► Table 10.21).
Epidemiology. The epidemiology of trichinellosis
is very complex due to the involvement of different
parasite species and genotypes, the large number of
potential host species, and the existence of different types
of transmission cycles. The occurrence of Trichinella
spp. both in domestic and wild animals, associated with
the consumption of raw or undercooked meat or meat
products, are important factors in the epidemiology of
human trichinellosis.
• Wildlife cycle (sylvatic cycle). This natural cycle
takes place independently from humans and domestic
animals in populations of wild animals. Transmission
occurs for the main part between carnivores by
predacious food intake or carrion-feeding. The infection
can be transmitted to other wild animals, e.g. wild boars.
Humans may become infected directly, e.g. with T.
spiralis by consumption of meat of wild boars or with
T. nativa by bear meat or seal meat. Parasites may also
be transmitted to domestic animals, e.g. horses, and
with their meat to humans. Wildlife cycles are known
to occur in all Trichinella species( ► Table 10.21).
• Synanthropic cycle. T. spiralis is predominantly
mediated in synanthropic cycles. The parasite circulates
in pig populations where it is transmitted by feeding of
insufficiently heated kitchen slops or abattoir waste,
ingestion of conspecifics and possibly also by ear or tail
biting. Sources of infection for pigs may be carcasses of
Muscle cell
Fat cell
Trichina/la larva
Capsule
Fi gure 10.91. Trichina/la spiralis: encapsulated larva in rat
muscle, histological section (capsule about 3OO-7OOx2OO-
300 µm) (Photo: IPZ).
wild animals as mustelids, foxes, rats( ► Figure 10.90).
Otherwise, rats and wild carnivores may acquire a T.
spiralis infection if they have access to abattoir waste.
• Importance of various hosts. Carnivores play
the major role in the epidemiology of mammalian
trichinellosis. Apart from monospecific infections, (1j
:g
polyspecific infections with 2-3 different species in 0..
0
one host have been reported. Major reservoir hosts in C
Europe are foxes, raccoon dogs, badgers and martens.
w
Wild boars and domestic pigs are likewise important
and are mainly infected with T. spira/is or T. britovi, in
the latter case when the wildlife cycle in the fox merges
with the domestic cycle. Other Trichinella species are
rare (for instance, in Germany T. pseudospiralis in wild
boars). Wild and domestic ruminants can be infected
experimentally with Trichinella spp. but are without
epidemiological importance. Horses are rarely involved;
however, the meat of infected horses, imported from
North and South America or countries in eastern
Europe, has caused several heavy outbreaks of human
trichinellosis in Europe. Presumably, these animals were
fed meat of wild carnivores and forbearing animals
which was illegally used to fatten the horses.
• Tenacity of muscle larvae. Muscle larvae may
survive the death of their host for some time. Thus,
encapsulated T. spiralis and T. britovi larvae remain
infectious in decaying meat for up to 4 weeks at-22 °C
and 100% relative humidity and up to 300 days at 2-4 °C. en
The resistance to freezing temperatures varies with the .c
species and the host( ► p. 381). For example, larvae
of T. nativa, which is endemic in arctic and subarctic
·a5e
regions, may sur�ive deep freezing temperatures(-18 °C) I
for months or years. In contrast, T. nelsoni, occurring in
Africa, is highly sensitive to cold but survives at higher
temperatures in decaying musculature for a long time.
Muscle larvae of T. spirnlis resist drying and curing of
meat as well as most smoking procedures.
Occurrence. Information on the geographical
distribution of the various Tri chine/la species is presented
in ► Table 10.21. According to current knowledge,
4 species occur in Europe; in most countries several
species are present. T. britovi is found in many European
countries in wild carnivores, partly also in wild boars.
Q)
Also, T. spira/is occurs in a number of countries in this
·o
C
group of animals. This species is found in synanthropic '5
Q)
cycles, e.g. in Spain and in several countries in eastern �
and south-eastern Europe. Concerning the occurrence �
of T. nativa and T. pseudospiralis ► Table 10.21. (1j
C
·;::
Q)
J
Domestic pigs which are maintained under good
hygienic conditions in stables are generally free of C
Trichinella. According to previous reports(2008) from >.
0)
25 EU member states, 1,179 slaughter pigs out of 167.5 0
million investigated animals were found to be infected E
"iii
with Trichinella. The infected animals originated from 8
Cll
countries. In the same year, 891(208/100,000) wild boars Q..
I
 Part Ill. Parasites and parasitoses: metazoa
carried Trichinella spp. Wild carnivores are infected
more often, e.g. foxes (EE, LV, LT: 29-41%, DE: 0.3%)
and raccoon dogs (Fl: 19%, EE: 42%) (data from 2005
and 2007). Rats which were caught in pig stables in
Croatia were infected with Trichinella spp. at 22-80%.
The prevalence in horses imported from eastern Europe
was estimated at 0.36/100,000 several years ago.
Pathogenesis. Two phases are to be distinguished
in the course of trichinellosis: the intestinal phase and
the muscle phase.
• Intestinal phase. The Ll of T. spiralis, when
released from their capsules in the gastrointestinal
tract of a host, are superficially covered with a layer of
glycoproteins containing tyvelose (a highly antigenic
sugar: 3,6-dideoxy-D-arabinohexose). Possibly, these
glycoproteins protect the larva against enzymatic
digestion. The larvae infect intestinal epithelial cells
which subsequently are transformed to syncytin (each
out of> l 00 cells). Tyvelose-containing glycoproteins
also seem to play an essential role for cell invasion by the
larvae. They are synthesised in stichocytes and released
in the course of cell invasion (the total repertoire of
stichocyte secretions consists of >40 proteins). The
invasion can be inhibited in vitro by antibodies to
such glycoproteins. The intestinal infection may be
asymptomatic or associated with a catarrhalic, in heavy
cases also haemorrhagic enteritis.
• Muscle phase. Ll infecting striated muscle cells
initially induce degenerative processes but also transform
the myocyte into a 'nurse cell' by secreting mediators
which modify the host cell's gene expression. On the way
to be transformed to nurse cells, the infected muscle cells
loses their myofibrils and muscle-specific proteins (actin,
myosin, creatinc kinases) but shows proliferation of the
nuclei and mitochondria. Also, neighbouring cells may
be involved, e.g. with proliferating nuclei. Subsequently,
cellular infiltrations develop in the interstitial tissue
causing a transient non-purulent interstitial myositis
(leukocytes with varying proportions of eosinophils,
fibroblasts, foreign body giant cells). After completion of
the capsule formation around Lhe larva, a kind of resting
state develops: interstitial infiltrations almost disappear
and uninfected neighbouring cells appear normal again,
Q)
C: a stage which may persist for many years (see above).
·r;
'6
Q)
Immunology. lmmuno-dominant antigens differ
�
�
between larval and adult stages. These differences are
co apparently part of the immune evasion strategy of the
C:
·;::: parasile. Intestinal stages of 'f spiralis induce a mixed
Q)
j Thl/Th2 type response with dominating Th2 reactions.
Approximately two weeks p.i., a partial expulsion of the
-�
>, adult worms usually occurs. The mechanisms possibly
-
0)
0 correspond to similar effects in pigs against Trichuris
0
"iii suis and may involve the mucin Muc5ac (► p. 35).
co Accordingly, the expulsion of T. spiralis is delayed in
co
0... Muc5ac-deficient mice when compared to the wild type.
The establishment of larval stages in striated muscles is
obviously supported by immunosuppressive mechanisms
which downregulate inflammatory responses. Thus, Il­
l O-deficient mice respond to invading larvae in contrast
to wild-type mice by massive cellular infiltrations.
During the chronic infection, the efficacy of IL-10
decreases; the persistence of larvae is then obviously
assured by other Th2 dependent mechanisms.
Pigs infected with some hundreds of larvae may develop
a protective immunity which reduces the reproductivity
of female worms, and interferes with LI from subsequent
infections.
The onset of seroconversion ( lgG) in Trichinella spp .
infected pigs depends on the infi.:ction dose and occurs
at the earliest in the yd week p.i. Maximum antibody
levels are observed after 8-24 weeks. Considering the
common age of pigs at slaughtering, noticeable antibody
levels persist long enough to be used for diagnostic
purposes. An earlier drop is observed in infected horses
where threshold values are reached already 24-26 weeks
p.i. There is a high degree of cross-reactivity between
antigens from the various Trichinella species.
Clinical signs. Naturally acquired Trichinella
infections in animals are usually asymptomatic and
remain undetected. Serious experimental infections
with T. spiralis, however, may cause symptoms in various
host species. Pigs and puppies of dogs and cats may
develop severe catarrhal enteritis with diarrhoea and,
in dogs and cats, occasional vomiting in the first week
p.i. Later on, the clinical picture is determined by the
affected muscles, with myositis, stiffness and pain. Young
dogs and cats show myalgia, restlessness, convulsions
and oedemas around the eyes. Transient eosinophilia,
heart dysfunctions and difficulties in swallowing arc
common symptoms. In horses muscle dysfunctions,
increased serum levels of lactate dehydrogcnase, aldolase
and creatine phosphatase were reported.
Diagnosis. According to EU regulations (EC No.
853/2004 and EC No. 2075/2005) meat of domestic pigs.
horses and other potential carriers of 'J'ricl1i11ella species
intended for human consumption has to be officially
examined in EU member states for Trichine/111 lar1'ile
(see control below). Corresponding regulations arc in
force in Switzerland. Other states, e.g. the USA, desist
from such meat inspection. The standard diagnostic
procedure prescribed by the EU is the direct detection
of muscle larvae by digestion techniques ( ► p. 535:
► Figures 10.92 and 10.93). The isolated larvae haw
to be identified by morphological criteria considering
migrating larvae of ascarids (Ascaris, Toxocara) and
artefacts (hairs, plant fibres) in differential diagnosis.
Since 2011 the EU has approved the latex agglutination
test as a method equivalent to microscopic detection of
Trichinella larvae (EU No. 1109/2011). However, none of
 10. Phylum Nematoda (syn. Nematozoa) (threadworms or roundworms)
is
s
Figure 10.92. Trichina/la spira/is: muscle larvae In sediment of
digestion fluid (Photo: IPZ).
the methods allows a species differentiation. In case of
positive results, the samples are therefore to be sent to a
reference laboratory for genetic species determination.
Intra vitam diagnosis is possible by determining specific
antibodies and investigating (histology, DNA analyses)
muscle biopsies.
Therapy. Treatment of experimentally infected dogs
and cats 4-5 weeks p.i. with albendazole (SO mg/kg b.w.
p.o., every 12 hours for 7 days) reduced the number
of muscle larvae. Treatment of horses and pigs is not
considered useful.
Control. Trichinella infections in humans and
animals are notifiable in most member states of the
EU, in other European as well in many non-European
countries. In the EU, control of trichinellosis is based on
recommendations of the International Commission on
Trichinellosis, EU regulations (EC No. 854/2004; EC No.
2075/2005, etc.) and special legislation of various states.
• Measures for meat safety. Carcasses and meat
of domestic pigs, horses, wild boars, other wild or
farmed game and all other animal species susceptible
to Trichinella spp. intended for human consumption
are to be examined for trichinellosis, unless legislation
provides otherwise. All parts from animals infected
with Trichinella are to be declared unfit for human
consumption and must be destroyed.
Meat from potential Trichinella carriers may not be
imported into the EU unless it has been examined
in the country of origin. Under supervision of the
competent authorities, examinations for trichinellosis
can be omitted for pigs or meat derived from them
originating from farms which are officially certified as
'Trichinella-free' or from regions with a negligible risk
of Trichinella infection.
C1:l
:g
Q.
0
C
w
Figure 10.93. Tr/chine/la spira/1s: muscle larvae in a press
preparation (Photo: IPZ).
Meat of domestic pigs, not examined for trichinellosis,
can be certified as Trichinella-free, provided it has
undergone regular freezing treatment (e.g. 20 days at
-15 °C for meat up to 15 cm thick). However, a residual
risk remains if pigs are infected with T. britovi since
larvae of this species can survive -20 °C up to 3 weeks.
Generally, the freezing tolerance of Trichinella muscle
larvae varies with the species/genotypes and depends
also on the host species. T. nativa, T. britovi and genotype
T6 are known to survive long periods of freezing. Larvae
of T. nativa survive -18 °C in musculature of foxes and
bears for 4 and 5 years, respectively. Therefore, freezing
of meat is not safe for killing cold-resistant Trichinella
larvae. The same holds true for curing and drying of
meat. Gamma radiation can kill the larvae; low dose
radiation (up to 1.0 kGy) is permitted in the USA. Also,
a more recent technique of meat decontamination, the
High Hydrostatic Pressure (HHP) processing, kills
muscle larvae of T. spiralis.
A particular risk of infection exists in some countries due
to consumption of meat derived from home slaughtering
of pigs or game hunting, if meat inspection for Trichinel/a
is not regulated by national legislations or the regulations
are disregarded. In these cases, education and individual
prophylaxis are of particular importance. Heating the
meat (minimum core temperature 70 °c for 1 min)
reliably kills Trichfr1ella larvae.
• Measures in livestock. Trichinella infections in
domestic pigs under modern farming conditions are
extremely rare. They occur more often, however, in
geographical areas where pigs are kept in backyard farms
and are fed on untreated kitchen slops, abattoir waste,
carcasses of wild carnivores or fur-bearing animals.
Further, they are observed in pig husbandries where
potential carriers of Trichinella spp. (particularly rats and
other rodents, mustelids, foxes) have access and where
cannibalism between pigs is not prevented. Outdoor
 Part Ill. Parasites and parasitoses: metazoa
rearing of pigs bears the risk of Trichinella infections
if the pigs can feed on wild-living p arasite carriers
(rodents, foxes, wild boars).
According to EU regulation EC No. 2075/2005, pig farms
can be certified as 'Trichinella-free: provided compliance
with a set of very strict requirements (amongst others
rodent control and Trichinella prevalence <0.1% in wild
animals in the area, e.g. in foxes). Surveillance may be
p erformed by monitoring the Tricl1i11ella prevalence
in indicator animals (foxes). Slaughter pigs and meat
from such farms are exempted from examinations for
Trichinella. Similar regulations exist in the USA (sec
National Trichinae Herd Ccrtif1catlon Program).
Zoonotic importance. Trichinellosis is a zoonosis
of worldwide distribution. According to data published
in 2007, 22% of 198 countries had recorded Tric/1i11dla
infections in domestic animals, 33% in wildlife and
28% in humans. In the period 2008-2012, bctween 11
and l3 of 26 EU member states reported confirmed
cases of human trichinellosis 'Arith a total of 2,2 I 2 cases
(annually 223-750 cases), corresponding to an average
incidence of 0.06 cases per 100,000 inhabitants. In 2012,
29 l of 301 confirmed cases were reported from Romania
(149), Bulgaria (30). Latvia (41 ), Lithuania (28), Italy
(33) and Spain (10). The two main sources of human
trichinellosis in the EU are meat from backyard pigs
that are not examined for Trichinella, and wild boar
meal Most human cases of trichinellosis in Europe are
caused by T. spiralis and T. britovi, only a few cases by
T. pseudospiralis and T. nativa. Trichinellosis can affect
a few individuals or large groups of people (example:
2,659 persons). Recently (20 I 5), the global incidence rate
of reported human trichinellosis was estimated at 0.47
cases per I million inhabitants including the following
variations in the different WHO regions: Europe:
2.73; eastern Mediterranean: 0.004; Africa: 0.0019; the
Americas: 0.37; South-East Asia: 0.063; western Pacific:
0.34. However, the rates are much higher when adjusted
to underreporting (e.g. global rate 0.98).
.In humans, infection with 50-70 Trithinclla larvae per
person may already cause clinical symptoms (intestinal
phase: nausea, vomiting, gastrointestinal disorders, low
fever; mu de phase: myositis with muscular pain, facial
Q)
C: oedema, diffkulties breathing and swallowing, fever,
u C, Cocoma GJ, Luchanskl JB (2010) Evaluation ol
'6 oedemas of rhe C)1elid and face, exanthemas). Fatal
0)
cases may occur after hea,ry infections due to damage
to the heart muscle. On average. 80.5% of the patients
ro diagnosed in 2012 in the EU were hospitalised.
C:
·c
Q)
C: Selected references
>,
0)
0 Devleesschauwer B, Praet N, Speybroeck N, Torgerson PR,
0
·1n Haagsma JA, De Smet K, Murrell KD, Pozio E, Dorny P
{2015) The low global burden of tnch1neilos1s: evidence and
co
a.. 1mpbcat10ns. Int J Parasno1 45· 95-99.
Dupouy-Carnet J, Murrell KD (eds.) (2007) FAO/WHO/OIE
Guidelines for the surveillance, management. prevention and
control of trichinellosis. Paris, France: World Organisation for
Animal Health; ISBN: 92-9044-704·4.
EFSA (2014) The European Union Summary Report: Trends and
sources of zoonoses and zoonotic agents and food-borne
outbreaks in 2012. EFSA Journal 12: 3547.
EU (2004) Regulation (EC) No. 854/2004 of the European
Parliament and of the Council laying down specific rules for
the organisation of official controls on products of animal
origin intended for human consumption. Official J European
Union L 139, 30 April 2004.
EU (2005) Commission Regulation (EC) No. 2075/2005 laying
down specific rules on official controls for Trlch,nella in meat
Official J European Union L 338, 22 December 2005, pp.
60-82.
EU (201 1) Comm1ss1on lmplepenttng Regulation (EU) No.
1109/2011 of November 2011. Ott1c1al J European Union
L 287/23, 4 November 2011.
Frey CF, Schuppers ME, Muller N, Ryser-Deglorgis MP,
Gottsteln B (2009) Assessment of the prevalence of
Tr/chine/la spp. in red foxes and Eurasian lynxes from
Sw1tzer1and. Vet Parasitol 159: 295-299.
Gottsteln B, Pozlo E, NOckler K (2009) Epidemiology. diagnosis.
treatment, and control of trichinellosis. Clin Microbiol Rev 22:
127-145.
Kapel CMO (2000) Host diversity and biological characteristics
of the Trichlnella genotypes and their effect on transmisslOO.
Vet Parasitol 93: 263-278.
Korhonen PK, Pozlo E, La Rosa G, Chang BC, Koehler
AV, Hoberg EP, Boag PR, Tan P, Jex AR, Hofmann A,
Sternberg PW, Young ND, Gasser RB (2016) Phylogenomoc
and biogeographic reconstruction of the Trichinella complex
Nat Commun 7: 10513.
Mukaratirwa S, La Grange L, Pfukenyl DM (2013) Tnch,nel/a
infections in animals and humans in Sub-Saharan Afnca: a
review. Acta Trop 125: 82-89.
NOckler K, Serrano FJ, Bolreau P, Kapel CMO, Pozlo E
(2005) Experimental studies in pigs on Tnchine/la detection
In different diagnostic matrices. Vet Paras1tol 132: 85-90
Pozlo E (2011) Trlchinellosls. In: Palmer SR. Lord Soulsby.
Torgerson PR, Brown DWG, eds. Oxford Textbook of
Zoonoses. 2nd ed. Oxford, UK: Oxford University Press,
pp. 755-766; ISBN 978-0· 19-857002-8
Pozlo E, Zarlenga DS (2013) New pieces of the fnch!flel/J
puzzle. Int J Parasitol 43: 983-97.
Porto-Fett ACS, Call JE, Shoyer BE, Hill DE, Pshebnlskl
f9f'mentation, drying and/or high pressure processing on
v1ab1hty of L.Jstena monocvtogenes, Eschench,a coh 0157:H7.
Salmonella spp. and Tnch1nel/a spiralis in raw pork and Genoa
salam1. Int J Food Microbiol 140· 61-75.
 10. Phylum Nern atod
a (syn. Nematozoa) (threadworms or roundworms)

- superfamily Dioctophymatoidea

family Dioctophymatidae
Genera Oioctophyma and Hystriches g
Dioctophyma renale (syn. Dioctophyme renale). Giant cu
:g
ki dney worm. Males 14-45 cm, females 20-130 cm long, 0.
bloo d-red, long cylindrical oesophagus. Adults in the
0
C:
w
renal pelvis of minks and other mustelids, rarely also in
foxes, wolves, dogs, cats and humans. Cosmopolitan; in
some areas (Brazil) endemic in dogs. Human infections
rare (~20 reported cases). Eggs are shed with the urine.
Cycle includes aquatic Oligochaeta as intermediate
hosts. Infection usually by ingestion of paratenic hosts
(frogs, fish).

Histrichis tricolor in the proventriculus of wild and

domestic ducks, geese and fish-eating birds in Europe.

Se I ected references r:.:s:z:::=:::;:a:;::m:r.:ll:l!i:::=:::'.:I

Anderson RC (2000) Nematode parasites of vertebrates. Their

development and transmission. 2 nd ed. Wallingford, UK: CAB
International; ISBN 0-85199-421-0.
Rahal SC, Mamprim MJ, Oliveira HS, Mesquita LR,
Faria LG, Takahira AK, Matsubara LM, Agostinho
FS (2014) Ultrasonographic, computed tomographic, and
operative findings in dogs infested with giant kidney worms
(Dioctophyme renale). J Am Vet Med Assoc 244: 555-558.

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11. Phylum Acanthocephala (thorny-headed
or spiny-headed worms)

Diseases: Acanthocephaloses. the body wall (tegument), a complex syncytium with

Acm1tlw (G): thorn; ceplwle (G): head. Reference to the
proboscis, armed with hooks, located at the anterior end.
Acanthocephala are helminths of moderate veterinary
importance, but they deserve attention ns intestinal
parasites in ,vaterfowl, fish and some other vertebrates.
Some species are listed in ► Table 11. I.
Agents and life cycle. Adult acanthocephalans are
intestinal parasites of mammals, birds, reptiles, fish and
amphibians. They consist of an anterior proboscis, a
neck region, and an elongate tube-like part ('trunk'). The
proboscis is a cylindrical or spherical organ, armed with
arrays of hooks, which is retractable to a sack-like pouch
and used for attachment to the gut wall of definitive
hosts ( ► Figure I 1.1). Since acanthocephalans do not
have a digestive tract, nutrients are taken up through
few giant nuclei or numerous small nuclei, supported by
underlying connective tissue and muscles. The tegument
contains a lacunar system of interconnecting canals
which is filled with liquid and contributcs to transport
nutrients and other substances; it communicates with
two unique structures (lemnisci, �ingl. lernniscus) which
protrude at the front end from thl' inner body wall into
the body cavity and store lipids and liquid. Liquid plays
a role inter alia for regulating the hydrostatic pressure
during eversion of the proboscis. Acanthocephalans
are heterosexual and develop in indirect life cycles
with arthropods as intermediate hosts, according to
the following scheme ( ► Figure I I. I): Eggs, each
containing an acanthor larva with hooks, are shed
by a definitive host. If eggs arc ingested by a suitable
intermediate host, the larvae are released, enter the
body cavity and differentiate to the infective acanthella
stage. Definitive hosts become infected by ingestion of
infected intermediate or paratenic hosts.

1
Table 11.1. Examples of acanthocephalan species.

lpeclN, length (mm), and dlstrtbutlon (D) Deflnltlv• hosts Predllectlon site lntennedlateholtl

Q_rder Oligacanthorhynchlda
Macracanthorhynchus hlrudlnaceus f domestic pig. wild boar, small Intestine beetles (lnrvao): may I
r; �: 50- ICX); '• 1 : 200•650 1 occasionally carnivores, rarely
1 and dung beetles, etc. I
D: worldwide humans
Prosthenorchls elogans new world monkeys small Intestine. cockroaches. beetles 1
,!-:: 20-40,
r 'r : 30-65 occasionally large
0: South America [ intestine
Order Echinorhynchida
Echinorhynchus truttae
c'- 8-11; ',.: 15-20
1:
I
1 salmonid fish l intestine arnphlpods:
Garnrnandao
D: Europe
Acanthocephalus anguil/ae fish: cypnrnds, pike, eel, intestine freshwaler 1sopods:
-1,!: 5-9. •.: 10-35 salmonids etc. I Asel/us
_D:_ Europe 1
Order Polymorphida
Polymorphus mlnutus duck, swan, other species of ntestine amphipods:
,! ! 2-3.�. 6-10 water birds, rarely chicken Gammaridae 1
D: Eurasia, Nortl1 Amenca
1 (

Filicollis anatis duck, goose. wild water birds intestine freshwater ,sopods:

I
-� �: 6-8, ';; :10-26 mm Ase//us 1
D: Eurasia
Order Neoechinorhynchida
Neoechinorhynchus rutili fish: cyprirnds, salrnonids, 1 intestine ostracods
cJ: 2-8, ry: 5-10 eels
D: Eurasia, North America
1 Small fish may serve as paratenic hosts.
♦

Anterior end
W1th proboscis

Infected Now World

monkey

Adult parasite In Intestine

Acanthella larva

Hatched acanthor
larva

Developing juvenile
stage
Figure 11. 1.
Life cycle of Prosthenorchis e/egans (Graphics: IPZ, S. Ehrat).

I ..,
Part Ill. Parasites and parasitoses: metazoa

Occurrence and epidemiology. Macracantho­ ' ,,�\

rhynchus hirudinaceus, a giant acanthocephalan, has a /
worldwide distribution. In Europe, it occurs mainly in I /.
feral pigs ( e.g. local prevalences in TR 19%, in ES 53%), i\
IJ .
I
rarely in free-ranging domestic pigs. Prosthenorchis ' I
species are parasites of New World monkeys;
occasionally they create problems in captive monkeys
• I "
(see below). Polymorphus and Filicollis infections can I If \
cause disease in water fowls with access to natural waters ll,, \'
under extensive maintenance conditions. In freshwater '\ :� �.
fish, and rarely in marine fish, acanthocephalans are I
I
\.•�" \I \... \
;

represented by many species, e.g. in eels of the Rhine ,J' I,_

river with 6 species, including Acm11/wceplwlus 1111g11il/ae Figure 11.2. Intestine of a monkey with Prosthanorchis infecti on
and A. rhinensis. Depending on the involved species (Photo: IPZ, J. Eckert).
and infection intensity, acanthocephalans can exert
significant adverse effects.
Zoonotlc importance. Accidentally, humans
The occurrence of acanthocephalans depends on the acquire intestinal infections with Macmcanthocepha/11s
presence of suitable intermediate hosts. Repeatedly, /1irudinaceus (from pigs), M. i11gens (from raccons),
Prosthenorchis species were introduced by New World Moniliformis moniliformis (from rodents) or some other
monkeys from Latin America to other continents. acanthocephalan species ( ► Table 15.2, p. 513).
There - instead of Latin American cockroaches - other
cockroach species took over the role of intermediate
hosts (vicarious intermediate hosts). For example, in Selected references
some European zoos native cockroaches (Blattella
germanica) transmitted Prosthcnorchis spp. to other Crompton DWT, Nickol BB (1985) Biology of the
monkey species, e.g. chimpanzees. Acanthocephala. Cambridge. UK: Cambridge University
Press: ISBN 0-521-246741.
Pathogenesis and clinical signs. Acanthocephalans Mehlhorn H (ed.) (2008) Encyclopedia of Parasitology. 3rd ed.
can be differentiated into non-perforating and Berlin, Germany; Springer: ISBN: 978•3-540-48994-8.
perforating species. While the proboscis of the former Taraschewski H (2000) Host-parasite interactions 1n
causes shallow lesions at the attachment site, the latter Acanthocephala: a morphological approach. Adv Paras1t01
species can penetrate deep into the intestinal wall. As an 46: 2-179
ex.ample, the infection of monkeys with Prothenorchis Yazwinskl TA, Tucker C, Featherston H, Johnson Z, Wood•
elegans is mentioned here. The infection can remain Huels N ( 1997) Endectocidal efficacies ol cloramocttn 111
asymptomatic or is associated with uni.pccific dinicnl naturally parasitized pigs, Vet Poros1tol 70: 123· 128
signs, such as inappelence, progressive weakness and
emaciation. In the small lnte61inc, bul also in colon nnd
caecum, single or aggregates of several ocnnthocephalans
can be found attached 10 the mucosa, some of them
penetrating with the proboscis to the subserosa, causing
granulomatous nodules; perforation of the bowl wall
occurs occasionally ( ► Figure 11.2).

Diagnosis, treatment and control. Diagnosis in

living animals: detection of typical eggs containing an
acanthor larva armed with hooks (SAF or sedimentation­
flotation method). Post mortem; detection of adult or
juvenile parasites. Therapy: In pigs doramectin (Ix 0.3
mg/kg b.w. i.m.) was partially effective (62%) against
Macrt1Cllt1tlwrhyncl11Js. A better efficacy (86-100%)
was obtained with ivermectin in daily doses of 0.1
or 0.2 mg/kg b.w., applied in feed for 7 consecutive
days. According to case reports, fenbendazole (2x 20
mg/kg b.w./d for 5 d p.o.) was effective in monkeys
against Prostl,enorchis and well tolerated. Waterfowl:
tentatively fenbendazole (2x 20 mg/kg b.w./d for 5 d
p.o.). Intermediate host control is only possible under
certain conditions, e.g. in enclosures of monkeys.
12. Phylum Annelida (segmented worms)
Annulus (L): ring. Reference to annulation of the body.
Within the phylum Annelida (-17,000 species) the
subclass Hirudinea (leeches) is of veterinary and medical
interest.
Characteristics and life cy cle. Hirudinea (about 300
species) are 1-30 cm long annelids, with a dorsoventrally
flattened, or rarely cylindrical body, consisting of a fixed
number (32-34) of inner segments (Acanthobdellida
30), each corresponding to 2-14 outer annulatfons. The
tegument is commonly coloured black, green, brown, or
red, sometimes with flashy spots or stripes; bristles are
lacking (except Acanthobdellida). Adult leeches have an
anterior oral sucker and a larger posterior adhesion disk
(acetabulum), which can be attached to surfaces in the
habitat or on a host and are used as supporting holdfasts
for movements. Hirudinea are hermaphrodites with a
direct life cycle. After mutual copulation they release up
to 200 eggs in a cocoon. Juvenile stages hatch from the
eggs and develop into adults; this development may take
a few years. Hirudinea, which occur in fresh water and
moist terrestrial habitats (most species) or in seawater,
live as predators or as parasites of amphibians, fish, water
birds and mammals, including humans.
Representatives of the order Gnathobdellida, including
the well-known medicinal leech Hirudo medicinalis,
are characterised by 3 pharyngeal jaws, armed with
about 100 small teeth, which are used like a saw to
scarify the skin of hosts for blood-sucking, leaving
behind a tri-radial wound. In members of the order
Rhynchobdellida the jawless foregut is transformed
to a protrusible and retractable proboscis, whereas
the Pharyngobdellida, lacking jaws or proboscis, are
characterised by a very long, non-protrusible pharynx
with a Y-shaped cross section. Blood-sucking leeches
secrete bioactive substances into the wound, including
an anticoagulant (hirudin) (see below), and are able
to ingest large amounts of blood exceeding 10 times
their own weight. The blood is stored in diverticula
of the crop, excessive water and minerals are excreted,
and the remaining concentrated material is protected
against premature degradation, apparently with the help
of symbiontic bacteria. Thus, the food can subsist for
months so that leeches may not require feeding for up
to more than one year.
Species and significance. Most species of leeches
are temporary, blood-feeding parasites of the skin
and mucous membranes of the upper respiratory and
digestive tract. Their pathogenic effects include small
bleeding lesions at the attachment site, blood losses
and obstructions in nasopharnygeal and oropharyngeal
passages. Depending on the intensity of the infestation
and the size of the host, blood losses may lead to severe,
life-threatening anaemia.
Piscicola geometra (2-5 cm) and Hemiclepsis marginata
(up to 3 cm) are skin parasites of fresh-water fish,
endangering predominantly young fish. Theromyzon
tessulat11111 (1-5 cm) parasitises nasopharyngeal cavities
of water birds (ducks, geese) and can cause severe
disease. Li111t1atis t1ilotica (up to 10 cm) occurs in the
Mediterranean region, northern Africa and Middle East
and lives in water holes, ponds or creeks. In such habitats,
leeches invade the nasopharyngeal cavities, trachea and
oesophagus of drinking animals (ruminants, horses, dogs)
and can cause life-threatening obstructions, swellings
and bleedings. Similar infestations have rarely occurred
in humans, some with a history of drinking unfiltered
water. In humid tropical and subtropical regions (Asia,
Australia, Madagascar), blood-sucking terrestrial
leeches (Haemadipsidae, order Gnathobdellida) can
be an annoying problem to animals and humans. These
leeches reside on the vegetation and attach quickly to the
skin of a bypassing host - sometimes in large numbers
- at any accessible site (e.g. humans: neck region, legs,
arms), causing small bleeding wounds. In some regions
they are regarded as a 'formidable pest' or 'vampire
worms'. In the Amazon region, the large Haementeria
gl1iliat1ii (order Rhynchobdellida) (up to 30 cm) attacks
vertebrate animals and humans. Leeches are vectors of
several agents, e.g. trypanosomes of fish and reptiles.
The role of medicinal leeches is discussed below.
Diagnosis and therapy. Leeches can be diagnosed
macroscopically on body surfaces; endoscopy is used
for detecting them in body cavities. Gentle removal of
the leeches after topical application of drops of vinegar
or lidocain has been recommended for therapy.
Medicinal leeches. Since ancient times, leeches
have been employed for treatment of certain diseases.
Of 15 species, classified as medicinal leeches,
Hirudo medicinalis (European medicinal leech =
m.1.), H. orientalis (Caucasian m.l.) and H. verbana
Q)
(Mediterranean m.l.) are used in Europe, with H. C
·c:,
verbana as a species most commonly available from '6
Q)
certified leech farms. During a blood meal, leeches �
secrete saliva into the wound, containing more than 100 �
bioactive substances. One of the best known components (1j
C
·;:::::
is hirudin, a potent inhibitor of blood coagulation, Q)
which has been successfully used for antithrombotic j
therapy; it is now available in a recombinant isoform. C
Moreover, anti-inflammatory, immunomodulating, >,
-
Ol
potentially analgetic and many other substances
0
0 ,! II
have been identified in the saliva, even antimicrobial ·u5
I
I I:
substances, which induce lysis of bacterial cells. It
Ii
(1j
is assumed that these substances are released by the a..
I
 PM Ill. Poms1tati anct porosltoses: metozoa

leeches to protect their symbionts from other harmful

bacteria. The antithrombotic effects ofleech saliva and
'hirudotherapy' as a measure of bloodletting are widely
accepted, but many of the reported beneficial cffects
regarding a broad spectrum of human and animal
diseases arc unexplained.

Selected references

Borda E, Oceguera-Figueroa A, Siddall ME (2008) On tho

classification, ovolulion nnd b1ogoouruphy of terrostrlnl
haemad1pso1d leochos (H1rud1nIdo . Art,ynchobdolhdn:
Hirud1niforme�). Mol Phylogonet Evol 46: 142-54.
Hartmann-Schrader G ( 1993) Slnmm Annelida, R1ngolwiim10f
odor Gllodorw0rmor. In: Gruner HE (ed.) Lehrbuch der
Spoz1ellon Zoolog10. 5. Aull. Bond I: W1rbelloso T1oro. 3.
Toll. Jena. Germany. G. F1schor, pp, 276-469: ISBN 3-334-
00339-6.
HIidebrandt JP, Lemke S (201 I) Small bite. largo Impact­
saliva and sahvory molecules In lhe modlclnol leecll, Hlrudo
mod1c1110/1s. Naturw1ss 98: 095-1008.
Kutachera U (2012) Tho Hlrudo mod,cinalis species complex.
Naturwl!l!l 99:433-434.
Rajael SM, Khorram H, Ansari Mood M, Mashhad! Rafle
S, WIiiiama DL (2013) Oral lnfastatoo with leech L/mnatls
m/ot/cJJ In two m1xod-brood clogs. J Small Anim Pract 55:
648-651.
Sobczak N, Kantyka M (2014) H1rudolherapy In veterinary
modIctr10. Ann Pararntol 60: 89-92.

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13. Phylum Pentastomida (incertae sedis)
(so-called tongue worms)
Diseases: Pentastomidoses.
Pente(G): five; stoma (G): mouth(explanation see text).
Pentastomida are a phylogenetically old group of
parasitic metazoa, whose existence in the Cambrian
is documented by 500 million years old fossils. Their
relation to arthropods is obvious, but their systematic
position is controversial since many years. Currently,
two hypotheses prevail: (a) a close relationship to the
Branchiura (subclass of crustaceans) in the phylum of
,1rthropods sensu stricto, and (b) the allocation to a 1995
newly established taxon 'Panarthropda', comprising the
free-living velvet worms (Onychophora or 'clawbearers'),
waterbears(Tardigrada) and arthropods(Arthropoda).
Because of the uncertain systematic position the
pentastomids are treated here as a separate phylum.
Adult stages of pentastomids(about 125 recent species)
are 1-16 cm long, dioecious, worm-like, cylindrical,
rarely dorsoventral flattened, usually yellowish-white
colored metazoans, divided into a short forebody(head)
and long hindbody(trunk)( ► Figure 13.1). The anterior
end exhibits a mouth opening and two pairs of slotted
openings of cuticular pockets, each containing a hook;
in the Cephalobaenida(see below) the hooks are located
at the tip of leg-like protuberances. These structures
function as holdfast organs and are regarded as remnants
of limbs. The five openings have led to the misleading
designation 'Pentastomum' ('five mouths'). The
hindbody exhibits numerous differently pronounced
annulations ( ► Figure 13.2). The thin and flexible
body wall is covered by a chitin-containing cuticle. The
internal organs include the digestive tract with mouth
and anus, male or female reproductive organs and the
nervous system. Respiratory and circulatory organs
are missing, excretion happens through specialised
epidermal cells. Of particular importance are glands
excreting a substance that covers the entire cuticle (see
below).
Adult pentastomids are obligatory parasites of the
respiratory tract of terrestrial vertebrates. The phylum
Pentastomida is divided into two orders: Cephalobaenida
and Porocephalida. The Cephalobaenida include inter
alia the genera Cephalobaena and Raillietiella (lung
parasites of reptiles and amphibians) and Reighardia(air
sac parasites of seabirds); members of the Porocephalida
are the genera Armillifer and Porocephalus(lung parasites
of snakes) as well as Linguatula (nasopharyngeal
parasites of mammals). Linguatula serrata parasitises
Figure 13.1. Armlllifer sp. female from a snake (Photo: IPZ).
carnivores and L. arct/ca cephalic sinuses of reindeer.
About 90% of the pentastomid species are parasites
of reptiles (snakes, crocodiles, lizards). Pentastomids
are common in the tropics and subtropics, some
species occur also in regions of colder climates. As
far as known today, most pentastomid species pass
through indirect life cycles with fish, amphibians,
reptiles or mammals as intermediate hosts. However,
some species seem to develop in direct cycles with or
without facultative alternation of hosts. The life cycle of
L. arctica is regarded as direct, but the involvement of
arthropods as intermediate hosts cannot be excluded.
As an example of the Pentastomida Linguatula serrata
(family Linguatulidae) is described here.
Linguatula serrata (tongue worm)
Disease: Unguatulosis in carnivores.
Lingua (L): tongue; serratus (L): serrated. Reference to
the parasite's body shape with its many annulations.
Agent and life cycle. The adult stages of L. serrata
live on the mucosa of nasopharyngeal spaces - including
nasal passages and frontal sinuses - of dogs, other canids
(fox, wolf), and felids. Males about 2 cm long, females
(J)
up to 13 cm; yellowish-white, dorsoventrally flattened C:
body, tongue-shaped with approximately 90 annulations ·u
(J)
( ► Figure 13.2). Females lay numerous eggs, containing I '
�
a primary larva(nymph), which are discharged in nasal
mucus to the exterior or, if they had been swallowed, C:
excreted in faeces. With contaminated food or water ·;:::
they are ingested by herbivorous intermediate hosts
(e.g. rodents, rabbits, domestic and wild ruminants, pig, .!;
;i
horse, camel) or by aberrant hosts, including humans I I
(see below). In intermediate hosts primary larvae !
0
(equipped with a penetrating apparatus and clawed
legs) hatch from the eggs, penetrate the gut wall, migrate
·u5 I, II
I
to various organs (lymph nodes, liver, lung, etc.), and (il
Q_
I
Part Ill. Parasites and parasitoses: metazoa
b
Figure 13.2. (a) Linguatula serrata, adult pnmsito: (bl forobody
(Graphics: IPZ, A. Seeger); (c) Llngllatula ogg (Photo: IPZ,
F. Grimm).
encyst in organ tissues thus forming small nodules
(few mm in diameter). Migrntion of primary lnrvne
via lymph and blood vessels has been described for L.
serrata, but some authors anticipate a dim:t migration
from the gut via the abdominal and thoracic cnvities
to organs. The former migration route is supported
inter alia by the fact that nymphal stages are frequently
found in mesenteric and medinstinul lymph nodes.
Within 6-7 months, the encysted parasites undergo
a metamorphosis, including 10 moultings, resulting
in infective terminal stages (4-5 mm long), which can
leave the capsules and move around in body cavities.
Definitive hosts become infected by ingestion of organs
containing terminal stages, which migrate directly from
the throat, but mostly from the stomach via oesophagus,
to the nasal cavity and develop there after another moult
into adults. The prepatent period is approximately 6
months; females can survive up to 2 years, while males
die much earlier.
Occurrence. L. serrata in dogs is common in many
a.reas of the world, but it is scarce in Europe. In Iran
(2003), 62% of 143 strny dogs were infected. Cats are
rarely aberrant hosts for the developmental stages, as
well as humans (see below). In endemic areas, encysted
nymphal stages are frequently found in domestic and
wild animals, e.g. in 18% of 480 buffaloes in India or in
20% of 132 camels in Iran (data from 2014).
Pathogenesis and clinical signs. In the lung of
hosts (e.g. snakes) pentastomids feed on blood and
lymph, and in the nasopharyngeal spaces of mammals
on mucus and cell debris. Pentastornids living in the
lungs discharge from glands a lipid-rich secrete which
covers their body surface; its composition is similar to a
protective secrete produced in the lungs of vertebrates.
Apparently, the secreted products of pentastomids are
involved in the immune evasion. Ling11atula infections
of dogs are asymptomatic or associated with clinical
signs, such as inflammation of mucous membranes in
nasopharnygeal cavities, nasal catarrh and discharge,
sneezing, secondary bacterial infections and impaired
sense of smell. Infections of intermediate hosts (e.g.
ruminants) are usually asymptomatic.
Diagnosis and therapy. Detection of eggs in the
nasal mucus or faeces. Faeces are mixed I:10 with 5%
potassium hydrox.ide solution and thereafter repeatedly
sedimented in water; the sediment is further processed
with the flotation technique, using zinc chloride solution
as flotation medium ( ► p. 526). The 11val eggs (90x70
�tm) contain a primary larva (see above)(► Fig ure
13.2). Eggs from nasal mucus may ht: covered by a
sticky externnl layer. Therapy: mcch,111ical removal of
parasites; effective drugs are not known , the off-label
use of macrocyclic lactones appears just ifled.
Zoonotic importance. Humans .:an accidentally
acquire pentastomid infections by ingestion of
food contaminated with eggs of L scrrata or other
pentastomids (e.g. Armil/ifer annillalus, A. moniliformis,
Poroceplralus sp.; final hosts are snakes). Cases are
predominantly reported from the Middle East and
other Asian or African regions. Typically, the infection
results in asymptomatic visceral pentastomidosis
with development of nymphal stages in internal organs
(e.g. liver, mesentery, bowel wall). If raw organs from
herbivores, infected with terminal larvae of L. serrata,
are ingested by humans, nymphs (occasionally adult
stages) settle in nasopharyngeal spaces (nasopharyngeal
pentastomidosis) and rarely in the eye. Repeated
consumption of organs with Linguatu/a stages can
cause severe allergic reactions ('marrara syndrome' or
'halzoun').
Selected references
Bl>ckeler W, Richllng I, Sattmann H (2010) Pentastom1den,
Pentastomosen und lhre humanmed1zische Bedeutung.
Denisia 30: 411-426.
Bamorovat M, Zarandl MB, Mostafavi M, Kheirandish R,
Sharifi I, Radfar MH (20·\4) The prevalence of Linguatu/J
serrata nymphs In mesenteric and mediast1nal lymph nodes
in one-humped camels (Came/us dromedanus) slaughtered
in Rafsanjan slaughterhouse, Iran. J Parasit Dis 38: 374-377.
Lavrov DV, Brown WM, Boore JL (2004) Phylogenetic position
of the Pentastomida and (pan) crustacean relationships. Proc
8101 Sci 271: 537-544.
Meshgl B, Asgarian O (2003) Prevalence of Lmguatula serrata
infestation in stray dogs of Shahrekord, Iran. J Vel Med B
Infect Dis Vet Public Health 50: 466-467.
Poore GC (2012) The nomenclature of the recent Pentaslomida
(Crustacea), with a list of species and available names. Syst
Parasitol 82: 211-240 and 83: 249.
Rieley J, Haugerud RE, Nilssen AC (1987) A new species
of pentastomid from the nasal passages of the r eindeer
(Rangifer tarandus) in northern Norway, with speculation
about its life-cycle. J Nat Histor 21: 707-716.
 13· Phylum Pentastomida (incertae sedis) (so-called tongue worms)

Lee MSY (2010) A_rthropod molecular divergence

sanders KL,
Cambrian ong1n of pentastom ids. System
times and the
63 -74 .
Biodiv 8:
J
V. a si w a l AK, Shanker D (2014) Infection rates of
SUdan
serrata nymphs in mesenteric lymph nodes from
Unguatula
water buff aloes in North India. Vet Parasitol 205: 408-411.
i JE, Maas A (2006) A new late Cambrian
waroszek o, Repet
sk
and a review of the relationships of this parasite
pentasto mid
group. Trans Roy Soc Edinburgh Earth Sci 96: 163-176.
 14. Phylum Arthropoda (arthropods)
Ar thron (G): limb, joint; pous, gen. podos (G): foot.
Summary
• Many arthropod species are important as ecto- or
endoparasites of animals and humans, as vectors
of pathogens, as poisonous animals or as household
and storage pests. Particularly Important are the
acari (mites and ticks) and the insects. The main
characteristics of the phylum are:
• Exoskeleton (cuticular skeleton) from sclerotised
matrix and stratified chitin micelles; secreted from the
epidermis and periodically shed and replaced during
lt development (ecdysis: moulting).
• Body consists of heteronomous (non-uniform)
segments, which are combined in groups to form
functional units (tagmata); segmented limbs
(arthropodla) with real joints.
• Open vascular system, dorsal cardiac vessel with
lateral openings; body cavity (haemocoel or mlxocoel)
with haemolymph.
• Mouthparts with different functions, digestive tract
with foregut and hlndgut (ectodermal) and midgut
(entodermaij.
• Different types of glands (e.g. salivary glands) and
specialised excretory organs.
• Ventral nerve cord, various sensory organs.
• Respiratory system present (gills, tracheae) or absent
(respiration directly through cuticle).
• Almost always separate sexes, usually sexual but also
parthenogenetlc reproduction. During development
from larval to adult stage, morphological and
physiological transformations (metamorphosis) of
various extent.
Arthropods have always played an important role in
domestic and wild animals as causati.ve agents of skin
diseases and as nuisance pests. Even more significant
is the vector role of certain arthropod species that can
transmit numerous pathogens, including zoonotic ones.
In the last two decades, unexpected and sometimes
dramatic developments with regard to vector-borne
diseases have occurred, driven by increasing globalisation
QJ
and environmental changes including climate change.
An example is the sudden outbreak of the virus-induced
·u
C
'6 bluetongue disease in ruminants in August 2006 in the
QJ
north-west of Central Europe, the efficient transmission
c
c.u
of the pathogen by indigenous biting midges ( Culicoides
C ob soletus group) whose vector competence was
·;::
QJ previously unknown, and the subsequent rapid spread
of the disease. The establishment of exotic ('invasive')
C species of mosquitoes in Europe, such as the Asian
>,
Ol
0
0
'in
c.u
0..
tiger mosquito (Aedes albopictus) and the Asian bush
mosquito (Ae. japonicus), is worrying as they are proven
or putative vectors of various pathogens of humans or
animals. Ticks transmit the causative agents of numerous
infectious diseases, which include Lyme disease, various
forms of encephalitis of humans as well as babesioses and
theilerioses of domestic animals. The use of molecular
biological methods now provides enhanced capabilities
for accurate identification and characterisation of vectors
and pathogens as well as for the study of complex
epidemiological relationships, the knowledge of which
is an important prerequisite for implementing effective
control measures. For the control of ectoparasites of
domestic animals, efficient drugs are available, the use of
which requires consideration of many aspects, including
environmental impact and sustainability.
A simplified classification of parasitologically relevant
arthropods is provided in► Table 14.1.
Selected references
Aspock H (ed.) (2010) Krank durch Arthropoden. Denisia 30.
ISSN: 1608-8700.
ESCCAP Control of ectoparasites in dogs and cats. Available
at: www.esccap.org.
Kettle DS (ed.) (1995) Medical and veterinary entomology. 2nd
ed. Wallingford, UK: GABI International; ISBN 0-85196-83.
Marquardt WC (ed.) (2004) Biology of disease vectors. 2nd ed.
Amsterdam, the Netherlands: Elsevier; ISBN 0-12-473276-3.
Medlock JM, Hansford KM, Schaffner F, Verstelrt V,
Hendrickx G, Zeller H, Van Bortel W (2012) A review of the
Invasive mosquitoes In Europe: ecology, public health risks,
and control options. Vector Borne Zoonotlc Dis 12: 435-447.
Mehlhorn H (ed.) (2012) Arthropods as vectors of emerging
diseases. Heidelberg, Germany: Springer; ISBN 978-3-642-
28841-8.
Mullen G, Durden L (eds.) (2009) Medical and veterinary
entomology. Amsterdam: Elsevier; ISBN 978-0-12-372500-4.
Russell RC, Otranto D, Wall RL (2013) The encyclopedia of
medical and veterinary entomology. Wallingford, UK: GABI
Publishing; ISBN 978-1-78064-037-2.
YJalker A (1994) Arthropods of humans and domestic animals.
A guide to preliminary identification. London, UK: Chapman
& Hall; ISBN 0412-57280.
Wall R, Shearer D (2001) Veterinary ectoparasites: biology,
pathology and control. 2nd ed. Oxford, UK: Blackwell Science;
ISBN 978-0-632-05618.
 14. Phylum Arthropoda (arthropods)

Table 14.1. Simplified and selective classification of parasitic arthropods.

dom 1 : Eukaryote, 8ubk1119cRfm1

um: Arthropoda1

SUbphylum: Amandlbulata (Chellcerata)

Cl111: Arachnida C
0
SUbclass: Acarl (mites In the large sense • t icks and mH•• In the ttr1ct ..,,..,
u
..:::
Ordar Famlly Oentta2 "in
(/)

Metastigmata (lxodida) lxodidae3

Cu

Amblyomma. Anocentor. (Boophilus)4 , Dermscentor,

HBf!f!!Bphysalls, Hyalo_m'!_IB, lxodes. F!!_1fplcef!h&lus__
Argasidae3 Argas, Carias, Ornithodoros, Otoblus
Mesostigmata (Gamaslda) Dermanyssldae DermanyssuJ, Uponyssoides
Macronyssldae Ophlonyssus, Ornlthonyssus
Halarachnldae Pneymonyssoldes, Pneumonyssus. Roillietlo
Rl1lnonyssldae Sternostoma
Laelaptldae Eulaelaps, 1-laemogamasus, Hlrstlonyssus, Laelaps,
f-----------, Tro�lael!!P!.. _ __
Varroldae
------- Euvarroa, Varroa
Prostigrnat 1 1, )mbidlformes) Demodicldae Demodex
Cheyletiellidae ____ _____
Chey/etiella, Ornlthocheyletia
Syrlngophilldae Syringophllus
Tromblculidae Neotrombicula, Tromblcula
Psorergatidae
---------------------1
Psorergates
--------i--�
Myobiidae Myobia, Radford/a
Pyemotidae Pyemotes

----+Ti_ars _ a
_ _o_ne_mid _ e_ ____+--A_ac _r;�ap_is
__________________-1
Astigmata (Sarcoptilormes) Psoroptidae Chorloptes, Otodectes, Psoroptes
-------- -�
Sarcoptidae ___ _ Notoedre_s._ Sarc?_ptes, Tri!_acaru_s_ ____ ------1
Knemidocoptidae 15nemid�optes
'---------------- --1
Cytodite_s_____________ _____-
Cytoditldae
L:JstroJ:)horidae ---1
ystr_9phorus
_ -----------------1
Myocop�c:l_ae Myocoptes
Lamlnosloptldae _
__ J:_amlnosi9ptes_ ------- ---------1
Falcullferldae ------ Falculifer
�n�lgldae _ ___ L�ptosph�ra._!:Aegninia --------------1
Epldermoptldae _ Epldermoptes ______
_ _
�carld�e _ _ Ac<!:us, Cal<_Jglyphus, !t.f':9lyphus_ ,_7i�y_ro
p� ha '-- _s_____--1
_ �gu
Glycyp�gl_c:l__�e__ __ _ Glycyplmgus, Lepidoglyphus
------------!
y ldae ______ Dennatophagoldes
f-- ----------f-P...: r_ oglyph
Oribatida Schelorlbatldae
------------�- -------------------�
Scheloribates
Ceratozetidae
1
>-----------,-- --- - - ------------------<
Trichoribates I

Galumnidae
I

Galumna, Piloga/umna
lncertae sedis5 Pentastomlda (► p. 389)

I I
I I
 Part Ill. Parasites and parasitoses: metazoa

Table 14.1. Continued .

. . -
I �!,!l:'lph)!!um: Mandlbulata
1.Class: ellY,._staeea {ll>iantennata) {see ltext) "
t61ass:ln�
... -
--
..?'' •.. �
-
�;- - ' - ,� -,,
e�er Family Genus
,e Suborder - Subfam'ily ..
.
1' ..

Blattaria (cockroaches) Blattidae 8/atta, Periplaneta

Blattellidae Blattel/a
Phthiraptera (lice)
• Amblycera (chewing lice) Various families Gliricola, Gyropus, Hohorstiella, Menacanthus, Menopon,
Trimenopon, Trinoton
• lschnocera (chewing lice) Anaticola, Anatoecus, Bovicola, Campanulotes, Chelopistes,
Co/umbico/a, Cuclotogaster, Felico/a, Goniocotes, Goniodes,
Upeurus, Trichodectes
• Anoplura (sucking lice) Pediculidae Pedicu/us, Phthirus
Haematopinidae Haematopinus
. J. Linognathldae Linognathus, So/enopotes
Hoplopleuridae Haemod/psus, Polyp/ax
Heteroptera (true bugs) Clmicidae Clmex, Oec/acus
Reduviidae Rhodnius, Triatoma
Coleoptera (beetles) Nitidulldae Aethina
Diptera
• Nematocera (thread-horn flies) Culicidae
- Anophelinae Anopheles
-Culicinae Aedes, Coquillettidia, Cu/ex, Cu/iseta, Mansonia, Ochlerotatus,
Stegomyia
Psychodidae Lutzomyia, Phlebotomus, Sergentomyia
Simuliidae Austrosimulium, Cnephia, Prosimulium, Simulium
Ceratopogonidae Austroconops, Culicoides, Forcipomyia, Leptoconops
• Brachycera (flies) Tabanidae Chrysops, Haematopota, Heptatoma, Hybomitra, Silvius,
Tabanus
Braulidae Brau/a
Drosophilidae Drosophila, Phortica
Muscldae Haematobia, Hydrotaea, Morel/is, Musca, Ophyra, Stomoxys
Fannlidae Fann/a
Glosslnldae
·- G/osslna
Calllphorldae Ca/liphora, Chrysomya, Cochllomyla, Cordylobia, Lucilia,
--- '!O.!_0CB!!iphora___
Sarcorhagldae
-- - �--- Sarcopha9.a,
-- ·- ---- Wohlfahrt/a
----
Oestrtdae -
-Oestr!nae
---- Cee!Jenemyia, Oestrus, Pharyngomyia, Rhinoestrus
_:_Gaster�h��ae__ _ G_!Jst�rophl_l_u_s, Gyi:Estigma
Q)
T5
C ..:_ l:!YJX>?�!flina�-- Hypoderma, Oedemagena, Przhevalskiana
'6 -Cuterebrinae
f---·- ---- -
Cuterebra,
--- Dermatobia
Q)
� Hippoboscidae Crataerina, Hippobosca, Lipoptena, Melophagus, Neolipoptena,
cco �--- - - ----- �doly_'!_chia, (2mithomyia, Stenepteryx
C Siphonaptera (fleas) Pulicidae Archaeopsylla, Ctenocephalides, Echidnophaga, Pu/ex,
·;;::
Q) Spilof?._syllus, Xenopsylla
-·--
Ceratophytlidae Ceratcphyl/us
.£ Tungidae Tunga
>,
OJ 1 Latin designation of the taxonomic categories► Table 1.2, p. 18.
0 2 In bold: genera of particular relevance in veterinary medicine, zoonotic agents or typical examples of the family; alphabetical order
0
·u; of genera.
co 3 Subfamilies► Table 14.2.
co 4 Currently classified as subgenus of Rhipicephalus.
0... 5 Unclear phylogenetic and taxonomic position.
-
 14. Phylum Arthropoda (arthropods)

adults bears 4 pairs of legs and apically the usually

- Subphylum Amandibulata
14.1 Class Arachnida
- Subclass Acari (mites s.l.)
Arachne(G): spider; akari(G): mite.
Summary
• Acan (mites s.l.) Include the small, about 0.2�2 mm
long mites s.s. and the much larger ticks (engorged
females up to 30 mm).
• Characteiiatlca o f Acan: unsegmented body, 4 palra of
letis (larva& with 3 pairs of legs). Mouthparts: pedlpalpa
and chellcerae, separated from the body (gnathosoma).
Light sensory organs reduced or missing, tactlle and
chemical sensors well developed.
• Life cycle: egg - larva -+ nymph (sometimes several
stages) ..... adults (males and females).
• Classifica tion of Acarl Into Metastlgmata, Meso­
stigmata, Prostlgmata and Astlgmata according to
location and function of stigmata (respiratory openings)
(► Table 14.1).
• Importance: causative agents of skin diseases and
allergies In animals and humans, Important vectors of
pathogens, household and storage pests.
distinctly separated gnathosoma (= capitulum) with
2 pairs of mouthparts (pedipalps and chelicerae)
( ► Figure 14. l ). The ends of the unsegmented chelicerae
are usually stiletto- or scissor-shaped; the palps consist
of l -6 segments, the last of which often carries a claw. cuu
In the Mesostigmata and Metastigmata (ticks), the Cu
(/)
palps are distally fused to a basis capituli ( ► Figure (/)
ro
14.3) which ventrally bears an unpaired mouth part, the u
D
hypostome, which is serrated only in the Metastigmata
rJJ
(ticks). The part of the idiosoma carrying the legs is
called podosoma, the legless part behind opisthosoma.
Other names are also used for different body parts in
identification keys.
Adults and nymphs of the Acari have 4 pairs of legs
(larvae only 3; the 4 1h is regressed during embryonic
development). The llrst pair of legs is often modified
into capture or sensory organs. The walking legs usually
consist of 6 limbs ( ► Figure 14. I). Praetarsi, claws
and empodiae (very variable in form, membrane-like
appendices) are often genus-specifically differentiated.
Some mites (Astigmata and others) respire directly
through the cuticle; they have no stigmata. Other mites
have paired stigmata, which are connected via channels
to a finely branched tracheal system that not only serves
the respiratory system but also holds the internal organs
in position(► Figure 14.2).

The subclass Acari includes about 30,000 species, most
of which colonise diverse terrestrial habitats (moist
soils to deserts, even ice fields) and aquatic habitats as
free-living predators, herbivores or detritivores. In the
fauna of humus soil they often represent more than half
of all animal species.
Morphology. Mites are - apart from ticks - small
(usually <l mm). The body(idiosoma) is unsegmented,
but may have some sutures and grooves. The body of
Life cycle. The development of the Acari proceeds co
according to the following scheme: egg -+ larva-+ one "O
0
0.
or more nymphs-+ adults(males and females).
e
.c
t
This basic scheme is modified in some groups. Thus, <{
in most species, a larva hatches from the egg, but in
some it is a nymph. In some species only one nymphal
stage is developed, in others there are several that are
partly referred to as proto-, deuto- and tritonymph. A
distinct sexual differentiation occurs only in the adult

Gnathosoma
(=capitulum)
Hypostome---A Q)

·u
C

Peritreme 'o
Q)
2
Stigma
co
Tarsus C
·.::::
Pretarsus
\
Claw or other C
holdfast- - , , >,
1 0)
Anus 0
0
:!::'.
(/)
co
co
Figure 14.1. Scheme of a mite (Graphics: I PZ, A. Seeger; after Pratt 1963). 0..
 Part Ill. Parasites and parasitoses: metazoa

Palp

Female, dorsal view Male, dorsal view

Claw­
Pulvillus

Tarsus with
Hailer's organ

Genital
Anus--..__
opening
Anal groove-....,.<;l::...._
Coxa IV

"..._....._ll_Stigmatal
plate

Female, ventral view Male, ventral view

Figure 14.2. Scheme of lxodldae (hard ticks) (with the example of the genus Hya/omma) (Graphics: IPZ, A. Seeger: modified
after Walker et al. 2003).

stage. Frequently, one of the nymphal stages is inactive 14.1.1 Order Metastigmata (lxodida,
(development without feeding). The development ticks)
from larvae to adults is associated with moulting and is
interrupted, depending on the species and the situation, Meta (G): behind, after; stigma (G): scar, spot. Refers
by periods of rest or starvation. The development of to the location of the respiratory openings (stigmata)
(])
a generation varies from a few days to several years. which are posterior of the 4th pair of legs.
·u
C The number of eggs produced by a female ranges from
'6 about 10-10,000 (e.g. in some hard ticks). In general, the The Metastigmata (Ixodida, ticks) are obligate,
(])
� enormous prolific potential of many species of the Acari haematophagous ectoparasites of mammals, birds and
cco may lead to an explosive dissemination of a population. reptiles. About 10% of the approximately 900 species
C
·;::
parasitise domestic animals, especially cattle, sheep,
(]) horses and dogs. In veterinary and human medicine
j ticks are known as pathogens but are of paramount
.£ importance as vectors. There are two large families, the
>­
Ol Ixodidae (hard ticks) and the Argasidae (soft ticks),
0
0 as well as a minor monotypic family, Nuttalliellidae
·u5 (► Table 14.2).
�
co
0..
 14. Phylum Arthropoda (arthropods)

Table 14.2. Tick species (selection).

Family Genus Speclits2

• Subfamily • Subgenus (number of species)

lxodidae
rn
• lxodin ae lxodes(ca. 250) lxodes ricinus·, I. persulcatus', I. hexagonus·, I. canisuga',
I. triang!!J{ceps'
1-H _ _ap_
•_ _a_ em _ _ in_ae_--+_Ha
, h_,y_sal _ e _ ,_16_ 5,)_ ___ ____ t!_a'!!._maph�alis punctata·, H. concinna', H. inermis'
_ m_a,_p_, hy,_s_a_/is(
• Rhipiceph alinae _ p_h_a _lu_s-'-(8_0_,_) ________ Rhlplcephalu! sang_ulneus s.l.', R. bursa·, R. turanicus· _
R_h ip_ice_,_
f-- _, .
• Boophi/us(5) 3 Rhlpicepha/us (Boophilus) mlcroplus, R. (8.) decoloratus,
R. (B.)i!_rynulatus •
Dermacentor(35) Dermacentor marglnatus•, D. retlculatus•
•Hy alomminae Hyalomma(25) J::lyalo_!!lf_!I_B marginatum·, H. aegyptium·, H. lusitanlcum· _
• Amblyommlnae Amblyomma(140) Amblyomma hebraeum, A. varlegatum, A. americanum,
�- ca/ennens!?_
Argasidae
1-•_A_rg asin_ e
,._ _ _ a _ ___ rga_s 56)'----------- Argas reflexus ', Argas perslcus•
----1_A_,,._ _,___,
• Ornithodorinae Carios(88) Carlos capensis4 _ _ _ ___ _ _ __
Ornithodoros(37) Ornithodoros moubata ssp., 0. savignyi, 0. lahorensis,
0. erraticus·
Otobius(2) Otobius megnini
1 Not listed here is the family of Nuttalliellidae with only one species which opportunistically feeds on rodents, reptiles and birds in southern
Africa.
2 Bold: species of particular importance for practice in Central Europe; autochthonous species in Europe are marked with•.
3 The genus Boophi/us is currently classified as a subgenus of Rhipicephalus; for pragmatic reasons both the new and partly also the
previous nomencl a ture are used in this book.
4 Par asite of seabirds.
(1j
"O
0
Q.

Morphology
• Body (idiosoma). As in all Acari unsegmented,
oval, dorsoventrally flattened when unfed(► Figure
14.2). Adults and nymphs with 4 pairs of legs, larvae
with 3 pairs of legs. On the last limb of the legs(tarsi)
1 double claw, partly also pads(pulvilli). Ticks are the
largest Acari: unfed adults 2-7 mm long, engorged
females about 8-30 mm. All stages of hard ticks have
a dorsal hard cuticular plate(shield, scutum) which is
absent in soft ticks.
e
..c
t
<(
• Mouthparts. Pal ps(= pedipalps, with 4 segments)
and chelicerae are basally fused to the basis capituli. Basis
and mouthparts form the capitulum(gnathosoma),
which is separated from the body(► Figure 14.3).
Ventral to the capitulum and below the chelicerae is an
unpaired mouthpart, the hypostome, a rigid, immotile
piercing organ with teeth directed backwards. The
chelicerae are part of the piercing apparatus; the palps
bear sensilla and are mainly used for orientation.

(I)
C
·c3
Palp '6
Hypostome--...,...--i (I)
�
Palp Cheliceral �
(1j
sheath C
·;;::
Basis (I)
capituli
a b .5
>,
0)
0
0
Figure 14.3. Mouthparts of lxodidae.(a) Scheme of capitulum, ventral view(Graphics: IPZ, A. See ger; after Weyer and Zumpt
"iii
1966).(b) SEM picture(Photo: A. Aeschlimann).
ell
Cl.
 Part Ill. Parasites and parasitoses: metazoa

• Sensory organs. Ticks have different sensory

organs. Characteristic is the Hailer's organ which is
located in the tarsi of the first pair of legs in adults,
nymphs and larvae(► Figure 14.4).

• Stigmata. The stigmata constitute the opening

of the tracheal system: they are present in adults and
nymphs and are located posterior to the coxae of the
fourth pair of legs in hard ticks (► Figure 14.2) or
anterior in the soft ticks. Stigmata are often surrounded Figure 14.4. Tarsus of a hard tick with Hailer's organ (arrow}
by an oval stigmata} plate. (Photo: A. Aeschlimann).

Life cycle. The development of ticks takes place partly

in the habitat and partly on a host. It progresses through Characteristics of hard ticks and soft ticks. The
four stages: egg - larva(L) - nymph(N)(1 nymphal two major tick families differ in morphological features
stage in Ixodidae, 2-8 in Argasidae) and adult(A)(male and biological properties(► Table 14.3).
or female). In order to develop to the next stage, L, N and
A of ticks require a suitable host to suck blood(except
in the Argasidae). After a blood meal, ticks can survive
long periods of starvation.

Table 14.3. Characteristics of soft ticks and hard ticks.

Characteristic Soft ticks (Argasldae) Hard ticks (lxodldae)

Dorsal plate (scutum) absent present in all stages

Number of leg_palrs

-Adults
- - -
and-nymphs 4 4

-----
LaNae 3 3
Capitulum
Adults and nymphs ventrally located, not visible in dorsal view terminal, visible in dorsal view
- -�
l.aNae -- terminal terminal
Hailer's orga_n ____ present in all stages present in all stages

--- -- --··
Stlgmata/stigmatal plates
I-
Adults and nymphs small, anterior to the coxae of the 4 th pair large, posterior to the coxae of the 4th pair
- ---- of 199s of legs
l.aNae -------- absent (respiration through cuticle) absent (respiration through cuticle}
Adhesive pads (pulvllll at tarsi
Adults and nymphs absent present
-- --
f---
l.aNae - - present present
Coxal gland
- -
(adults) present absent
i------

Sexual dimorphism slight (males and females very similar) distinct (males: scutum covers entire
dorsal surface; females: scutum covers
only anterior third of dorsal surface)
Q)
C
·o Development egg -+ laNa -+ several nymphal stages
-+ adult
egg -+ laNa -+ nymph -+ adult
'6
Q)
� Oviposition repeatedly, <500 eggs/batch once, > 1000 to around 10,000 eggs/batch
Habitat typically arid typically humid to semiarid
al
C
·c Duration of blood-sucking process 20-30 min (laNae: 1 week) 2 to around 14 days
Q)
Increase in body weight after blood- up to 12 fold up to 120 fold
feeding
C
Periods of starvation 20 days (laNae), 5-7 years (adults) 1 month to around 1 year
>-
0)
0 Age up to 14 years up to several years
0 Duration of a generation 6 to around 12 months 2 months up to several years
·u5
al
al
0...
 14. Phylum Arthropoda (arthropods)

Family lxodidae (hard ticks)

A
• Diagnosis. Adult ticks, particularly fully engorged
Ixos (G): mistletoe and derived glue; ixodes (G): ixos­
females, are easily recognisable on the skin by
like, analogously: sticky. Refers to the clinging of ticks
adspectlon; smaller stages (unfed larvae and nymphs)
to the host. are often overfooked. Species identification of ticks
by specialists.
Summary • Therapy and control. Different options depending E
/JJ
on animal and tick species, Infestation Intensity and
• Genera and morphology. Important genera: lxodes,
Importance of the tick Infestation. Dog and cat: low
Haemaphysafis, Hyalomma, Amblyomma, Dermacentor,
number of ticks can be removed mechanically, in
Rhipicephalus and Boophilus with numerous species.
case of heavier Infestation application of acaricldes.
The fonner genus Boophilus Is nowadays considered
Prophylaxis: application of acarfcide-collar (dog) or
a subgenus of Rh/plcephalus ( ► Table 14.2). All stages
topical application of cer tain acarlcldes (spot-on,
with dorsal plate (scutum) and other phenotyplc
spray)( ► Table 19.16, p. 565). Cattle: tick control
characteristics ( ► Table 14.3 and ► Figure 16.19,
rarely needed In temperate climates; If necessary, use
p, 553).
of flumethrfn (pour-on). Tick control in other areas:
• Life cycle. Egg ..... larva (L) ..... nymph (N) .... adult (A).
acarlclde application In cattle and sheep as spray
Before developing to the next stage, ticks must take
or dlpa.
a blood meal on a host. Depending on the number of
hosts that are Infested by a generation, a distinction Is
made of 3-host, 2-host and 1-host hard ticks.
Morphology. The characteristics of the hard ticks
• Occurrence. Ticks mainly occur In humid to semi-arid
which have a dorsal shield (scutum) are listed in
habitats from the tropics to north of the Arctic Circle. In
large areas of Europe, lxodes rlclnus (European sheep ► Table 14.3 and are shown in ► Figures 14.2 to 14.6.
tick, castor bean tick) Is the most common and most The encl of the movable chelicerae bear sharp, serrated
Important hard tick species. Further lxodes species (e.g. scissors(chelae), whose digits pierce the skin of the host
I. hexagonus, hedgehog tick, /. canlsuga, fox tick) as and move back and forth(► Figure 14.5). Thus, the skin
well as species of the genera Rhipicephalus (especially is cut open with the teeth that are directed sideways and
R. sanguineus, brown dog tick) and Derrnacentor (D. backward(principle pull saw). The hypostome pierces
marginatus, sheep tick, D. reticulatus, marsh tick) also the skin that is cut open by the chelicerae and is anchored
play a role. there with its teeth. The palps are spread sideways and
• Epidemiology. Most of the European hard ticks are lie flat on the skin of the host. The double claw on the
3-host ticks; their developmental cycle Includes a co
tarsi and the well-developed pulvilli enable lxodidae to 1J
distinct seasonality and mostly several host species. An 0
Q.
walk on smooth skin and on vertical surfaces. Behind 0
exception is R. sanguineus: abundant In warmer climate
zones, spread to northern areas; almost exclusively the fourth pair of legs in nymphs and adults are the .c:
t
infests dogs. Development in warmer climate zones large stigmata! plates (► Figure 14.2) from which a <{
especially outdoors, In temperate climate zones In densely branched tracheal system emanates. The larvae
buildings and protected kennels. have neither stigmata nor tracheae(respiration through
• Imm unology. Ticks produce various compounds In the cuticle). In females and males, the genital opening
their salivary glands that are Inoculated Into the host. (porus genitalis) is ventrally located, usually between the
Most of them serve to overcome the host defence
Qnhibitlon of haemostasis, prevention of Inflammation,
suppression or modulation of Immune responses).
lmmunosuppresslon favours the transmission of
patlilogens. Host animals (e.g. cattle) develop only
partial Immunity to repeated Infestations with ticks.
• Pathogenesis, clinical signs. Local lesions at the sites
of bite; the scarred sites of bite cause leather damage.
Systemic effects (especially In warm countries): non­
specific toxlcosis (tick worry), particularly In ruminants,
after heavy tick infestations, and specific toxlcosls,
caused by toxins In tick saliva (sweating sickness, tick
paralyses).
• Vector role, zoonotic significance. Hard ticks can
transmit viruses, bacteria (rickettsia, spirochaetes and
others), protozoa, fungi and nematodes to domestic
and wild animals and partly also to humans (► Table
14.4 and 14.5). In Europe, their greatest significance is
as vectors of the tick-borne encephalitis virus (TBEV)
and various species of Borre/is, Ehrlich/a, Anap/asma

• and Babesia .
Fig ure 14.5. Scheme of a hard tick while blood-feeding
(Graphics: IPZ, A. Seeger; after Walker et al. 2003).
 Part Ill. Parasites and parasitoses: metazoa

lxodes ricinus Haemaphysalis punctata

<.;? 3.0-4.0 mm O' 2.4-3.0 mm <.;? 2.5-3.5 mm cr 2.8-3.2 mm
(fully engorged up to 12 mm)

Rhipicephalus sanguineus Dermacentor reticulatus

<.;? 3.0-4.0 mm O' 3.0-3.8 mm <.j_) 4.2-4.8 mm cr 3.8-4.2 mm

Rhipicephalus (Boophi/us) annulatus Amb/yomma hebraeum

<.;? -2.6 mm cr 2.0 mm <.;> 5.0-7.0 mm cr 4.2-5.7 mm
Figure 14.6. Selection of hard tick species (Graphics: IPZ, A. Seeger).

coxae of the second pair of legs. The anus, ventrally near a blood meal at all. Engorged females leave the host
the posterior end of the opisthosoma, is surrounded by and lay eggs on the ground where the larvae hatch.
an anal groove whose shape is an important taxonomic Overall, most ticks species spend less than 10% of
C feature(► Figure 14.2). their lives as parasites on their hosts. In the course of
>,
CJ)
their further development, ticks use one or more hosts
0 Life cycle. Ticks develop through 4 stages as described as blood donors. Depending on the number of hosts
0
·u; above. Blood feeding on a host usually takes 2-6 days involved, ticks are designated as 3-, 2- or I-host ticks;
co in larvae or nymphs, and 5 to about 10 days in females their development is as follows with moultings from
co
(L and males of most species, provided that the latter take larva to nymph and from nymph to the adult stage:

• 3-host ticks: ground: egg - larva j 1st host: larva !
ground: larva - nymph j 2 nd host: nymph !
ground: nymph - adult j yd host: adult ! ground:
oviposition of females.
• 2-host tick: ground: egg - larva j 1 st host: larva -
nymph ! ground: nymph - adult j 2nd host: adult !
ground: oviposition of females.
• 1-host tick: ground: egg - larva j 1st host: larva -
nymph -+ adult ! ground: oviposition of females.
Some species of ticks are euroxenous, i.e. they can infest
man y differerit host species, such as lxodes ricinus >200
species(mammals, birds, reptiles, see below). Other,
stenoxous species are specialised and infest only a few
host species, such as species of the subgenus Boophilus
which parasitise almost exclusively cattle.
• Host finding. An important phase in the
development of ticks is the localisation of a host. To
this end, hard ticks have developed two main strategies,
with the developmental stages of a species being capable
of following different strategies.
Most species (I. ricinus, etc.) are 'ambushers' which
climb up the vegetation along game tracks, trails and
hiking paths, in walkways of mice, on edges of pastures,
resting places of wild and domestic animals, with the
raised first pair of legs waving and thus exposing the
Hailer's organ. When the legs are spread, the sensilla of
this organ are sufficiently wide apart so that signals from
a host can be located. The 'hunters' among hard ticks
(Amblyomma, Hyalomma, etc.) leave their hiding places
on the ground, localise animals over some distance and
then move in the direction of the potential host.
• Sensory organs. For finding and identifying hosts
and habitats, hard ticks have a sophisticated sensorium.
This includes the Hailer's organ( ► Figure 14.4) with
sensilla for vibration, temperature, humidity and volatile
substances; light sensory organs: eyes(in Amblyomma,
Hyalomma, Dermacentor, Rhipicephalus, Boophilus);
photosensilla (Ixodes); chemosensilla on palps and tarsi
of the first pair of legs for skin contact, and sensilla on
the chelae of the chelicerae for contact with tissue fluids.
• Stimulus perception. Hard ticks, even those
that have no eyes, can perceive light intensity with
photosensilla. Localisation of hosts by eyes was
demonstrated in the camel tick Hyalomma dromedarii
(range of vision up to 18 m). Volatile substances are
perceived by receptors: CO2 with two antagonistic
receptors(a receptor with a maximum sensitivity of
0.04% CO 2 - the tick remains inactive; another receptor
with a sensitivity of 0.1-5% CO 2 - the tick is activated
and approaches the CO2 source, the host); H 2S -
highly sensitive receptors for H 2S and also for ethyl
mercaptan, dimethyl sulfoxide; sexual pheromones -
mostly 2,6-dichlorophenol and others; inorganic and
organic volatile substances released from the host, e.g.
14. Phylum Arthropoda (arthropods)
ammonium, diethyl ketone, pelargonic acid, ortho-nitro
phenol, benzaldehyde, isobutyric acid. The pattern of
volatile substances is host-specific.
• Infestation of the host. Roughly four phases can be
distinguished: ( 1) activation of the tick and localisation co
of the host, (2) appetence behaviour of the tick, (3) co
E
contact of the tick with the host, and(4) attachment of 0)
U)
the tick on the host. (U
1. Activation. First, seasonally and diurnally favourable <1J
.,;�
temperature and humidity conditions prompt the
ticks to leave their hiding place on the ground and
to climb up the vegetation. There, chemical(volatile
substances) and physical signals(vibrations, higher
temperature) of the host at a distance of up to 5 m
are perceived by the sensilla of Hailer's organ.
2. Appetence. Host-specific signal patterns allow
specialised ticks to identify their hosts. Then,
they approach and contact the host. Males in
search of females are triggered by pheromones to
infest or switch a host (important for intrastadial
transmission, see below).
3. Contact. The sensilla of the chelicerae and palps
enable to identify predilection sites for blood feeding.
The search process may take several hours. Already
during the appetence and contact phases, infective
stages of some pathogens develop in the salivary
glands.
4. Attachment. The scissors of the chelicerae cut
through the epidermis and partially the dermis. co
Subdermal blood-filled pools are caused by the -0
0
e
effects of vasoactive mediators and cytolysins 0.
( ► Figure 14.5). Rather primitive hard ticks (Ixodes, .c
t:::
Hyalomma, Amblyomma) have long chelicerae and �
a long hypostome, which are deeply anchored in the
dermis. Ixodes females insert their long hypostome
deeply in the cutis with little or no protection by
'cement'(cement substance formed by the salivary
glands). Ticks that are better adapted to their
hosts have shorter mouthparts (Haemaphysalis,
Dermacentor, Rhipicephalus). These ticks attach
themselves with the hypostome as well as by forming
a cement cone. Highly evolved hard ticks have a
reduced hyp ostome which does not penetrate the
dermis. Boophilus ticks form a cement cone and
an adhesive plate which adheres firmly to the skin.
The larvae of some other genera attach in a similar
way because the mouth parts of these larvae are very
short.
• Feed intake. After a preparatory phase of up to one
day without feed intake, a 2-phase blood-sucking process
follows: the first phase lasts from 2 to about 5 days in
pre-adult stages and about 5-10 days in females. Host
tissue is digested extra-intestinally. Ticks take up fluid
and cells from the pool, digest them immediately and
slowly gain weight(approximately 10 times the weight
of the unfed tick). Some ticks excrete large amounts
of dark faeces (see Dermacentor marginatus). The
 Part Ill. Parasites and parasitoses: metazoa
second phase is short and lasts only 12-24 h. During
this rapid process, ticks ingest tremendous amounts of
blood (Dermacentor andersoni about 4 ml), which is
concentrated by excreting fluid from the salivary glands.
The idiosoma offemales expands like a balloon to 1-2
cm length, associated with a 70- to 120-fold weight gain.
The second phase is completed by the detachment from
the host through the action of special enzymes. Then,
digestion of the ingested blood is initiated. Larvae of
some species (Boophilus and others) ingest only liquefied
tissue but no blood.
Occurrence and epidemiology. Ticks have adapted
during their evolution not only to their hosts but also
to their habitats where they must complete their non­
parasitic development, including diapause, and must
survive until finding a new host. Ticks spend by far the
greatest part of their lifetime in their habitat. They have
succeeded in conquering almost all terrestrial habitats
from the tropics to beyond the Arctic Circle, from
extremely humid to arid regions. Soft ticks can even
live in extremely arid habitats. Therefore, the occurrence
of a tick species is much more determined by the habitat
than the host. Wherever man migrated with his domestic
animals to a new region, some local tick species moved
from indigenous to the new hosts. However, there are
striking examples of ticks that have spread with domestic
animals to other regions or continents where the ticks
could establish themselves, such as the spread of the
Asian cattle tick (Rhipicephalus [Boophilus] microplus)
to Australia and the New World, or the African brown
dog tick (Rhipicephalus sanguineus) over the entire
tropics, subtropics and large parts of the temperate
zones. The epidemiology of ticks, which are mostly
extremely dependent on a habitat, is determined by
climate, weather and features of habitats, the availability
of hosts and species-specific factors. Because of their
high reproductive potential, very high abundances may
occur, especially in anthropogenic habitats with high
host densities, such as sheep or canle pastures. Ticks
even occur in cities, in gardens, parks, forest areas and
green spaces of recreational areas where the conditions
are favourable for contacts with humans and their
companion animals. In parks In Bavarian towns, 15
to >50 specimens of Ixodes ricinus were found per 100
m 2, and 30 per 100 m 2 on lawns adjacent to forests in
Q)
the UK. Recent data indicate a worrying tendency for a
·o
C
'6 spread of various tick species, e.g./. ricinus (northwards
Q)
� and to higher mountain areas), /. persulcatus (from
east to west) and Dermacentor reticulatus (spread to
cu new areas in Central Europe). It is obvious that higher
C
·c temperatures in the wake of climate change may lead to
Q)
j increased and prolonged active phases of ticks during the
C year. For example,/. ricinus ticks were active in a wooded
>­ area near Berlin during the mild winter of 2006/2007.
Ol
0
0
It has been known for a long time that migrating birds
'cii can transport ticks over long distances. Pathogens can
cu be detected and identified in such ticks through DNA­
cu
Q_ based tests. Here are a few examples: 191 /. ricinus larvae
and nymphs were collected from songbirds (blackbird,
thrush species, robin, great tit) at Greifswald (northern
Germany) in 2007 and DNA of various pathogens was
detected: Babesia divergens (prevalence 2.6%), B. microti
(2.1 %), Anaplasma phagocytophilum (2.6%), Rickettsia
spp. (7.3%). In Norway (2003-2005), 21 % of I. ricinus
nymphs from four species of migratory birds contained
detectable Borrelia DNA. These data provide important
epidemiological evidence but do not allow to draw any
conclusions on the infectivity of the pathogens and the
effective vector role of ticks.
Vector role. Ticks can transmit as vectors viruses,
bacteria (rickettsiae, spirochetes, etc.), protozoa, fungi
and nematodes to domestic and wild animals and
humans. For domestic animals, ticks are by far the most
important vectors of pathogens, as shown in ► Table
14.4 (more detailed information ► Table 14.5, p. 409).
The mode of transmission of pathogens by ticks is
complex. Mechanical transmission ( ► Glossary, p. 620),
if occurring at all, is epidemiologically not significant;
biological transmission is the rule. Transmission of
pathogens to the host usually is inoculative, rarely
by ingestion (Hepatozoon) or contaminative (Coxiella
burnetii). Transmission pathways in ticks can be
summarised in a simplified manner as follows:
• Stadial transmission. (a) A tick stage becomes
infected on a host and transmits the pathogen to another
host (intrastadial transmission). (b) A stage becomes
infected (e.g. larva), but only the next stage (nymph)
transmits the pathogen to a host (stadium-to-stadium
transmission). (c) The pathogen persists over at least
two moultings during the development of the tick, i.e.
from the infected larva through the nymph to the adult
(transstadial transmission).
• Transovarial and vertical transmission.
Transovarial transmission, i.e. transmission of a
pathogen from female to eggs, is the prerequisite for
vertical transmission by which a pathogen is passed from
the parent generation to the stages of the F 1 generation
and further to at least the F2 generation without a new
infection by blood ingestion ( � of the P-generation-+
egg - L - N - � the F 1 generation - egg of the F2
generation, etc.).
• Transmission by co-feeding. In case of
simultaneous infestations of a host with infected and
non-infected ticks, the latter can acquire pathogens
that were inoculated by the former, probably in an
adjacent or a jointly used pool. This is also possible with
unresponsive hosts, in which the pathogens inoculated
by the ticks can survive only for a short period of time.
• Sexual transmission. The pathogens (rickettsiae,
African swine fever virus) infect the spermatophores
 14. Phylum Arthropoda (arthropods)

Table 14.4. Hard ticks as vectors of pathogens (selection) (information in ► Table 14.5 is more detailed and ranked by pathogen).

..
�-
-:---� - ·,

Jlck species Pathogene transmltt8d by 1ICkll (Nleellon)

�
fi,Dlatrlbutlon 1 V: vlrUNe, 8: becarta. P: protoaoe, H: helmlnth8
Z: aoonotlc �
,:,
ro
lxodes ricinus
D: Europe: from Iceland to Russia; N Africa
V: tick-borne encephalitis virus (rBEV) (Z), looping-ill virus (Z)
8: Anaplasma phagocytophilum (Z), 8orreJia spp. (Z), Rickettsia helvetica (Z),
co
E
Francisel/a tularensis (Z) ,Ql
P: Babesia divergens (Z), 8. capreoll, �: venatorum (Z), 8. microti (Z)_
lxades hexagonus 8: Borre/ia burgdorleri (Z)
D: NW, C, S Europei N Africa
Rhiplcephalus sangulneus
- ··- 2
8: Anaplasma platys, Ehrlichia canis, Rickettsia conorii (Z)
D: tropics, subtropics, Mediterranean region, P: Babesia vogeli, B. gibsonf, Hepatozoon canls
locally indoors also further north and east (UK, H; Dlpetalonema dracunculoldes, Cercoplthlfilarla grassii
NO, PL and other European countries)
Dermacentor marglnatus
- --
--
8: Cox/el/a bumetlt (Z), Ricketts/a slovaca (Z), Franclsella tutarensis (Z)
D: S, C, E Europe; C Asia P: Babes/a cabal/I, T118/lerla equl -
,---
Dermacentor retlculatus
-
B: Ricketts/a slovaca (Z), R, rsoultll (Z), Frsnclsella tularensls (Z)
D: S, C, E Europe; C Asia P: Babes/a Caba/II, B. csnls, Thellerla equl
Haemaphysalis punctata
-
P: Babes/a major, B. motes/, Theiler/a orlentslls
D: Europe from Soain to S Scandinavia; C Asia
Hya/omma marglnatum V: Crimean-Congo haemorrhagic fever (CCHF) virus (Z)
D _:.Mediterranean area;�N A.frica;J; Asia P: Theiler/a equl ..

1 C: Central; E: East; N: North; NW; North-west; S: South.

of male ticks and are transmitted to the females during
copulation.
Immunology. Ticks inoculate saliva into their host
during the blood-sucking process and thereby 'dispose
of ' excess fluid and ions from the host blood as well as
antigenic, toxic or other metabolites of their metabolism
• Inflammatory reactions. Inflammatory reactions
can lead to the isolation of the mouthparts of the tick
through demarcation. This is counteracted by the
following substances in tick saliva: cement (inhibition
of skin reactions), anti-histamine activity (prevention of co
mast cell-associated inflammation), carboxypeptidase 'O
0
(destruction of anaphylatoxins, bradykinin, C3), e
Q_

('renal function' of salivary glands). The saliva of ticks
also contains a rich, genus- or even species-specific
spectrum of >30 active ingredients that interfere with
the physiology of the host. For example, proteolytic
enzymes initiate and widen lesions, such as the piercing
canal and the pool, especially in Boophilus. The pool
( ► Figure 14.5) is further enlarged by the accumulation
of neutrophils that release hydrolysing enzymes from
their granules. The contact of hard ticks and host is,
compared to other haematophagous ectoparasites, long
and intimate, which opens the opportunity for the host
for defence, which is primarily based on haemostasis,
inflammation and immunity. Most ingredients in tick
saliva are therefore directed against these defence
mechanisms.
• Haemostasis. The host tries to prevent the
blood flow during feeding of the tick by platelet
aggregation, vasoconstriction and blood clotting.
Various substances in the tick saliva are directed against
anaesthetics (reduction of grooming and other defence .c
t
reactions of the host). Because of the degradation of the <(
host-derived, pain-inducing bradykinin, 80% of tick
bites remain unnoticed in humans.
• Immune reactions. Tick infestations usually
trigger allergic reactions, both immediate (type I) and
delayed reactions (typ e IV). Of special significance
is the delayed reaction with a cutaneous basophilic
hypersensitivity (Jones-Mote reaction), which is involved
in rejection reactions against ticks. Furthermore, de- or
hyposensibilisation and unresponsiveness are possible.
The interactions between host and tick depend not
(1)
only on the tick species but also on the host, the tick C:
·5
stage and the phase of the blood-sucking process. '6
Ticks can modulate the immunological defence (1)
�
mechanisms of the host with active ingredients in their
saliva. Thus, mediators with the following effects are co
described. Inhibition: alternative complement pathway, -�
C:

(1)
these mechanisms: apyrase (prevention of platelet phagocytosis, NK cells, the formation of oxygen radicals
aggregation), prostaglandins (PGE2 PGF2), prostacyclin and many effects of cytokines and the formation of .£
' >-
or similar compounds (prevention of vasoconstriction), IFN-y. Furthermore, anaphylatoxins are inactivated. The 0)
anticoagulants (inhibition of thrombokinase and factor immunosuppressive effect of tick saliva protects the 0
0
X of the coagulation cascade). ticks during the long blood-sucking phase. Furthermore, ·u;
the immunosuppression enables or facilitates the
co
CL
 Part Ill. Parasites and parasitoses: metazoa
transmission of pathogens. This is an important factor
for the high vectorial capacity of ticks.
Despite the immunosuppressive effect of tick saliva,
a partial immunity usually develops. After repeated
infestations, the number and weight of engorged ticks as
well as the number of their offspring are in some cases
significantly lower than after a first infestation. However,
this immunity wanes with continued infestations with
highly specialised ticks. For example, dogs become
susceptible again after the 2nd to 4th infestation with R.
sanguineus and therefore act as lifelong effective hosts
for this tick species. Due to insufficient development
of host immunity, an alternative strategy for vaccine
development is pursued. By vaccinating the host with
a 'hidden' antigen, which occurs in the tick gut, the
formation of specific antibodies is stimulated which are
taken up by the tick when blood feeding and which cause
dysfunction of the tick gut by binding to the antigen
(► p. 569).
Some breeds of cattle in the tropics, especially Zebu
cattle (Brahman) are partially resistant to hard ticks.
They continue to be bred for resistance. A complete
resistance to the cattle tick Rhipicephalus (Boophilus)
microplus seems feasible.
Pathogenesis and clinical signs. Ticks can cause
local lesions and systemic diseases in the hosts and act
as vectors of pathogens.
• Local lesions at the site of bite. The trauma of
the tick bite corresponds to the size of its mouthparts
which are small in highly evolved ticks, but very large in
primitive adult ticks (Jxodes, Hyalomma, Amblyomma),
particularly in females. Bites of nymphs or larvae usually
cause only minor skin reactions that often go unnoticed.
At the biting site there may be various changes:
hyperaemia, erythema, itching, necrosis, ulceration
or bleeding with subsequent inflammation involving
eosinophils, later thickening of the skin and formation
of nodules or granulomas, often regressing only after
weeks. Complications from secondary infections or
myiasis are possible. Scarred tick bites cause significant
leather faults in slaughtered animals.
Q)
C • Systemic effects. Systemic effects are caused
'<3
'6 by non-specific and specific toxicoses, which are of
Q)
L significance mainly in warmer climate zones.
Non-specific toxicosis. A non-specific toxicosis
co (tick worry) is triggered, e.g. by saliva of species
C
·;;::
belonging to the subgenus Boophilus in tropical
areas, in European (taurine) cattle breeds. This can
C lead to debilitating conditions as a result of large­
>- scale damage to the skin with secondary infections,
-
0)
0 metabolic disorders and significant weight loss. In
0
'cii case of massive infestations, also death may occur.
co Specific toxicoses. Specific toxicoses are Sweating
co
a.. Sickness and tick paralyses.
Sweating Sickness is an acute toxicosis caused by
epitheliotropic and immunogenic toxins in the saliva
of Hyalomma truncatum and other ticks in South Africa
and India. Calves, sheep, goats and pigs are affected,
and they show the following symptoms: profuse
sweating, lacrimation and salivation, acute dermatitis,
and diphtheroid stomatitis. Secondary infections are
common.
Nearly 50 species of ticks (Ixodidae and Argasidae)
produce in their salivary glands usually species­
specific neurotoxins (proteins) which can cause tick
paralysis in animals and humans. The toxins block the
neuromuscular junctions in particular by preventing the
release of acetylcholine. The main paralyses are caused
by females of Dermacentor andersoni in the west and D.
variabilis in the east of North America (grazing animals,
dogs, cats, humans), by Rhipicephalus evertsi sspp. and
lxodes rubicundus in South Africa (mostly sheep and
goats) as well as by /. holocyclus (mostly calves, dogs,
horses, humans, etc.) in Australia. In Argas (P.) walkeri
it is the larvae that cause paralysis. A single female of D.
andersoni can kill a human. The first symptoms become
evident about 5 days after tick infestation. Following the
timely removal of the ticks, the hosts rapidly recover.
It is only in I. holocyclus infestations that symptoms
get worse even after removal of the ticks. In this case,
administration of an anti-toxin is a possible therapy.
Most of the older animals in endemic herds are immune.
The immunity is species- or even strain-specific.
Diagnosis. Tick infestation, especially of engorged
females, is easily recognised by the owners of domestic
animals or by hunters in game animals. However,
infestations with the smaller larvae and nymphs often go
unnoticed. For species identification, ticks are carefully
detached from the animal and promptly sent alive (in a
small vessel with moistened cotton wool at the bottom)
to a specialised institution. In case of longer transport
times, ticks should be preserved in 70% ethanol. Unfed
ticks that are searching for a host can be collected in
their habitat by so-called 'flagging', whereby a white
cloth is slowly drawn over the vegetation of the habitat.
The active, dark tick stages cling to the underside of the
cloth. Other tick species can be detected in burrows,
nests or resting places of their hosts. Characteristics of
hard tick genera ► Figure 16.19, p. 553.
Therapy and control. Principally, an integrated hard
tick control that involves other means in addition to the
use of acaricides is recommended. The corresponding
options vary depending on host animal, tick species
and the significance of the tick infestation. In this book,
some examples of control options in different animal
species are listed (ruminants ► p. 582, dog and cat
► p. 606). Non-chemical options for tick control are
very limited (e.g. keeping grazing animals away from
known tick habitats, use of resistant breeds, vaccines,
► Table 18.1, p. 569).

Significance for humans. Hard ticks transmit the
causative agents of major human diseases, including
zoonotic pathogens. In Europe, these are mainly
the causative agents of Lyme disease and tick-borne
encephalitis(TBEV)(► Table 14.5, p. 409).
Genus lxodes
The genus lxodes, with about 250 species, is the largest
genus of ticks (► Table 14.2). Ixodes species occur
worldwide, about 15 species in Europe. By far the most
common and most important species is Ixodes ricinus
( ► Figure 14.6).
lxodes ricinus (wood tick, castor bean tick,
common sheep tick)
Ixodes(G): ixos-like, analogously: sticky; rlcinus(L):
ancient Roman name for the castor bean plant. Refers to
the engorged female tick that resembles the ricinus seed.
Morphology. S?- � unfed between 3.0 to 3.6 mm long;
black scutum(dorsal plate) and orange alloscutum (=
dorsal area not covered by the scutum)(► Figure 14.6).
Fully engorged � � about 1 cm long and steel blue. o' d'
2.4-2.8 mm long, the black scutum covers the entire
dorsal surface. Unfed nymphs 1.3-1.5 mm, unfed larvae
about 0.5 mm long. Both have a small, black scutum
and a gray alloscutum.
Life cycle and epidemiology. I. ricinus is a three­
host tick(► Figure 14.7). The blood feeding process
lasts in the larvae only 2-3 days, in the nymphs up to
5 days and in females one week, possibly 2-3 weeks;
males do not take blood. Copulation usually takes place
on the host(cf. I. hexagonus). After falling off the host,
the engorged females lay about 3000 eggs under plant
debris on the ground. A generation lasts for at least 1 ½
years, mostly 2-3 years, rarely 4-5 years. Every unfed
stage can survive for at least l year.
I. ricinus is adapted to humid habitats(>75% r.h.) with
a dense, permanently moist detritus layer (95-100%
r.h.) as it occurs mainly in deciduous and mixed forests
with herb and shrub layers. There are similar habitats,
permanently shaded by the vegetation, in moors and
heaths, as well as on extensive pastures with shrubs, trees
and old, tall grass or herbage, but also in comparable
parks and house gardens as well as along highly vegetated
paths. The thicker the layer of decaying leaves and other
plant debris, the more suitable is the habitat for I. ricinus
populations.
The seasonal activity of I. ricinus starts at air
temperatures of 7-10 °C and lasts in Central Europe
usually from March to November with two activity
peaks, the first from May to June and a smaller second
one in September. At high temperatures (>30 °C) in
mid-summer, activity of ticks decreases. During the
14. Phylum Arthropoda (arthropods)
active phase, the hungry stages climb up on plants, larvae
up to about 20 cm, nymphs to 50 cm, adults up to -80
cm(never on higher trees!) and wait for a host. When
humidity decreases around noon, the ticks wander back
to the detritus layer on the ground. Nymphs move up to
10 m horizontally in 24 h. Ticks overwinter inactively in Ctl
dormancy, and they remain active in this period only at co
E
mild temperatures. The seasonal activity in the spring 0)
:;::;
en
can start explosively after long winters. Ctl
�
I. ricinus has a very wide host range including about
200 species of vertebrates(mammals, birds, reptiles)
(► Figure 14.7). The larvae remain near the ground
and attack mostly small mammals(Muridae, Microtidae,
Soricidae), particularly bank vole ( Clethrionomys
glareolus), yellow-necked mouse (Apodemusflavicollis)
and wood mouse (Apodemus sylvaticus), as well as birds
and larger mammals. Nymphs and adults have a greater
vertical and horizontal radius of activity. They infest
small mammals, birds, reptiles (lizards) and larger
mammals. Common hosts are deer, fox and raccoon
dog in the sylvatic cycle, as well as sheep, cattle, dog
and humans in the synanthropic cycle. More than two­
thirds of the ticks found on humans were nymphs, one
fourth females.
Occurrence. The distribution area of/. ricinus extends
from Portugal to the Caspian Sea - rarely further east -
and from the south of Scandinavia to North Africa, in
habitats from the plains to altitudes of 2,000 m above Ctl
-0
sea level. Since 1980, the limit of distribution of this 0
e
Q.
tick species in Sweden has shifted northwards by 5
degrees of latitude(61° N-+ 66° N). More northern of .c
t
the distribution limit in Scandinavia, the Baltic States <(
and Russia, the habitat is occupied by/. persu/catus. In
the warmer Mediterranean climates of southern Europe,
North Africa and Lebanon, /. ricinus generally prefers
forested areas at higher altitudes. ln Central Europe, there
are plenty of suitable habitats for I. ricinus, especially in
largely forested regions. Tick densities in such habitats
were 300/100 m2(also ► p. 402). Infestations with this
tick species therefore occur from the North Sea to the
Alps in game, domestic animals and humans throughout
the season on a regular basis, later less frequently until
December. Eight tick species were identified on dogs in
Germany, with prevalences for lxodes spp. as follows:
0)
I. ricinus 84%, l. hexagonus 9.3%, I. canisuga 6.2%. In a C
study performed in the region of Berlin/Brandenburg
·u
'6
0)
(2003), the tick population of 242 dogs consisted of �
I. ricinus(46.5%), Dermacentor reticulatus(45.6%), I. �
hexagonus(8.8%), and Rhipicephalus sanguineus(0.1%). Ctl
C
·;::
0)
Pathogenesis and clinical signs. I. ricinus infests j
head, neck, extremities and the ventral parts of the C
trunk of domestic animals. Predilection sites on grazing >,
Ol
animals are the inguineal and perinea! regions, the inner 0
0
surface of the front and hind legs and the head; on dogs ·enCtl
head, especially ears; on humans' legs, torso and arms,
Ctl
on children's heads, especially the hairline behind the 0...
 Part Ill. Parasites and parasitoses: metazoa

Blood feeding

3rd host

Exuvia

Nymph,
fully fed

2nd host
Blood feeding

Accidental host

Figure 14.7. Life cycle of /xodes rlclnus (Graphics: IPZ, S. Ehret).

ears and in the neck. Strong infestations can cause local its preferred hosts hedgehog, fox, polecat, badger and
skin reactions and decreasing performance in cattle and dog(► Figure 14.8).1. hexagonus is frequently found on
sheep (weight, milk or wool). farm and hunting dogs which had contact with hedgehog
nests. The hedgehog tick can thus establish stable
Q)
C Vector role. I. ricinus is of paramount importance endemic foci in the vicinity of dogs (kennel. wooden
·c3
'6 because of its enormous vectorial capacity. In Europe, shed), but also in urban habitats. Males do not usually
Q)
::E this species is particularly important as a vector of the infest hosts, but remain in the hosts' resting places
following pathogens: tick-borne encephalitis virus where they mate with the engorged females. All stages
co
C (TBEV), louping-ill virus, Anap/asma and Borre/ia are active throughout the year because of the balanced
c
·Q) species as well as Babesia divergens, B. capreo/i and B. temperature conditions in the nests, but their activity
j microti (► Table 14.5, p. 409). is particularly high in spring and autumn. I. hexagonus
,£; transmits Borre/ia burgdorferi s.l., and rarely TBE virus
>,
0)
lxodes hexagonus (hedgehog tick) (both transstadially and transovarially) (► Table 14.5).
0

·enco
0
This 3-host species affects many different hosts, including
humans, but rarely sheep, cattle or horses. The species
co
a.. is adapted to the microclimate in burrows or nests of
---
Figure 14.8. Dog infested with lxodes hexagonus (Photo: IPH,
K.T. Friedhoff).
lxodes canisuga (fox tick)
The 3-host fox tick usually lives in fox or badger dens; it
also affects other mustelids and dogs, especially hunting
and herding dogs that have contact with fox dens. The
species may become endemic in kennels (Cave: Ixodes
canisuga can easily be confused with I. ricinus). Vector
of Borrelia burgdorferi s.l.
lxodes trianguliceps (vole tick)
This 3-host species has adapted to mice, especially to
the bank vole ( Clethrionomys glareolus). Other hosts are
species of the genera Arvicola, Microtus and Apodemus
and shrews (Soricidae), rarely cats, hedgehog, mole
and others. Ixodes trianguliceps transmits Anaplasma
phagocytophilum and probably Borrelia burgdorferi and
Babesia microti.
Ixodes frontalis is an ornithophilic species that is
suspected of causing toxicosis in birds via its toxic saliva
(avian tick-related syndromes). Its range extends from
the UK to western Russia, including inter alia CH, CZ,
DE, FR and the Scandinavian countries.
Genus Haemaphysalis
The approximately 165 species of the genus
Haemaphysalis (► Figure 14.6) are scattered around
the world; most species occur in Africa and South Asia.
In western and Central Europe, three species are native:
H. punctata, H. concinna and H. inermis.
Haemaphysalis punctata (red sheep tick)
Haima (G): blood; physa (G): bladder; punctum (L):
sting, point.
14. Phylum Arthropoda {arthropods)
Morphology. Relatively small, pale or reddish brown
ticks without pigments,�� 3.0-3.5 mm, fully engorged
�10 mm long; <3<3 2.8-3.2 mm.
Life cycle and epidemiology. H. punctata is a 3-host
tick. Larvae and nymphs infest small mammals and C'O
birds, often including migratory birds, rarely lizards; co
E
adult ticks use sheep and cattle as hosts, occasionally 0)
:;:;
goats and horses as well as cervids, rabbits, hedgehogs Cl)
C'O
and mustelids. Adults can be found on cattle particularly a,
�
on udder and inner thigh areas. H. punctata is especially
active in spring and summer,but affects cattle throughout
the grazing season. A generation develops in 1-3 years
depending on habitat conditions.
Occurrence. The distribution area covers almost
all of Europe (except Ireland) from the south of
Scandinavia to North Africa and east to central Asia.
This tick sporadically occurs in very different habitats,
on moist, densely vegetated, but woodless terrain. In
Central Europe, there are only focal habitats with low
population densities.
Vector role. H. punctata can transmit the following
pathogens: Babesia major, B. motasi and Theileria
orientalis (► Table 14.5, p. 409).
Haemaphysalis concinna (relict tick)
Concinna (L): delicate. <U
'O
0
e
a.
H. concinna (3-host tick), very similar to H. punctata,
has a distribution area ranging from France eastward to ..c
t:::
China and Japan. In Europe, it is rare and mostly occurs <(
in pristine deciduous and mixed forests. Adult ticks
infest cervids, particularly roe deer, also rabbits, cattle,
horses, dogs and cats. Larvae and nymphs parasitise roe
deer, hedgehogs, rodents, birds and reptiles. All stages
can be found on roe deer mainly from March to June
and October. This tick plays a minor role as a vector
(TBE, Siberian typhus, tularaemia).
Haemaphysa/is inermis (winter tick)
Inermis (L): unarmed.
Q)
H. inermis is a rare, very small, 3-host tick (length: T5
C
�� 2.0-3.5 mm, fully engorged :s:8 mm; <3<3 2.4-3.0 '6
mm). Distribution: mainly in France, throughout Q)
�
the Mediterranean region, including the Balkans and C'
Poland, and eastward to Iran and South Asia. Adult ticks C'O
C
parasitise mainly cervids, but also foxes, hedgehogs, as ·.::
Q)
well as cattle, sheep, horses and occasionally humans.
Larvae and nymphs infest rodents, other small mammals .s
and insectivores. Larvae and nymphs can hardly be >,
0)
detected on the hosts because they fall off after only 0
0
a few hours, and then enter diapause. Moulting of the
·u;
nymphs usually occurs after one year. Adult ticks are
co
active in winter (November to April). H. inermis prefers CL
Part Ill. Parasites and parasitoses: metazoa
deciduous and mixed forests, meadows and mountain
slopes. This tick species has no relevant vector role
(TBE, etc.).
Genus Rhipicepha/us
The genus includes about 80 species, mostly found
in Africa. In Europe, especially the morphologically
and genetically similar species of the Rhipicephalus
sanguineus group (R. sanguineus s.l.) are important.
These closely related species (R. sanguineus s.s., R.
turanicus, R. pusillus, etc.) are often confused. The genus
Boophilus is now assigned as a subgenus of the genus
Rhipicephalus(see below).
Rhipicephalus sanguineus s.s. (brown dog
tick, kennel tick)
Rhipis (G): fan; kephale (G): head; sanguineus (L):
bloody, blood red.
Species and morphology. The validity of many
species of the R. sanguineus group was and still is
controversial. North of the Alps, there is only R.
sanguineus s.s. which almost exclusively occurs on dogs.
Rarely, other Rhipicephalus spp. are imported with horses
or other hosts. The reddish females of R. sanguineus s.s.
are unfed between 3 to 3.8 mm, engorged up to 1 cm
long. The dark brown males(3 to 3.8 mm long) have a
stronger fourth leg pair. Nymphs are 1.4-1.6 mm long
(► Figure 14.6).
Development, occurrence and epidemiology.
R. sanguineus is a 3-host, monotropic tick, i.e. all stages
almost exclusively infest dogs, rarely(<I 0%) other hosts,
mostly cats. R. sanguineus was originally found in Africa
and in the Mediterranean area, but has spread with dogs
almost worldwide over the entire tropics and sub-tropics
to the temperate wne(about 35° S to 50° N). For over 40
years, R. sanguineus has regularly and Lo a considerable
extent been imported with travelling dogs mainly from
Spain, Italy, Greece and France to central, western and
northern Europe. There, autochthonous populations
have established over the past decades in urban habitats,
up to Norway. R. sanguineus in some cities is now more
common on dogs than /. ricinus. The brown dog tick
has adapted to sub-humid habitats within the activity
radius of dogs, i.e. outdoors south of the Alps, but almost
exclusively indoors and in protected kennels ('kennel
tick') north of the Alps. Thus, stable endemic foci are
occurring in animal shelters, kennels and dog schools,
veterinary practices and even in apartments. There, the
ticks are active all year round due to continuous high
or moderate temperatures, whereas south of the Alps
they are active in the environment only from March to
October (also in tourist centres such as Rome). Houses
with gardens are favourable habitats in the urban centres
of southern Europe. The rural habitats are characterised
by sparse vegetation; R. sanguineus is hardly ever found
in forests. The ticks develop above 18 °C and 50% r.h. In
winter, they enter into diapause, except in sufficiently
warm rooms. Under favourable conditions, however, a
generation will take only about 3 months, north of the
Alps about 1 year. Adults can starve up to 19 months.
Pathogenesis and clinical signs. R. sanguineus is
very well adapted to dogs and mostly causes only slight
skin reactions on these hosts. An evolving immunity
wanes after 2-4 infestations; therefore, dogs can act as
suitable hosts throughout most of their life.
R. sanguineus does not usually parasitise humans. In
some regions(e.g. Sicily), however, children are affected,
mainly by larvae. The alleged attacks on humans, sheep,
goats, horses, cattle and other hosts on the shores of
the Mediterranean sea(up to about 250 km inland) are
probably caused by R. turanicus(see below).
Vector role. R. sanguineus is an important vector
which can transmit the following pathogens(► Table
14.5): Anaplasma platys, Rickettsia conorii, Ehrlichia
canis, Hepatozoon canis, Babesia vogeli, B. gibsoni,
Dipetalonema dracunculoides and Cercopithifilaria
grassii.
Rhipicepha/us bursa
Bursa(L): pouch. Refers to the engorged female.
R. bursa is a 2-host tick. The main hosts are sheep,
cattle, goat and horses, rarely dogs and humans. In
sheep, ears, perinea) and inguineal regions are most
likely to be infested. The tick is well adapted to sheep
and causes hardly any skin reaction. It prefers semi-arid
habitats on grassy slopes at low to medium altitudes and
steppe pastures. The distribution area extends around
the Mediterranean(except Egypt), the Middle East and
further to Iran and Kazakhstan. The northern border
in Europe stretches from the Iberian Peninsula through
southern France, Switzerland, the Balkans, Romania, and
the northern Black Sea coast to the Caucasus.
Vector role. R. bursa is an important vector for
Anaplasma marginale, A. ovis, Babes/a ovls, Thei/eria
ovis and T. equi.
Rhipicephalus turanicus
Turanicus (L): belonging to Turan, Turanian. Turan
(Persian) for Turkestan.
The species was often confused with R. sanguineus or
R. sulcatus. There are several strains of R. turanicus, at
least one in the Palaearctic and some in the Afrotropical
region. R. turanicus is a 3-host tick with the widest host
range of the R. sanguineus group species. Larvae and
nymphs prefer rodents, hedgehogs, rabbits and birds,
adult ticks infest sheep, goats and horses, rarely pigs,
 14. Phylum Arthropoda (arthropods)

Table 14.5. Tick-borne infectious agents (selection). Supplement to ► Table 14.4, p. 403.

,,,l ,,1,1 1 \j,111 ·�---�-�1_._ i_....:.,.,.fP..:Jlu�...:0iLt, 1 (1V) and verte

tJ1�·,.,__..}t__1 ",,,.__ .:.1 ·:
·11 ,,�1•l·11r_:J,11 IL!J..tl:...l'..- l_l!11_,'\:,.,r .._ 1.....,JJ ...._1_•�,..:j• 1!.�,(' J,)1
. - .
Virus

Asfarviridae
cu
E
0)
African swine fever-virus (ASFV) A: African swine fever IV: Ornithodoros moubata-complex, �
D: Sub-Saharan Africa; S America; S en
0. erraticus ro
Europe; Caucasus-region; Russia VH: warthog, bush pig, wild boar, domestic
pig 2
Bunyaviridae
Crimean-Congo haemontiaglc fever H: Crimean-Congo IV: Hyalomma rufipes, H. marginatum,
virus (CCHV) h aemorrhagic fever H. truncatum, Dermacentor marginatus
--_D_: S
_ , _S_ _ _E_u _ro_,_p_e _; A_f ri__ ca_;_ S_W_ A_sl_a
E _ an_ dE ----- ---- ---1 VH: leporlds, rode nts, cattle, sheep, human
t ---+ -
Nairobi sheep disease virus (NSOV) H: Nairobi sheep disease (NSD) IV: Rhlplcepha/us appendiculatus,
D:E, C, S Africa; India A: NSD Haemaphysalls spp.
1-----------------'--- -----------'-...:. V_H:.. .:..::.
sh... :1:P_:_;• goat, rat, human
:..e:.:
e
Reoviridae
Colorado tick fever virus (CTFV) H: Colorado tick fever IV: Dermacentor andersonl
D: N America VH: rodent s (gopher, wood rat, othe rs),
r------------------t------------1 human
Eyach virus (EYAV) H: similar to TSE IV: lxodes rlclnus, I. ventallol
D: N America;Europe VH: rabbit, human
Flaviviridae
T ick-borne encephalitis (TBE) virus
-European subtype H: meningoencephalitis IV: lxodes riclnus,E-Europe: /. persulcatus
D: C, N,EEurope (many countries) A: TSE in dog, horse VH: rodents l,Apodemus, Mlcrotus, Myodes),
insectivores, cattle, goat, shee p, c ervids, dog,
fox, human
- Far eastern subtype H: Far eastern TSE IV: lxodes persulcatus Ctl
'D
D:E Russia; China; Japan VH: mammals, human 0
0..
- Siberian subtype H: Siberian TSE IV: lxodes persulcatus 0
D: Ural; Siberia; FarEast Russia VH: mammals, human .c
t::'.
Kyasanur forest disease virus (KFDV) H: Kyasanur forest disease IV: Haemaphysalis spinigera, H. turturis <(
D: India; China; Saudi Arabia A: disease In monkeys VH: rode nts, human
Louping-ill virus (LIV) H: encephalitis IV: lxodes ricinus
D: Scotland; Wales;England; Ireland A: Louping ill of sheep VH: small mammals, birds, sheep, goat,
cattle, cervids, dog, othe rs, human
Omsk haemorrhagic fever virus H: Omsk haemorrhagic fever IV: Dermacentor reticulatus, lxodes
(OHFV) A: muskrats, birds apronophorus
D: Russia 0/1/ Siberia) VH: rodents l,Arvicola, Microtus, muskrat),
human

Bacteria

Anaplasmataceae
Anaplasma marginale A: malign bovine anaplasmosis IV: Rhipicephalus (Boophilus) microplus,
D: Tropics and subtropics; America; R. (B) annulatus, Rhipicepha/us spp., Q)
Africa; Asia; Australia; alsoE, S, C Dermacentor spp. C
Europe (north to AT and CH) VH: Cattle, buffalo, bison, other wild :Q
'D
ruminants Q)
2
Anap/asma centra/e A: benign bovine anaplasmosis IV: Rhipicephalus simus
D: as A. marginale VH: cattle
c.'
Ctl
C
Anaplasma bovis A: bovine anaplasmosis IV: Amblyomma variegatum, Rhipicephalus -;::
D: Africa; N, S America; Asia appendiculatus, Hyalomma spp.,
Dermacentor andersoni, other
W: cattle, buffalo C
>,
Anaplasma ovis A: anaplasmosis of small IV: Rhipicephalus bursa, R. turanicus, 0)
0
D: Mediterranean; MiddleEast; Africa; ruminants Dermacentor marginatus, D. silvarum 0
USA VH: sheep, goat, wild ruminants ·u;
co
co
a.
 Part Ill. Parasites and parasitoses: metazoa

Table 14.5. Continued.

Anaplasma phagocytophilum H: human granulocytic IV: Europe:lxodes ricinus, I. triangu/iceps;

- (formerly: Ehrlichia phagocytophila, E. anaplasmosis (HGA) Asia, E. Europe: /. persulcatus;
equi and HGA agent) A:bovine, ovine, equine, canine, USA: lxodes scapularis, I. pacificus
D: northern hemisphere:N America to feline granulocytic anaplasmosis VH: sheep, cattle, horse, dog, cat, rodents,
Asia wild ruminants, fox, others, human
Anaplasma platys A:cyclic thrombocytopenia in IV:Rhipicephalus sanguineus
(formerly:Ehrlichia platys) dogs VH:dog
D: as vector tick R. sanguineus (► Table
14.4)
Anaplasma pullorum A: aegyptianellosis IV:Argas persicus, A. reflexus, A. walkerae
(syn. Aegyptiane/la pullorum) VH:chicken, turkey and other birds
D: Africa; Asia; Europe
Ehrlichia canis A: canine monocytlc ehrlichiosls IV: Rhipicephalus sanguineus, 0ermacentor
D: worldwide:tropics; subtropics, (CME) variabills
W, S, C Europe VH:dog, other canids
Ehrlichia chaffeensis H:human monocytic ehrlichiosls IV:Amblyomma americanum
D: USA; C, S America; Asia (HME) VH: white-tailed deer, human
Ehrlichia ewingii H: Human granulocytic IV:Amblyomma americanum
D: USA; Africa; Asia ehrllchlosls (GE) VH: white-tailed deer, dog, human
A:canine GE
Ehrlichia ruminantium H: rare infection IV: Amblyomma variegatum, A. hebraeum
(syn. Cowdria ruminantium) A: cowdriosls (heartwater) of VH: cattle, sheep, goat, antelope, dog, human
D:tropical Africa; Caribbean ruminants
Neoehrlichia mikurensis H: neoehrlichiosis IV: lxodes riclnus, I. persulcatus, I. ovatus
D:Europe (CH, DE, IT, SE, RU and A: neoehrllchlosls (dog) VH:rodents, dog, human
others); Asia
-------- ----�-----------.....------------------1
Rickettsiaceae
Ricketts/a africae H: African tick bite fever IV:Amblyomma variegatum, A. hebraeum
D: Sub-Saharan Africa; Caribbean; VH:human, cattle, sheep, goat, other
Oceania
-------------+------------+-------------------<
Ricketts/a aeschllmannii H: tick bite fever IV:Hyalomma marginatum, H. rufipes,
D:Europe; Africa Rhipicephalus appendiculatus
VH:human
Ricketts/a conorli (4 subspecies) H: Mediterranean spotted fever, IV; Rhipicephalus sanguineus, R. turanicus,
D: Mediterranean countries; Africa; India; Fievre boutonneuse R. pusillus, R. s/mus
Russia --------1 VH:human, dog, rodents
Ricketts/a he/vet/ca H: tick bite fever IV: /xodes rlclnus
D: Eurasia VH: human
·-- -- ----- --------t-------------------i
Ricketts/a slblrlca mongo/otlmonae H: Lymphangltls-assoclated V: Hyalomma asiatlcum, H. truncatum,
D: N, C Asia; Africa; Europe: S France rlckettslols (LAA) H. anatollcum
---- ----- ------------1------"- -----------� VH: human, other?
Ricketts/a slovaca, R. raou/t/1 H:tick-borne lymphadenopathy IV:Dermacentor marg/natus, D. reticulatus
D:W. Europe to C Asia (TIBOLA), Dermacentor- VH:human, (animals not well documented)
borne necrosis erythema and
lymphadenopathy (DEBONEL)
Q)
c:: Ricketts/a rlckettsii H:Rocky Mountain spotted fever IV: Dermacentor andersoni, D. variabilis,
·0 D: N, S America lxodes scapularis, Amb/yomma americanum,
'6 Rhipicephalus sangulneus, others
Q)
� VH: small mammals: leporids, opossum,
other, human
cu
c:: Coxiellaceae
·c
Q)
Cox/el/a burnetii H: 0-fever (OF), coxiellosis IV: Dermacentor marginatus, 0. andersoni,
D: worldwide (except New Zealand) A: OF in sheep, goat, cattle and Amblyomma americanum, others
c:: others. VH: sheep, goat, cattle, wild ruminants,
>- others, human
0>
0 Francisellaceae
0
·u5 Francisella tularensis H:tularaemia IV: lxodes rlcinus, Dermacentor marginatus,
cu D: Europe; Asia; N America A: tularaemia D. reticulatus, 0. andersoni
cu
0.. VH:hare, rodents, human
 14. Phylum Arthropoda (arthropods)

Table 14.5. Continued.

·.r-_tf\ttl�,.r
..,

.
�·_ �,�
.u
�-, ,"$..'�.... - ....
' ' ,c
' '--·
,, I l11,•l,1 \( l t . ' - ' I � ·�

�" .

Spirochaetaceae
Borrelia burgdorferi s.s., B. garinii, B. H: borreliosis, Lyme-borreliosis IV: Europe: /xodes ricinus, I. hexagonus,
afzelii, B. spielmanii, B. bavariensis A: borreliosis In dog, cat, horse I. canisuga, I. trianguliceps, E-Europe, Asia:
D: Europe; Asia I. persulcatus
VH: sheep, cattle, horse, dog, cat, rodents,
others; human
Borre/ia burgdorferi s.s. H: Lyme disease IV: lxodes scapularis, I. paclficus
D:USA VH: rodents, others, human
Borrelia duttonii H: endemic relapsing fever IV: Ornlthodoros moubata-complex
D: Sub-Saharan Africa VH: human
Borrelia hermsli H: relapsing fever IV: Ornllhodoros hermsl
D:USA;Ganada VH: small mammals (mice, squirrels, others),
human
Borrelia anserina A: borrellosis of goose IV: Argas perslcus
D: Tropics; subtropics; sporadically In VH: goose, duck, chicken, turkey
Europe
Other bacterial groups
Dermatophilus congolense H: accidental Infection IV: mechanical: Amblyomma variegatum,
D: Tropics; subtropics; single cases in A: bovine dermatophilosls other tick species, also flies
Europe VH: cattle, sheep, goat, horse, camel, others,
humans
Mycoplasma haemofe/1s, Candldatus4 A: feline/canine infectious IV: lxodidae? (also► fleas, p. 504)
M. haemominutum, M. turicensis; M. anaemia (worldwide) VH: cat; dog
haemocanis
- ,'
Protozoa
- _,._ r � �•[! � � " �- �--· � •'I.: ,
Adelaida
Hepatozoon canis A: hepatozoonosis IV: Rhipicephalus sanguineus s.l. co
"O
D: S, C Europe; Asia; Africa VH: dog, red fox, jackal, hyena, cat, others 0
a.
Hepatozoon fe/is A: hepatozoonosis IV: (not documented) e
..c
D: S Europe; Asia; Africa VH: cat t::'.
<(
Hepatozoon americanum A: hepatozoonosls IV: Amblyomma maculatum
D:USA VH: dog, coyote
Piroplasmida: Babesiidae
Babesia bigemina A: bovine babeslosis, Texas IV: Rhipicepha/us (Boophilus) microp/us,
D: Tropics, subtropics: Africa; Australia; fever R. (B.) annulatus, R. (B.) deco/oratus,
Asia; C, S America: S. Europe R. evertsi
VH: cattle
Babesia bovis A: bovine babesiosis IV: Rhipicephalus (Boophilus) microplus,
D: similar to B. bigemina R. (B.) annulatus
VH: cattle
Babesia divergens H: accidental infection IV: Europe except north: lxodes ricinus;
D: Europe A: bovine babesiosis, redwater N Europe: /. persu/catus
fever VH: cattle, cervids, human
Q)
Babesia major A: babesiosis IV: Haemaphysa/is punctata C
D: Europe; N Africa VH: cattle ·c3
'6
Babes/a occultans A: babesiosis IV: Hya/omma rufipes Q)
VH: cattle
cco
D: S, W Africa
Babes/a ovata A: babesiosis IV: Haemaphysalis /ongicornis
C
D: E Asia VH: cattle ·c
Q)
Babes/a ovis A: ovine babesiosis IV: Rhipicephalus bursa, R. turanicus,
D: S Europe; Africa: Asia; Cuba Hyalomma excavatum
VH: sheep C
>,
Babes/a motasi (avirulent) A: apathogenic IV: Haemaphysa/is punctata, lxodes ricinus? OJ
0
D: W, C, N Europe VH: sheep, goat 0
Babes/a motasi (virulent) A: ovine babesiosis IV: Haemaphysalis punctata, Russia: ·u5
D: S Europe; Africa: Asia; Cuba Rhipicephalus bursa
co
co
VH: sheep, goat a..
Part Ill. Parasites and parasitoses: metazoa

I··i
Table 14.5. Continued.
., , ':">'H'M ,-.n""-"'��\���

r,F":_:'.0t0�0..;hJi1: :titntD,W1t'!ID0'lrhil�1.ti
�(l-:m , ·: lf
' tiJ1B7®wi'm" �0
·ji ,•
,;..,ivJIJ�;,11 ,... -�., -
�G::l!w�@D�giftti'.tJ�fQ)
���- ·--��.:.:,/, •• __·1•1!!•' �-t/v"�•· -' � ,,,·-�- .. iS}� _..,!._,,,_t.._ .

Babesia capreoli A: babesiosis of wild ruminants IV: lxodes ricinus

D: Europe VH: roe deer, red deer, reindeer, others
Babesia venatorum H: accidental infection IV: lxodes ricinus
D: Europe: AT, CH, DE, IT A: babesiosis of wild ruminants VH: wild ruminants, human
Babesia caballi A: equine babesiosis IV: Europe: 0ermacentor marginatus,
D: S Europe; tropics; subtropics (except 0. reticulatus; C. Asia: 0. nuttalli, 0. silvarum;
Australia) New World: 0ermacentor f/\nocentor) nitens;
South Africa: Hyalomma truncatum
VH: squids
Babesia trautmanni A: porcine babesiosis IV: Rhipicepha/us turanicus, R. simus
D: Africa; S Europe, Russia VH: pig
Babesia perroncitoi A: porcine babesiosls IV: R. sanguineus?, 0. reticulatus?
D: Africa; Italy VH: pig
Babesia canis A: canine babesiosis IV: 0ermacentor reticu/atus
D: W, S and E Europe, foci in C. Europe, VH: dog, other canids
Asia
Babesia rossi A: canine babesiosls IV: Haemaphysalis leach/ (syn. H. elliptica)
D: Africa: South Africa, Sudan VH: dog, other canids
Babesia vogeli A: canine babeslosls IV: Rhipicephalus sanguineus
D: N, S America; Africa; Australia; Japan: VH: dog, other canids
S Europe
Babesia gibsoni A: canine babesiosis IV: Rhlplcephalus sanguineus, Haemaphysa/is
D: N Africa; America: Asia; Australia bispinosa
VH: dog, other canids
Babes/a conradae A: canine babesiosis IV: Rhipicephalus sanguineus?
D: California VH: dog
Babes/a annae5 A: canine babesiosis IV: /. hexagonus?
(syn. 8. vulpes, Theiler/a annae) VH: dog, fox
D: ES, PT, DE
Babes/a fells A: feline babesiosis IV: Haemaphysalis leach/ (syn. H. e/liptica)
D: S Africa
>------- ·--
VH: cat, other felids
Babes/a m/crot/-complex H: babesiosis IV: Europe:/. ricinus, I. trianguliceps;
D: N America: Asia (rarely Europe) A: rodent babesiosis N. America: /. scapularis; Japan: /. ovatus?
VH: rodents, human-
- --- ---· -----+-----'-- ---------l
B, duncanl H: accidental Infection IV: (not documented)
D:USA VH: human, no other host known
Pir�plasmlda: T_hellerlldae
Cytauxzoon fells A: feline cytouxzoonosls IV: USA: Amblyomma amer/canum,
D: N, S America Dermacentor varlabilis?
___ _ __ VH: wild fellds (lynx, �nther, e_uma), c_al _
Cytauxzoon sp. A: feline cytauxzoonosis IV: Dermacentor spp.? I. rlclnus?
Eur:_op��s. IT,£�. g_ti _ VH: ���c!_ls_ __
Thellerla annulata A: Mediterranean theileriosis IV: Hyalomma anatollcum
D: Mediterranean countries: Near and VH: cattle, water buffalo
Middle East; C. Asia to China----
Theiler/a orlentalls (syn. T. buffell) A: apathogenlc IV: Haemaphysa/1s spp.
D: Eurasia: Australia VH: cattle, water buffalo
Theiler/a mutans A: benign bovine theileriosis IV: Amblyomma variegatum
D: Sub-Saharan Africa; Caribbean
--- _ __ ------+ -VH_: cattle, African buffalo
Theiler/a parva 6 A: East Coast fever IV: Rhipicephalus appendiculatus
D: E, C Africa VH: cattle, African buffalo
Thellerla parva 6 A: Corridor disease IV: Rhlpicephalus appendiculatus
D: s, E, C Africa _____ _____ VH: cattle, African buffalo
Theiler/a lestoquard/ A: malign theileriosls of sheep, IV: Hyalomma anatolicum
(syn. T. hirc1) goat VH: sheep, goat
D: SE Europe; N Africa; Near and Middle
East
 14. Phylum Arthropoda (arthropods)

Table 14.5. Continued.

·r
�f. ,. l �--�.J),._.,.1.i\:.iJ.1 •�---...:,,lr1
1• ..�)\�
1,.iJ,_JL_..J. I II{,�1�/
, �tI�., , ·Ji/
· ·••1·1h� 1 �f
':
l�11i_;,. t.,111\1- ,,..:,;._' -{11\rtL•'.:!\'i:'."J•::O.:Ji,,�.',
' '1,...
,'t,,. · .�f<
:\ • '!fl. r"·: ·,.,,.� "
¥
-1.. ,
" -- ----�..-.,�
..
- ·-- ---✓ � - • � � ' _..._ ... ' ., .. - ._... •• • - �

Theileria ovis A: benign theileriosis of sheep, IV: Rhipicephalus bursa, R. turanlcus

D: S Europe; N Africa; Near and Middle goat VH: sheep, goat ca
East; S Russia ca
E
Theileria equi A: theileriosis of equids IV: Dermacentor marglnatus, D. reticufatus, Ol
(syn. Babesia eqw) Rhlpicephafus bursa, R. turanicus,
:,::::;
ca
Cf)

D: S Europe; tropics; subtropics (except Rhipicephafus spp., Hyafomma spp.;

Australia) S. America: R. (8.) micropfus 2
VH: equids
1 . / .i ·--
Helmlntha
' ,_.:

Fllarioidea
- -
Acanthochel/onema viteae A: rodent filartosis (model IV: Ornithodoros moubata
Infection!_ ___ -VH:----
Mer/ones
Cercopithlfilarla grassll A: apathogenlc IV: Rhlplcephalus sangulneus
(formerly: O/petalonema grassll) VH: dog
D: S Europe; Africa; S America
Dipetalonema dracunculoldes A: apathogenlc IV: Rhlp/cephatus sangulneus
D: Europe; Africa; Asia VH: d�g.!-. fo��yena
Macdonald/us oschel A: filarlosls of snakes IV: Ornlthodoros talafe, 0. puertoricensis
D: reptile husbandry VH: snakes
1 Abbreviations: N: North, E: East, S: South, W: West, C: Central.
2 Note that some pathogens are transmitted not only by ticks.
3 ? = epidemiological evidence, but vector role not secured.
4 Candidatus: preliminary taxonomic status for currently not cultivable organisms.
5 This species is genetically close to Theiler/a but lacks biological characteristics for the assignment to this genus.
6 Strains of T. parva differing in biology and epidemiology; markers for their differentiation currently not available; historically known as T.
parva parva, T. parva lawrenci.
C\:l
"O
0
cattle and dogs. In sheep, especially the ears are infested. America, East Africa from South Africa to Tanzania, Q.

The ticks are active in a Mediterranean climate mainly
from March to June and from September to November.
A generation usually develops in about 70-130 days. R.
turanicus prefers sub-humid to semi-arid habitats. The
distribution of the Palaearctic strains includes Central
and South Asia, as well as the Mediterranean coastal
regions up to 250 km inland. R. turanicus is endemic
in Iberia, southern France, Italy, Ticino/CH and in the
Balkans. The ticks are occasionally introduced to other
regions. R. turanicus is a major vector for Anaplasma
ovis, Rickettsia conorii, Babesia trautmanni, Theileria
equi(not the Afrotropical strain) and T. ovis(► Table
14.5).
■ Subgenus Boophilus
Bos(L): cow, ox, cattle; philos (G): friend; philein (G):
to love.
Rhipicephalus (Boophilus) microp/us and other
species
Morphology, species and occur rence. All five
species of the subgenus infest cattle and rarely other large
mammals(horses, sheep, wild ruminants) in the tropics
and subtropics. Important species are: Rhipicephalus
(Boophilus) microplus(cattle tick): Australia, Asia, Latin
Madagascar, recently spread to West Africa; R. (B.) .c
t::'.
decoloratus (blue tick): Sub-Saharan Africa; R. (B.) <{
annulatus (Texas fever tick): North Africa, belt south
of the Sahara from Senegal to Ethiopia, southern Europe,
Asia Minor, regionally in Latin America, earlier in
southern USA(► Figure 14.6),
Life cycle and epidemiology. All species of the
subgenus Boophilus are 1-host ticks and adapted to cattle.
Development on cattle from larvae to engorged females
lasts about three weeks, oviposition on the ground 1-2
weeks. Five to six generations per year may develop in
the tropics under favourable conditions (about 28 °C,
>80% r.h.).
Pathogenesis and clinical signs. Infestations cause
significant damage(meat, leather) in susceptible taurine
cattle and a high lethality in cases of severe exposure.
Over 800 million of the approximately 1,100 million
head of cattle worldwide are exposed to infestation
with Boophilus ticks. In the tropics, Boophilus ticks
are considered the most important parasites of cattle,
especially since they not only primarily harm the cattle
but also transmit pathogens causing serious infectious
diseases.
 Part Ill. Parasites and parasitoses: metazoa
Vector role. All Boophilus species transmit: Anaplasma
marginale; R. (B.) microplus, R. (B.) annulatus: Babesia
bovis; R. (B.) microplus, R. (B.) annulatus, R. (B.)
decoloratus: Babesia bigemina, B. microplus, Theileria
equi ( ► Table 14.5).
Genus Dermacentor
The genus Dermacentor comprises about 35 widespread
species in Asia, Europe, Africa and the New World.
The following species are mainly of interest as vectors
(► Table 14.4 and ► Table 14.5): D. marginatus and
D. reticulatus (see below); D. silvarum, D. nuttalli and
other species in Asia (Siberia, Mongolia, China); D.
andersoni, D. variabilis, D. occidentalis, D. albipictus
in North America; Anocentor nitens, the tropical horse
tick in Latin America, is usually assigned to the genus
Dermacentor as D. (A.) nitens.
Dermacentor marginatus (ornate sheep tick)
Derma (G): skin; centeo (G): to bite; margo (L): margin.
Morphology. The unfed � � are 4.6-5.4 mm long, the
oo 4.8-5.8 mm, and engorged females up to 15 mm.
Life cycle and epidemiology. D. marginatus is a
3-host tick. Larvae and nymphs infest mice, other small
mammals, rabbits and occasionally birds; adults infest
mainly sheep but also cattle, horses, dogs and humans
as well as cervids, rabbits and hedgehogs. Larvae are
active in the northern hemisphere particularly in June,
nymphs in July. In Central Europe, adult ticks have a
first activity peak in March and April and a lower one
in September and October. Blood-fed females enter
diapause in autumn and start to oviposit only in spring.
A generation usually develops within l year. Sheep
are therefore infested already from March on by the
overwintered adults (cf. lxodes ricinus). The predilection
sites of the ticks are neck and back where the wool turns
brownish due to the ticks' faeces.
Occurrence. D. marginatus is adapted to warm, dry
habitats ( <600 mm of precipitation per year; coldest
month on average �l 0C). This species colonises dry
grassland, scrubland and sparse forests. The distribution
Q)
area of D. marginatus extends from Morocco to Spain,
·u
C
'6 southern and central France, Italy, south-eastern Europe,
Q)
� Germany, Poland and further east to Central Asia. In
Central Europe, there are a few foci, especially in sheep
co pastures on sunny slopes.
C
·c
Q)
Vector role. D. marginatus is the most important
.£ vector of Coxiella burnetii in Europe. Further pathogens
>,
0)
that can be transmitted include: TBE virus (transmission
0
0
is possible, though not effectively, see Ixodes ricinus),
·u5 Anaplasma ovis (eastern Europe, Central Asia, other
vector also D. silvarum), Rickettsia slovaca, Francisella
co
a..
tularensis, Babesia caballi and Theileria equi ( ► Table
14.5).
Dermacentor reticulatus (ornate sheep tick)
Rete (L): net; reticulum (L): small net.
Morphology. Adults of D. reticulatus have - unlike
D. marginatus - a rear-facing spur on the second palp
segment. The coxae I have a tightly fitting large spur
outside. Since the morphology is unusually variable,
Dermacentor species have often been confused
(► Figure 14.6 and ► Figure 16.19, p. 553).
Life cycle and epidemiology. Larvae and nymphs
of D. reticulatus (3-host tick) infest small mammals
(rodents, insectivores, mustelids), rarely also birds;
adult ticks feed on wild mammals (cervids, foxes, hares,
hedgehogs) and domestic animals, especially dogs and
horses, in certain regions also on cattle and sheep and
occasionally on humans. The first peak of adult activity
is in spring (March to June), the second in autumn
(August to November). Females lay 3,000-4,500 eggs.
The generation time is 1 or 2 years.
Occurrence. D. reticulatus prefers humid forest and
meadow habitats. Its distribution area extends from
western, southern and Central Europe (ES, UK, FR,
IT, CH, AT, BE, DE, PL) eastward to Central Asia. In
central France, this species is the most common tick on
dogs, whereas R. sanguineus prevails in southern and the
lxodes species in northern France. In UK, D. reticulatus
occurs along the coast of south-west England and Wales,
where above all cattle are infested. Suitable habitats are
island-like foci in forests or along rivers. As a result
of introductions by dogs from endemic areas abroad
(Hungary, France, etc.), new foci have established, e.g.
in Germany and Switzerland. Suitable habitats have
probably been created due to abandoning or restoration
of agricultural land and undisturbed propagation of
hosts (small mammals, game).
Vector role. D. reticulatus can transmit the following
pathogens: Rickettsia slovaca, Francisel/a tularensis,
Babesia caballi, B. can is and Theileria equi ( ► Table
14.5).
Genus Hyalomma
Hyalos (G): glas; omma (G): eye.
The characteristic features of this genus (25 species)
include the eyes, to which the genus name refers. Species
of the genus Hyalomma are found in arid and semi­
arid regions of Africa, Asia and southern Europe. H.
anatolicum is an important vector for Theileria annulata,
T. equi and T. lestoquardi (► Table 14.5). There are
no autochthonous Hyalomma species in northern and
Central Europe, but larvae and nymphs are introduced

by migratory birds, adult ticks with turtles. These are
mostly H. marginatum (birds) or H. aegyptium (turtles).
Hyalomma marginatum
Large brown 2-host tick; length � � 5.0-6.5 mm,
engorged �20 mm; c3c3 4.0-5.6 mm with dark scutum.
Larvae and nymphs parasitise birds for a total of 12-26
days during which they may be transported far to the
north. In southern Europe, e.g. in Spain, adults infest
domestic animals, e.g. cattle, equines, dogs but also foxes,
wild boars and hares. The autochthonous distribution
area of H. marginatum extends across southern Europe,
almost all of Africa and South Asia. North of the Alps
(up to UK, DK, NL) only pre-adult stages have been
identified. H. marginatum transmits viruses (Crimean­
Congo fever, etc.), Babesia occultans and Theileria equi.
Hyalomma aegyptium
The 3-host tick H. aegyptium is morphologically similar
to H. marginatum. Adults infest mostly turtles, but also
lizards, hedgehogs, dogs and equids in southern Europe;
pre-adult stages mainly birds. H. aegyptium is adapted
to arid habitats, mostly in the resting areas of turtles.
Distribution areas: southern Europe, including southern
France; Africa (North Africa from Morocco to Egypt,
South Africa) and South Asia. The tick is very often
introduced with turtles to Central Europe, but has never
become indigenous. The species does not act as vector
in domestic animals or humans.
Genus Amblyomma
Amblys(G): blunt; omma(G): eye.
The most important of the approximately 140 species
of the genus Amblyomma (► Figure 14.6) occur in
Sub-Saharan Africa and in the New World in tropical or
subtropical, humid regions, but not in Europe. Important
species are: A. hebraeum(bont tick) in southern Africa,
particularly south of the Zambezi; A. variegatum
(tropical bont tick), eastern Central Africa and some
Caribbean islands; A. pomposum(highland bont tick),
Angola and western Central Africa; A. americanum(lone
star tick), USA, Atlantic coast to central Texas, north to
Iowa; A. maculatum(Gulf Coast tick), South Carolina
to Texas; A. cajennense(Cayenne tick), from southern
Texas to Argentina.
All Amblyomma species are 3-host ticks. They infest
many mammals, birds, reptiles and sometimes even
amphibians. In Sub-Saharan Africa, mostly heavy
infestations are seen in cattle, sheep and goats. Humans
are infested by larvae and nymphs on cattle pastures.
Most Amblyomma species cause painful skin lesions
(inflammation, necrosis, ulceration, granulomas, and
bleeding). This alone significantly affects performance
(meat, leather, milk). In South America, A. cajennense is
14. Phylum Arthropoda (arthropods)
a nuisance for horses that suffer greatly from the lasting,
extensive and very painful skin lesions. Humans are
mainly affected by nymphs, whose bites cause severe
itching and necrosis that heal only after months. Some
Amblyomma species are important vectors(► Table
14.5). co
cu
E
Family Argasidae (soft ticks) 0)
�
co
(/)
Argas (G): poisonous animal.
2
Summary
• Morphology and ,,,.cl••• lrnportaM genera: Atga!J,
Ornlthodoros and Otoblus. In central and northern
Europe, only Argss refleJ<Us (pigeon ttei<) Is o1
elgnlflcance. Soft tick• nave no soutum and differ In
other morphological and blologloal characteristics from
hard ticks.
• Life cycle. Egg - larva --; mostly 4• 7 (minimum 2;
maximum 8) nymphal etagee -. adults. Blood feeding
usually lasts enly 20-30 min.
• Occurrence, adverse effects. Argasldae are primarily
found In arid, southern reglor:is, eome species In
temperate zones of the northern hemisphere. A.
reflexus, highly adapted to house pigeons, can be
found In coeler climates of Europe only In buildings,
not outdoors. l'he species continues to be a nuisance,
affecting occasionally other bird species (wild birds,
chicken) and mammals (e.g. horses, humans). A.
reflexus has no role as a c::arrler of pathogens, but other
species are vectors; some species cause toxicoses. co
-0
0
Q.
The family Argasidae includes three subfamilies with a ..c.
t
certain medical importance: Argasinae, Ornithodorinae <(
and Otobinae( ► Table 14.2).
Morphology. Soft ticks have no scutum, males and
females hardly differ morphologically(► Table 14.3;
► Figure 14.9). The capitulum is ventral and not visible
from above, except for the larvae which have a terminal
capitulum. The claws of nymphs and adults have no
pu1villi, but they are present in larvae of some species
and allow them to climb up on smooth surfaces, such as
glass vessels( ► Figure 14.10). The small stigmata! plates
are anterior to the fourth pair of legs. Eyes are absent
in most species. The cuticle is leathery and structured.
Q)
T5
C
Life cycle and occurrence. Soft ticks usually have '5
4-7(also 2-8) nymphal stages, each of which infests a host �
Q)
and sucks blood. Moulting to the next nymphal or to the
adult stage occurs in the environment. Like hard ticks, C
co
·;:::
soft ticks are also 'pool feeders'; they rapidly ingest a large Q)
amount of blood and thereby increase their body weight
up to 12-fold. Excess fluid is excreted through coxal C
glands which end near the coxae I. Adults can repeatedly >,
CT>
suck blood. After blood feeding, which lasts only 20-30 0
0
min(rarely a few hours), the ticks leave the host. Later, :t=
Cl)
the females lay up to 500 eggs. The larvae of Argas spp.
attach to the skin of their host for about 1 week; they take
co
Cl..
Part Ill. Parasites and parasitoses: metazoa
Dorsal surface with
protuberances
(mammillae)
Dorsal view
Figure 14.9. Scheme of Argasidae as exemplified by Argas (Graphics: IPZ, A. Seeger; after Walker et al. 2003).
r,
Figure 14.10. Argas ref/exus: (a) dorsal view; (b) ventral view (length: 6.5-11 mm); (c) larva (Photo: IPH).
only one blood meal. Larvae of Ornithodoros spp. and
adults of Otobius megnini do not ingest food. Argasids
occur worldwide, but the medically important species
are restricted to certain regions (see below). Almost
all species are adapted to arid habitats that are in the
vicinity of their hosts: birds' nests, dovecots, caves, etc.
Some soft ticks, which have a total life span of up to 14
years, can survive in their habitat for 5-7 years without a
host. With these enormous physiological achievements,
some Argasids are true survival specialists.
• Subfamily Argasinae
GenusArgas
Argas reflexus (pigeon tick)
Morphology. Females of the pigeon tick (length 6.5-1l
mm) are dorsoventrally flattened and gray to red-brown
(► Figure 14.l0a, b). The dorsal surface has a fringe,
separated by a suture, with ridges radiating outwards.
The cuticle is granulated and bears dorsally numerous
differently sized discs (mammillae). Males are similar
to females, but are usually smaller (5-7 .5 mm long);
they can be differentiated on the basis of the genital
\ Mouthparts
•
- �
.'
o, . Genital opening
Stigma
Anus
Ventral view
opening, which is absent in nymphs (3.5-6.5 mm long).
Larvae have a terminal capitulum and very long legs
(► Figure 14.l0c).
Life cycle. Copulation takes place away from the
host after each blood feeding (► Figure 14.11). After
each blood meal, females lay a batch of about 80 eggs
in hideouts near the hosts. The duration of the entire
developmental cycle with 2-4 nymphal stages depends
on the availability of hosts and the microclimate in the
habitat; favourable conditions are about 30 °C and S0-
80% r.h. Usually, a generation develops in 2-3 years.
Occurrence and epidemiology. This tick which
originated from warmer regions can be found in
cooler climates in Europe only in buildings and similar
microhabitats, where high summer temperatures are
ensured. Therefore, the northern distribution limit
in Europe is 55° N. The domestic pigeon (Columba
livia domestica) is the main host for all stages of A.
reflexus. Other rare hosts are further species of pigeons,
swallows, swifts, barn owls, jackdaws, sparrow birds and
occasionally the domestic chicken. Humans and horses
in contact with habitats of A. reflexus are also affected.
 14. Phylum Arthropoda (arthropods)

C'O
Actldental host co
E

"o
0)
-:;:::;
(/)
C'O

�
Egg

Blood
Moulting to
adults ]
�Larva

feeding
Blood

Moulting to Moulting to 1
nymph 4 nymph1 �

Moulting to (\ /Blood
nymph 2 \ ), ing
., � co
. "'O

�-�/':>,r�
0

e
Q.

.c
t
<(

Figure 14.11. Developmental cycle of Argas ref/exus (Graphics: IPZ, S. Ehrat).

The nesting and resting places of pigeons in dovecots,
neglected attics, old or decaying buildings with warm,
dark hideouts are the preferred habitats in which the
pigeon ticks hide during daytime. At night, they attack
their hosts, taking blood for about 20-30 min and
then immediately retreat to their hideouts. The larvae,
however, remain on the host for about 1 week and can be
effectively disseminated. Unfed larvae survive for at most
the development of a generation is estimated to take 3-11
years. Nevertheless, thousands of nymphs and adults
can be found in inhabited buildings, particularly in big
cities. After expulsion of pigeons from their nesting sites,
the pigeon ticks, in search of hosts, can invade adjacent
inhabited rooms and attack humans, especially during
the active phase in spring and summer. In Berlin, pigeon
(l)
ticks were found in about half of the inhabited nesting T5
C

1 year, nymphs and adults in contrast survive starvation places and in 14% of empty nests, some of which had '5
periods of 3-5, at the most 9 years. A. reflexus has the been abandoned for years. �
(l)

lowest net water loss rate of all arthropods tested to date cco
and is also highly tolerant of extreme temperatures, Pathogenesis and clinical signs. In pigeons and C
including frost. This ensures survival in dry attics where other birds, ticks preferentially bite at featherless sites on ·;;::

enormous temperature fluctuations occur. The higher the inner surface of the thighs, under the wings and at
temperatures in buildings from spring to autumn allow the neck. Red-blue, bloodshot wheals form at the biting C

completion of the embryonic development of the ticks site (0 about 1 cm). Pigeons are restless at night, are >.
0)
which then enter diapause. Eggs cannot hibernate. devitalised and have a poor flight performance. In case 0
0
Therefore, development of a larger Argas population of repeated infestations, the considerable blood loss (up ·u;
in a building lasts a few years, even under favourable to 0.3 ml per blood meal) can lead to life-threatening
co
conditions. Because of diapause in each post-larval stage, anaemia and death in nestlings and young birds. 0...
 Part Ill. Parasites and parasitoses: metazoa

Diagnosis. Upon suspicion, illuminate and inspect

nesting or resting places of pigeons. Black faecal stains
and white-yellow exuviae (shed cuticle) in hideout areas
are reliable indicators for the presence of pigeon ticks.

Control. Control by drastically reducing the populations

of feral pigeons in cities and repeated treatment of
hideout areas of the pigeon ticks with acaricides by
pest controllers. Recolonisation should be prevented Figure 14.12. Ornithodoros moubata: female with eggs (Photo:
by introducing structural measures to keep out pigeons IPZ).
and eliminate hideouts.

Significance for humans. In humans, the almost
always nocturnally occurring tick bites cause itchy
papules with local erythema (mild form) or mild to
severe local skin swelling, lymphangitis, and fever
caused by an allergy (delayed type IV). An IgE-mediated
allergy (immediate type I) can lead to high-grade disease
with urticaria, bronchial obstruction and possibly
unconsciousness. The bites leave small scars which
persist for a long time.
Argas (Persicargas) persicus (chicken tick)
This species, whose original distribution area is in the
south of the Palaearctic region, has been dispersed
with chickens to all other zoogeographical regions
(probably except the Neotropical region), including
southern Europe. A. (P.) persicus may occur in high
density in poultry houses and cause losses due to the
painful bites and heavy blood consumption (vector role,
► Table 14.5). The larvae of the species of the subgenus
Persicargas can cause toxicosis (severe paralysis) and
transmit Borrelia anserina and Anaplasma pullorum.
- Subfamily Ornithodorinae
Genus Ornithodoros
0rnithes (G): birds; dory (G): lance, spear (according to
other sources doros [G]: leather pouch).
humans there; another strain lives in caves or resting
places of mammals (warthogs, anteaters, porcupines).
During the day, these soft ticks hide in dark hideouts,
even in clothes of people who thereby spread the ticks
(► Figure 14.12).
0. moubata and other synanthropic 0rnithodoros spp.
( 0. moubata complex) are vectors of the causative
agent of endemic relapsing fever, Borrelia duttonii, in
humans ( ► Table 14.5). The borreliae persist in the tick
population by transstadial and transovarial (= vertical)
transmission for at least 5 generations. Only nymphs
transmit borreliae with their saliva; adults release them
in the secretions of the coxal glands onto the skin of
the host.
Ornithodoros moubata porcinus
0rnithodoros moubata porcinus transmits the African
swine fever virus (ASFV) in a sylvatic cycle in
warthogs. ASFV replicates in the intestinal epithelium
of the ticks and is transmitted in the tick population
transstadially and transovariaHy as well sexually with
the spermatophores of males. ASFV also is transmitted
by 0. erraticus. Occurrence: north-western Africa and
in semi-arid regions of the Iberian peninsula (in the
south of Portugal, in the Spanish provinces of Salamanca,
Badajoz, Huelva).
Other Ornithodoros species

The genus 0rnithodoros differs from the genus Argas by 0rnithodoros savignyi (eyed tampan or sand tampan)
a highly wrinkJed integument, the absence of the suture has 2 pairs of simple eyes posterior to the coxae I and
on the body edge and other characteristics ( ► Figure coxae III and IV. Occurrence: in arid regions of Africa,
14.12). Development: egg -+ larva -+ 151 -5111 nymphal
Q)
Arabia, India and elsewhere, hides in the sand or in the
·u
C:

'6 stage -+ adults. The larvae do not feed but moult, ground at resting places of camels, cattle, equines and
Q)
� usually still in the egg integument, directly to the first humans in order to infest them; not considered a vector.
c nymphal stage. 0rnithodoros hermsi, 0. coriaceus, 0. parkeri and 0.
ell
C: turicata in some regions in the USA or South America
·.::
Ornithodoros moubata (eyeless tampan) of rather minor importance. Other 0rnithodoros species
transmit filariae, e.g. of snakes (Macdonaldius oschei)
C: 0rnithodoros moubata is of particular medical and in terrariums.
>,
0)
veterinary importance as a vector. Occurrence: several
0
0
subspecies and strains with different epidemiology in
·u5 arid and semi-arid areas of southern Africa. A strain
ell
ell
of 0. moubata inhabits huts and affects chickens and
Q._

• Subfamily Otobinae
Otobius megnini occurs in North America, Africa and
India. Females are not parasitic and do not feed; they
Jay eggs in hidden places in stables; the larvae infest
hosts, especially horses and cattle, and colonise the ear.
After a few weeks or months, nymphs leave the host and
continue to develop in the environment.
c::"1-----•
Selected references
Angelakis E, Raoult D (2011) In: Palmer SR, Lord Soulsby,
Torgerson PR, Brown DWG (eds.) Oxford Textbook of
Zoonoses. 2nd ed. Oxford, UK: Oxford University Press,
pp. 92-101; ISBN 978-0-19-857002-8.
Bowman AS, Nuttal PA (eds.) (2008) Ticks: biology, disease
and control. New York: Cambridge University Press; ISBN
978-0-521-86761-0.
Chomel B (2011) Tick-borne infections In dogs - an emerging
infectious threat. Vet Parasitol 179: 294-301.
Dante-Torres F, Chomel BB, Otranto, D (2012) Ticks and tick­
borne diseases: a one health perspective. Trends Parasitol
28: 437-446.
Dautel H, Dippel C, Kammer D, Werkhausen A, Kahl 0
(2008) Winter activity of lxodes ricinus in a Berlin forest. Int
J Med Mirobiol S1: 50-54.
Dobler G, Aspock H (2010) Durch Zecken ubertragene Arboviren
als Erreger von lnfektionen des Menschen. In: Asp6ck H (ed.)
Krank durch Arthropoden. Denisia 30: 467-499.
Estrada-Pena A, Bouattour A, Camicas JL, Walker AR
(2004) Ticks of domestic animals In the Mediterranean region.
Houten, the Netherlands: Atalanta; ISBN 84-96214-18-4.
Gigandet L, Stauffer E, Douet V, Rais 0, Moret J, Gern
L (2011) Prevalence of three zoonotlc Babes/a species in
lxodes ricinus (Linne, 1758) nymphs In a suburban forest In
Switzerland. Vector Borne Zoonotlc Dis 4: 363-366.
Gray J, Dante-Torres F, Estrada-Pena A, Levin M (2013)
Systematics and ecology of the brown dog tick, Rhlpicephalus
sanguineus. Ticks Tick Borne Dis 4: 171-180.
Hildebrandt A, Franke J, Meier F, Sachse S, Dorn W, Straube
E (201O) The potential of migratory birds in transmission of
Babesia spp., Anaplasma phag ocytophilum, and Ricketts/a
spp. Ticks Tick Borne Dis 1: 105-107.
Hillyard PD (1996) The ticks of north-west Europe. In: Barnes
RSK, Crothers JH (eds.) Synopses of the British Fauna (New
Series), No. 52. London, UK: The Natural History Museum;
ISBN 1-85153-2579.
Hubalek Z, Rudolf I, Nowotny N (2014) Arboviruses pathogenic
for domestic and wild animals. Adv Virus Res 89: 201-275.
Hubalek Z, Rudolf I (2012) Tick-borne viruses in Europe.
Parasitol Res 111 : 9-36.
Jongejan F, Kaufman WR (eds.) (2003) Ticks and tick-borne
pathogens. Dordrecht, the Netherlands: Kluwer Academic
Publishers; ISBN 1-4020-1450-3.
Jonsson NN, Piper EK, Constantinoiu CC (2014) Host
resistance in cattle to infestation with the cattle tick
Rhipicepha/us microplus. Parasite lmmunol 36: 553-559.
14. Phylum Arthropoda (arthropods)
Kiewra D, Lone E (2012) Epidemiological consequences of
host specificity of licks (lxodida). Ann Parasitol 58: 181-187.
Medlock JM, Hansford KM, Bormane A, Derdakova M,
Estrada-Pena A, George JC, Golovljova I, Jaenson
TG, Jensen JK, Jensen PM, Kazlmlrova M, Oteo JA,
Papa A, Pfister K, Plantard 0, Randolph SE, Rizzoli
A, Santos-Sliva MM, Sprong H, Vial L, Hendrickx G ,
ro
Zeller H, Van Bortel W (2013) Driving forces for changes �
O>
in geographical distribution of lxodes ricinus ticks in Europe. ro
(/)
.I
Parasit Vectors 6: 1.
Norval R, Horak IG (2004) Vectors: ticks. In: Coetzer JAW, Tustin
RC (eds.) Infectious diseases of livestock. 2nd ed. Oxford,
UK: Oxford University Press, pp. 3-42; ISBN 0-19-576169-3.
RarV, Golovljova I (2011)Anap/asma, Ehrlich/a, and 'Candidatus
Neoehrllchla' bacteria: Pathogenicity, biodiversity, and
molecular genetic characteristics, a review. Infect Genet
Evol 11: 1842-1861.
Reuben Kaufman W (2010) Ticks: physiological aspects with
Implications for pathogen transmission. Ticks Tick Borne
Dis 1:11-22.
Rizzoli A, Silaghl C, 0blegala A, Rudolf I , Hubalek Z, Foldvari
G, Plantard 0, Vayssler-Taussat M, Bonnet S, Spltalska
E, Kazimirova M (2014) lxodes ricinus and Its transmitted
pathogens in urban and peri-urban areas in Europe: new
hazards and relevance for public health. Front Public Health
2:251.
Salman M, Terres-Call J (eds.) (2012) Ticks and tick-borne
diseases. Geographical distribution and control strategies
In the Euro-Asia region. Wallingford, UK: GABI Publishing;
ISBN 978-1-84593-853-6. ell
Sonenshlne DE (1991, 1993) Biology of ticks (2 volumes). New "O
0
York, NY, USA: Oxford University Press; ISBN 0-19-505910-7 a.
and 0-19-508431-4. .c.
t
Wall A, Shearer D (2001) Veterinary ectoparasites: biology, <(
pathology, and control. 2nd ed. Oxford, UK: Blackwell
Science: ISBN:0-632-05618-5.
Walker A (1994) Arthropods of humans and domestic animals.
A guide to preliminary identification. London, UK: Chapman
& Hall; ISBN 0-412-57280.
Walker AR, Bouattour A, Camicas JL, Estrada-Pena A,
Horak IG, Latif AA, Pegram AG, Preston PM (2003)
Ticks of domestic animals in Africa: a guide to identification
of species. Houten, the Netherlands: Atalanta; ISBN
0-9545170-0-X.
 Part Ill. Parasites and parasitoses: metazoa
14.1.2 Order Mesostigmata (syn.
Gamasida)
Meso- (G): middle; stigma (G): scar, spot. Refers to the
location of the stigmata.
Of this order, especially the genera Dermanyssus and
Ornithonyssus are important as ectoparasites of poultry.
Main characteristics of the species: mostly large (::;2 mm),
long-legged and very actively moving mites; pretarsus
with adhesive pad (pulvillus) and double claw; stigmata
between coxae III and IV (hence Mesostigmata); larvae
without stigmata (respiration through cuticle); thin
cuticle dorsally and ventrally reinforced by mostly
species-specifically shaped plates; elongated gnathosoma
I•
with 2 palps and retractable, slender chelicerae with
terminal scissors (chelae).
Family Dermanyssidae
This family includes Dermanyssus gallinae and
Liponyssoides sanguineus which are obligate haemato­
phagous, temporary ectoparasites of birds and mammals.
Genus Dermanyssus
Dermanyssus gal/inae (chicken mite, red mite)
Disease: Dermanyssosls in poultry. ti
Derma (G): skjn; nyssein (G): bite.
Summary
• Dermanyssus gall/nae Is a common ectoparaslte of
birds, especially In chicken flocks.
• Morphology. Females with long, stiletto-shaped
chellcerae; unfed flat-oval, grey-white: after blood
feeding cylindrical In shape, dark blue to black: length
0.7 to at,out 1 mm, depending on tht degrH of
engorgement,
• Development In the vicinity of the host from egg -
larva -+ 2 nymphal stages .... adults. Larvae take no
food, the other stages are obligately haematophagous;
the mites usually Infest their host only at night. The
0) development of a generation lasts only 7 days under
C primarily chickens worldwide, often other commercial
·o favourable conditions. Adults can survive without
'6 feeding for several months.
0)
� • Occurrence, epidemiology. D. gall/nae Infests primarily
chickens wor1dwlde, but also many other species of
co
C birds. In Intensive farming of chickens In stables, there
·;;::
0) are favourable conditions year-round: often explosive
propagation. Introduction of mites Into flocks mostly
C with Infested wild birds, but also with poultry, persons
>, and objects.
Ol
0 T
0
·u;
co
co
0...
Clinical signs, adverse effects. Bites of o. gallinae
cause considerable itching. Symptoms: among others
restlessness, nervousness, damage to the plumage,
anaemia (pale combs), reduced performance (egg
laying, fattening); high economic damage.
• Diagnosis. Detections of mites in their hideouts or on
the animals, at necropsy in the mucus of the beak cavity
or in the ear canal. Differential diagnosis: Ornithonyssus
sylviarum.
Control. Empty stables: thorough cleaning and, if
necessary, use of acaricides. Treatment of utilised
stalls often unavoidable, especially in laying hen farms:
spraying the environment of the animals (cages, nest
boxes, feeders, etc.) with phoxim (2,000 ppm, 2x
with Interval of 7 days, withdrawal period must be
observed) or spinosad ( ► p. 611). Alternative: mite
traps impregnated with an acaricide.
• Zoonotic Importance. D. gal/inae infests humans and
occasionally other hosts (dogs, cats, rabbits, horses,
etc.) and causes bite reactions.
Morphology. Females are unfed flat-oval, grey-white
and about 0.7 mm long; after ingestion of host blood
cylindrical, dark red to black blue and about l mm long.
They have long, stiletto-shaped chelicerae with tiny
chelae that are visible only under high magnification.
The anal plate is about as wide as long; the anus lies in
the posterior half ( ► Figure 14.13). Males have only a
single ventral plate. Eggs about 400x260 µm.
Life cycle. D. gallinae is a temporary ectoparasite
of chickens and other birds. Development takes place
in the environment of the hosts and proceeds from
the egg through a larval stage and two nymphal stages
(protonyrnph and tritonymph) to adults. Nymphs and
adults are haematophagous; they infest their hosts almost
only at night and suck blood for½ to l½ h; larvae do not
feed. After a blood meal, females lay a few eggs. Under
favourable conditions (e.g. in chicken houses at 20-25 °C
and 70% r.h.) the development of a generation takes only
7-12 days. Temperatures below -20 °C or above +45 °C
are fatal for D. gallinae. Adult mites can survive at low
temperatures for 5-9 months without feeding.
Occurrence and epidemiology. D. gal/inae infests
poultry (turkey, goose), pigeons, caged birds, many
wild birds (sparrows, starlings, etc.) and occasionally
mammals (horses, dogs, rabbits, etc.) and humans if
no birds are available. D. gallinae is the most common
and most damaging ectoparasite in poultry facilities,
which under intensive farming conditions often provide
year-round favourable conditions for development of
the parasite. The mites stay in hideouts (under perches,
in cracks and crevices in the nests, etc.) during the day
and attack the hosts at night for blood feeding. At high
density, however, some mites also remain on their hosts
during the day. The following prevalences in chickens
 14. Phylum Arthropoda (arthropods)

I
co
Cheli co
E
CJ)
·..::;
(/)
0
(/)
Q)
Genital opening ----➔,,r.lL+.!,I� 2

Fi gure 14.13. Dermanyssus gallinae �: dorsal and ventral view (Graphics: IPZ, A. Seeger; after Baker et al. 1967).

under different farming conditions were found in some
European countries (DK, FR, NL, UK): cage rearing
up to 87%, barn system up to 83%, free ranging hens
up to 80%.
At stable temperatures of 20-25 °C, a female lays a total
of about 300 eggs. At lower or higher temperatures,
fewer eggs are laid and at larger intervals. Development
and survival rate are favourable at 70-90% r.h. and 20-
37 °C (max. lifetime of females up to about 5 months,
of protonymphs up to 6 months). At 5 °C, few mites
survive nine months without feeding. The mites are very
susceptible to low air humidity. Introductions of mites
are possible via infested wild birds, poultry, persons
or objects.
Clinical signs and adverse effect. Bites of D.
gallinae are painful and cause considerable itching.
Symptoms of infestation include restlessness and
nervousness, skin irritation, secondary injuries, damage
to the plumage and feather loss (caused by constant
picking at mites); in case of severe infestation anaemia
(pale combs) of unknown origin (probably not only
blood loss, but also inhibition of erythropoiesis);
reduced performance (egg laying, fattening); apathy,
weight loss and cachexia; furthermore, rhinitis, otitis
externa, conjunctivitis (caused by invading mites);
increased mortality in the flock.
can be infected with salmonella (Salmonella enteritidis)
under natural conditions and remain carriers for a longer
period of time.
Diagnosis and control. D. gallinae is best detected
macroscopically or with a magnifying glass in hiding co
-0
places (bearing areas of the perches, corners of cages 0
0.
and nests, cracks and crevices in walls) and also directly 0
on the chickens in the morning shortly after the end of ..c:
t'.
the dark phase. At high mite abundances, females and <{
nymphs may be aggregated into clumps in hiding places.
Necropsy: dead mites in the mucus of the beak cavity,
rarely in ear canal or in plumage. Special procedures
using mite traps have been developed for quantifying
mite density and determining the population dynamics
in flocks. Differential diagnosis: Ornithonyssus sylviarum
(► p. 422). Control ► p. 611.
Zoonotic importance. Other than birds, D. gallinae
also infests dogs, cats, horses, humans and other hosts
that have contact with the hiding places of the mites.
The very mobile mites can rapidly abandon bird nests
Q)
(sparrows, pigeons, etc.) after fledging of the nestlings C
"c:5
and migrate into apartments over larger distances, where '5
Q)
pets and people are affected. Itchy erythema and papules �
develop especially on the trunk and limbs. People �
working in chicken houses are particularly vulnerable. Cl:)
C
·;;::
Q)

The economic damage caused by D. gallinae is estimated

j
C
to be high, e.g. annually€ 11 million in NL. D. gallinae >,
0)
can transmit various virus and bacterial species under 0
0
experimental conditions, but an epidemiological
significance for most pathogens has not been
·en
demonstrated. However, it is documented that the mites
Part Ill. Parasites and parasitoses: metazoa
Genus Liponyssoides
Liponyssoides sanguineus
(syn. Allodermanyssus sanguineus)
Liponyssoides sanguineus (house mouse mite) is very
similar to D. gallinae; it occurs on house mice, brown
rats and other wild rodents in Europe, Africa, Asia and
North America. The mites can cause skin irritation in
humans and transmit Rickettsia akari, the causative
agent of rickettsial pox.
- Selected references------•
Huber K, Zenner L, Bicout DJ (2011) Modelling population
dynamics and response to management options in the poultry
red mite Dermanyssus gallinae (Acari: Dermanyssldae). Vet
Parasitol 176: 65-73.
Harrington D, Robinson K, Guy J, Sparagano O (2010)
Characterization of the immunological response to
Dermanyssus gallinae Infestation in domestic fowl.
Transbound Emerg Dis 57: 107-110.
Moro CV, De Luna CJ, Tod A, Guy JH, Sparagano OAE,
Zenner L (2009) The red poultry mite (Dennanyssus gallinae):
a potential vector of pathogenic agents. Exp Appl Acarol
48: 93-104.
Nordenfors H, Hoglund J (2000) Long term dynamics of
Dermanyssus ga/linae in relation to mite control measures
in aviary systems for layers. Brit Poultry Sci 41: 533-540.
Sparagano OA, George DR, Harrington DW, Gianaspero
A (2014) Significance and control of the poultry red mite,
Oermanyssus gall/nae. Annu Rev Entomol 59: 44 7-466.
Zenner L, Bon G, Chauve C, Nemoz C, Lubac S (2009)
Monitoring of Dermanyssus gall/nae In free-range poultry
farms. Exp Appl Acarol 48: 157-166.
Family Macronyssidae
Summary
• Mites of this family are etatlomuy, obligate haemato­
phagous parasites; there are 2 genera of veterinary
Importance: Omlthony,sus (0. sylv/arum, 0. bacotl,
O. bursa) in mammals and birds and Ophlonyssus
(0. natrfcls) In reptiles.
• Of these species, O. syfvlarum has the greatest
Importance as a parasite of gallinaceous birds; this
species must be considered In the diff81'8ntlal diagnosis
of Dermanyssus gall/nae.
Genus Ornithonyssus
Ornithonyssus sylviarum (northern fowl mite)
Disease: Ornithonyssosis in poultry'. I
0rnis (G): bird; nyssein (G): to bite.
Morphology and life cy cle. Females are 0.5-0.8
mm long, depending on the degree of engorgement.
0rnithonyssus sylviarum differs from Dermanyssus
gallinae by the conspicuous chelae (scissors) on the
chelicerae and the longitudinal-oval anal plate with the
anus in its front half. In contrast to D. gallinae, the entire
development of 0. sylviarum from egg to 2 nymphal
stages to the adults takes place on the host and takes only
5-12 days. Eggs (about 300 µm in length) are deposited
in lumps at the base of the feathers, especially in ventral
areas. In the developmental stages, only protonymphs
and adults take blood meals, whereas larvae and
tritonymphs do not feed. The mites survive only 1-5
weeks off the host.
Occurrence and epidemiology. 0. sylviarum is an
important ectoparasite of poultry, especially chicken, in
Europe, North America, Australia and New Zealand,
and also in other regions. Wild birds are reservoir hosts,
mammals are transiently infested. The prevalences of 0.
sylviarum in poultry in Europe are not known.
Clinical signs and adverse effect. Severe
infestations can lead to itching, swelling or incrustation
of the skin, worsening of feather conditions and loss,
weakness, anaemia, weight loss and loss of performance
(eggs, fattening).
Diagnosis. Macroscopic detection (magnifying glass)
of mites and their eggs on feathers, especially in the
abdominal area, or microscopic examination of feather
samples. Differential diagnosis: Dermanyssus gal/inae.
Control. Disinfestation of the barn before restocking
(see Dermanyssus) and measures against the introduction
of mites. Treatment with phoxim, as recommended
for Dermanyssus infestation (see above), could also
sufficiently reduce 0rnithonyssus infestations.
Ornithonyssus bacoti (tropical rat mite) tl
0. bacoti occurs not only in the tropics, but worldwide in
mice, rats, hamsters, gerbils, many wild rodents, and also
in dogs, cats and birds. This mite is usually introduced
to pet animals through purchases from breeding farms
or pet shops, but also by wild rodents. The most striking
symptoms in domestic rodents are restlessness, rough fur
- 14. Phylum Arthropoda (arthropods)
and itching. All developmental stages take a blood meal
on their host animals which lasts for a maximum of 20
min and mainly takes place at night. After blood feeding,
the mites often retract into a hiding place near their
hosts. The developmental cycle takes about l -2 weeks
in apartments; therefore, large mite populations build
up within a few months. Adult, fully engorged females
are approximately 0.6-l.l mm long, males are slightly
smaller. 0. bacoti can be differentiated from closely
related species (e.g. 0. sylviarum) using morphological
features.
Mites on animals are controlled with different acaricides
approved for the affected species. In addition, infested
apartments must be disinfested, which can cause
significant costs and potentially also liability claims
against the seller of the animals.
Even if suitable host animals are present, humans
and other hosts may be infested. Typical symptoms
are intensely itchy, erythematous papules arranged in
groups. In particular, children with close contacts with
their pets are often affected.
0rnithonyssus bursa (tropical fowl mite)
0rnithonyssus bursa is found almost exclusively in the
tropics and subtropics in chickens, pigeons and other
birds.
Genus Ophionyssus
0phionyssus natricis (common snake mite) fJ
0phis (G): snake; nyssein (G): to bite.
Adults of 0. natricis are large (0.6-1.3 mm long), unfed
yellowish brown and blood-fed red to blue-black. After
uptake of blood, females lay eggs in the terrarium or in
nearby hiding places. The entire development takes 2-3
weeks. Blood-fed females can survive 5-6 weeks without
host. 0. natricis is worldwide the most common and
most pathogenic ectoparasite of snakes in pet shops, zoos
and private animal husbandry; lizards are also affected.
Newly acquired snakes should be carefully examined
and, in case of a tentative diagnosis, be isolated, treated
with fipronil and kept in disinfested containers (see
references).
Zoonotic importance. Mites of the genera
0rnithonyssus and Ophionyssus also affect humans and
cause itchy, mostly papular skin lesions, and in children
also vesicular exanthema as well as secondary effects
due to scratching. Limbs and trunk are mainly affected.
Selected references cw-=------
Mullens BA, Owen JP, Kuney DR, SzijJ CE, Klingler KA (2009).
Temporal changes in distribution, prevalence and intensity
of northern fowl mite (Ornithonyssus sylviarum) parasitism
in commercial caged laying hens, with a comprehensive co
economic analysis of parasite impact. Vet Parasitol 160: E
116-133. 0)
:;::;
(/)
Owen JP, Delany ME, Cardona CJ, Bickford AA, Mullens 0
en
BA (2009) Host inflammatory response governs fitness in Q)
�
an avian ectoparasite, the northern fowl mite (Ornithonyssus
sylviarum). Int J Parasltol 39: 789-799.
Pizzi R, Meredith A, Thoday KL, Walker A (2004) Ornithonyssus
bacotl Infestation on pets In the UK. Vet Rec 154: 576.
Family Halarachnidae
Hals, gen. halos (G): salt, grain, sea; arachne (G): spider.
Refers to Halarachne (seal mite).
Summary
• Mites 1111 the respiratory tract or ear canal at mammals.
• Life cycle of species af the subfamily Halarachnldae:
larvae are active, proto- and deutonymphs on the other
hand are Immobile stages that do not Ingest feed.
Genus Pneumonyssoides
co
Pneumonyssoides caninum (canine nasal mite) "O
0
Cl.
Pneuma (G): air, wind, breath; nyssein (G): to bite.
Adult mites l-1.5 mm long, cream-coloured, highly
mobile, with long, 5-segmented palps, but short
chelicerae. Parasitic in the nasal passages and sinuses
of dogs in North America, South Africa, Australia and
Europe, there especially in Scandinavia (prevalence
in Sweden 20%), but only sporadically in central and
southern Europe. Transmission probably by direct
contact with infested dogs. Foxes and cats are not
affected. Pathogenesis and clinical signs: usually only a
mild, transient rhinitis (sneezing, sniffling, coughing,
nasal discharge, etc.) with normal general condition.
Diagnosis: detection of mites in nasal secretions or by
using endoscopy. Treatment: selamectin (6 mg/kg b.w.
spot-on) 3x in 2-weekly intervals or milbemycin oxime
(2 mg/kg p.o.) 3x interval of 7 days.
 Part Ill. Parasites and parasitoses: metazoa
Genus Pneumonyssus
Pneumonyssus simico/a (lung mite of
monkeys)
P. simicola is a parasite in the lungs of monkeys, especially
rhesus monkeys (Macaca mulatta). The mites live in
groups in tubercle-like nodules containing pigment.
Direct transmission from animal to animal by coughing
and sniffling. The infestation is usually unapparent.
Genus Raillietia
Raillietia spp. (ear mites)
A. Railliett, French parasitologist, 19. Century; auris
(L): ear.
R. auris parasitises the ear canal of livestock bovines,
especially of cattle in North and South America,
Australia and Europe (prevalence in Italy about 20%).
The oval, about 1 mm long mites live near the tympanic
membrane under a plug consisting of inflammatory
products and probably feed on epidermal cells, but
not on blood. The infestation is usually unapparent
and is rarely associated with an otitis media which is
often purulent. Clinical signs: include continuous head
shaking, head tilt, disturbance offeed uptake. Treatment:
flumethrin 1 %, apply 3 ml directly into the ear canal.
R. caprae in goats (USA, Central and South America).
Family Rhinonyssidae
Of the Rhinonyssidae, Sternostoma tracheacolum
(tracheal mite) (length 0.5 mm) is important as a parasite
of the respiratory tract (trachea, air sacs, bronchi, lung
parenchyma, rarely on the liver) of many wild and
domesticated birds, especially canaries (e.g. prevalence
54% in Swit1,erland), other flnches (Gouldians, others)
and rarely budgerigars.
Selected references
Gunnarsson L, Zakrlsson G, Chrlstensson D, Uggla A
Q)
(2004) Efficacy of selamectin in the treatment of nasal mite
C
·c3
(Pneumonyssoides caninum) infection in dogs. J Am Anim
'6 Hosp Assoc 40: 400-404.
Q)
� Krametter-Froetscher R, Leschnlk M, Hoegler S,
c
co
Loewenstein M, Baumgartner W (2006) Occurrence of the
C ear-mite Raillietia auris in cattle in Austria. Vet J 171: 186-188.
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Family Laelaptidae
This large family comprises free-living and parasitic,
haematophagous species that are usually found on
wild rodents and in their caves and occasionally on
rodents kept as pets. Species of the genera Laelaps,
Eulaelaps, Haemogamasus, Hirstionyssus. Eulaelaps
and Haemogamasus have been identified as causing
skin irritations and dermatitis in humans. Of particular
importance are Tropilaelaps species as bee parasites.
Genus Tropilae/aps
Tropilaelaps clareae
Disease: Tropl/ae/aps Infestation of bees.
Tropilaelaps clareae is a reddish-brown, longitudinal­
oval mite (about 0.9-1.0x0.5 mm), significantly smaller
than the transverse-oval Varroa destructor. In South
East Asia, T. clareae crossed over about a century
ago from their original hosts, giant honeybees, to
the imported Western honeybee, Apis mellifera, with
which this mite subsequently spread to other parts of
Asia (including Iran, China, Korea). A closely related
species, T. koenigerum, occurs in Sri Lanka, Nepal,
Borneo and Thailand. In Europe, these mites have not
yet been detected, but there is a risk of introduction.
The infestation of honey bees with Tropilaelaps spp. is
listed by OIE as a notifiable disease. Control► p. 612.
Family Varroidae
Genus Varroa (Varroa mites)
Varroa destructor
Disease: Varroosls (colloquially varroatosls) in bees.
Marcus Terentius Varro, Roman scholar and beekeeper,
who wrote a book about bees in 100 BC. Varroosis
is often referred to as varroa disease or varroatosis;
the latter name does not conform to international
recommendations (► p. 40).
Summary
Morpholo8Y, species. Varroosis of the European honey
bee (Ap/s mel/ifera) is caused by Varroa destructor.
F�males of II. destructor are particularly remarkable
for their transverse-oval shape and size (1.1-1 .7 x 1.3·
Life cyc:le. Varroa mites parasitise on larval and adult
bees, Reproduction: females lay eggs in the brood cell
•
before capping. Development to protonymph in the egg

A into adults(always only 1 rS per brood cell). Only females
- deutonymph - adults. The fertilised females leave
the brood cell together with the hatching bee. Total
development from egg to females within about 8 days.
• Epldemlology. Varroosls Is now the most common
bee disease In Europe. Spread of mites from colony to
colony through infested worker bees or drones, through
swarming and other factors.
• Pathogenesis, cllnlcal signs. Varroa mites harm
adult bees and their brood through withdrawal of
haemolymph; death of bee brood, malformations of
emerging bees which are not viable. losses In the
bee colony arise gradually. The Infestation Is lowest In
spring. With Increasing brood activity and the beginning
of the drone rearing In April, the number of mites In the
colony steadily Increases. In addition, Varroa mites can
transmit various viruses and Increase the predisposition
to other brood diseases.
• Diagnosis. Detection of Varroa mites In deposits on
the floor of the bee hives, In the bee brood and on
adult bees (macroscopically or with magnifying glass).
• Control. Elimination ls not possible. Reduction of mite
Infestation through 'care' and application of acaricldes.
Approved compounds (partly country-specific): formic
acid, flumethrln, coumaphos and thymol (problems:
resistance and residues). Government measures
(notifiable disease, control).
Morphology and species. Varroosis of the European
honey bee Apis mellifera is caused by Varroa destructor
(until 2000 incorrectly referred to as V. jacobsoni which,
like several other Varroa species, are host specific and do
not infect A. mellifera). � � of V. destructor(► Figure
14.14a) are brown, transverse-oval and large (length
1.1-1.7 mm, width 1.3-1.6 mm), the rare rSrS are round
to oval and smaller(length 0.9 mm, width 0.8 mm). The
female's back is completely covered by a convex plate
which bears, like the dorsal side, many short setae. The
eight short but robust legs with large tarsal adhesive pads
are usually curved and protrude only slightly beyond
the edge of the broad back plate.
Life cycle. The mites sit on abdomen or thorax of
adult bees and penetrate with their chelicerae the
exoskeleton between sclerites to suck haemolymph.
For reproduction, a female migrates into a brood cell of
the honeycomb just before capping with a preference for
the drone brood. Shortly after, the female lays up to six
eggs which develop into protonymphs. They leave the
'
.·,1 ,;
r
,'-r- - .
.,· \\y...,. --', , . ·,)\·,'''
• •. '.\ ...., /I
Figure 14.14. Varroa mite: (a) female (1.1 x1 .6 mm); (b) Varroa � on bee brood; (c) bee damaged by Varroa (Source: Novartis).
14. Phylum Arthropoda (arthropods)
embryonic membranes and develop via deutonymph
and pre-adult stages (proto- and deutonymphs) suck
haemolymph of the bee brood(► Figure 14.14b). Males
cannot feed because their chelicerae are converted for
sperm transfer. Copulation takes place in the sealed
brood cell. Thereafter, the males die. Fertilised females
leave the brood cells together with hatching bees. The
total development from egg to female lasts about 1 week.
The reproductive rate of mites depends on the duration
of the capping of the brood celJs. The longest duration
is in brood cells of drones with 24 days, allowing the
development of 1 male and up to 4 females. Females
live in summer 2-3, in winter 5-8 months, and outside
of the colony no longer than 5 days.
Occurrence and epidemiology. Varroosis is now
the most common bee disease and has destroyed many
thousands of bee populations especially in Europe and
Asia in the past few decades. Probably back in the
middle of the last century in eastern Russia, V. destructor
changed its host, from the eastern honey bee Apis cerana
to the very susceptible European honeybee A. mellifera.
With the long-range transport of bees, V. destructor first
arrived in western Russia(1964) and then in Germany
(1971), United Kingdom (1992) and in other Central
European countries. In South America, varroosis has
been widespread since 1971, in North America since
1987, and in Africa since 1975. Mites are distributed
from colony to colony through contact between drones m
and workers outside of their respective hives, by robber 'O
0
bees as well as over long distances through swarming. 0.
0
Beekeepers can facilitate the spread by migratory .c
t
beekeeping, transfer of bees between colonies or selling <{
queens or colonies(► Acarapis woodi, p. 434).
Pathogenesis and clinical signs. Varroa mites
damage the adult bees and their brood through
withdrawal of haemolymph. Damage to the breed
occurs by the time a brood cell has been infested with
1-2 mite females. Bees hatching from an infested cell are
significantly smaller, and their life span is considerably
shortened. In case of heavy infestations, young bees have
malformations(shortened abdomen, stunted wings and
legs) and are not viable(► Figure 14.14c).
The damage caused by Varroa mites in bee colonies
occurs gradually over the course of several years. The
Part Ill. Parasites and parasitoses: metazoa
infestation is lowest in spring. With increasing activity
of the brood and the beginning of drone rearing in April,
the number of mites in the colony steadily increases. Up
to 90% of mites develop in the drone brood, and only
a few in the worker brood. Beekeepers do not notice
damage at this point. Heavily damaged bee colonies
collapse in late summer after honey yield, in early fall
after the winter feeding or during the winter. In the
final stage of varroosis, there are only a few hundred
bees and the queen left in the hive. Usually it is only
in the yd or 4th year after a primary infestation with
Varroa that the colonies collapse if there is no efficient
control. Simultaneous infections are likely to have a
decisive role, especially those caused by the Deformed
Wing Virus (DWV).
Diagnosis. Bees with shortened abdomen and
malformed wings are always suspicious. An infestation
with Varroa mites is demonstrated by examining debris
(containing dead mites) from the bottom of the hive,
of bee brood (preferably 18 days old drones or 13 days
old worker brood) and bees (examination of 200-300
frozen bees). For more information, see references.
Differential diagnosis: Tropilaelaps clareae, Euvarroa
spp. and numerous free-living mites that can colonise
the hive. The bee louse, Brau/a coeca ( ► p. 474), cannot
be confused with any mite species.
Control. Infestation of honey bees with Varroa spp.
is an OIE-listed notifiable disease. As elimination of
varroosis currently seems impossible, control measures
aim at reducing the number of mites to below the damage
threshold by 'care' (beekeepers language) and the use of
acaricides (details ► p. 612).
Selected references .....e::::;::::.:::.m1ZC:c:ai::c::::i
Anderson DL, Morgan MJ (2007) Genetic and morphological
variation of bee-parasitic Tropl/aelaps mites (Acarl:
Laelapidae): new and re-defined species. Exp Appl Acarol
43: 1-24.
Forsgren E, de Miranda JR, lsaksson M, Wei S, Fries I
(2009) Deformed wing virus associated with Tropilaelaps
mercedesae Infesting European honey bees l,Apis mellifera).
Exp Appl Acarol 47: 87-97.
Le Conte Y, Ellis M, Ritter W (2010) Varroa mites and honey
bee health: can Varroa explain part of the colony losses?
Apidology 41: 353-363.
Martin SJ, Highfield AC, Brettell L, Villalobos EM, Budge
GE, Powell M, Nikaido S, Schroeder DC (2012) Global
honey bee viral landscape altered by a parasitic mite. Science
336: 1304-1306.
Rosenkranz P, Aumeier P, Ziegelmann B (2010) Biology and
control of Varroa destructor. J lnvertebr Pathol 103 Suppl
1: S96-S119.
Sammataro D, Gerson U, Needham G (2000) Parasitic mites
of honey bees: life history, implications, and impact. Annu
Rev Entomol 45: 519-548.
14.1.3 Order Prostigmata (syn.
Trombidiformes)
Pro- (L): front; stigma (G): scar, spot. Refers to the
location of the stigmata in the anterior part of the body.
From this order, particularly the genera Demodex,
Cheyletiella and Trombicula are important as
ectoparasites of dogs and cats. In addition, Acarapis
woodi is of interest as a bee parasite. An important
feature is the position of the stigmata in the front part
of the body (gnathosoma or anterior podosoma).
Family Demodicidae
Demos (G): sebum; dex (G): wood worm. Probably refers
to the similarity between adult Demodex mites and so­
called 'wood worms'.
Genus Demodex (follicle mites)
Disease: Demodlcosis.
Summary
• Morphology, species. Strictly host-specific coloniser
of hair follicles and sebaceous glands of almost all
mammals (depending on host species, one or more
Demodex species), pathogenic especially in the dog.
Characteristics: small (0.2-0.3 mm), typical cigar-like
shape, very short legs, short mouthparts.
• Life cycle, epidemiology (D. canis). Development in
hair follicles: eggs -> 1-2 larval stages -+ 2 nymphal
stages-> adults. Postpartal transmission from mother
to offspring through skin contact during suckling,
especially In the first days of life.
• Pathogenesis. Certain breeding lines of dog_s are
predisposed to the disease. Intensive multiplication
of D. canls, damage to the hair follicles (alopecia),
secondary colonlsatlon with bacteria. Generalised
demodlcosls due to suppression of T-cell functions,
hardly any Influence on humeral Immunity.
• Clinical signs. Several forms in dogs: demodicosis of
juveniles or adults, localised or generalised, especially
as squamous, pustular or squamo-papular forms.
Demodieosis (nodules, rarely pustules) also occurs in
goats, cattle and pigs, more rarely in cats and horses.
• Diagnosis. Clinical picture and microscopic
identification of numerous Demodex mites or eggs.
• Therapy. Demodlcosis of dogs: localised forms:
palliative treatment. Otherwise weekly washings
or whole-body dips with 0.05% amitraz solution or
monthly 1 x amitraz/metaflumlzone until no more mites
are detected after clinical cure. In case of pronounced
symptoms, monthly or weekly moxidectin spot-on or
a single oral administration of fluralaner. Generalised
demodlcosls may require Intensive treatments over
weeks or months, cure rates 60-80%.
T
 14. Phylum Arthropoda (arthropods)

clear whether the occasionally found short forms, such

• Prophylaxis. Dogs of bteedlng lines In which
demodlcosls has occurred, should not at aU or only
under eertalr, condition!!, be used for breeding.
Prevention of other diseases and stress (exaggerated
111klh care1 cortleold treatments, etc.),
Morphology and species. The mites of the only
genus of the family are ectoparasites of many mammalian
species and of humans. The closely related species are
strictly host-specific; however, a host can harbour several
species: horse: D. equi; cattle: D. bovis; sheep: D. ovis:
goat: D. caprae; pig: D. phylloides; dog: D. canis, D. injai
and Demodex sp. (short form); cat: D. cati, D. gatoi and
Demodex sp. (middle form); mouse: D. musculi; rat: D.
ratti; guinea pig: D. caviae; golden hamster: D. c:rlc:eti
(short form) and D. aurati; humans: D. follic:ulorum
and D. brevis.
Demodex species are tiny, 0.2-0.3 mm long, cigar-shaped
mites with striated surface of the rear body, very short
legs and short mouthparts (► Figure 14.15). It is not
as in the dog, are valid species or phenotypic variants.
Life cycle. Demodex mites live in hair follicles and
more rarely in sebaceous glands; only the copulation
occurs on the skin surface in pores (► Figure 14.15). co
Males die after 3-5 days; females migrate into follicles co
where they lay about 20 lemon-shaped eggs (70-90x 19- E
O>
'.,:::;
25 µm) from each of which one six-legged larva hatches
e
en
which a further moulting to a second larva. Then, two 0...
nymphal stages (proto- and deutonymph) develop, and
finally the adult mites. The overall development takes
2-3 weeks,
Occurrence and epidemiology. Demodex mites
occur worldwide ns colonisers of the skin of almost all
mammals. They usually behave as commensals but are
potentially pathogenic, especially in the dog. A low­
grade Demodex infestation is common in healthy dogs;
in some areas, prevalences up to 85% were determined.
In contrast, disease caused by these mites is much
rarer. Nevertheless, demodicosis is among the 10 most
common dermatoses of dogs; it occurs less frequently

Deutonymph

/ .. ............ ..........................................

stages

Egg

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'r-\l'� --------../ l

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0
from bitch to suckling puppies 0
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Figure 14.15. Life cycle of Demodex canis (Graphics: IPZ, S. Ehrat).
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 Part Ill. Parasites and parasitoses: metazoa
in cats. Demodicosis is regionally significant in goats
and pigs; its importance is usually low in cattle, horses
and sheep.
Demodex mites are permanent-stationary parasites that
cannot survive in the natural environment of their hosts,
not even for short periods of time (but under laboratory
conditions in water up to 3 weeks). Therefore, changing
the host is difficult for them but possible under the
specific conditions of the postpartum period (altered
hormonal status of females, immunologically naive
juveniles, close and prolonged contact with the skin as
well as warmth and humidity during suckling).
Pathogenesis and immunology. In the genesis and
the course of demodicosis, differences in animal species
are to be noted. An example is demodicosis of the dog,
which is caused by D. can is; harmful effects of the other
species occurring in dogs (see above) are not known.
The mites squeeze into the hair follicle where they
multiply, move forward to the hair root, loosen the hair
from its moorings (resulting in hair loss), and finally
also penetrate the sebaceous glands. The progressive
propagation of mites causes a bagginess of hair
follicles and sebaceous glands. The mites irritate the
follicular keratinocytes, pierce them with their needle­
like chelicerae and suck them dry. This induces cell
hyperplasia, increased formation of follicular keratin
as well as hyper- and dyskeratosis. Colonisation of hair
follicles by bacteria causes pustules (purulent folliculitis,
see below) with a tendency to spread (disintegration of
hair follicles, formation of further pustules and boils).
lmmunopathological processes are of basic pathogenetic
significance.
In some breeding lines, there is a hereditary
predisposition for the disease, the genetic basis of which
remains largely unknown. MHC (type 11) expression is
significantly increased in the skin of young dogs with
generalised demodicosis. Often, dogs with generalised
Q)
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0
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Figure 14.16. Demodicosis in dog. (a) Advanced squamous form (Photo: IPH/IPZ); (b) pustular form with pyoderma (Photo:
co
a.. IPZ, K. Wolff).
demodicosis suffer from immunosuppression with
increasing pyoderma. Treatments with corticosteroids
or cytotoxic agents, concurrent diseases (neoplasms,
distemper, endocrinopathies, etc.) or particular stresses
(oestrus, pregnancy, dentition, malnutrition, etc.) are
considered enabling factors. Ultimately, the reasons
for a generalisation of demodicosis are still unknown.
Dogs of all breeds can develop demodicosis. Quite
often littermates become ill, suggesting a hereditary
predisposition.
Clinical signs in the dog. Clinically, a distinction
is made between the frequent demodicosis in young
a11imals (age 3-18 months) and the less common disease
in older dogs (> 1 ½ years, often >4 years). The disease
can be localised or generalised, and occurs as squamous,
pustular or squamo-pustular form (other forms see
below).
• Squamous form (most common form). ► Figure
14. 16a. Localisation: usually starts at the head (forehead,
nose, lips, around the eyes, ears, except the tips), limbs,
rarely trunk. Mostly localised. Changes: scaly eczema
with bran-like deposits, alopecia, erythema, folliculitis,
cracks, wrinkles, skin thickening (hyperkeratosis), no
or only slight itching (see mange). Animal group and
course of disease: mostly young dogs <l year, about
90% of cases resolve spontaneously within 1-2 months,
the others can be progressive.
• Pustular form. ► Figure 14.16b. Localisation:
localised or generalised condition (i.e. at least 5 local
lesions, an entire body region or at least 2 paws affected).
Changes: complications from secondary infections
with bacteria (staphylococci, etc.); erythematous
papules, pustules (blue-red, 'red mange'), scabs, skin
thickening (dyskeratosis, parakeratosis), wrinkling,
suppurative folliculitis, superficial or deep pyoderma,
furunculosis; usually no itching, but pain; peripheral
lymphadenopathy, anorexia, lethargy, sepsis. Animal
group and course of disease: older dogs > 1 ½ to -4

years, _often with an underlying disease. Prolonged
course of the disease, often fatal outcome (or euthanasia)
without treatment.
• Other forms. Alopecia-form: almost only focal
alopecia, especially on the head. Pododemodicosis:
predominantly pustular, mostly in young adult dogs
on all 4 paws; chronic forms may be accompanied
by pyoderma and develop into the generalised form.
Otodemodicosis: changes in the external ear canal
(ceruminous otitis externa, often pruritus).
Clinical signs in other domestic species.
Demodicosis is rare in cats. Lesions caused by D. cati are
similar to those in dogs and are usually restricted to head
(eyelids, chin, ear canal) and neck. D. gatoi demodicosis
is characterised by pruritic and potentially contagious
skin conditions. In goats, cattle and pigs, Demodex
mites can, due to their strong reproduction, greatly
expand the hair follicles and cause node formation in
the skin (>500,000 mites were found per node in pigs).
This formation of nodes causes a pressure atrophy of
the dermis and thus leather damage. In pigs, pustules
can also develop around snout and eyes, occasionally on
the neck, chest and belly. Horses rarely fall ill. Changes
especially on head, neck, back or front legs.
Diagnosis. Identification of mites: squeeze a skin
fold of the affected area between your fingers until
the contents leak from the hair follicles; scrape this
off firmly (until capillary bleeding occurs) and smear
on a slide for microscopic examination, possibly take
deep skin scrapings at several places and examine
using the KOH method ( ► p. 525). In case of heavy
infestation, mites can also be observed in faeces of dogs
(flotation technique). Mite detection is meaningful only
in conjunction with clinical symptoms; few mites in the
absence of skin lesions only proof an infestation, but
not a disease. In some cases with severe changes, mite
detection is not successful. T hen, a biopsy should be
taken for a histological examination.
Therapy. Localised squamous demodicosis of young
dogs should not be treated with acaricides, but only
palliatively as most cases spontaneously resolve within
1-2 months. Treatment is necessary in the absence of
spontaneous healing and signs of generalisation.
• Basic therapy. Shearing, if necessary; compresses
with cleaning, disinfecting and scab peeling properties;
washings, dips and re-fattening of skin (acetylsalicylic
oil or the like).
• Specific treatment. Full body washing or dips
with 0.05% amitraz solution every 5-7 days until
clinical cure and thereafter until no live mites (eggs)
are detectable within 2 months. In severely debilitated
14. Phylum Arthropoda (arthropods)
dogs, a 0.025% solution must be used. Prognosis fo r
recovery from generalised demodicosis after a treatment
period of 6 months on average 60-80%. For demodicosis
of dogs the following treatments are also approved:
moxidectin + imidacloprid: 2.5 mg/kg b.w. + 10 mg/
kg spot-on, at least 2-4x at monthly intervals, as well
as amitraz + metaflumizone: 20 mg/kg b.w.+ 20 mg/kg, ro
spot-on, 1x every 4 weeks ( ► Table 19 .16, p. 602). In
E
0)
:,:::;
case of pronounced symptoms, 1x weekly moxidectin
e
(/)
+ imidacloprid spot-on or a single administration of 0...
fluralaner at a minimum dose of 25 mg/kg b.w. showed
promising results.
• Adjunct therapy (always required in cases
of pustular form). Antibiotics, vitamin supplements
and possibly locally benzoyl peroxide containing
shampoos 1 x daily to empty hair follicles. The value of
immunostimulation is controversial.
Prophylaxis. The following options exist: (a) do not
use bitch and puppies for breeding after presence of
demodicosis is confirmed, and (b) approve bitches for
further breeding only after their offspring have remained
healthy until the age of 18 months. Other measures for
dogs at risk (genetic background!): avoidance of stress
and corticosteroid treatments, good animal husbandry,
especially no exaggerated or incorrect skin care.
Selected references, cu
l:J
0
Beale K (2012) Feline demodicosis: a consideration in the itchy Q.
0
or overgrooming cat. J Feline Med Surg 14: 209-213. ..c:
t
Fourie JJ, Llebenberg JE, Horak IG, Taenzler J, Heckeroth <{
AR, Frenals R (2015) Efficacy of orally administered fluralaner
(Bravecto ™) or topically applied imidacloprid/moxidectin
(Advocate®) against generalized demodicosis in dogs. Paras
Vectors 8: 187.
Gortel K (2006) Update on canine demodicosis. Vet Clin North
Am Small Anim Pract 36: 229-241.
It V, Barrientos L, L6pez Gappa J, Posik D, Dfaz S, Golijow
C, Giovambattista G (2010) Association of canine juvenile
generalized demodicosis with the dog leukocyte antigen
system. Tissue Antigens; 76: 67-70.
Lowenstein C, Beck W, Bessmann K, Mueller RS (2005)
Feline demodicosis caused by concurrent infestation with
Demodex cati and an unnamed species of mite. Vet Rec
157: 290-292.
Mueller RS, Bensignor E, Ferrer L, Holm B, Lemarie S,
Paradis M, Shipstone MA (2012) Treatment of demodicosis
in dogs: 2011 clinical practice guidelines. Vet Dermatol 23:
86-96.
Singh SK, Dimri U (2014) The immuno-pathological conversions
of canine demodicosis. Vet Parasitol 203: 1-5.
 Part Ill. Parasites and parasitoses: metazoa

Family Cheyletiellidae
Palpal claw---��
Most species of the family Cheyletiellidae are free­
Empodium
living predators that feed primarily on other mites; (= serrated seta)
however, some species of the genus Cheyletiella live as
ectoparasites of mammals.

Genus Chey/etiel/a (fur mites)

Disease: Cheyletiellosis.
a

Cheilos (G): lip.

Summary
• Morphology, species. Fiur mites are common In
dog (Cheyletiella yasgurl), cat (Ch. blakeQ, rabbit (Ch.
parasltovorax); man is an aberrant host. Characteristics:
adult mites 0.2-0.5 mm In length, with long, stiletto­
shaped chellcerae and characteristically short, strong
palps with inward-pointing claws.
• Life cycle, epidemiology. Complete development
on the host: egg - larva -2 nymphal stages ....
adults; duration around 3 weeks. Eggs are contained
l
• I
in a cocoon-like structure that is attached to hair.
Transmission upon contact. Survival of adults without Figure 14.17. Chey/et/el/a parasltivorax: (a) female (length:
a host in a cool environment for at least 1 O days.
200-500 µm); (b) Cheyletiella, anterior part of body (Graphics
Cheyletlella species can colonise several host species,
a: IPZ, A. Seeger; after Baker et al. 1967; b: Photo: IPZ).
temporarily also humans.
• Occurrence In rabbits up to 70%, In dogs and cats
around25%.
• Pathogenesis, cllnlcal signs. In dog and cat: Life cycle, epidemiology and occurrence. The
unapparent Infestation or severely scale-producing and whole development process occurs on the host and lasts
prurltlc chronk: eczema, especially on head, shoulder about 3 weeks. Eggs (about 230x 100 µm) are contained
and back area. in a cocoon-like structure which is attached to the hair a
• Dlagno81s. Clinical finding and detection of mites and few millimetres above the skin. The development occurs
eggs on the animal. Method of choice: adhesive tape according to the scheme: egg -+ larva -+ 2 nymphal
technique. stages -+ adults. With their strong claws on the palps,
• Therapy. Topical treatment of dogs and cats with
the mites cling to the fur or migrate through pseudo­
acarlcldes, e. g. flpronil or selamectln (► Table 19.16,
p. 602).
tunnels in epidermal detritus ('walking dandruff'). The
• Zoonotlc Importance. Upon contact with Infested
mites pierce the epidermis with their sharp chelicerae
domestic animals, Chey/etlella mites can temporarily and ingest lymph that is leaking. In a cool environment,
Infest humans and cause skin alterations, adults can survive at least IO days without a host, pre­
adult stages only 2 days.

Morphology and species. Cheyletie/la species are The motile mites can migrate very quickly from infested
(J)
C common in dog (Cheyletiella yasguri), cat (C. blakei), hosts to other hosts upon contact, especially to juveniles
·c3
'6 rabbit ( C. parasitovorax). These species with little host that are kept in groups (breeding establishment, kennel).
(J)
� specificity can also infest other animal species (e.g. A transfer of mites from the immediate surroundings
c
co
C. yasguri on cat, C. b/akei fox) and temporarily also of infested hosts is probably also possible.
C humans. The species are morphologically very similar
·;::
and difficult to distinguish. The large, about 200-500 The distribution of fur mites is worldwide. Prevalences
µm long, ovoid adults have stiletto-shaped chelicerae reach about 70% in rabbits and 25% in dogs and cats.
C and characteristically short, strong palps with inward­
>­ pointing claws ( ► Figure 14.17). The strong legs of Pathogenesis and clinical signs. In dogs and
CJ)
0 the very rapidly moving adults have narrow, comb-like cats, Cheyletiella most commonly cause chronic eczema
0
"ii.i structures (empodia) at the ends of the tarsi, instead with itching and mild to severe dandruff, especially
co of claws. on head, shoulder and back. In some cases, symptoms
co
0.. are absent or they are so inconspicuous that the mite
 14. Phylum Arthropoda (arthropods)

infestation is initially overlooked. More rarely, dermatitis Family Syringophilidae

with hyperesthesia and hair loss, sometimes with
papules and crusting, can develop, particularly in cats
(miliary dermatitis). Removal of a portion of the mites
and eggs by frequent grooming of cats can lead to a
less conspicuous disease course as compared to dogs.
Symptoms are causally related to the mite bites and to
allergic reactions to mite antigens. In some animals, there
is a discrepancy between intensity of mite infestation and
degree of itching. In these animals, a cross-sensitisation
caused by Cheyletiella against Dermatophagoides spp.
(house dust mites) could be substantiated. In these cases,
exfoliative erythroderma or skin reactions were observed
as with sarcoptic mange.
Diagnosis. The method of choice for detection of mites
and eggs is the adhesive tape technique ( ► p. 525). T he
KOH technique( ► p. 525) is suitable for investigating
superficial skin scrapings as well as dandruff and hair
that are combed out. Best results are said to be achieved
with samples obtained using vacuum cleaners. Mites or
eggs are often found in the faeces(flotation technique).
Contact animals should also be investigated as there are
often unapparent infestations.
Therapy. Treatment of dogs and cats with topical
formulations of acaricides(e.g. fipronil or selamectin, see
► Table 19 .16, p. 602). If necessary, repeat the treatment
several times at intervals of 2-4 weeks; in addition,
treat all contact animals and perform environmental
treatment with acaricides (see flea control ► p. 606).
Genus Syringophilus (quill mites)
Syringx (G): flute, tube; philos (G): loving, pleasant.
cu
Syringophilus species parasitise quills of wing and tail cu
E
feathers of chicken, turkey, pigeons, pheasants, canaries, 0)
:.::;
etc. These mites have an elongated body, short and CJ)
0
compact legs and long setae, especially at the edge of the
rear body ( ► Figure 14.18). Unlike in Cheyletidae, claws
at the end of the palps are missing. The most common
species are S. bipectinatus in chickens and S. columbae
in pigeons. Infestations remain asymptomatic; only very
rarely does a heavy infestation cause some feather loss.
- Selected references s:;.Jcz::::::ol5il:;;:r:;;:::a;,im
Farkas R, Losson B, Cozma V (2015) Cheyletiellosis. In:
Beugnet F, Halos L (eds.) Parasltoses & vector borne diseases
of cats. Lyon, F rance: Meriel S.A.S., pp. 181-184. ISBN
978-2-9550805-0-4.
Hansen 0, Mencke N, Pfister K, Beck W (2006) Efficacy of a
formulation containing imidacloprid and permethrin against
naturally acquired ectoparasite Infestations (Ctenocephalides
felis, Cheyletiella parasitovorax, and Listrophorus gibbus) in
rabbits. Intern J Appl Res Vet Med 4: 320-325.
Loft KE, Willesen JL (2007) Efficacy of imldacloprid 1O
percenl/moxidectln 2.5 percent spot-on in the treatment of ro
cheyletiellosis In dogs. Vet Rec 160: 528-529. "'O
0
Saevlk BK, Bredal W, Ulsteln TL (2004) Cheyletiella infestation 0.

Zoonotic importance. In case of contact with
infested pets, mites(mostly C. yasguri or C. blakei) can
temporarily colonise humans and cause skin alterations,
including itching, erythematous macules and papules
with central necrosis, especially in preferred contact
areas(arms, upper part of body).
in the dog: observations on diagnostic methods and clinical .c
t'.
signs. J Small Anim Pract 45: 495-500. <(
Wagner R, Stallmelster N (2000) Cheyletiella dermatitis in
humans, dogs and cats. Br J Dermatol 143: 1110-1112.
White SD, Rosychuk RA, Fleseler KV (2001) Clinicopathologic
findings, sensitivity to house dust mites, and efficacy of
milbemycln oxlme treatment of dogs with Cheyletiella sp.
Infestation. Vet Dermatol 12: 13-18.

Family Trombiculidae

Genus Trombicula (harvest mites, red bugs,

scrub itch mites) Q)
C
·5
'6
Q)
Disease: Troml!lieulosis.

ro
C
·;:::
Thrombos(G): thrombus, blood clot. Q)

-�
>,
0)
0
0
Figure 14.18. Syringophilus bipectinatus � (length: 825-1,050 "iii
µm) (Graphics: IPZ, A. Seeger; after Baker et al. 1967).
ro
0...
 Part Ill. Parasites and parasitoses: metazoa
Summary
• Morphology, species. The most imp0rtant species in
Europe is Trombicula (syn.: Neotrombicula) autumns/is.
• Life cycle, epidemiology. Development in the soil, only
larvae (6 legs, reddish), and often in large numbers,
infest mammals, birds amd humans, particularly in late
summer and autumn.
• Pathogenesis, clinical signs. Moderate to severe skin
reactions with moderate to almost unbearable Itching,
occasionally convulsions or, epileptic seizures.
• Diagnosis, therapy. Detection of reddish mites and bite
reactions on the animals. For therapy see Chey/et/el/a.
Morphology and species. About 50 of the more
than 1,500 trombiculid species have parasitic larval
stages while the free-living nymphs and adults feed on
detritus or prey on other arthropods. These mites are
known under various common names (harvest mites,
autumn mites, chiggers, scrub itch mites).
The roundish, pale yellow, but mostly orange to brick
red (natural colour), 0.2-0.3 mm long, six-legged larvae
have a small, five-cornered scutum with 5 barbed, short
setae and 1 pair of long fine sensory hairs dorsally behind
the prominent gnathosoma ( ► Figure 14.19). Further
characteristics are: tooth-like chelicerae, palps robust
with terminal claw and 30-50 pinnate setae on the dorsal
body. The free-living adults are about 1-2 mm long;
the body appears somewhat constricted by a distinct
waist. Trombicula autumnalis is of particular veterinary
medical concern in Europe.
Life cycle, epidemiology and occurrence.
Females of T. autumnalis lay numerous eggs in moist,
humus-rich soils. In summer and autumn, the positively
phototactic, six-legged larvae hatch and migrate upwards
on blades of grass, other plants, fallen leaves, etc., and
gather by the hundreds at the highest points, questing
for hosts. The larvae have no distinct host specificity
and in their habitat attack mainly rodents, but also many
other mammals, birds (especially ground dwelling birds)
Q)
·u
C
'6
Q)
� trombiculosis foci on sunny days), clinical findings
� and macroscopic (magnifying glass) and microscopic
ro
C
·;;::
Q)
C few days after larvae have dropped off the host. Often,
>,
0)
0
0
"in
ro Figure 14.19. Trombicula autumnalis larva (length 200-450 µm)
ro
n.. (Graphics: IPZ, A. Seeger; after Piekarski 1954).
and humans. Larvae attach themselves to the skin of the
hosts to ingest extraintestinal, partially digested host
tissues (see below) and fall to the ground after a few
days (�3). There, they develop over several 8-legged
nymphal stages to adults. Development is interrupted
by resting (quiescent) periods. In temperate climates,
T. autumnalis usually develops only one generation
per year, females can live > 1 year. Nymphs and adults
hibernate deep in soil.
In temperate climates, larvae which are only active at
temperatures above 16 °C occur from mid-July to end of
October (autumn, harvest mite). They are particularly
active on warm, sunny, dry days in late afternoon. The
preferred habitats (trombiculosis foci) are areas in
overgrown gardens and parks, forest edges, especially on
dry meadows (calcareous soils) and less often on fields.
Frequently, individual animals are attacked en masse
by hundreds or thousands of mite larvae. A transfer of
larvae from host to host does not occur.
Trombicula (Eutrombicula) alfreddugesi, very similar
to T. autumnalis and known as chiggers, is the most
widespread species in North and South America. T.
(Eutrombicula) sarcina is an important sheep parasite
in Australia.
Pathogenesis and clinical signs. Larvae attach
to the host at thin-skinned predilection sites, e.g. in
dogs and cats on their paws between the toes, in the
inguinal region, on the eye ring and bridge of the nose. In
cattle, the lower tail surface and the inner thigh areas are
commonly affected, and in sheep and goats the bridge of
the nose, eye ring and ears. The larvae initially cut with
their chelicerae through the stratum corneum. Salivary
gland secretions produce a deep-reaching hyaline tube
(stylostom), through which extraintestinally liquefied
tissue and, accidentally, blood components are ingested.
The tiny lesions created by the larvae as well as the
secreted saliva can cause mild to severe skin reactions:
moderate to almost unbearable, persistent itching,
erythema, hives, blisters, crusts, secondary alopecia,
excoriations due to scratching, occasionally convulsions
or epileptic seizures. Symptoms can persist for several
days after larvae have dropped off the host.
Diagnosis. Anamnesis (season, contact with
evidence of red larvae confirm the diagnosis.
Therapy and prophylaxis. Dermatitis disappears a
a palliative treatment suffices. If mites are present, a
treatment may be considered, e.g. in dogs and cats with
fipronil or selamectin or in dogs with a permethrin-
pyriproxyfen combination ( ► Table 19. I 6, p. 602). As
- 14. Phylum Arthropoda (arthropods)
preventive action, humans and animals should avoid
known Trombicula foci during the season.
Significance for humans and vector role.
Hwnans are also infested by Trombicula larvae(lower
limbs, proximal thigh, waist). In Europe, trombiculids
are not known to be vectors of pathogens; in eastern
and southern Asia Leptotrombidium species transmit
Orienta(formerly Rickettsia) tsutsugamushi to rodents,
insectivores, and humans (Tsutsugamushi fever).
Family Psorergatidae
Psora (G): scabies, mange; ergates (G): workers,
perpetrators.
Adu.It mites of the genus Psorergates are from a dorsal
view almost circular, tiny ( <0.2 mm), with almost
radially arranged, compact legs whose limbs appear
fused( ► Figure 14.20).
In the USA, infestation of sheep with Psorergates ovis
is considered eradicated, but it remains an important
ectoparasitic mite in parts of Australia, New Zealand,
South Africa and South America. P. bos has been found
on cattle in the USA and UK; this species probably
also occurs in Central Europe. Since the infestation
is often asymptomatic, it is rarely noticed. In UK,
dandruff, alopecia and skin thickening were ascribed
to an infestation. P. simplex infests house mice (Mus
musculus) and occasionally laboratory mice, causing
small white nodules in the hair follicles which might
become inflamed. Prevalences in wild populations may
reach 80%.
Figure 14.20. Psorergates simplex (;! (length ca. 190 µm)
(Graphics: IPZ; A. Seeger; after Baker et al. 1967).
Family Myobiidae (fur mite of mice)
Mys (G): mouse.
Myobiidae are established worldwide; they are small
mites of rodents, insectivores and bats. In veterinary cu
medicine, two closely related species are of interest: cu
Myobia musculi ( ► Figure 14.21) in laboratory mice E
O>
:;:::;
and Radfordia ensifera in laboratory rats. Characteristics CJ)
of these mites are: small size (about 0.3 m m long), Cl..
elongated, striking lateral protrusions between the leg
pairs 2/3 and 3/4; cuticle striated, needle-like chelicerae,
tiny palps. The first pair of legs is strongly modified and
sturdy, with a terminal claw-like structure for clinging
to hairs of the host. Female mites glue their eggs singly
at the base of hair. Development into adults occurs via
2 larval and nymphal stages in 2:12 days. The mites feed
on tissue fluid, but also on blood components. Heavier
infestations cause dermatitis with alopecia, pruritus,
especially on head and neck. M. musculi is frequently
associated with Myocoptes musculinus. Both species can
transiently infest other laboratory rodents. Detection
of mites and eggs in skin scrapings, in combed-out
skin material, also with the tape method ( ► p. 525)
and coproscopically (flotation technique) ( ► p. 526).
Treatment with acaricides(e.g. ivermectin p.o. or s.c.).
It is important to avoid re-introduction by practising
professional care of laboratory rodents.
Family Pyemotidae cu
-0
0
a.
Tiny, 0.13 to 0.3 mm long mites, which colonise grain,
hay, wood, and other stored products and which live on
e
.c
t:::
insect larvae which they paralyse with poison and then <(
suck out. The entire embryonic and post-embryonic
development takes place in the body of the female, so
that sexually mature animals are born. In the course
of this development, the rear body of the female swells
considerably('ball belly'). Two species can infest pets
(especially horses) and humans worldwide: the straw itch
Q)
C
·c3
Q)
�
�
m
C
·c
Q)
C
>.
O>
0
·c;;
Figure 14.21. Myobia musculi ';! (length 390-495 µm)(Graphics:
cu
IPZ, A. Seeger; after Baker et al. 1967). Cl..
 Part Ill. Parasites and parasitoses: metazoa

mite, Pyemotes ventricosus, and particularly the grain Summary

itch mite P. tritici. Their bites cause papules, blisters and
• Morphology, species. Acarapis woodi (length around
very itchy striae. The infestation occurs most frequently
100-180 µm) develops in the trachea of honey bees
in the summer months. Since it is an accidental, transient (internal mite) and is the agent of tracheal mite disease.
infestation, a palliative treatment suffices. Other Acarapis species largely are non-pathogenic
ectoparasites (external mites) of honey bees.

- Selected references c=:=====::::1 • Life cycle, epidemiology, distribution. Transmission

Andrews AH, Baker A, Fox M, Brizuela C (1997) Cattle
skin condition in Britain associated with the cattle itch mite
Psorobia bos. Vet Rec 140: 183.
Losson B, Farkas R, Cozma V (2015) Trombiculosis. In: Beugnet
F, Halos L (eds.). Parasitoses & vector borne diseases of cats.
Lyon: Merial S.A.S., pp. 180-190; ISBN 978-2-9550805-0-4.
Perris EE (1995) Parasitic dermatoses that cause prurltus In
horses. Vet Clin North Am Equine Pract 11: 11-28.
Pilsworth RC, Knottenbelt DC (2005) Trombiculidiasls. Equine
Vet Educ;17: 9-10.
Scholer A, Maler WA, Kampen H (2006) Multiple environmental
factor analysis in habitats of the harvest mite Neotrombicula
autumnalis (Acari: Trombiculidae) suggests extraordinarily
high euryoecious biology. Exp Appl Acarol 39: 41-62.
Smal D, Jasmin P, Mercier P (2004) Treatment of Neotrombicula
autumnalis dermatitis in dogs using two topical permethrin­
pyriproxyfen combinations. J Small Anim Pract 45: 98-103.
Family Tarsonemidae
Tarsos (G): sole of foot; nema (G): thread. Relates to the
long bristles of the tarsi.
Genus Acarapis (tracheal mite)
Disease; Acaraplosls, tracheal mite disease in honey
bees.
of the mites directly from bee to bee; young bees i n
their first 4-5 days of life are susceptible. Mites spread
among bee colonies as a result of purchase of infested
colonies or queens, by swarming drones and worker
bees as well as by robber bees. A. woodi is distributed
worldwide and endemic in Europe.
• Pathogenesis and signs. The internal mites puncture
the tracheal wall and ingest haemolymph. Possible
damages to the bees: obstruction of air circulation,
general weakness, inability to fly, death especially in
spring, possibly with other factors contributing.
• Diagnosis, control. Detection of the internal mites by
microscopic examination of tracheae from the thorax.
The tracheal mite disease is an OIE-listed notifiable
disease and conditionally subject to control in some
countries. Control predominantly through cleaning,
disinfection and prophylactic measures, rarely by
application of acaricides.
Morphology and species. Of the several Acarapis
species, only A. woodi (syn. Tarsonemus woodi), the
tracheal or internal mite, parasitises in the tracheae of the
European honey bee (Apis mellifera) and less often the
Asian or Indian honey bee (A. cerana). Various external
mite species with different predilection sites are non­
pathogenic or only slightly pathogenic but are important
in differential diagnosis. The very small � � ( 100- I 80
µm) and ii (80-100 µm) of A. woodi bear dorsally long
setae and are apparently divided into a propodosoma
and a hysterosoma with transverse grooves. The tarsi
IV have no claws or empodia, but only setae ( ► Figure
14.22).

Life cycle. Adult mites infest young bees and colonise

Akari (G): mite; apis (L): bee. almost exclusively the front tracheal pair of the thorax
near the apertures of the spiracles where the entire

Q)

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C

'6
Q)
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ro
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Q)

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0 b
0
"iii
ro Figure 14.22. Acarapis woodi: (a) infested part of trachea of bee; (b) female (length 100-180 µrn) (Photo a: IPZ; Graphics b:
ro
0... IPZ, A. Seeger; after Baker et al. 1967).
 14. Phylum Arthropoda (arthropods)

development takes place (approximately 2 weeks). 14.1.4 Order Astigmata

There are often several generations in the same trachea.
Females lay 7-10 very large (about 130 µm) eggs, in
which a large six-legged larva develops. After about
one day of development, the larva enters a dormant
stage and further develops into an eight-legged nymph
that hatches and reaches the adult stage after a further
moulting. Larval and adult stages puncture the tracheal
wall and ingest haemolymph.
(Sarcoptiformes)
Miles of this order lack stigmata and tracheae; respiration
is through the thin integument. Some species are
very important as agents of different forms of mange
in domestic and wild animals or as agents of scabies
of humans. Other species are storage mites or cause
allergies.

Epidemiology and occurrence. A. woodi has spread Family Psoroptidae

with the European honey bee almost worldwide (except
Australia and New Zealand) and is endemic in many
European countries. Disease: Psoroptldosls.

Mated females leave the tracheae as these become

strongly infested, and infest other bees only upon direct
contact (no migration from the environment in the
hive or on flowers). Only young bees until 4 days of
age are susceptible, because the bristles which cover the
apertures of the spiracles are later strongly chitinised
and the mites can no longer penetrate. Prevalence is
highest at the start of the breeding period in early spring
and towards its end in autumn. Spread of mites from
colony to colony is through robber bees, by swarming
drones and worker bees, but also through the purchase
of infested queens or colonies. Affected colonies tend
to swarm and thereby facilitate the spread.
Psoroptidae are statlom1ry, permanent, long-legged and
large (up to about 800 µm) mites, which do not penetrate
the skin, but live superficially on the skjn in the coat or
in the ear. Three genera are of veterinary importance:
Psoroptes (feeds mainly on tissue fluids), Chorioptes and
Otodectes (feed on skin components) ( ► Table 14.6).
Genus Psoroptes
Disease: PsoroptiG mange.

Pathogenesis and signs. Restlessness, abnormal Psora (G): scabies, mange. (lj
V-shaped wing position, inability to fly, weakness, -0
0
and increased mortality of bees may be evidence of Summary
Q.

A. woodi infestation. The Acarapis infestation causes ..c

loss of haemolymph, the formation of scabs by leaking
haemolymph in the area of the puncture sites in the
trachea, and leads to a dark discoloration caused by
bacterial growth and the glue with which eggs are
attached to the wall of the tracheae ( ► Figure 14.22).
Additional factors, such as infections with other
pathogens, need to be considered in the pathogenesis
of A. woodi infestation.
Diagnosis and control. Diagnosis by microscopic
detection of mites in tracheae. Tracheal mite disease is
an OIE-listed notifiable disease and conditionally subject
to control in some countries ( ► p. 612)
Selected references
• Morphology, species. Characteristics of the adults of t'.
<(
this genus: oval body shape, length of � � up to 800
µm, gnathosoma longer than wide and pointed, the
long legs bear a long, 3-Jolnted pretarsus with trumpet­
shaped and sucker-like pulvillus. Psoroptes species
Infesting mainly ruminants and rabbits are summarised
In ► Table 14.6.
• Life cycle. Egg - larva - proto- and trltonymph -+
adult; 1 generation requires around 2-3 weeks for
development. The mites llve superficially on the skin,
and feed on body fluids of the host.
• Occurrence. Global occurrence In ruminants, equids
and rabbits. In Europe, Psoroptes mange occurs in
sheep, some cattle breeds, rabbit, rarely goat, and
very rarely horse. Cl)
• Epidemiology. Transmission of mites is mainly by direct C
·5
contact with animals; Psoroptes mites survive about '6
2-3 weeks off the host; contaminated pens, vehicles, Cl)

utensils, pieces of wool can act as source of infestation.

McMullan JB, Brown MJ (2009) A qualitative model of mortality 1111 sheep, mange outbreaks most frequently occur (lj
C
in honey bee l.;l.pis mellifera) colonies infested with tracheal in the aut1:1mn or winter. Rarely, there is a reciprocal ·;;::

mites l.;l.carapis wood1). Exp Appl Acarol 47: 225-234.
Sammataro D (2006) An easy dissection technique for finding the
tracheal mite, Acarapis woodi (Rennie) (Acari: Tarsonemidae),
in honey bees, with video link. Int J Acarol 32: 339-343.
transmission of Psoroptes mites between sheep and
cattle. In cattle (Belgian blue and related breeds), bulls
are particularly affected by mange during stabling in .£
>,
winter. In rabbits in breeding or fattening systems, ear 0)
0
mange is the most important ectoparasitosis; rabbits

..
0
Sammataro D, Gerson U, Needham G (2000) Parasitic mites
kept in<ilividually as pets, however, rarely become ill. ·u;
of honey bees: life history, implications, and impact. Annu
(lj
Rev Entomol 45: 519-548. Q_
 Part Ill. Parasites and parasitoses: metazoa

rather suggest the existence of a single species (.P. ovis)

A
• Immunology, pathogenesis, clinical signs. Alle�ic
reactions to mite anti!i}ens initially cause a p>erivascwlar,
exudative dermatitis, later papules, cliUsts, exudation,
scabs, skin thickenin€J, hair loss, associated with
intense itching. The clinical picture depends or:i the most
animal species(► Table 14.6). A prrimary infestation
induces a partial, tem):)Orary immuAity(duration in cattle
2-5 months).
• Diagnosis. Detection of mites in crusts or skin
scrapings(KOH technique). ELISA for herd diagnosis
in sheep and cattle.
• Therapy and control. Treatment of sheep with
macrocyclic lactones {ML) �vermectin 0.2 mg/kg b.w.
s.c., doramectin 0.3 mg/kg l.m.), moxldectln (1.0 mg/
kg b.w. s.c.) or in specific Indications by acarlclde dips
(phoxim). Therapy In cattle preferably with ML by pour­
on application (doramectln, eprlnomectln, lvermectln,
moxidectin: all at 0.5 mg/kg b.w.) or with flumethrln (2
mg/kg b.w.). For elimlnatlon of mange In stocks, use
ML with residual activity; when using shorter acting
acaricldes, repeated treatments at least once In the
interval of 7-1 O days are required.
Morphology and species. Adult Psoroptes mites
( � � 560-820 µm, oo
380-570 µm long) are larger than
Sarcoptes and Chorioptes mites; they have an elongated,
pointed gnathosoma and long legs with long, 3-jointed
pretarsi and trumpet-shaped sucking-like pulvilli.
Pretarsi are lacking on the yd pair of legs of females
and the short 4th pair of legs of males ( ► Figure 14.23).
Several species are described in the genus Psoroptes
( ► Table 14.6). The high variability of morphologic
characteristics and the very small genetic differences
(possibly with the exception of P. natalensis).
Life cycle. Females live on the skin of their hosts for
about 2 weeks ( 11-42 days) and during this time deposit
30-80 large, oval eggs (about 250 µm long), from which
larvae hatch after � 10 days and which develop over two
nymphal stages (proto- and tritonymph) into adults. The
development of a generation takes about 3 weeks (�21
days). The mite population doubles about every week.
All stages ingest feed. For this purpose, they puncture
the epidermis and suck tissue fluid (sometimes blood)
or ingest exudate without biting. Some species prefer to
infest the inside of the auricle and the external auditory
canal (rabbit, goat and horse); others colonise parts of
the trunk ( ► Table 14.6).
Occurrence. Psoroptes mange is common worldwide
in ruminants, equines and rabbits. In cattle, the disease
is regionally limited (e.g. BE, UK, IT, USA), especially
in fattening herds. As observed in BE, cattle of the
Belgian Blue breed are more affected by the infestation
than dairy cattle (e.g. Holstein Frisian breed) in which
clinical symptoms are rare. Psoroptes mange of sheep was
regarded as eliminated in some countries (e.g. Australia,
New Zealand, Canada, USA, Scandinavia, UK); in
Scotland it appeared again in 1973, after elimination
in 1952. In many countries in Europe, Asia, Africa and
Latin America this psoroptic mange is still widespread
in sheep and of major economic importance. In goats,
Psoroptes causes ear mange that occurs worldwide.
Psoroptes infestation is also known in wild ruminants
(e.g. North America: bighorn sheep [ Ovis canadensis ],
elk [Cervus elaphus]; Poland: bison [Bison bonasus)).
In Europe and in other regions, rabbits often suffer

Table 14.6. Species of the family Psoroptldae as causative agents of mange.

'I
Genu, �nd epe�lo, 1 Hott, o,..... Prevalence In Dlltrlbutlon
Europe2
r
Genus Psoroptes Psoroptes mange
Psoroptes ovis sheep body mange +++ cosmopolitan
(syn. P. bovis, P. equ,) cattle body mange +-+++

-
equids, camel and others body mange +
Q)
C Psoroptes cunicu/i rabbit ear mange +++ cosmopolitan
·c:; (P. ovis var. cuniculi) goat, horse, sheep ear mange +
Q)
Psoroptes nata/ensis water buffalo, cattle, horse body mange ? southern Africa, (Europe)
�
Genus Chorioptes Chorioptes mange
co
C Chorioptes bovis cattle tail mange + cosmopolitan
·;:::
horse, sheep foot mange ++
goat back mange +
-� Chorioptestexa nus cattle3 tail, foot mange +++ Eurasia; America
>,
Ol Genus Otodectes Otodectes mange
0
0 ++
·enco Otodectes cynotis dog, cat. other ear mange
1 The validity of the species concept within the genus Psoroptes is questionable.
cosmopolitan

co 2 +: very rare, +: rare, ++:common,+++: very common.

a.. 3 Chorioptes texanus has been described in goats in Florida and Israel, but so far not in small ruminants in Europe.
 14. Phylum Arthropoda (arthropods)

Pretarsus: Pretarsus:
3 segments, small 3 segments, small
sucker-like pulvlllus pulvillus

9 Psoroptes <:! Psoroptes

Pretarsus: Pretarsus:
very short, large very short, large
cup-shaped pulvillus cup-shaped pulvillus

9 Chorioptes <:! Otodectes

co
-0
0
a.
.c
t
<(

Pretarus: Pretarsus:
long, unsegmented, long, unsegmented,
small pulvillus small pulvillus

9 Sarcoptes 9 Notoedres
(anus terminal) (anus subterminal)

Figure 14.23. Mange mites (Graphics: IPZ, A. Seeger; after Baker et al. 1967).

from Psoroptes ear mange caused by P. cuniculi. In
contrast, Psoroptes mange has become very rare or even
completely disappeared in horses in Europe, with the
exception of parts of southern and eastern Europe ..
Epidemiology. Psoroptes mites can survive about 2-3
weeks off the host. Transmission of mites is mainly
by direct contact with animals; the parasite can also
be acquired in a contaminated environment (barns,
vehicles, contaminated pasture fences) or can be
transmitted with grooming and other equipment,
brushes in pens, wool scraps and others. Sources are
often asymptomatically infested animals from the own or
from a foreign flock (e.g. purchase of animals, temporary
accommodation of breeding animals, animal transport,
mixing of groups of animals on common pastures). Mites
can persist unnoticed for at least one year in retreat
sites, e.g. in sheep behind the ear or in the infraorbital
or interdigital pits.
Because Psoroptes mange is highly contagious, rapid and
even epidemic spread can occur in sheep. Outbreaks
are possible at any time, but they occur most frequently
in autumn during sheep migration or in winter during
stabling. All sheep can be infested, regardless of race, age
and gender, but lambs seem to be particularly susceptible.
Part Ill. Parasites and parasitoses: metazoa
Since P. ovis mites of sheep are fairly host-specific,
mutual transmission of mites between sheep and cattle
under natural husbandry occurs rarely, if at all, and only
regionally. Rather, in most regions epidemiologically
separate host-specific strains appear to exist. In Europe,
no other reservoir host of P. ovis than sheep has so far
been identified.
In goats, long-haired breeds (Angora etc.) are especially
affected. Reciprocal transmissions of Psoroptes mites
between rabbits and goats could be substantiated, but
not between goats and sheep.
In cattle Psoroptes mange occurs regionally. It is spread
in Europe mainly through trade. Outbreaks occur mainly
during stabling in winter, and bulls are particularly
affected. In larger herds, Psoroptes mange can often
endemically persist undiscovered for several years. In
dairy herds the disease is rarer.
Ear mange caused by P. cuniculi is the most important
ectoparasitosis of rabbits. Asymptomatically infested
rabbits represent the main reservoir. Rabbits in breeding
or fattening holdings are mainly affected; pet animals
only rarely.
Immunology. In cattle, sheep and other species
Psoroptes mites initially cause a superficial perivascular,
exudative dermatitis, histologically corresponding
to an allergic reaction: highly oedematous skin and
infiltrations with eosinophils, mast cells and plasma
celJs. These changes are attributed to a hypersensitivity
reaction to mite allergens, with a reaction of the type
I (early-type) playing a central role. Sequelae include
increased inflammation, crusting and traumatic changes
as a result of the severe itching. Serum antibodies can be
detected in sheep as early as 2 weeks after experimental
infestation with P. ovis and before the onset of clinical
symptoms. In cattle, immunity that develops after a
Figure 14.24. Psoroptes mange. (a) Body mange of sheep. (b) Magnification of part of Figure (a) (Photo: U. Wree, E. Riedel).
(c) Ear mite of rabbit (Photo: IPZ).
first infestation can significantly reduce the population
density of mites after a re-infestation (100 to 1,000
times). However, immunity is not of long duration (in
cattle 2-5 months).
Pathogenesis and clinical signs. In the
pathogenesis, other factors such as secondary bacterial
infections may play a role in addition to allergic processes
(see above). For each host species, Psoroptes mange
manifests in different clinical signs.
• Sheep. Skin lesions in the densely woolly body
regions of neck, shoulders, back and flanks: initially
papules, later serous exudates, forming dry, yellowish
crusts, surrounded by a border of inflamed skin; fleece
brightening, patchy or extensive hair loss, gradually
thickening of the skin and formation of wrinkles. From
the beginning, intense itching: restlessness, continuous
rubbing, biting and scratching with the hind leg, so that
the fleece deteriorates and the skin is additionally hurt
by excoriations ( ► Figure 14.24a, b ). Other symptoms:
wool loss, weight loss, and death.
• Cattle. Body mange initially with the formation of
papules and crusts on withers, neck, tail, also on the
back and flanks, with a tendency to spread. Crusts and
hair can easily be detached from large areas; below there
are usually masses of mites. Severe itching: significant
unrest, the animals scratch and lick themselves. The
resulting self-trauma weakens the animals so that they
lose weight considerably. If >40% of the skin is affected,
the animals may die. Leather damage resulting from
Psoroptes mange is low. In animals with skin lesions of
severe exudative dermatitis, enlarged regional lymph
nodes and increased adrenal gland weights with
hyperplasia of the adrenal cortex have been observed.
The latter changes are indicative for a chronic stress
reaction caused by the infestation.

• Goat. Mostly ear mange limited to the pinna and
the ear base; only rarely are other parts of the body
also affected (neck, back, tail), especially in long-haired
breeds.
• Rabbit. Ear mange with some solid crust formation
(puff paste-like, brownish-yellow) in the ear canal in the
inner ear, often with massive mite infestation. Rarely
spread to the outside or to the middle and inner ear
(then there is often a Pasteurella infection: head tilt)
(► Figure 14.24c).
• Horse. Lesions of body mange usually start in
regions with long hair (mane base, tail), spread over
the saddle position, the shoulder and the croup.
Occasionally, there is ear mange in horses, presumably
caused by P. cuniculi ( ► Table 14.6).
Diagnosis. Mite detection in crusts and skin scrapings
(KOH technique, sensitivity 20-89%). In sheep and
cattle, ELISAs are used for specific antibody detection
for herd diagnosis (cross-reactions with Chorioptes spp.
observed). P. ovis and P. cuniculi can be differentiated
in specialised laboratories by slight morphological or
genetical differences.
Therapy and control. For treatment in sheep,
dipping with a suitable acaricide (e.g. with phoxim),
or systemic treatment with ivermectin (0.2 mg/kg b.w.
s.c.), doramectin (0.3 mg/kg b.w. i.m.) or moxidectin
(1.0 mg/kg b.w. s.c.). Treatment must, without exception,
cover all animals of the flock and should be repeated
if necessary after 2 weeks. The allergy-related mange
symptoms can persist for several weeks after the
killing of all mites. For the treatment of cattle, pour­
on formulations of the pyrethroid flumethrin (2 mg/kg
b.w.) or the macrocyclic lactones (ML) doramectin,
eprinomectin, ivermectin and moxidectin (all at 0.5
mg/kg b.w.) are particularly suitable. For some MLs,
there also are formulations available for injection.
Withdrawal periods need to be observed for edible
tissues and milk; only for eprinomectin and moxidectin
there are no such periods for milk. Control of Psoroptes
ear mange in rabbits, ► p. 607.
14. Phylum Arthropoda (arthropods)
Genus Chorioptes
Disease: Chorioptes mange.
Chorion (G): leather.
CJ)
Summary ·.;:;
en
<(
• Morphology, species. Chorloptes mites: � �, ca. 400-
600 µm long, chewing mouth parts, legs extend beyond
the lateral edge of the body, cup-shaped adhesive
pulvlllus on undivided, short stems. 1\vo valld &pecles,
which morphologically differ only slightly: Chorloptes
bovls and C. texsnus.
• Life cycle. Complete development (egg ..... larva .....
2 nymphal stages - adult) In around 3 weekl. Mites
live on akin and feed on epldermal cells, tallow and
exudatee.
• Epidemiology, occurrence. TranemlAlon by direct and
Indirect contact. In Europe Chorloptes mange affects
mainly dairy herds (tall mange), rarely sheep and horse
(foot mange).
• Pathogenesis and cllnlcal signs. Chorloptes mites
cause a hypersensitivity reaction. Consequences are
severe Itching, superficial, perlvascular dermatitis, skin
thickening, acanthosls, sponglosls, parakeratosls,
keratlnlsatlon (dandruff), and formation of exudate.
Lesions: alopecla, erythema, scales, crusts, scabs.
• Diagnosis. Detection of mites (KOH procedure ► p.
525) In skin scrapings.
cu
• Therapy and control. In cattle, treatment with -0
0
macrocycllc lactones (ML) or pyrethrolds as pour-on, a.
foot mange In horse and sheep with local washing
treatments with acarlcldes (see below). Usually, two
.c
t:'.
treatments at an Interval of 7-10 days are required, at <(
least with the washing treatment. Dlslnfestatlon of stalls
and prevention of Introduction Into the herd.
Mor phology and s pecies. Mites of the genus
aa
Chorioptes (� � 400-600, 300-450 µm long) are
smaller than Psoroptes mites but larger than Sarcoptes
mites. Characteristics of Chorioptes mites: gnathosome
approximately as long as wide, chewing mouth parts
(feed on skin debris), tarsi with short, undivided pretarsi
with large, cup-shaped adhesive pulvilli. Females lack
pretarsi at the third pair of legs ( ► Figure 14.23). There
are probably only two valid species: Chorioptes bovis and
C. texanus ( ► Table 14.6), which can be morphologically
and genetically differentiated. The following information
generally relates to Chorioptes spp. In Europe, C. texanus
often occurs in cattle and occasionally in cervids, while
in horses and sheep mostly C. bovis is found. C. texanus
has been found in the USA and Israel in small ruminants,
but not in Europe so far.
Life cycle and occurrence. The complete develop­
ment (egg, larva, proto- and tritonymph, adult) takes
about 3 weeks. The mites do not penetrate the skin, but
feed by chewing on epidermal cells, sebum and exudate.
 Part Ill. Parasites and parasitoses: metazoa
Preferred sites are densely hairy skin of the extremities or
the base of the tail in cattle. The cosmopolitan Chorioptes
mites are the most common agents of mange in cattle
and horses.
Epidemiology. Chorioptes mites are transmitted by
direct and indirect contact. The mites can survive at
least 3 weeks off the host (a maximum of 10 weeks under
experimental conditions). In cattle, Chorioptes mange is
a problem especially in dairy herds. Mange prevalence
can vary considerably over the season (38% during
stabling versus 9% during grazing). The risk of mange
was rated higher in stanchion barns than in pen barns,
but this was not confirmed in a study in Switzerland.
Predisposing factors for Chorioptes mange in cattle
are unfavourable housing climate (high humidity and
temperature), lack of light and a high stocking rate.
Chorioptes mange is less common in sheep and horses
than in cattle. In Central Europe, isolated cases of foot
mange were diagnosed in sheep in recent years.
Pathogenesis. In the initial phase Chorioptes mites,
like other mange mites, cause a hyp ersensitivity reaction
(immediate type I), which is accompanied by severe
itching. Superficial perivascular dermatitis with cellular
infiltration (especially macrophages, lymphocytes,
and plasma cells) leads to a thickening of the skin.
The epidermis is very rugged (acanthosis, spongiosis,
parakeratosis), keratinisation is significantly increased
(dandruff ), and in case of severe reaction there is also
exudate (with neutrophils). Typical lesions develop,
such as alopecia, erythema, scales, crusts and scabs.
The lesions can result in leather damage, particularly
in cattle (small, dull, dark, hardened spots).
Clinical signs
• Cattle. Tail mange with changes at the base of the
tail, in the perineum, the udder and the inside of the
hind limbs: after hair loss bran-like coatings (flakes)
and crusts and scabs. Symptoms: significant unrest,
especially at night (the animals trample, mince, beat,
rub and lick themselves). This disordered behaviour
can lead to self and foreign traumatisation (injuries by
kicking, contused wounds, hematomas on teats and
(l.)
other parts of udder).
C
TS
i5 • Sheep. Foot mange, mostly as mild, chronic disease
(l.)
� at hind legs, rarely forelegs, especially between the
c
co
dew-claws, in the fetlock, and in rams on the scrotum.
C Inflammation of the scrotum in breeding rams may cause
·;::
(l.) disorders of spermatogenesis and mating inactivity.
Prevalence, intensity of infestation and degree of lesions
C increase with age of sheep.
>,
CJ)
0 • Horses. Mostly foot mange with changes usually
0
'ui in the fetlock of the hind legs, rarely front legs or on
co the base of the tail. Long hair at the fetlock favours the
co
a.. infestation which explains the higher prevalence in cold-
blooded horses. Symptoms of foot mange: severe itching,
eczema with scales and crusts, later hyp erkeratosis
and development of wrinkles, often with tallow, greasy
surface, also with ulceration (dermatitis verrucosa).
Diagnosis. Based on clinical findings, several skin
scrapings are taken from the predilection site (preferably
from several animals of the herd) and examined
microscopically after preparation (KOH technique).
Therapy and control. Because of the manner of their
feed intake (see above), Chorioptes mites are usually only
inadequately affected by macrocyclic lactones (ML)
when injected systemically. Pour-on formulations of
ML and pyrethroids available for cattle on the other
hand have a good effect (see Psoroptes). For foot mange
in sheep, a local washing treatment with phoxim (0.05
to 0.1% solutions) is indicated. The same applies for
foot mange of horses (off-label use of phoxim). In
persistent cases, place extremities for 5 min in buckets
with working solution. Local washing treatments need
to be repeated once or several times at intervals of 7-10
days; the number of pour-on treatments depends on
the clinical and parasitological findings. Severe lesions
should also be treated palliatively. Disinfestation of
the stalls can be achieved by a 10-week vacancy or
by thorough cleaning and spraying with an acaricide.
Prophylaxis: see Psoroptes.
Genus Otodectes
Otodectes cynotis (ear mite)
Disease: Otodectosis (ear rmange). I
Oto (G): ear; dectes (G): biting, chewing; kyon (G): dog.
Summary
• Otodectos cynotls Is a Chorioptes-llke mite. Occurrence
frequent In oat, dog, fox imd other carnivores.
, Ollnloal algr,s: ear mange, therapy: s pot-on with
selameictln or l�ally with acariclde-containing ear
plugs.
Morphology and occurrence. All Otodectes mites
that occur worldwide in cats, dogs, lynx, foxes (red fox,
arctic fox), ferrets, other mustelids (mink, pine marten,
beech marten) belong to the species 0. cynotis. The mites
( � � 350-500 µm) have short, undivided pretarsi with
bell-shaped adhesive pulvilli (in � � they are missing at
the third and fourth pair of legs; ► Figure 14.23). Eggs
are large (about 170-200 µm), oval and white.
Life cycle. The overall development from egg over 1
larval and 2 nymphal stages to adult mites takes about
3 weeks. The eggs are attached by the female to the skin
■
of the ear canal. Adult mites live for about 2 months. All
stages feed on epidermal cells and exudate. The mites
are not host-specific and they are easily transmitted by
direct contact from host to host, often from cats to dogs,
especially to young animals. All contact animals must
therefore be considered as infested. Living mites are
found not only in the outer ear canal and inside the ear,
but also in the skin of the trunk. At high humidity (r.h.
�80%) and low temperatures, the mites can survive off
the host for months, but die quickly in the dry air in flats.
Cats and foxes are the preferred hosts and reservoir hosts
(prevalence: owned domestic cats in a recent European
multicentre study: 17%, red and arctic foxes in farms
38-100%, wild red foxes <10%, healthy dogs 1-3%).
About half of the otitis cases in cats and $10% in dogs
are caused by 0. cynotis. The infestation persists without
re-infestation for at least 9 months.
Immunology and pathogenesis. Mites parasitise
on the skin in the ear canal and the outer ear. They
sensitise the skin by their antigens and cause local
allergic reactions. The external auditory canal is filled
with cerumen, exudate, mite detritus and also blood.
This mixture forms a dark, greasy, waxy and, further
distal, crumbly mass.
Clinical signs. In cats variable symptoms of an otitis
externa: massive excretions in the ear canal without
itching, but also severe pruritus with minimal excretion.
Originating from the ear, dermatitis may spread to the
scalp. Independent of symptoms, 50-2,000 mites were
counted per ear canal. In dogs, rather small excretions
with mostly vigorous ear itching are typical. Generalised
Otodectes infestation is very rare. Secondary infections
(bacteria, yeasts) can lead to purulent otitis in all hosts;
mites can then often no longer be detected.
Diagnosis. Detection of mites is often successful with
the otoscope. Moreover, some material can be removed
with a cotton swab or a small sharp spoon from the ear
canal and transferred to a tube with a drop of water.
Mites leave the substrate at room temperature within
1 hour. Furthermore, smears of the removed material
can be examined microscopically either directly or after
brightening with KOH.
Therapy and control. Initially, careful palliative
treatment of the ears is recommended. Systemic therapy
is preferable to local treatment because mites can also
reside outside of the ear. Spot-on treatment of cats or
dogs with selamectin or with imidacloprid/moxidectin
has proven to be effective(► Table 19.16, p. 602). It is
recommended to repeat the treatment at intervals of 4
weeks (ML), until no more mites are detected. Contact
animals should also be treated, and the environment
decontaminated.
14. Phylum Arthropoda (arthropods)
Zoonotic importance. 0. cynotis rarely settles
temporarily in humans and can cause a papular
dermatitis, only exceptionally an otitis externa.
Selected references
C'O
ro
Baker AS (1999) Mites and ticks of domestic animals. London: E
Ol
The Stationary Office: ISBN 0 11-3100-493. en
Beugnet F, Bourdeau P, Chalvet-Monfray K, Cozma V, <(
Farkas R, Guillot J, Halos L, Joachim A, Losson B,
Miro G, Otranto D, Renaud M, Rinaldi L (2014) Parasites
of domestic owned cats in Europe: co-Infestations and risk
factors. Parasit Vectors 7: 291.
Blutke A, B6rjes P, Herbach N, Pfister K, Hamel D,
Rehbein S, Wanke R (2015) Acaricide treatment prevents
adrenocortical hyperplasia as a long-term stress reaction
to psoroptic mange In cattle. Vet Parasltol 207: 125-133.
Cozma V, Losson B, Farkas R (2015) Mange (otodectic &
notoedric). In: Beugnet F, Halos L (ed.) Parasitoses & vector
borne diseases of cats. Lyon, France: Merial S.A.S., pp.
171-178. ISBN 978-2-9550805-0-4.
Hamel D, Joachim A, L6wensteln M, Pfister K, Sllaghi C,
Visser M, Winter R, Yoon S, Cramer L, Rehbein S (2015)
Treatment and control of bovine sarcoptic and psoroptic
mange infestation with ivermectin long-acting injectable
(lvomec(®) Gold). Parasitol Res 114: 535-42.
Jacober P, Ochs H, Torgerson PR, Schnyder M, Deplazes
P (2006) A method for sheep scab control by applying
selective treatment based on flock serology. Vet Parasitol co
136: 373-378. -0
0
e
a.
Le Sueur C, Bour S, Schaper R (2011) Efficacy and safety of
the combination imidacloprid 10%/moxidectin 1.0% spot­ .c
t
on (Advocate(®) spot-on for small cats and ferrets) in the <(
treatment of ear mite infection (Otodectes cynotis) in ferrets.
Parasitol Res 109 Suppl. 1: S149-S156.
Losson BJ (2012) Sheep psoroptic mange: an update.Vet
Parasitol 189: 39-43.
Lusat J, Bornstein S, Wall R (2011) Chorioptes mites: re­
evaluation of species integrity. Med Vet Entomol 25: 370-376.
Phythian CJ, Phillips KA, Wall R (2013) Farmer perceptions of
the prevalence and management of Psoroptes ovis infestation
In sheep flocks in southwest England. Vet Rec 172: 290.
Serre C, De Bleecker K, Deprez P, Levecke B, Charlier
J, Vercruysse J, Claerebout E (2012) Risk factors for
Psoroptes ovis mange on Belgian Blue farms in Northern
Q)
Belgium. Vet Parasitol 190: 216-221.
·u
c:::
Siegfried E, Ochs H, Deplazes P (2004) Clinical development '6
and serological antibody responses in sheep and rabbits
2
Q)
experimentally infested with Psoroptes ovis and Psoroptes
cuniculi. Vet Parasitol 124: 109-124. co
c:::
·;:::::
Wall R, French N (1999) Sheep scab: its biology and control. Q)
Vet Parasitol 83: 175-330.
Wall R, Kolbe K (2006) Taxonomic priority in Psoroptes mange .£
mites: P. ovis or P. equi? Exp Appl Acarol 39: 159-162. >,
CJ)
Zahler M, Hendrikx WML, Essig A, Rinder H, Gothe R 0
0
(2000) Species of the genus Psoroptes (Acari: Psoroptidae): ·u5
A taxonomic consideration. Exp Appl Acarol 24: 213-225. co
co
0....
 Part Ill. Parasites and parasitoses: metazoa
Family Sarcoptidae (burrowing mites)
Disease: Sarcoptes mange and related forms.
Sarx, gen. sarcos(G): flesh; koptein(G): to bite, to wound;
scaber (L): rough, shabby.
Burrowing mites are stationary, permanent parasites,
whose morphology is adapted to living in the epidermis.
Three genera are of veterinary importance: Sarcoptes,
Notoedres and Trixacarus.
Genus Sarcoptes
■
IDisease: Sarcoptic mange, sarcoptosls.
Summary
• Morphology, species. The genus has only one species,
Sarcoptes scabfef, with specialised varieties in different
host species (pig, cattle, dog, human, etc.). Smell mites
(300-500 µm ��). short legs with long, undivided
pretarsus and small, bell-shaped adhesive pulvilll,
anus terminal. Causative agent of sarcoptlc mange of
animals and scabies In humans.
• Life cycle. Burrowing mites are stationary, permanent
parasites. Females dig burrows of up to 1 cm length In
the epidermis, there ovlposltlon and further development
(egg - larva - proto- and tr1tonymph - adult mite).
Overall development 2-3 weeks. Mites Initially Infest
especially the sparsely hairy skin of head, neck, auricle,
from where they spread to other body regions.
• Occurrence, epidemiology. Worldwide distribution
of sarcoptlc mange In domntlo and wild animals.
In Europe, often In domettlo pig, Int common In
dog, rarely In Ctlttle, sheep and goat( ► Table 14.7).
Transml88Ion of mltN by dlrwct contact and lndlntetly
via contaminated environment. Sll'OOptlc mltN can
eurvlve up to 3 wNkl In the damp, cool ollmat1 In
stables. Varieties of s. ,cab/II.,. u1u1lly holt•speclflc,
so although they are tranlftrrld to othtr hoeta they
do not colonlee perman,ntly. Howtver, red fo><N are
reservoir ho1ta for doge(► Table 14,7).
Q) • Pathogeneele, lmmunologv, Skin changes and
C
symptoms of aarcoptic mange are primarily triggered
·c3
'6 by allergic reaction, to mite antlgene.
Q)
� • Cllnlcal elgn1. Slmllarltlee In all species: Itching,
c
co
erythema, papular or papulo-Ye8icular and Inflammatory
C lesions, parakeratosls, hyperkeratoal1 with cruetlng,
·;::
Q) skin damage from acratchlng and rubbing, alopecla
and to some extent secondary bacterial Infections with
C pyoderma. Severe changes lead among other things
to weight loss, abnormal behaviour, systemic diseases
>,
CJ)
0 and death (especially In piglet. and foxes). Differences
0 In course of disease and predllectlon sites of mange
·u5 in the host species.
co
co T
a..
•
• Diagnosis. Mite detection in deep ski
specific aRtibody detection (pig, dog)
• liherapy, eontrol. Macrocyclic lact0nes
pyrethroids and 0�anoph0sphates are
sarcoptic mites. Through the use of Ml!
with other measures, sareoptic mar,ige
on a large scale in pig herds (► p. 590).
• Zoonotlc Importance. Sarcoptes scablelwf
animal species Oncluding dog, fox, cattle, pig
as mites of related genera (Notoedres, Trixa
see below) can temporarily infest humans and ea
pseudoscables.
Morphology and species. Adult mites are small
(length:�� 300-500 µm, r3r3 200-300 µm) and circular
in plain view; their gnathosoma is short and compact.
Only the two front pairs of the short legs protrude from
the body edge(► Figure 14.23). The two front pairs of
legs(in r3 also the fourth pair) carry a long, unstructured
pretarsus with a small bell-shaped sucker-like pulvillus.
The dorsal surface of the idiosoma has transverse
ridges and bears long bristles and centrally small,
triangular scales. The anus is terminal (cf. Notoedres
and Trixacarus).
The only species of the genus Sarcoptes is S. scabiei.
The physiologically specialised sarcoptic mites
infesting different hosts are - also based on molecular
characterisation - considered as varieties of S. scabiei
(► Table 14.7).
Life cycle. After copulation on the skin of the host,
the females of sarcoptic mites dig burrows of up to 1
cm in length in the epidermis(stratum granulosum and
spinosum), up to 5 mm per day( ► Figure 14.25). There,
mite secretions cause the dissolution of the intercellular
cell association of keratinocytes (acantholysis). The
cytoplasm of epidermal cells serves as feed for the mites.
In each tunnel there is only one female. For about 2
months, females lay 1-3 oval, large eggs( ½ body length
of the female) per day, which are deposited singly in
bulges of the tunnel. A six-legged larva hatches a few
days after oviposition, which develops in the tunnel or
in hair follicles via proto- and tritonymph to the adult
mite. After copulation which takes place on the skin,
the male dies. The overall development lasts 2-3 weeks.
Sarcoptic mites prefer sparsely haired skin, usually on
head and neck, but especially in the auricle. From there,
they spread to other body regions.
Occurrence and epidemiology. Sarcoptic mange
is found worldwide in domestic and wild animals(fox,
chamois, etc.). In Europe, it is common among domestic
pigs though with strong local differences (prevalence
of 5% of herds in Denmark, up to 92% in Bulgaria).
Sarcoptic mites were detected in Germany in 1997
in 45% of the farms (n=SO) and in 19% of the sows
(n=l,035). In some areas, prevalences could recently
 14. Phylum Arthropoda (arthropods)

Table 14.7. Species of the fa m ily Sarcoptidae.

Variety Host Disease Prevalence In Central

Europe1

bovis cattle Sarcoptes mange +

horse

----------------
equi
ovis sheep co
E
rupicaprae _ goat, chamols_ ___________ goat (1, cha�is + +_ 0)
_ __ :.:;
Cl)
camel/ --�cam _el__ ---- ------- ++ <(
- --1-
72 new world camelids +

su_ls_ ____ -�g__ __ +++

dog, lox, other canids,

---
canlslvulpes dog+/++, fox+++, ferret+
lynx, raccoon, mustelids
ham ster (+)
homlnls humans, primn�--- Scables +
+
Notoedres cat/ cat3 Notoedrosls +/++
rabbit• +
Notoedres murls rat +
Notoedres muscu/1 mouse3 +
THx1c1rus cav/ae Guinea Trlxacarosls
1 +++: very common, ++: common, +: rare, (+): very rare.
2 ?: unknown.
3 In cat and mouse rarely also S. scablei.
4 In rabbits rarely also S. scabiel var. canls.

f/:�
. rotonyrnph
Tritonymph
a.
e

� Larva
Male
Female

Eggs
---- ()a)© o----
Mite refugium:
auditory canal

Transmission of mites from

animal to animal
Q)
C
T5
'6
Q)

co
C
·.::::
Q)

C
>,
0)
0
Transmission of mites Mite refugium: 0
from the environment tarsal flexure ·u5
co
Figure 14.25. Life cycle of Sarcoptes scabiei var. suis (Graphics: IPZ, S. Ehrat). 0...
 Part Ill. Parasites and parasitoses: metazoa
be considerably reduced due to control measures (see
below). In areas with endemic sarcoptic mange in fox,
the disease also frequently occurs in dogs; dogs in
contact with foxes are more often infested. Sarcoptic
mange in red foxes occurs in some countries focally or
widespread (including CH, FR, DE, northern IT, SE,
DK). After its introduction in SE (1975), the parasite
spread almost all over the country within 8 years, leading
to high mortality in the red fox population, and also
affected arctic foxes (Alopex lagopus), lynx (Lynx lynx),
farm foxes and domestic dogs. Sarcoptic mange is rare
in cattle, sheep and goat; this form of mange can be
regarded as eliminated in the horse in Europe (► Table
14.7). Sarcoptic mange endemic in the Alpine region
(east of Switzerland) causes mortality of up to 20% in
chamois during major outbreaks. This form of mange
also occurs in the Alpine and Iberian ibex, and rarely
in cervids.
Sarcoptes mites are usually transmitted by direct animal
contact, especially in group-housing in stables (flock
disease). In pigs, mites migrate from the sow to the piglet,
but can also be transmitted upon contact at a later age.
In addition, indirect transmission from a contaminated
environment (stable, run-out yard, transport vehicles) or
by appliances (stable equipment, grooming equipment,
etc.) is possible. Mites can survive in skin debris under
damp, cool stable conditions (ca. 10 °C) for up to 3
weeks, especially in litter, brooms, brushes, etc. Even
outdoors, they remain viable for a long time in crevices
of wooden poles or tree bark and on wire meshes. Under
housing conditions, mange occurs year-round in pig
herds, and usually in winter or early spring in cattle.
Most host-specific varieties of S. scabiei accidentally
infest other hosts, but do not reproduce. Nevertheless,
they can cause skin changes (pseudoscabies), e.g. in
humans. However, there are exceptions, such as in
canids: S. scabiei var. canis/vulpes can be transmitted
between red foxes, dogs, other canids, lynx, raccoon
and likely mustelids regardless of the season.
Pathogenesis and immunology. After experimental
primary infestation of pigs that previously had no contact
with sarcoptic mites, mange develops in different phases
Q)
which can be summarised in a simplified manner as
follows:
·u
C
'6
Q)
� • Incubation. 2-3 weeks p.i.: minor local skin reactions
cco by burrowing mites, no symptoms or minor itching.
C intake, to reduced physical fitness, weight loss, abnormal
·;:::
Q) • Hyperergic phase. From the 2nd to the 3rd week
j p.i., severe itching, erythema, papules, excoriations, also
-� papulovesicles (► Figure 14.26a). From the yd to the 7th
>,
week p.i., continuing itching with highest intensity at the
-
0)
0
0
beginning (5th to the 8th week), then gradually easing;
·a; parakeratosis, hyperkeratosis, crusting, some persistent
co papules. Seroconversion after week 5 p.i. Duration of this
co
0..
phase is about 4-5 months. Thereafter, clinical symptoms
gradually subside. At this stage, there are initially allergic
reactions of the delayed type ( type IV) and later of the
immediate type reactions (type I), the latter dominate
towards the end of this phase ( ► Figure 14.26b).
• Desensitisation. Allergic reactions and clinical
symptoms recede; the animals remain carriers of mites.
Sarcoptic mange is essentially an immunopathy,
caused by complicated processes. In the first phase
of the infestation, the host reacts to the invasion by
keratinising the burrows of the mites which react with
increased salivation to boost keratolysis. If the defence
reaction of the host suffices, the mites are rejected,
with excess keratin and self-healing. At the same time,
immunological reactions to mite antigens (e.g. from
saliva, body components, faeces, eggs) begin that cause
allergic reactions of the delayed type ( type IV) and then
the immediate type (type I), and they also activate
effector cells. After antigen presentation in local lymph
nodes and migration of antigen-specific T-cells into
the dermal reaction area, a cascade of other processes
follows. Thus, keratinocytes - important components of
SALT (skin-associated lymphoid tissue) - secrete a broad
spectrum of cytokines, which activate, among others,
Langerhans cells, dermal dendritic cells, macrophages
and other effector cells. At the same time, immediate
allergic reactions mediated by IgE antibodies develop. In
the area of the dermal lesions, cell infiltrates of variable
composition are created (neutrophils, T-lymphocytes,
plasma cells, eosinophils, macrophages, mast cells).
Neutrophils release oxygen radicals and proteolytic
enzymes, which likely contribute in immune hosts to
reduce the mite infestation.
Pigs of all ages from herds that have been free of mange
for some time are highly susceptible to S. scabiei. This
is evidenced by rapidly spreading mange outbreaks in
such herds originating from introduced mite carriers
(e.g. breeding boars).
Clinical signs. Common clinical signs in the various
animal species that are affected by sarcoptic mange
include itching, erythema, papular or papulo-vesicular
and inflammatory skin lesions, hyperkeratosis with
crusting, skin damage from scratching and rubbing,
alopecia and to some extent secondary bacterial infections
with pyoderma (► Figure 14.26). Severe changes of this
kind lead among other things to disturbances in feed
behaviour, generalised diseases and deaths (especially in
piglets). In infested pigs, weight gain was significantly
lower and feed conversion efficiency was reduced by
2% as compared to mange-free animals, even under
favourable husbandry conditions. Economic losses are
estimated at € 100 annually per sow.

Figure 14.26. Sarcoptes mange: (a) in pigs, papules on skin, acute phase of infestation (Photo: IPZ); (b) with crust formation,
chronic mange (Photo: IPH); (c) in cattle (Photo: A. Lieblsch); (d) in dromedary (Photo: IPZ).
Skin lesions caused by sarcoptic mites are primarily
found in sparsely haired parts of the body.
• Pig. Lesions and mite refugia are often located in
the inner ear, behind the ear, the nose, the neck and back
as well as in the bends of joints. Particularly striking are
the thick scabs and crusts in chronic (hyperkeratotic)
mange; the initial papular changes are often overlooked
(► Figure 14.26a, b).
• Cattle. Itching, locally thinning hair, dandruff
and skin thickening with wrinkles on head and neck,
shoulder, udder, tail and back. Infestation sometimes
occurs with hardly noticeable symptoms and gradually,
partly with significant symptoms and rapid spread in
herds(especially in fattening units)( ► Figure 14.26c).
• Sheep and goat. Sarcoptic mange manifests
primarily as head mange, but has a tendency to spread
to other parts of the body.
14. Phylum Arthropoda (arthropods)
cr!
"O
0
a.
e
..c
t::
<(
• Wild ruminants. Regional occurrence of Sarcoptes
mange in chamois, ibex and rarely in cervids. In chamois,
mange often leads to severe disease and death.
• Dogs. Changes often on ears and head, with
tendency to spread to chest, ventral abdomen and legs
(elbow); the back is usually not affected. Puppies and
young dogs become sick more frequently than older
animals.
• Cats suffer rarely from Sarcoptes mange, but rather
from Notoedres mange(see below).
• Other host species. ► Figure 14.26d. The
formerly common and feared Sacoptes mange of the
horse no longer occurs in central and northern Europe;
the compulsory notification has now been abolished in
most European countries. In AT, with 'mange' infested
or suspicious equidae must be treated by a veterinarian
according to the Protection of Animals Act(§ 39). The
 Part Ill. Parasites and parasitoses: metazoa
suspected causative agents of the rare cases of mange in
horses are mites of foxes. In rabbits, mice, hamsters,
hedgehogs, among others, Sarcoptes infestations are
rarely observed.
Diagnosis. Skin lesions and itching are important
indicators of Sarcopes mange, but can only constitute a
tentative diagnosis. The etiologic diagnosis is made by
direct or indirect detection of mites.
• Pig. For the direct detection of mites, skin material
(several cm2) is deeply scraped (until capillary bleeding
occurs) with a surgical curette at several lesions of the
skin, especially in the transition zone to healthy tissue.
Inner ear, ear base, nose and flexures are refugia of the
mites and therefore suitable locations for the collection
of samples. In herd examinations, samples of several
animals and animal groups have to be taken. The skin
scrapings are stored in tightly sealed plastic or glass
containers and examined in the laboratory for the
presence of mites ( ► p. 525) (Decontaminate utensils
after use in a herd in 70% ethanol or by heat). In chronic
mange, the skin is usually populated by only a few mites.
The sensitivity of direct detection of mites can drop in
such cases to <10%. Of great significance is the control
of eradication programmes for the certification of
Sarcoptes-free breeding flocks. Best results are obtained
with a combination of the following examination
findings: (a) clinical findings (lesions and chafing index),
(b) microscopic findings (skin scrapings), (c) serological
findings (ELISA: serum, colostrum) and (d) carcass
inspection (pinnae; possibly serology). ELISA, although
of relatively low sensitivity (60 to >80%), results together
with microscopic findings in a reliable herd diagnosis,
particularly in older sows and their piglets; ELISA is also
suitable for epidemiological studies. Carcass inspections
can be an inexpensive alternative to serological tests.
After eradication of mange in a herd, specific serum
antibodies persist in a part of the animals for 5 months
to 1 year; specific colostrum antibodies even longer.
• Other host species. By direct detection of mites as
described above. In the dog, edge of ear, elbow and tarsal
joint are the considered predilection sites. An ELISA for
the specific detection of antibodies is also available for
Q)
this species (sensitivity and specificity about 85-90%).
·u
C in dogs. Parasitol Res; 107: 279-283.
'6 Therapy and control. Effective substances for the
Q)
� treatment and control of Sarcoptes mange of farm animals
are different macrocyclic lactones and some acaricides
(U
C from the group of pyrethroids and organophosphates.
·;::
Q) Cattle, sheep and goat are to be treated as for Psoroptes
mange ( ► p. 439). In pigs, injection treatment with
C ivermectin (0.3 mg/kg b.w. s.c.), with ivermectin orally
>,
CJ)
as premix (0.1 mg/kg b.w./d for 7 d) or doramectin
0
0
(0.3 mg/kg b.w. i.m.) has proven successful. For the
"iii eradication of sarcoptes mange in swine herds ► p. 590.
(U
Against Sarcoptes mites in dogs, selamectin (spot-on,
at least 2 treatments, 4 weeks apart), or imidacloprid +
moxidectin (monthly, spot-on, 2-3 treatments) have been
used with success ( ► Table 19 .16, p. 602). Importantly,
all dogs in a contact group, even those not obviously
diseased, must be treated, and the closer environment
of the dogs must b e decontaminated (resting areas,
blankets).
Zoonotic importance. In humans, mange or scabies,
caused by Sarcoptes scabiei var. hominis, is transmitted by
close contact from person to person and is not a zoonosis.
However, Sarcoptes species of numerous animal species
(including dogs, foxes, cattle, pig, camel) as well as mites
of related genera (Notoedres, Trixacarus) can migrate to
humans and cause the clinical signs of pseudoscabies.
In pseudoscabies, in contrast to scabies, itching already
occurs a few hours after the infestation with mites,
which penetrate the epidermis and cause papules and
papulovesicles but usually neither dig tunnels nor
multiply. The changes disappear spontaneously in the
absence of re-infestations; mites cannot usually be
detected on humans. According to previous reports, S.
scabei var. canis can remain some time on humans and
even produce eggs, but clear information is lacking.
.. Selected references
Birrer S, Neff F, Zimmermann W (2004) Sarcoptes scabiei
var. suis-lnfektion: eine seroepidemiologische Studie mil
Blut- und Kolostralmilchproben zur Oberwachung und
Zertifizierung der medikamentosen Tilgung der Rauda in
Schweinezuchtbetrieben. Tierarztl Prax 32: 88.
Casals R, Kevin P, Dalton KP, Javier Millan J, Ana Balseiro
A, Oleaga A, Solano P, Goyache F, Prieto JM, Parra F
(2014) Primary and secondary experimental infestation of
rabbits (Oryctolagus cuniculus) with Sarcoptes scabiei from
a wild rabbit: factors determining resistance to relnfestation.
Vet Parasltol 203: 173-183.
Davidson RK, Bornstein S, Handeland K (2008) Long-term
study of Sarcoptes scablei Infection In Norwegian red foxes
(Vulpes vulpes) indicating host/parasite adaptation. Vet
Parasitol 156: 277-283.
Feather L, Gough K, Flynn RJ, Elsheikha HM (2010) A
retrospective investigation into risk factors of sarcoptic mange
Goyena E, Ruiz de Ybanez R, Martinez-Carrasco C, Balseiro
A, Alonso de Vega F, Casais R, Prieto M, Garcia-Marin
JF, Berriatua E (2013) On the aggregated nature of chronic
Sarcoptes scabiei infection in adult pigs. Vet Parasitol 192:
301-306.
Hejduk G, Hofstatter K, Lowenstein M, Paschke R, Miller
I, Joachim A (2011) Characterisation of Sarcoptes scabiei
antigens. Parasitol Res 108: 309-315.
Rodriguez-Cadenas F, Carbajal-Gonzalez MT, Fregeneda­
Grandes JM, Aller-Gancedo JM, Rojo-Vazquez FA
(2010) Clinical evaluation and antibody responses in sheep
 14. Phylum Arthropoda (arthropods)

after primary and secondary experimental challenges with

the mange mite Sarcoptes scabiei var. ovis. Vet lmmunol
lmmunopathol 133: 109-116.
Vercruysse J, Geurden T, Peelaers I (2006) Development and
Bayesian evaluation of an ELISA to detect specific antibodies
to Sarcoptes scablei var. suis in the meat juice of pigs. Vet
Rec 158: 506-508.
co
Zahler M, Essig A, Gothe R, Rinder H (1999) Molecular E
analyses suggest monospeclficity of the genus Sarcoptes _g>
t5
(Acari: Sarcoptidae). Int J Parasitol 29: 759-766. <!.

Genus Notoedres

Figure 14.27. Notoedres mange In cats (Photo: IPZ. Small

Disease: Notoedres mange, notoedrosls. Animal Clinic, ZOrlch).

Noton (G): back; eclres(G): seat. Refers to the dorsal
position of the anus of the mites.
Summary
• Notoedres cati is the causative agent of Notoedres
mange in cats , which is very similar in appearance to
Sarcoptes mange, usually starts on the head and then
may spread to the legs and other body areas.
rapidly succumb 10 severe notoedrosis, but also older
cats emaciate, become apathetic and die after 4-5 months
ifleft untreated. The disease thrives in the face of poor
animal husbandry(stray cats), malnutrition and other
diseases( ► Figure l4.27).
Diagnosis and therapy. Detection of mites in skin
scrapings. Differential diagnosis: especially Sarcoptes
(rare) and Otodectes. Against notoedrosis of cats,
selamectin(3 treatments at intervals of two weeks with

aa
Morphology and species. Notoedres species are 6 mg/kg b.w., spot-on)(off-label use). According to case
small(�� approx. 225 µm, about 150 µm long), reports, also a full body treatment with fipronil spray co
nearly circular mites in plain view, with concentric rings has proven to be effective. This substance can also be "'O
0
in the dorsal cuticle and a subterminal anus(terminal used to treat contact animals(including dogs)( ► Table Q.

in Sarcoptes). Gnathosoma very short, short compact 19.16, p. 602). Disinfestation of the environment is not .c
t::
legs with long, unstructured pretarsi as in Sarcoptes required because of the short life span of the mites. <!.
( ► Figure 14.23 ). The most important species is
Notoedres cation cats, other felines (especially lynx) Genus Trixacarus
and occasionally on fox, dog and rabbit. Because the
experimental transmission from cat to rabbit is difficult, Trixacarus caviae causes a disease in guinea pigs that
it is suspected that host-specific varieties(N. cati var. corresponds to Sarcoptes mange, and migration to
cuniculi) exist(as in S. scabiei). Other species on rodents humans is not unusual.
► Table 14.7.

Life cycle, occurrence and epidemiology. Selected references

The development largely resembles S. scabiei,
transmission occurs by direct contact, rarely indirectly Cozma V, Losson B, Farkas R (2015) Mange (otodectic &
via contaminated environment. Life span of mites off notoedric). In: Beugnet F, Halos L (eds.). Parasitoses & vector
Q)
the host barely three days. Notoedrosis of cats occurs borne diseases of cats. Lyon, France: Merial S.A.S., pp.
·o
C

worldwide, but is rare in northern and Central Europe 171-178; ISBN 978-2-9550805-0-4.
(prevalence <2% for stray cats). In rabbits, notoedrosis ltoh N, Muraoka N, Aoki M, ltagaki T (2004) Treatment of
2
Q)

is a rare infestation. Notoedres cati infestation in cats with selamectin. Vet Rec
154: 409. co
C
·;;::
Pathogenesis and clinical signs. Pathogenesis Ryser-Degiorgis MP, Ryser A, Bacciarini LN, Angst C, Q)
similar to Sarcoptes infestation. Clinical signs: severe Gottstein B, Janovsky M, Breitenmoser U (2002)
itching, first lesions on the edge of ears, rapid spread Notoedric and sarcoptic mange in free-ranging lynx from .£
over the ears, the forehead, the entire head and neck, Switzerland. J Wildl Dis 38: 228-232. >.
Ol
later generalisation; first tiny papules, then thickening 0
0
of the skin with formation of wrinkles and formation ·en
of crusts(hyp erkeratosis), bran-like coating as well as
co
excoriations as a result of scratching. Young cats very Cl..
Part Ill. Parasites and parasitoses: metazoa
Other families of the order Astigmata
Astigmata include more families of mites that have some
significance especially in birds and rodents. Family
Knemidocoptidae: Knemidocoptes pilae: causative agent
of beak mange in budgerigars, less common in other
parrots; K. mutans: causative agent of scaly leg disease
of gallinaceous birds; K. gallinae: causative agent of a
disease of the plumage of gallinaceous birds. Family
Cytoditidae and Laminosioptidae: Cytodites nudus (air
sac mites) and Laminosioptes cysticola (nodule mite) in
gallinaceous birds. Family Falculiferidae, Analgidae
and Epidermoptidae: feather and skin mites in poultry.
Family Myocoptidae and Listrophoridae: different
species colonise the coat of small mammals (mice,
guinea pigs) or felidae.
Selected reference
Dabert J, Mihalca AD, Sandor AD (2011) The first report of
Knemidocoptes intermedius Fain et Macfarlane, 1967 (Acari:
Astigmata) in naturally infected European birds. Parasltol
Res 109: 237-240.
Free-livi ng mites as pathogens
The order Astigmata contains a number of families
with free-living mites that have some significance
as pathogens. These are mites with lengths of about
300-700 µm, partially very hairy and differing in
morphology from the parasitically living Sarcoptidae
and Psoroptidae by various characteristics, including a
claw-like empodium on the pretarsus ( ► Figure 14.28).
Some of these species are described below:
Figure 14.28. Tyrophagus lintnerl S1 (length about 600 µm)
(Graphics: IPZ, A. Seeger; after Baker et al. 1967).
• Family Acaridae. Acarus siro (syn. Tyroglyphus
farinae) (flour mite); Tyrophagus putrescentiae (mould
mite) in houses on stored products of all kinds, often a
pest in humid new buildings, also in hives. Caloglyphus
berlesi in flour, bran, in animal stables, bee hives, on
food of plant and animal origin.
• Family Glycyphagidae. Glycyphagus domesticus
(storage mite) is very common on stored products of all
kinds, also in bee hives; G. destructor (syn. Lepidoglyhus
destructor) (plum mite) very often in hay, straw, grains
and dried fruit.
• Family Pyroglyphidae. Dermatophagoides
pteronyssinus (European house dust mite) in inhabited
houses in beddings, resting sites, other hiding places,
feed on skin scales and other organic material.
These mites contain potent allergens (e.g. in integument,
faeces and saliva) which can cause allergic diseases with
skin lesions, or respiratory or intestinal symptoms in
humans and rarely in animals.
Selected references
Bensignor E, Carlottl DN (2002) Sensitivity patterns to dust
mites and forage mites in atopic dogs: 150 cases. Vet
Dermatol 13: 3 7 -42.
Farmakl R, Sarldomichelakis M N, Leontldes L,
Papazahariadou MG, Gioulekas D, Koutinas AF (2012)
Dust mite species In the households of mite-sensitive dogs
with atoplc dermatitis. Vet Dermatol 23: 222-245.
►-!

14. Phylum Arthropoda (arthropods)

-Subphylum Mandibulata 14.3.1 Order Blattaria (cockroaches)

14.2 Class Crustacea
(crustaceans)
Crustaceans differ from Amandibulata by the possession
of two pairs of antennas and 3 pairs of mouthparts, by a
different body structure and the number oflimbs. They
are mentioned here because some genera play a role as
ectoparasites of fish, e.g. Ergasilus, Lernaea and Argulus
('fish lice'). Furthermore, crustaceans have signitkance as
intermediate hosts ofhelminths (including Paragonimus,
Diphyllobothrium, Dracunculus).
14.3 Class lnsecta (insects)
In (L, prefix): in; secare (L): to cut. Refers to the
segmented body.
Summary
• Insects (hexapoda) are characterised by the following
features (► Figure 14.29):
- Body divided into three parts: head, thorax and
abdomen.
- 3 pairs of legs, one or two pair of wings which are
reduced or absent In some cases.
- 1 pair of segmented antennas.
- Mouthparts with different functions.
- Complex eyes (compound eyes) or small frontal eyes
(ocelli).
- Partially morphological adaptations to the parasitic
way of life, e.g. loss of wings or eyes.
• Life cycle:
- Hemimetabollc life cycle (Incomplete metamorphosis):
juveniles resemble the adults, no pupal stage.
- Holometabollc life cycle (complete metamorphosis):
juveniles differ morphologically from the adults;
metamorphosis takes place In the pupal stage that
does not Ingest feed.
Blatta (L): cockroach.
Cockroaches are large, dorsoventrally flattened insects
with long, many-segmented antennae and 2 pairs of
true or reduced wings. Most species occur in the tropics
and subtropics. A number of species were introduced
to temperate zones and now live in buildings and play
a role mainly as storage pests in kitchens, bakeries,
apartments, warehouses, hospitals, etc. Sometimes they
are very numerous in stables, e.g. in poorly managed
pig and poultry farms, in zoos and pet shops. These
cockroach species have chewing mouthparts, they are
omnivorous or vegetarian, are mainly active at night
and have a hemimetabolic development for which they
need a warm and moist environment. Under favourable
conditions adults live up to 2 years. They are easily
displaced in transport containers (e.g. containers with
fruit or baked goods, kitchen waste). For humans they
are nauseating, they can also mechanically transmit
numerous pathogens (including Salmonella, Shigella,
Escherichia coli, fungal spores), and they also act as
intermediate hosts (e.g. for Hymenolepis diminuata,
Gongylonema spp., Prosthenorchis spp.). In Europe,
the kitchen cockroach (Blatta orientalis, length 20-25
mm) and the German cockroach (Blattella germanica,
length 10-15 mm) are common; the American cockroach
(Periplaneta americana, length 30-50 mm) and some
other species are less common. ro
-0
0
a.
.c
t::
<(

Head Thorax Abdomen

Compound
eye Salivary gland

Labru
Mandi
1 st maxi Coxa
2nd m Trochanter Genital pore
Femur Receptaculum seminis
Ovary
Suboesophageal
ganglion � Nerve cord
Tarsus
Figu re 14.29. Scheme of an insect (Graphics: Enke Verlag).
 Part Ill. Parasites and parasitoses: metazoa

14.3.2 Order Phthiraptera chewing lice of mammals and birds, however, Ischnocera
are the dominating lice of mammals. T he tarsi have one
Phtheir (G): louse; pteron: wing. or a pair of claws. Lice of domestic animals and pets are
1-2 mm long. Most bird lice have similar sizes, some,
14.3.2.1 Suborders Amblycera and e.g. Anaticola anseris of geese, are up to 4 mm long.
lschnocera (chewing lice)
The chewing lice that frequently occur on companion
Amblyis (G): blunt; ischno (G): slender; keras (G): horn. animals and their specific hosts are listed in ► Table
Refers to the shape of the antennas. 14.8. B. limbatus is more prone to infest angora goats
and is a worldwide problem in mohair production, but
Summary does not permanently infest goats of other breeds. Pigs
and rabbits have no chewing lice. The main lice of birds
• Morphology, species. Wingless, mostly 1-4 mm long,
are given in ► Table 14.8; the most important species
dorsoventrally flattened Insects; permanent-stationary
ectoparasltes of mammals and birds; head usually
are Menacanthus stramineus (chicken body louse) and
wider than the first thorax segment, antennas 3 to Menopon gallinae.
5-segmented, chewing mouthparts. High biodiversity.
• Life cycle. Eggs (nits) are glued to hairs or feathers, Life cycle. Phthiraptera have a hemimetabolic life
hemlmetabolic development with 3 larval stages from cycle; therefore, pre-adult (=larvae) and adult stages are
egg to adults (males and females) In 4 weeks. Feed on very similar ( ► Figure 14.31). Reproduction is usually
components of the skin or feathers and bacteria, and sexual, with some species also being parthenogenetic.
partly on blood (Amblycera).
• Occurrence, epldemlology. High specificity for
Individual species, partly for specific body regions.
Mostly cosmopolitans. In Europe, chewing lice are
common In cattle and sheep herds, often In mixed
infestations with sucking lice. Transmission of all
stages from animal to animal through contact, also by
persons and equipment. Adult chewing lice survive off
the host 2-4 weeks. Pronounced seasonal fluctuations
In population densities on mammals, with the strongest
Infestations occurring In winter and spring. Chewing
lice are very common parasites of poultry.
• Pathogennle, cllnlcal algne. Chewing lice Irritate,
cause Itching and self-wounding (excortatlons). In sheep
significant fleece and skin damage (leather damage);
In other mammals usually multlfactortal disease, but
In case of mase Infestation skin changes/lesions up
to weeping eczema and reduced dairy and fattening
performance. Bird lice cause Itching, feather damage
and skin lesions.
• Therapy, control. In cattle and sheep, pour-on or
spray treatments with Insecticides Qnjectlon treatment
with macrocycllc lactones Insufficient), In birds use of
Insecticide powders. Repeat treatment as nits are not
affected.

Q)
Morphology and species. The suborders Amblycera
and Ischnocera, formerly classified as suborder
·o
C

'6 Mallophaga (Mallos (G): wool; phagein (G): eat. Refers

Q)
� to the diet) contain >2,600 species. The body of the
c chewing lice is dorsoventrally flattened; the head is
co
C usually wider than the first thorax segment ( ► Figure
·;::
Q) 14.30). The two suborders differ most clearly at the
antennae (Amblycera: 4 segments, in a groove lateral
C of the head; Ischnocera: antennas clearly visible, 3-5
>,
0)
segments). Maxillary palps (2-4 segments) are found
0 only in the Amblycera. Amblycera can open blood
0
·u5 vessels with their biting mandibles. The mandibles of
Ischnocera are perpendicular to the bottom of the head. Figure 14.30. Chewing lice: (a) Bovicola bovis � (length about
co
0.. Eyes are mostly present. In both suborders there are 1.5 mm) (Photo: IPZ); (b) Bovico/a bovis in fur of a cow (Photo:
IPG).
 14. Phylum Arthropoda (arthropods)

Table 14.8. Selection of chewing lice1 on mammals and birds.

~

HOit Chewing UM of mammals Host Chewing llce of birds

Bovicota2 bovis (I) chicken Menopon gallinae (A), Menacanthus stramineus (A).
I
Cattle
Goniocotes gallinae (I), Goniodes gigas (I), Goniodes
disslmilis (I), Cuclotogaster heterographus (I), Lipeurus

Sheep
-
Bovlcola ovis (I)
-
caponis (I)
�key .Menacanthus stramineus (A), Chelopistes melagr/dis (I) -
- -
Cu
,.__
(l)
0.
cu
- -
Bovicola caprae (I), Bovicola limbatus (1) 3, dove Hohorstiella lata (A). Columblcola columbae (I).
'-
Goat £
Bovicola (Holakarlikos) crassipes (I) Campanutotes compar (I) --
.c
Q_
Horse Bovlcota (Wernecklella) equl (I) goose Anatlcola anseris (I). Anatoecus lcteroldes (I). Trinoton
anserinum (A) --
Donkey Bovlcola (Wernecklella) equl trslnl (I), duck Anaflcola crasslcornls (I). Anatoecus dentatus (I),
Bovlcol� (Wernecklells) oce//atus Trinoton c,uerquedulae (A) ·--
Soutll American Bovtcola bl8vlceps (I)
camellds -
Dog Trlchodectes canls (I)
Cat Felico/a subrostratus (I)_ -
Guinea pig Gllricola porcelli (A), Gyropus ova/ls (A),
Trlmenopon hlspidum (A)
1 (A): Amblycera, (I): lschnocera.
2 Synonym of the genus Bovicola: Dama/In/a.
3 Mainly on angora goats.

a,
"O
0
e
0.
.c
t:::
<(

Imago

Eggs (nits)
Larva 3
Moulting attached to
a hair
Larva 1

Q)
C
·13
'6
Q)
2
c
cu
C
·;:::
Q)
j
C
>,
0)
0

Transmission through contact .....

0
·u;
�
Fi gure 14.31. Developmental cycle of Bovico/a bovis (Graphics: IPZ, S. Ehrat).
cu
Q_
 Part Ill. Parasites and parasitoses: metazoa
Females glue their eggs (nits) to hair or feathers. After
4-12 days, larvae 1 hatch which develop over 2 more
larval stages in about 3 weeks and three moultings into
adult males and females.
Chewing lice live on the skin surface close to the
hair base or in the plumage; they feed on skin scales,
lipids and bacteria, bird lice also on parts of feathers.
Amblycera also ingest blood, in the case of bird lice
after biting into the quills. All stages decompose the
feed outside, insalivate and ingest it. Endosymbionts
provide the digestion of keratin.
Occurrence and epidemiology. Most species of
chewing lice are cosmopolitans. In Europe, chewing
lice are frequently found in bovine herds. Thus, B. bovis
was observed in 28% of 30 dairy herds in Norway. In
a representative survey in Germany (2002), B. bovis
was found in 39% of 968 farms. Also in sheep herds
lice are common (e.g. 10.7% of the farms in the UK).
In horses, chewing lice are rare in Central Europe
but high prevalences (40%) were reported in Iceland.
Since Phthiraptera are highly host-specific, there is
no transmission between various host species, with
the exception of sheep and goat. Infestation occurs by
contact among animals, and both larvae and adults
can migrate to another host. Transmission can also
occur indirectly via brushes attached in pen barns for
cattle as well as via animal keepers and shearers with
their equipment and their clothing. Adult lice live on
the host for l-2 months, and off the host in moderate
temperatures for 2-4 weeks. B. ovis can survive in
untreated, stacked sheep wool for about 4 weeks.
The spread of lice in a group of animals occurs relatively
slowly. In studies with B. ovis, it took almost one year
after incorporating infested animals in a lice-free herd
until clinical symptoms appeared. In another study, lice
had spread from an affected animal within 22 weeks to
84% of animals in a sheep flock. Population densities
of chewing lice are often characterised by fluctuations.
In cattle and sheep, highest densities occur In winter
and early spring. Very high infestation intensities can
be reached, e.g. > l million per sheep. The reduction
of infestation in sheep in late spring and summer was
attributed to shearing and seasonal changes in weather
Q)
conditions, but according to recent studies this might
·u
C
'6 not hold true. In sheep, there are large individual and
Q)
� breed-dependent differences in susceptibility to B. ovis.
2:-
co
C Cyclical changes in the number of parasites also occur
·.:
Q) in lice of birds. According to studies on wild birds, there
j is a proliferation of parasites particularly during the
C breeding season.
>,
Ol
0 Immunology. The lifestyle of chewing lice would
0
·en suggest that there is no distinct immunological reaction
co of the host. Studies in sheep, however, show that B.
co
0... ovis induces the formation of specific antibodies, the
activation ofT-cell populations as well as hyp ersensitivity
reactions (types I and II) in the skin that play a role
in the pathogenesis of skin lesions. In addition, sheep
appear to control infestation intensities of B. ovis
by immunological means but it is unclear by which
mechanisms this is accomplished.
Pathogenesis and clinical signs. Infestation
with lice is usually well controlled by healthy
domestic animals and remains asymptomatic. In sick,
malnourished or poorly kept animals, however, there can
be mass propagation (multifactorial disease). Clinical
manifestations occur according to seasonal changes in
population densities of lice, especially during housing
periods in winter and early spring.
In infested cattle and sheep, the dermis shows
inflammatory infiltrates with eosinophils and basophils
as well as mononuclear cells with increased proportions
of CD3, CD4 and MHC class II-expressing cells. Lice by
their movement on the skin cause itching, resulting in
the clinical pictures of excoriation, squamous changes
and thickening of the skin, in sheep also considerable
wool damage. The fleece is shaggy, single tufts of hair
protrude, and there is local alopecia. In sheep, goat and
cattle, fattening and milk production are reduced in
periods of heavy infestations with chewing lice. After
tanning, leather damage is found (cockle). In dogs
and cats, the coat is dull and flaky; focally, there occur
excoriations and alopecia. Predilection sites are head
and back. Among pet animals, especially guinea pigs
are affected by chewing lice; the main symptoms are
similar to those in dogs and cats.
In poultry (and other birds), the various species of
chewing lice affect different body regions. Menacantlrus
stramineus, the most important species in poultry, lives
on the skin in regions of the chest, back and cloaca(
area. The parasite like other Amblycera bites into the
quills which causes feather death. Infestations of chicks
manifest as damage to the downy plumage. lschnocera
feed on feather parts. Beyond this direct feather damage,
the lice cause itching with their partially very lively
movement.
Vector role. Lice of carnivores (Trichodectes carlis,
Felico/a subrostratus) can - in addition to fleas - be
intermediate hosts of Dipylidium.
Diagnosis. In case of mass infestation, parasites can
be detected in parted hair and fleece coat, in birds
in the feathers, with the naked eye or with the aid
of a magnifying glass (but sensitivity in case of low
infestation in sheep is about 2%). It is helpful to shear
hair at frequently affected parts of the body (e.g. head,
shoulder, pelvic area in cattle) and scrape the skin
surface with a scalpel. Alternatively, the adhesive tape
method can be used ( ► p. 525). Exposing wool samples
to strong light for 10 min causes lice to migrate away

from the hair and renders them easily detectable with
a stereo-microscope. Hair samples can also be analysed
with the KOH method ( ► p. 525). Nits on hair are
microscopically recognisable. Bird lice nits are often
detectable by macroscopic examination of feathers,
because a large number of them frequently adhere
to single feathers. M. stramineus lays eggs in clusters
particularly on feathers in the cloacal region.
Treatment and control. For the treatment of chewing
lice in cattle, pour-on formulations of pyrethroids
(cyfluthrin, deltamethrin, flumethrin) and macrocyclic
lactones(ML)(doramectin, eprinomectin, ivermectin,
mox.idectin) are approved. Furthermore, phoxim can be
used as spray(dosages ► Table 19.4, p. 583). Injectable
formulations of ML are not very effective against
chewing lice. For the therapy in sheep, deltnmethrin
(pour-on) and phoxim(spray or dip treatment) among
others are available (dosages ► Table 19.4). Shearing
before treatment increases the efficiency significantly.
For sheep with a thick fleece, dip or spray treatment
should be preferred over the pour-on application. Goats
can be treated with the preparations approved for sheep
(off-label use). In horses, phoxim can be used in spray
and wash treatments(off-label use). For the treatment
of carnivores, fipronil and selamectin are approved
among others( ► Table 19.16, p. 602).
Pyrethroids and macrocyclic lactones can be expected
to have a residual action over 5-7 weeks. Repeated
treatments should only be performed if the initial
therapy and follow-ups are unsuccessful In other cases,
treatment has to be repeated after 7-10 days as nits
are not adequately affected. Resistance to pyrethroids,
organophosphates and insect growth regulators has been
demonstrated in B. ovis.
For the treatment of bird lice, all well-tolerated
insecticides(pyrethroids, carbamates, organophosphorus
compounds) can be used, preferably in powder form.
Treatments should be repeated after 1-2 weeks because of
insufficient effect on nits. Nests and resting areas should
be included in the treatment. In poultry, off-label use
of preparations is currently necessary due to a lack of
approved drugs. Dust boxes with sand plus diatomaceous
earth, kaolin clay or sulphur are recommended for free­
range poultry since dustbathing can contribute to the
control of M. stramineus.
Selected references
Crawford S, James PJ, Maddocks S (2001) Survival away from
sheep and alternative methods of transmission of sheep lice
(Bovicola ovis). Vet Parasitol 94: 205-216.
Harbison CW, Jacobsen MV, Clayton DH (2009) A hitchhiker's
guide to parasite transmission: the phoretic behaviour of
feather lice. Int J Parasitol 39: 569-575.
14. Phylum Arthropoda (arthropods)
Heath AC, Bishop DM, Cole DJ, Pfeffer AT (1996) The
development of cockle. a sheep pelt defect, in relation to
size of infestation and time of exposure to Bovicola ovis. the
sheep biting louse. Vet Parasitol 67: 259-267.
James PJ (1999) Do sheep regulate the size of their mallophagan
louse populations? Int J Parasitol 29: 869-875.
Johnson KP, Shreve SM, Smith VS (2012) Repeated adaptive
divergence of microhabitat specialization in avian feather lice.
BMC Biol 10: 52. .c:
Levot G (2012) Unstable pyrethroid resistance in sheep body
E
0.
lice Bovicola ovis (Schrank), (Phthiraptera: Trichodectidae)
and Its implications for lice control in sheep. Vet Parasitol
185: 274-278.
Shu D, Pfeffer A, Pernthaner A (2009) Cutaneous cytokine gene
expression and cellular responses in lambs infested with the
louse. Bovicola ovis. and following intradermal injection of
crude louse antigen. Vet lrnmunol lmmunopathol 129: 82-92.
Zlotorzycka J, Elchler W, Ludwig HW (197 4) Taxonomie und
Blologie der Mallophagen und Uiuse mitteleuropaischer
Haus- und Nulztlef8. Parasitol, Schriftenreihe. Band 22.
Jena. Germany: G. Flsctier.
14.3.2.2. Suborder Anoplura (sucking lice)
Anoplos (G): unarmed; ura (G): tail. Refers to the
unarmed rear body, in contrast to bees, wasps, etc.
Summary
CTl
• Morphology, species. Wingless, 2-6 mm long, v
dorsoventrally flattened, blood-sucking, permanent­ 0
0.
stationary ectoparasltes of mammals and man. 0
In contrast to chewing lice, head narrower than
..c
t'
the first thorax segment. Of veterinary Importance: <{
representatives of the families Haematoplnidae and
Llnognathldae. High host specificity, sometimes several
species per host species; not on cats and birds.
• Life cycle. Females glue eggs (nits) on hair.
Hemlmetabollc development over 3 larval stages in
3-4 weeks. Transmission by contact. All stages suck
blood several times a day, usually survive off the host
only for 4-7 days.
• Occurrence, epidemiology. Infestation in cattle and
pigs common, In other domestic animals rare. Often
seasonal dynamics with highest Infestation intensity
In winter. Poor housing conditions promote the
proliferation of lice.
• Pathogenesis, cllnlcal signs. Lice bites are extremely
Irritating, lead to exeariations ar,id skiR damage with
aloli)ecia, skin thlckenin@, accasionally eczema
(lmmunopathologlcal 0riglra). Reductlen af milk and
fattening performance. cr1
C
• Therapy, control. Use of insecticides af different ·;;::
groups of active substances as pour-on or spray.
Some Ji)reparations require repeated applications due
to insufficient effect on nits. Improvement of housing
C
>-
CORditions. 0)
0
0
·en
cr1
a..
 Part Ill. Parasites and parasitoses: metazoa

Morphology and species. Sucking lice are wingless, Table 14.9. Sucking lice (Anoplura) (selection) and their hosts.
dorsoventrally flattened, with relatively thick abdomen
1F-amily and species
.. l!!ength Host
and a head which is narrower than the first thorax ,,
(�!j(mm)
segment and bears easily observable 3-5 segmented . ""'"'
antennas. The piercing-sucking mouthparts are highly Haematopinidae
adapted t o the parasitic lifestyle and are invisible Haematopinus eurystemus 3.0-3.5 cattle
externally. Eyes are present in the Pediculidae, but are
Haematopinus suis 4.5-6.0 pig
absent or reduced in other groups of lice.
Haematopinus asini 2.5-3.5 horse, donkey
The skin of the hosts is pierced by 3 stylets. There is one Linognathidae
claw( ► Figure 14.32) on the tarsi. Sexual dimorphism Linognathus vituli 2.5-3.0 cattle
is minor, but males are usually smaller than females. Linognathus stenopsis 2.5-3.0 goat
Like other insects that depend on blood in all stages, Linognathus ovillus 2.0-3.0 sheep
lice harbour symbiotic microorganisms that reside in Linognathus setosus 1.8-2.5 dog, fox
a so-called mycetome in the midgut. So/enopotes capillatus 1.5-2,0 cattle
Hoplopleurldae 1
Representatives from three families( ► Table 14.9) infest
Haemodipsus ventricosus 1.3-1.5 rabbit
domestic and pet mammals, with the exception of cats,
as well as primates. Another family, Echinophthiriidae, Polyp/ax serrata 1.0-1.4 mouse
occurs in seals and sea lions. The sucking lice of humans Polyp/ax spinulosa 1.3-1.6 rat
1 Also a member of the family is the genus Pedicinus which occurs
belong to the Pediculidae (Pediculus humanus with the
2 ecotypes P. h. capitis: head louse and P. h. corporis: on Old World primates.
body louse; Phthirus pubis: pubic louse).
to hair or bristles of the host. Depending on the species,
Sucking lice of the families Haematopinidae and the first larvae hatch after 1-3 weeks from the nits. After
Linognathidae which infest domestic animals differ every 3-6 days they moult into the next larval stages and
morphologically at the first pair of legs which are into adults, so that the overall development is completed
significantly smaller than the other legs in the in about 3-4 weeks. Females lay 5-8 (total> 100) eggs per
Linognathidae, while all legs are of similar size in day and like the males can reach an age of 3-4 weeks.
the Haematopinidae. Haematopinidae have strongly
chitinised, laterally projecting so-called paratergal plates Occurrence and epidemiology. The more common
on the abdominal segments( ► Figure 14.32). species occurring in Europe are listed together with
their hosts in ► Table 14.9. According to data from
Life cycle. Sucking lice have a hemimetabolic Germany, Solenopotus capillatus was detected in 12% of
development over 3 larval stages, which are somewhat 968 tested cattle herds; Haematopinus eurysternus and
smaller than adults, but resemble them both morpho- Unognathus vituli in about 4% of the farms. The latter
1.ogically and with regard to their way of life( ► Figure species mainly occurs on calves. On sheep and goat,
14.33). Mated females, like the chewing lice, glue the sucking lice generally have little significance in Europe
capped eggs, so-called nits, with a water-insoluble glue (except UK). Reliable data on the prevalence in pigs are

Antenna

Claw

Q)

·o
C

'6
Q)

c I
.

.' �
,
co

-· .. �
C
·c
Q)
'·
' ••�-- Paratergal
,!:; plates
>, • ...;
:ti
OJ
0
0
'iii a

co
0... Figure 14.32. Sucking lice: (a) Haematopinus suis (length 4-6 mm); (b) Nits of lice in hair coat of cattle (Photo: IPZ).

Transmission through contact
Figure 14.33. Development cycle of Haematoplnus suis (Graphics: IPZ, S. Ehrat).
scarce. In Germany, 15-40% of the farms are suspected
of being infested. Pigs in SPF (specific-pathogen-free)
systems are Haematopinus-free (cf. Sarcoptic mange).
Sucking lice are rare in equines and dogs in Europe.
Transmission occurs by contact between animals or
indirectly, e.g. by cleaning utensils or roller brushes
that are often mounted in pen barns of cattle. Most lice
species are monoxen, some euryxen. Therefore, lice
from a host species do not move to other animal hosts
or humans (except very closely related host species).
Animals are never a source of infestation for humans.
Anoplura are dependent on regular blood meals and
therefore survive only 4-7 days off their host. An
exception is L. stenopsis. This parasite of sheep and
goat survives starvation periods longer than 2 weeks
in the resting places of the host. Lice infestations of
cattle display a clear seasonal dynamics, being highest
inwinter and early spring, and dropping abruptly with
hair replacement in late spring. In other hosts, such
seasonal variations are less pronounced.
14. Phylum Arthropoda (arthropods)
Cl)
-< -_ ·
-,.
/99 (nit) On
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Immunology. Salivary antigens of Anoplura induce
the formation of specific antibodies in their hosts. Field
observations in cattle and other domestic animals have
revealed that young animals are more affected by lice
than older animals. Together with experimental studies
in rodents, this suggests that persistent infestations
can provoke a partial immunity, causing a reduction
in the lifespan of females and a reduced hatching rate
of their eggs. The mechanisms are not understood.
Hypersensitivity reactions of the immediate type might
play a role, as increased mast cell densities occur in the
skin of immune rodents. However, in sheep there are
also lymphocytic infiltrates around the puncture area.
In sensitised rodents, hyp ersensitivity reactions of type
III (Arthus reaction) with accumulation of neutrophils
at the puncture site occur after reinfestation with lice.
Pathogenesis and clinical signs. All stages of
sucking lice take blood meals several times a day, thus
causing continued irritation of the animals. The highly
itchy bites lead to scratching and thus to excoriations
and secondary infections. The amounts of blood
withdrawn are low at about 0.1 mg per meal; however,
 Part Ill. Parasites and parasitoses: metazoa
blood withdrawal can definitely be a harmful factor in
case of mass infestation of young animals.
On cattle, Haematopinus eurysternus (short-nosed cattle
louse) mainly infest the head (around eyes, ears, basis
of the horn), the back to the base of the tail, and the
flanks. Linognathus vituli (long-nosed cattle louse) and
Solenopotes capillatus (small blue cattle louse) mainly
colonise head, neck and dewlap. Mass infestations and
clinical manifestations are usually limited to winter and
early spring. Clinical signs include alopecia, squamous
dermatitis, skin thickening, and sometimes crusty
deposits after skin injury. Severe infestation leads to
significant losses in dairy and fattening performance, in
calves also anaemia. With the hair replacement in late
spring, the clinical picture can improve dramatically
with a decline in infestation intensity.
Sheep rarely have sucking lice, goats frequently. The
infestation occurs mainly on the front of the body.
The preferred localisations of H. asini in horses are
mane and tail-head; sometimes the lice also infest the
end of the limbs above the hooves. Distinct clinical
manifestations with alopecia and dermatitis are rare,
'.;· but then associated with stress and poor husbandry.
Obviously, due to the localisation of the parasites in
mane and tail-head, there is not always such a clear
improvement as in bovines with hair replacement in
spring.
Lice infestations of pigs are common in conventional
husbandry in stables, and are largely independent of
the age of the animals. Lice are found mainly on the
back of the pigs as well as at thin-skinned areas such as
axillae, grip and inner side of ears. Because of the itchy
punctures the animals scratch and rub, leading to skin
lesions with crusty surfaces. The constant disturbance
of the animals affects weight gain.
L. setosus infests the areas of eye and ear and the anterior
back of dogs and foxes. In dogs, the infestation usually
only occurs on very poorly kept animals. Rabbits and
rodents are rarely infested by lice, either as pets or under
laboratory conditions.
(I)
Vector role. Animal lice generally are considered as
·u
C
having no epidemiological role in the transmission of
disease agents, although it has been demonstrated in a
recent study from Hungary that approximately 50% of
C1J
C the examined lice from cattle, goats and pigs contained
·c
(I) Anaplasma DNA. The body louse of man can transmit
e.g. pathogenic rickettsiae (Rickettsia prowazekii) and
.£ borreliae (Borrelia recurrentis).
>,
O>
0 Diagnosis. Lice are detected on the skin at the
·en predilection areas macroscopically or with a magnifying
C1J
glass. Because of its size and dark colour, H. suis on pigs
C1J
0.. is the easiest to detect. Other Haematopinus species and
Linognathus spp. often form small groups (lice nests).
The small, translucent and rather singly occurring
adults of S. capillatus on cattle, however, can easily be
overlooked. The approximately 1 mm long nits are light
blue to grey depending on the species, and can be found
at the base of hair. In case of mass infestation, there can
be large numbers of closely positioned eggs ( ► Figure
14.32).
Treatment and control. For the control of lice in
ruminants, several active substances are available:
macrocyclic lactones (ML) (doramectin, ivermectin,
eprinomectin and moxidectin as pour-on and injectable
solutions), pyrethroids ( deltamethrin, permethrin:
pour-on or spray) and phoxim (spray, wash treatments)
(► Table 19.4, p. 583). Except for the ML which have a
long bioavailability and are effective until some weeks
after application, treatments must be repeated after
1-2 weeks because eggs are not adequately affected.
In Hypoderma-endemic areas, ML should not be used
in cattle in the period from December to mid-March
( ► p. 495). In pigs, phoxim (spray) 2 times at intervals
of 1-2 weeks or ML are used. Because of its long residual
action, repeated treatment is not required for the latter.
For the horse, ML for oral administration and phoxim
as wash solution (off-label use) are available. Infested
dogs can be treated with fipronil or selamectin ( ► Table
19.16, p. 602). Some of the substances can also be used
as insecticide collars. In all other cases, it is necessary to
treat the dogs again after 2 weeks, because the nits are
not adequately affected. An alternative is fipronil (spray
treatment) whose effect is immediate and lasts for at least
4 weeks. Skin lesions and pruritus, however, persist for
2 weeks or longer despite absence of lice. Disinfestation
of stables and resting areas is not necessary if it is
guaranteed that they are not used for a period of at
least 8 days (= period that lice cannot survive off the
host; except L. stenopsis, see above).
Se I ected references a......:::::::::::::::::===-_-:.i
Braae UC, Ngowl HA, Johansen MV (2013) Smallholder pig
production: prevalence and risk factors of ectoparasites. Vet
Parasitol 196: 241-244.
Colwell DD (2014) Life history parameters of the cattle long­
nosed sucking louse, Unognathus vituli. Med Vet Parasitol
28: 432-437.
Hornok S, Hofmann-Lehmann R, de Mera IG, Meli ML, Elek
V, Hajt6s I, Repasi A, Gonczi E, Tanczos B, Farkas R,
Lutz H, De la Fuente J (2010) Survey on blood-sucking lice
(Phthiraptera: Anoplura) of ruminants and pigs with molecular
detection of Anaplasma and Rickettsia spp. Vet Parasitol
174: 355-358 .
Leonardi MS (2014) Faster the better: a reliable technique to
sample anopluran lice in large hosts. Parasitol Res 113:
2015-2018.
 14. Phylum Arthropoda (arthropods)

Light JE, Smith VS, Allen JM, Durden LA, Reed DL (2010)
Evolutionary history of mammalian sucking lice (Phthiraptera:
Anoplura). BMC Evol Biol 10: 292.
Milnes AS, Bailey M, Knowles TG, Coles GC, Green LE,
Day MJ (2007) An immunohistochemical assessment of the
cutaneous immune response to louse infestation in cattle. J
Comp Pathol 136: 240-249.
Otter A, 1\vomey OF, Bates P (2003) Anaemia and mortality
In calves infected with the long-nosed sucking louse
(Linognathus vituh). Vet Rec 153: 176-179.
www.phthiraptera.lnfo.
mattresses, behind furniture, in cracks of the wall, in
laying nests of chickens, etc.) and come out to suck
blood at night. A closely related species is the pigeon
bug (Cimex columbarius), which parasitises pigeons,
swallows and other birds. Occasionally, Cimicids migrate
from bird nests into homes and annoy people with their co
bites, e.g. the pigeon bug or the swallow bug( Oeciaws
....(D
hirundinis). Bugs of the family Reduviidae (genera o_
0
Triatoma, Rhodnius, etc., kissing bugs) play a role as Q,)
0
vectors of Chagas disease in Latin America(► p. 69). 0

14.3.3 Order Heteroptera (true bugs)
Heteros(G): different; pteron(G): wing. Relates to the
special feature of the forewings which are strongly
chitinised only at the base.
Adults of the hemimetabolic bugs have two pairs of
wings or wing rudiments. In Europe, the veterinary
importance of bugs is very limited. The bed bug Cimex
/ectularius (family Cimicidae), which predominantly
affects humans and occasionally animals(e.g. chicken),
used to be frequent but has become rare. However, in the
last two decades an increase of C. lectularius populations
has been reported from European countries, the USA
and Australia. Adults of this species are about 3-6 mm
long, their body is dorsoventrally flattened, the wings
are greatly reduced, the long proboscis can ventrally
be folded under the front body(► Figure 14.34). The
development from egg, over 5 juvenile stages, to adult
lasts about l ½ months under favourable conditions.
Bugs have to take blood several times during their
development. They can survive for up to I year without
a blood meal, allowing them a long persistence in
rooms where they keep hidden during the day(under
Selected references
Delaunay P, Blanc V, Del Giudice P, Levy-Bencheton A,
Chosldow O, Marty P, Brouqul P (2011) Bedbugs and
Infectious diseases. Clin Infect Dis 52: 200-210.
Delaunay P (2012) Human travel and traveling bedbugs. J Travel
Med 19: 373-379.
Moore DJ, MIiier OM (2009) Field evaluations of insecticide
treatment regimens for control of the common bed bug,
Cimex lectularius (L). Pest Manag Sci 65: 332-338.
14.3.4 Order Coleoptera (beetles)
Koleos (G): sheath; pteron (G): wing. Relates to the
hardened forewings which protect hindwings and
abdomen.
Cl3
The holometabolic Coleoptera(beetles) are the largest -0
0
a.
order of the Insecta, accounting for approx. 40% of
the species. They are generally of minor veterinary
e
.c
t
significance, be it as mech,mical vectors of pathogens or <(
as worldwide intermediate hosts of helminths, mainly of
poultry (Raillietina cesticillus, Choanotaenia infudilum,
Ecl1inolepis carioca; ► Table 9.13, p. 221). Furthermore,
they may cause dermatological problems due to the
vesicating fluid produced by the adults of some species
or the setae of larvae that can penetrate the skin.

A striking exception with ever increasing significance

is the small hive beetle Aethina tumida. The beetle
originated from Sub-Saharan Africa, where it is
considered a minor pest of bees. It has spread to North
and Central America(1996), Egypt(2000) and Australia
Q)
(2002) where it has established and causes considerable
·u
C

damage to Apis mellifera honeybee colonies. A. tumida

is a statutory notifiable pest across Europe. In 2004,
�
it was detected in cages of imported bees in Portugal
(2004) but the outbreak was quickly contained and the
cCl3
C
pest insect eliminated. At the end of 2014, A. tumida ·;::
infestations were identified in southern Italy in several
apiaries. Consequently, European countries have stopped .s
the import of bees, bumble bees, apiculture products and >.
0)
equipment from the affected regions. Females of this 0
small(5 mm in length), dark brown to black beetle lay the 0
Figure 14.34. Cimex lectu/arius (length of unfed stage: 4-5 mm) ·u5
eggs in clutches in crevices of the hive or in the capped
(Photo: IPZ). brood cells. The creamy-white larvae bear 3 pairs of long co
Q_
Part Ill. Parasites and parasitoses: metazoa
forelegs; they grow up to 12 mm in length. Larvae feed
on brood, honey and pollen; they damage combs, and
faecal contamination may cause fermentation of honey.
Pupation takes place in soil near the hive. A. tumida can
have several generations per year ( 1-6) depending on
the environmental conditions. Newly emerged adults are
strong fliers; they infest new hives at distances of up to 10
km. A light infestation may go unnoticed; heavy larval
infestations may result in the structural collapse of the
colony, and the presence of adult beetles may cause the
adult bees to abandon the hive. An early diagnosis can
be made by detecting adult beetles which typically seek
shelter when exposed to light. Larvae can be detected if
infestations are moderate to high. Different trap systems
have been developed to collect adult beetles. Control
measures include the destruction of infested apiaries and
the mechanical (ploughing) and chemical destruction of
larvae in the surroundings of hives. Due to the presence
of alternative hosts (bumble bees, feral bees), elimination
of the small hive beetle is considered impossible once it
is well established (also► p. 612).
Selected reference
OIE (2013) Small hive beetle infestation. Available at:
http:/ /tinyurl.com/nf32vyu.
14.3.5 Order Diptera (flies)
Di-(G): two;pteron (G): wing. Refers to the two-winged
adult flies.
Summary
• The order Olptera with the suborders Nematocera
('thread-horn flies') and Brachycera ('short-horn flies')
contains numerous parultologlcally significant species.
• Adult Dlptera, llke all lnNCtl, have 8 leg1, and they have
a pair of wings; thtlr mouthparts are of the piercing­
sucking or llcklng■-1cklng type, but they can be greatly
reduced.
• The fife cycle 11 holometabolou1 from egg over HVeral
larval 1tag11 and pupa to the Imago etage,
• Nematocera tmag01 ueuelly have a llender body and
tong antennae, which QOnel1t of elx or more segments;
the tarvee have a head capsule.
Adults of Srachycera appear mo,a stout-bodied and
have short antennae, which are composed of three
main segments; the head capsule of larvae (maggots)
Is reduced or absent.
Numerous species of this order are of veterinary and
medical importance as pests, as vectors of viruses,
bacteria, protozoa and helminths, and as parasites of
skin and other organs. The order Diptera is classically
divided into the suborders Nematocera ('thread-horn
flies') and Brachycera ('short-horn flies') (see below).
Another classification comprises three suborders,
Nematocera, Brachycera(Tabanids and relatives) and the
Cyclorrhapha (flies). It should be noted that in English
all Diptera with the exception of Culicidae('mosquitoes')
are called flies, in contrast to other languages which
differentiate between Brachycera(e.g. German: 'Fliegen';
Dutch: 'vliegen'; French: 'mouches') and Nematocera
('Mi.icken'; 'muggen: 'moustiques').
The main characteristics of Diptera are listed in the
summary; more details are given in the following
sections. In contrast to various other groups of insects,
Diptera have only one pair of wings; the original second
pair of wings is converted into halteres which play a role
in the coordination of flight (► Figure 14.35). Wings
are mostly transparent and kept flat side by side or one
above the other at rest; so-called wing veins (► Glossary,
p. 620) provide important clues for the identification of
genera and species.
- Suborder Nematocera ('thread­
horn flies')
Nema (G): thread; keras (G): horn. 'Thread horns'; refers
to the long and multisegmented antennae.
Nematocera are usually(exception: Simuliidae) slender,
long-legged dipterans with thread-like, 6 to approx.
30-segmented antennas with homonomer structure(=
homogenous segments) (► Figure 14.35). They have
4 to 5-segmented maxillary palps. Females of blood
sucking species have piercing-sucking mouthparts.
Larvae are eucephalic(with head capsule) with chewing
mouthparts; there are always 4 or more larval stages.
Nematocera are, except Simuliidae, slow flyers. The
Labellum-�
Mouth­ ----Palp
parts
Antenna ---l,1----­Compound
eye
Thorax
Haltere
Abdomen
Cerci
Figure 14.35. Culicidae: scheme of a female Culicinae
(Grap hics: IPZ, A. Seeger; after Weyer and Zumpt 1966).
 14. Phylum Arthropoda (arthropods)

somatic needs of adults for energy and nutrients can
be met in both sexes by plant juices (nectar); females of
many species require blood for egg production (males
of Nematocera do not feed on blood). Blood meals
are taken at intervals of several days. Of veterinary
importance as direct pests or as vectors of pathogens
are 4 families: Culicidae, Psychodidae, Simuliidae and
Ceratopogonidae.
Family Culicidae (mosquitoes)
Culex (L): mosquito.
Summary
• Morphology, species. Culicldae are 4-10 mm long,
slender, long-legged mosquitoes; females have long
piercing-sucking mouthparts. Important subfamilies
and genera are: Anophelinae (genus Anopheles)
and Culicinae (genera Cu/ex, Aedes, Ochlerotatus,
Stegomyia, Cu/iseta, Coquillettidia); worldwide >3,000,
in Europe 100 species of Culicidae.
• Life cycle. Oviposition in standing water or on soil of
floodplains. The eucephalic, mobile larvae hatch in the
water and develop over 4 stages to pupae which are
also mobile. Duration of development under favourable
conditions 8-21 days. Some species (e.g. Cu/ex pipiens)
develop up to seven generations per year in Europe.
• Occurrence, epidemiology. According to availability
of the preferred larval habitats (e.g. floodplains, ponds,
small natural [tree holes, puddles] or artificial [rain barrels]
accumulations of water), large mosquito populations
can locally arise, e.g. of the flood mosquito Aedes
vexans or the house mosquitoes (Cu/ex and Culiseta
In the species-rich (>3,000 species) family, there are two
subfamilies - Anophelinae and Culicinae - of medical
or veterinary importance ( ► Table 14.10). In Europe,
there are about I 00 species. Among the Anophelinae,
only mosquitoes of the genus Anopheles are important
as a nuisance and as vectors of a number of pathogens,
especially malaria parasites of humans. In Europe, this
applied in past centuries especially for representatives of (1)
Cl
the An. maculipennis group, including An. atroparvus. cS
Among the Culicinae there are pronounced nuisance
mosquitoes in the genus Aedes (such as Ae. vexans)
which in humid areas and years become a torment for
humans and animals. In Europe, exotic Aedes species are
discovered again and again; two of them, Ae. albopiclus
(Asian tiger mosquito) and Ae. juponicus (Asian bush
mosquito) are invasive species and are widely established
in southern or Central Europe (updated distribution
maps of invasive species in Europe are available at
www.ecdc.europa.eu). They can act as vectors of
viruses, protozoa and nematodes. The same applies for
indigenous Culex species and Culiseta annulata which
mostly live near human settlements; the latter species
usually in lower numbers than Cu/ex spp. Coqui/letlidia
richiardii usually plays a role only at the local level (at
large lakes, lake land).
C'Cl
""O
0
Q.
0

-
species). Most mosquito species are crepuscular ..c
and some (e.g. house mosquitoes) nocturnal; forest t
<{
mosquitoes, Coquillettidia species and the Invasive
species Ae. albopictus (tiger mosquito) and Ae.
japonicus (Asian bush mosquito) are diurnal. Females

"'
,
of some species blood-feed on various vertebrates,
others prefer certain hosts. Cu/ex, Anopheles and
Cu/iseta species enter buildings.
• Pathogenesis, clinical signs, vector role. Mosquitoes
are a nuisance for animals and humans. Their main
a
/
/
importance lies in the vector role (e.g. Dirofilaria immltls,
West Nile virus; human malaria).
• Control. Limited options for protection from mosquitoes
by using repellents (including icaridin) on horses or
deltamethrin collar for dogs. Large-scale control see
below. Q)
T5
C

'6
Q)
2
Morphology and species. Culicidae are 4-10 mm c
C'Cl
long, slender, long-legged flies(► Figure 14.36). Females C
·;::
have a long, unsegmented proboscis with piercing­ Q)
sucking mouthparts, the mandibles and maxillae
in the males are regressed (no blood suckers). The C
IS-segmented antennas are usually strongly plumose b >,
0)
in males or with short hair in females. The maxillary 0
0
palps of males are long and bushy, those of the females Figure 14.36. Culicidae: (a)Aedesjaponicus, female; (b) Cu/ex ·en
short (exception: Anopheles) and sparsely hairy. pipiens, female (Photo: IPZ).
co
0...
 Part Ill. Parasites and parasitoses: metazoa

Table 14.10. Mosquitoes (Culicidae) (selection) in Europe, their breeding habitats and overwintering stages.

I
Sufamil_ y, and Species lBr.eeding•habitats Overwintering
,.genus stages
�- -, _
c-
-
,. ;\_-- _,.-- - ..., ~ ,_ -
Anophelinae
Anopheles An. messeae stagnant, plant rich, permanent waterbodies, also close to human mated females
An. maculipennis settlements
-� An. claviger
An. plumbeus tree holes larvae (eggs)
Culicinae
Aedes 1 Ae. vexans inundated areas, riparian forests (flood plain mosquitoes) eggs
Ae. sticticus
It:'
Ae. rossicus
Ae. cinereus
Ae. cantans swampy lowland forests, ponds (forest mosquitoes) eggs
- Ae. communis
Ae. punctor moors
.._ Ae. albopictus small natural or artificial containers eggs (larvae)
- Ae. japonicus
Ae. geniculatus tree holes eggs (larvae)
Cu/ex Cx. pipiens around human settlements; also in small containers (e.g. rain barrel, mated females
gutter) (house mosquitoes)
Cx. modestus swampy areas, reed-beds
Culiseta Cs. annulata around human settlements (large house mosquito) mated females
Cs. morsltans ponds, ditches in woods larvae
Coquillettidla Cq. richiardil,z old river beds, siltation zones 3rd larval stage
1 Including Ochterotatus!Stegomyia; changes in genus names and affiliations have been published (e.g. Aedes japonicus = Oc/Jlerotatus
ja{X)nicus = Hulecoeteomyiajaponlca), but it is recommended to use the traditional names until there is a consensus about the nomenclature.
2 Formerly Manson/a; this genus was split into the genera Coquillettidia and Manson/a, the latter occurring In the tropics.

Life cycle. Mating occurs soon after hatching of the
adults. Males produce a sound with their wings that
attracts females in a species-specific manner. With few
exceptions, females need blood meals to produce eggs
(autogenous species produce the first batch of eggs
without blood feeding). They lay I 00-150 eggs singly
(Anopheles, Aedes) or in batches(egg rafts; C11lex) onto
the surface of standing water (Anopheles, Cr,/ex) or to
edges of water bodies (Aedes) which are eventually
flooded ( ► Figure 14.37). The eucephalic, mobile larvae
hatch in the water and develop over 4 stages to pupae
which are also mobile. Larvae and pupae breathe at the
water surface. Coq11ill.ettidia species are the exception as
their larvae and pupae live submerged and cover their
Q)
oxygen demand by piercing air-ducting tissue of aquatic
·u
C
other Aedes species prefer to develop in forest ponds
and ditches(forest mosquitoes), while the larvae of the
invasive Ae. japonicus develop like Cu/ex species in small
artificial containers in urban areas (e.g. rain barrels),
but also in tree holes in the woods. The species of the
genera Culex and C11liseta are considered to be domestic
mosquitoes. The species of the genus Anopheles occur as
mosquitoes in open fields (An. claviger) and also around
human settlements (An. macullpennls). They usually
develop in sunny, clam and plant-rich water bo dies.
Aedes geniculatus and An. plumbe11s develop in tree holes
and also in artificial containers (e.g. old manure pits).
Overwintering females lay eggs in early spring. Rising
water levels (flooding) trigger Aedes larvae to hatch,

'6 plants. Development times to adult stages depend on but not all eggs hatch at the first opportunity. Instead,
Q)
� species and environment; 8-21 days are required under some of them remain in diapause and can survive for
c
co
favourable conditions. Overwintering stages are eggs in years until the next flooding. Because of the resistance
C the Aedes species, larvae in Coquillettidia spp., and mated to desiccation, these species can colonise new areas
·c females in the other genera( ► Table 14.10). ( = invasive species) after a long transport of eggs,
Q)

j e.g. in used car tires or in ornamental plants. Moist,

C Occurrence and epidemiology. T he species warm summers result in rapid generations and mass
>, occurring in Europe prefer specific larval habitats development of mosquitoes, culminating in July or
-co
0)
0 (► Table 14.10). Aedes vexans and Ae. sticticus colonise August. In Cx. pipiens, 6-7 generations per year are
0
·u5 inundated areas and riparian forests, and they are possible. In the genus Coquillettidia, only one generation
referred to as flood plain mosquitoes. Ae. cantans and per year develops; the mosquitoes hatch in June and July.
co
a..
 14. Phylum Arthropoda (arthropods)

.....
Q)
Q.
0

Anopheles female

en
-0
Pupal stages ot 0
a.
Anopheles or Culicinae 0
..c:
Anopheles eggs t::
Larva of Culicinae (Cu/ex, Aedes, etc.) <(

���WP
Larva of Anopheles

Figure 14.37. Developmental cycle of Culicldae (Graphics: IPZ, S. Ehrat).

Most mosquito species are crepuscular and some
nocturnal (e.g. the common house mosquito [Culex
pipiens] or tropical fever mosquitoes of the genus
Anopheles). Forest mosquitoes, Coquillettidia species
and the two invasive species Ae. a lbopictus and Ae.
very discriminating. At short distances, olfactory and
visual stimuli play a role. Through olfactory signals,
suitable body regions of the host are then selected to
puncture the skin surface. Culicidae suck blood from
Q)
capillaries; the duration of blood feeding is about 2 min;
·u
C

japonicus also bite during the day. Females of some each mosquito takes 2-3 µl blood. '6
Q)
species are indifferent feeders on all vertebrates; others 2
prefer certain hosts (ornithophilic, mammalophilic, Pathogenesis and clinical signs. Mosquitoes cause cco
anthropophilic species). Culex, Anopheles and Culiseta itchy lesions in animals and humans in response to C
species often invade buildings. salivary components. The effects of Culex bites usually ·;::
Q)
disappear overnight, while bites of other mosquitoes �
Host-finding over long distances (up to 20 m) occurs via are more persistent. Hypersensitivities that occasionally C

chemical signals, with CO 2 being the most important develop usually correspond to type IV. In case of mass >,
Ol
factor. In addition to non-defined components from propagation, mosquitoes can be a great nuisance to 0
0
sweat, octenol, 4-methyl phenol, lactic acid and domestic and wild animals, affecting their well-being ·en
short-chain aliphatic carboxylic acids have been and in exceptional cases also their performance. Well-
co
identified as attractants. Specialised species can be Cl..
 Part Ill. Parasites and parasitoses: metazoa

known and notorious are the massive Aedes plagues
in northern regions(including Scandinavia, Alaska).
Vector role. More important is the role of mosquitoes
as vectors of pathogens. Culicidae transmit parasites
(Plasmodium, filariae) and viruses(► Table 14.11).
Most important are species of the genera Anopheles
(as the sole vectors of malaria parasites of humans
[Plasmodiumfalciparum, P. ovale, P. vivax, P. malariae,
P. knowlesi) and Aedes (Ae. aegypti, Ae. albopictus) as
vectors of e.g. dengue virus. Around 30-35 of the world's
approximately 400 Anopheles species are suitable vectors,
and only 8 species are associated with stable malaria
endemic areas. The plasmodia of birds on the other hand
have a wide range of mosquito vectors. Many mosquito
species serve as intermediate hosts for many species of
filariae of humans and animals. Regional ecological
factors determine which species are the main vectors.
Particularly important is the occurrence of invasive
species, which can change the epidemiology of pathogen
transmission. Thus, transmission of Dirofilaria immitis,
which in Italy is transmitted by the nocturnal Cu/ex
pipiens, has increased there after the occurrence of the
diurnal Asian tiger mosquito.
The vast majority of arboviruses (arthropod-borne
viruses) are transmitted by Culicidae. The 400 pathogen
species belong to several virus families(► Table 14.11).
Transovarial transmission could be substantiated for
several viruses. Arboviruses play an important role
especially in tropical regions; the data given in ► Table
14.11 mainly relate to Europe.
Diagnosis. Diagnosis of mosquito bites occurs
clinically. As a group, mosquitoes are easily recognisable
by their general habitus and few characteristics; however,
the species identification is a task for specialists.
Anopheles mosquitoes can b e distinguished from
Culicinae (Aedes, Cu/ex) and others by their resting
posture on walls(► Figure 14.3 7).
Control. Individual prophylaxis can be done by
applying repellents. For horses, preparations with e.g.
icaridin are approved (EquiRepeW) which are sprayed
onto the hair coat or applied as a gel with a sponge. The
effect lasts only a few hours. A permethrin emulsion
(Wellcare•) with insecticidal and repellent effect used
for fly control can also be used against mosquitoes; it
probably has a persistency of effect of at least several
days. For use in dogs, deltamethrin-impregnated collars
are available(► Table 19.16, p. 602). In farm animals,
control measures against Culicidae are not usually
needed in Europe. Large-scale control measures are
primarily aimed at the larval stages.
• Control of larvae. Flood plain mosquitoes are
controlled with the application of ecologically largely
acceptable larvicidal proteins from Bacillus thuringiensis

Table 14.11. Culicidae as vectors of parasites and viruses (selection).

Ag,m Vertebrate hoeta1 Main vectors Endemic In Central Europe2

Protozoa -
�asmodium spp, humans Anopheles spp. - -
Plasmodium spp. birds Anopheles, Aedes, Cu/Isela, +
_Cu/ex spp.
-
Nematodes -
Dirofilaria immitis canlds (fellds) .. Cu/ex, Aedes, Anopheles spp. +
-
Dirofi/aria repens canids Anopheles, Aedes spp. + -
Setaria spp. ':l.!:1_9ulates Anopheles, Aedes, Cu/ex spp. + -
Brug/a spp. humans (fellds) Anopheles, Aedes, Cu/ex spp. - -
Wucherer/a bancroft.l humans Anopheles, Aedes, Cu/ex spp. -
- -
3
Q) Viruses
·u
C
Bunyaviridae
'6
Q) Tahyna hare, pig Aedes spp. (+)
� Batai (Calovo) cattle, horse, pig, wild boar Anopheles maculipennis (+)
c.'
(1j Lednice water fowl Cu/ex modes/us +
C
·;::
(])
Flaviviridae
West Nile wild birds Aedes, Cu/ex spp. +
-� Usutu wild birds Cu/ex, Aedes spp., etc. +
>,
0) Togaviridae
0
0 Sindbis wild birds Cu/ex, Aedes spp. +
·u5 1 Hosts important for the persistence of the cycle.
(1j 2 +:endemic,(+): questionable,-: not endemic.
3 Limited to virus species transmitted in Europe (after Aspock and Dobler, 2010; Hubalek et al., 2014).

israe/ensis(Bti)(specific for some nematoceran Diptera)
( ► p. 567). The proteins bind to receptors on intestinal
cells of mosquito larvae and form pores, causing the
larvae to die. The application in breeding habitats is
either by hand or over a large area, e.g. by helicopter(e.g.
Ticino, Switzerland; Ober-Rheinebene, Germany). For
the control of mosquitoes whose larvae develop in small
aquatic habitats ('container breeders'), the reduction of
these breeding facilities is important. Also important
is to include the participation of the population (in
the USA with the slogan 'turnover or throw away' with
respect to the breeding containers). Breeding habitats
which cannot be removed or covered are treated with
larvicides or growth regulators(Bti, Bacillus sphaericus
protein, methoprene, pyriproxyfen, diflubenzuron,
spinosad), which inhibit larval development up to 5
weeks(► p. 557).
• Control of adults. Small-scale control of Culicidae
is inefficient and only short-lived; it is used in Europe
against Ae. a/bopictus (to reduce its spread and outbreaks
oftransmitted pathogens). Large-scale control measures
are carried out in countries with warmer climates to
control malaria and arboviruses, and they are especially
directed against Anopheles species and Aedes aegypti. For
this purpose, pyrethroids(e.g. permethrin, deltamethrin)
and organophosphorus compounds (malathion,
fenitrothion, etc.) are mainly used nowadays and are
sprayed or misted in buildings or outdoors, depending
on the conditions. For the control of malaria, bed
nets impregnated with pyrethroids to protect humans
from Anopheles bites are used with great success. Over
the years, more than 50 species of mosquitoes have
developed resistance to different insecticide groups, so
that in some endemic areas effective mosquito control is
a challenge. Alternatives are therefore being developed,
such as attractive toxic sugar baits, containing a sugar
solution, an attractant and a poison (e.g. boric acid).
Mosquito females and males are attracted and killed
when ingesting the mixture.
Selected references L..:========u
Aspock H, Dobler G (2010) Durch Arthropoden 0bertragene
Viren - Steckbrief und Oberblick. In: Aspock H (ed.) Krank
durch Arthropoden. Denisia 30: 457-465.
Becker N, Petric D, Zgomba M, Boase C, Madon M, Dahl
C, Kaiser A (2010) Mosquitoes and their control. Berlin,
Germany: Springer; ISBN 978-3-54092873-7.
Bonizzoni M, Gasperi G, Chen X, James AA (2013) The
invasive mosquito species Aedes albopictus: current
knowledge and future perspectives. Trends Parasitol 29:
460-468.
Clements AN (1992) The biology of mosquitoes. I. London, UK:
Chapman & Hall; ISBN 0-412-40180-0.
Engler 0, Savini G, Papa A, Figuerola J, Groschup MH,
Kampen H, Medlock J, Vaux A, Wilson AJ, Werner D,
Jost H, Goffredo M, Capelli G, Federici V, Tonolla M,
14. Phylum Arthropoda (arthropods)
Patocchi N, Flacio E, Portmann J, Rossi-Pedruzzi A,
Mourelatos S, Ruiz S, Vazquez A, Calzolari M, Bonilauri
P, Dottori M, Schaffner F, Mathis A, Johnson N (2013)
European surveillance for West Nile virus in mosquito
populations. Int J Environ Res Public Health 10: 4869-4895.
Hubalek Z, Rudolf I, Nowotny N (2014) Arboviruses pathogenic
for domestic and wild animals. Adv Virus Res 89: 201-275.
Kampen H, Werner D (2014) Out of the bush: the Asian bush
mosquito Aedes japonicus japonicus (Theobald. ·1901)
(Diptera, Cullcidae) becomes invasive. Parasit Vectors 7: 59.
Petric D, Bellini R, Scholte EJ, Rakotoarivony LM, Schaffner
F (2014) Monitoring population and environmental parameters
of invasive mosquito species in Europe. Parasit Vectors 7: 187.
Schaffner F, Angel G, Geoffroy G, Hervy JP, Rhaiem A,
Brunhes J (2001) The Mosquitoes of Europe/Les moustiques
d'Europe. An identification and training programme (CD­
ROM). Montpelller, France: IRO Editions & EID Mediterranee:
ISBN 2-7099-1485-9.
Family Psychodidae (moth flies)
• Subfamily Phlebotominae (sand flies)
Phlebs (G): vein; tomein (G): intersect, to cut.
Summary
• Morphology and species. Small, up to 5 mm long, very
hairy (Including wings), brownish, long-legged Insects.
The wings are held erect over the body at rest. T he co
\J
subfamily Phlebotomlnae (sand flies) Includes among 0
a.
others the veterinary Important genera Phlebotomus
(Old World) and Lutzomyla (New World). .c
t
• Life cycle. Ovlposltlon In the soil, In rotting leaves, In <{
cracks In walls, basements, and In caves of rodents.
Development of 4 larval and the pupal stage.
• Occurrence, epldemlology, Phlebotomus species
are widespread In Africa, Asia, the Mediterranean and
the Middle East, and they occur locally In western
and Central Europe. They are nocturnal outdoor flies,
however, some species Invade buildings and bite there
during day.
• Vector role. Some Phlebotomus and Lutzomyla species
are vectors of Leishman/a species and other pathogens.
• Control. Protection of dogs against lelshmaniosls:
deltameth rln-lmpregnated collar or spot-on treatment
(deltamethrtn, permethrln, permethrln + imldacloprld,
► Table 19.16).
Morphology and species. Phlebotominae are small
(2-5 mm), hairy(including wing), brownish, long-legged
insects. The wings are held erect above the body at rest
(► Figure 14.38). The 16antenna segments differ slightly
between the sexes. From the family Psychodidae, only
the subfamily Phlebotominae(sand flies) with over 800
species is of medical importance. The genera containing
the most species are Sergentomyia and Phlebotomus in
the Old World and Lutzomyia in the New World. The
most important species are in the genera Phlebotomus
 Part Ill. Parasites and parasitoses: metazoa
Figure 14.38. (a) Phlebotomus mascitti (Photo: IPZ). (b)
Phlebotomus perfi/iewi with typical position of wings at rest
(Photo: T. J. Naucke).
and Lutzomyia, which take blood meals on humans
and mammals, and which can transmit Leishmania.
Sergentomyia spp. live mainly in the tropics and feed
on reptiles and amphibians.
Life cycle. After a blood meal, females lay usually
few ( ~SO) eggs in soil, decaying leaves, basements, wall
cracks and into caves of rodents, where there is sufficient
humidity. After hatching, 4 larval and one pupal stage
develop. Within the mummy-like pupa, wings and legs
are recognisable. Pupal rest may take a long time (3
months at 18-20 °C and 6-8 weeks at 25 °C). Palaearctic
species therefore often produce only one population of
adult flies per year, developing from eggs laid in early
summer. The larvae that emerge from eggs laid in late
summer are overwintering.
Occurrence and epidemiology. The genus
Phlebotomus is widely distributed in Africa, Asia,
in the Mediterranean and the Middle East. The best
development conditions are provided in warmer,
temperate and subtropical areas, with hot summers
and relatively cool winters, Phlebotominae occur in
central Asia up to 50° N. In arid areas, during hot day
conditions they remain in dark, cool pla,es with a humid
microclimate, e.g. in rodent tunnels. Central Europe
was considered almost free of sandflies, but there are
increasing findings of P. mascitti, a suspected Leishmania
(l)
vector. Focally, also P. perniciosus occurs, a species
known as vector of Leishmania donovani. Lutzomyia
·u
C
species in the New World prefer humid, tropical regions
(l)
� (rain forests).
co
C Phlebotomus spp. are nocturnal outdoor flies. Some
·;::
(l) species, however, such as P. papatasi and P. sergenti,
which are the important vector of Leishmania major,
C enter buildings, especially at night when attracted by
>­
O'l light, and then remain active there during the day.
0 Sandflies prefer to fly in damp, warm, calm weather.
·u; They cover only short distances (100-200 m) but are
co passively transported over longer distances by wind.
co
a.. In the northern regions of the Mediterranean basin
(southern France, northern Spain, northern Italy,
etc.), phlebotomes are active from May to October, in
southern regions (Sicily, southern Greece, southern
Spain, etc.) from March to November.
Clinical signs and vector role. Sandflies cause
painful bites; Phlebotomus and Lutzomyia species
transmit Leishmania. In Europe, especially in the
Mediterranean and in some other areas, Phlebo tomus spp.
are of veterinary importance as vectors of Leishmania
infantum ( ► p. 72); dogs provide an important reservoir
for these zoonotic agents. Moreover, sandflies are vectors
of various virus species, e.g. the causative agent (genus
Ph/ebovirus, Bunyaviridae) of the sandfly fever of
humans in the Mediterranean and in Asia Minor.
Diagnosis. Species identification is a matter for
specialists.
Control. The measures correspond to those discussed
for Culicidae, but in dogs aim primarily at preventing
leishmanioses. Deltamethrin-impregnated, waterproof
collars (Scalibor•) are available for dogs that offer an
effective protection (up to 90%) against sandfly bites
for 5-6 months. Spot-on formulations of permethrin or
a combination of permethrin and imidacloprid reduce
phlebotome landings in the first week by 80-90%. The
effects, however, subside significantly until the 28th
day. Therefore, with the preparations mentioned, only
limited protection can be achieved against infection with
Leishmania ( ► Table 19 .16, p. 602) and leishmaniosis
(► p. 72).
Ph/ebotomus species that stay indoors are drastically
decimated by measures taken against Anopheles spp.
(insecticide sprays). Removal of organic waste (garbage,
foliage, kitchen waste, manure) in settlements prevents
or at least impedes the development of larvae.
Selected references c....:======
Antoniou M, Gramlccla M, Molina R, Dvorak V (2013) The
role of indigenous phlebotomine sandflies and mammals in
the spreading of leishmaniasis agents in the Mediterranean
region. Euro Surveill18: 20540.
Depaqult J, Grandadam M, Fouque F, Andry PE, Peyrefitte C
(2010) Arthropod-borne viruses transmitted by Phlebotomine
sandflies in Europe: a review. Euro Surveill 15: 19507.
Fischer D, Thomas SM, Belerkuhnlein C (2010) Temperature­
derived potential for the establishment of phlebotomine
sandflies and visceral leishmaniasis in Germany. Geospat
Health 5: 59-69.
Naucke TJ, Lorentz S, Rauchenwald F, Aspock H (2011)
Phlebotomus (Transphlebotomus) mascittii Grassi, 1908,
in Carinthia: first record of the occurrence of sandflies in
Austria (Diptera: Psychodidae: Phlebotominae). Parasitol
Res 109: 1161-1164.
 14. Phylum Arthropoda {arthropods)

Ready PD (2013) Biology of phlebotomine sand flies as vectors

of disease agents. Annu Rev Entomol 58: 227-250.

Family Simuliidae (black flies)

Disease: Black fly plague and simuliotox1cosls. 'J

Simulare (L): look like, pretend. Reference to the name

of the family unclear.

Summary
• Morphology end species. The body of Slmullldae Is
more compact than of other Nematocera. Length 2-6
mm, usually dark In colour, thorax dorsally humped,
broad wings, short legs. Antennae of both sexes
composed of 9-12 short segments aligned like a row Figure 14.39. Group of Slmullldae (length about 4 mm) (Photo:
of pearls, without bristles. Important species In Europe: A. Liebisch).
Simulium erythrocephalum, S. ornatum, S. reptans and
S. equinum.
• Development in flowing waters. Oviposition on plants
in or near water, 6-9 larval and 1 pupal stage in cone­
like cocoon. In general several generations per year.
• Epidemiology. Wide occurrence in Europe. Flight period
from March to November, the main risk for domestic
animals are mass swarms in spring. Activity from early
morning until evening, depending on temperature, light
intensity and humidity. Females of black flies mainly
prefer cattle as blood donor, but also sheep, horses, co
u
etc., and select certain parts of the body depending 0
0.
on the host.
• Pathogenesis and clinical signs. Slmulildae Inject ..c:
t
salivary toxins causing vascular damage. Pinprick-like <t:
bleeding in the skin (ear, udder, vulva, etc.), petechlal
internal bleeding In various organs, oedema of the
subcutaneous tissue and internal organs (lung oedema!), Figure 14.40. Simulium damnosum, head of <S, electron
dyspnoea, tachypnoea, incoordlnation, recumbency.
micrograph (Photo: H. Mehlhorn).
Deaths are possible in case of mass Infestation (> 10,000
bites per cattle) within a few hours. In horses, they are
involved, besides Ceratopogonidae, In causing summer
eczema induced by saliva allergens. The family has been revised taxonomically in recent
• Vector role. Simuliidae are important In the tropics as years. It contains around 2,000 species in 24 genera.
vectors of Onchocerca species. Four genera are of veterinary significance:
Diagnosis, control. Anamnesis (only grazing animals • Simulium(> 1000 species) in all zoogeographic zones;
affected, usually in spring), typical bite reactions on • Prosimulium ( ~ 150 species) in Holarctic zones;
skin, symptoms, black flies on animal (auricle, udder, • Austrosimulium ( ~25 species) in Australia and New
belly) or in the environment. Symptomatic therapy; Zealand; Q)
C
prophylaxis: during risk period grazing at night or limit • Cnephia (6 species in Holarctic zone). TS
grazing during daytime to windy, rainy days. '5
The remaining mammalophilic species belong to
Morphology and species. Simuliidae are 2-6 mm another 15 genera. The 4 most important species in co
C
long, compact, dark insects with a Brachycera-like Europe are Simulium erythrocephalum, S. ornatum, S. ·;::
habitus and with a dorsally humped thorax(also called reptans and S. equinum (formerly classified in other
buffalo flies), short legs and broad wings(► Figure 14.39 genera, i.e. Boophthora, Odagmia, Simulium and -�
and 14.41). The antennae are similar in both sexes and Wilhelmia) ( ► Table 14.12). Other common species >-
0)
are composed of 9-12 short segments that are aligned are S. lineatum as well as Prosimulium hirtipes and P. 0
0
like a row of pearls, without bristles ( ► Figure 14.40). tomosvaryi. The species S. columbaschense (syn. S. ·u5
columbazcense) (Kolumbacz fly) used to be important
co
Cl..
 Part Ill. Parasites and parasitoses: metazoa

l
eactions to
rrows)

Imago
Eggs on
floating plants

e� .
Several larval stages
. ,,,,,..- ..
...:...:.==-
- ·:

Pupa

Figure 14.41. Developmental cycle of Slmullldae (Graphics: IPZ, S. Ehret).

Table 14.12. Important Slmulium species In Europe.

�• (fo,mw nllM) Pmlff'tel breedl"V h1bltat Wlttf quality I.an� type

I Simullum erythrocephalum vegetation-rich large streams to medium medium lowland from northern Germany
1
(Boophthora erythrocephala) rivers of plains to pre-alpine regions
I Slmullum reptans vegetation-rich streams and rivers high lowl1md to low mountain ranges
Q) ' Slmullum omatum general flowing waters (ecologically very low lowland, low mountain ranges,
(Odagmia ornata)
C
0
versatile species), prefers turbulent flow pre-alps
-0
Q) Simulium equinum streams with moderate, regular flow and low plains, low altitude and low
� (Wilhelmia equina) submersed vegetation mountain ranges
ccu
C
·c
Q) in the Danube region but they became less important approaching females. Females of most Simuliidae
due to environmental changes. species are haematophagous, as they require blood for
C egg maturation; males feed on plant juices. About l
>,
0)
Life cycle. The development of Simuliidae is bound week after blood feeding, females lay several times 150-
0 to flowing waters(► Figure 14.41). Mating occurs soon 600 eggs, depending on species, in gelatinous material
0
·u5 after hatching of the adults, with the males visually onto water plants, floating objects, stones or into the
cu orienting at detached, larger objects(e.g. trees, grazing flow channel. Females of some species gather for this
cu
Q_ animals) and forming swarms where they intercept purpose. Egg masses are laid onto aquatic plants spread

out flat (e.g. S. erythrocephalum) or attached in sticky
clumps to plants (e.g. S. ornatum). For S. ornatum,
accumulated clumps of 16 g fresh weight have been
observed. Larvae hatch under water and usually remain
close to the location of the eggs. They can produce a
network of threads in which they initially reside. Later,
larvae drift several hundred metres downstream, and
attach to suitable substrates (plants, stones or pieces
of wood) with the caudal adhesive disc. Some species
have adapted to very specific conditions. Thus, larvae
and pupae of S. noelleri occur in large numbers only in
outflows of ponds or below weirs. Larvae filter small
food particles from the water with apical mouth brushes.
Depending on temperature, it takes 3-8 weeks until
the last of the 6-8 (9) larval stages develops into the
pupa with a length of 4-12 mm. The cocoon is cone-like
shaped, with its open end facing downstream ( ► Figure
14.41 ). The pupae have tube-like respiratory organs
('gills'), their number being species-dependent (4-24).
The hatched adults crawl to the surface or rise to it in
an air bubble. Under summer conditions, development
is completed in 6-8 weeks. Female Simuliidae survive
up to 3 months. The overwintering stages are eggs and
larvae, partly pupae.
Occurrence and epidemiology. In Europe, there
are many Simuliidae species, e.g. 49 species in Germany.
The 4 main species are found throughout Europe. S.
erythrocephalum has the greatest importance along
the major streams and rivers in lowland areas to the
prealpine region. S. ornatum, S. reptans and S. equinum
(the latter species often associated with S. lineatum) are
more likely to be found in hilly regions. P. hirtipes and
P. tomosvaryi also occur in mountain areas. The factual
occurrence of the species is determined by their specific
habitat requirements ( ► Table 14.12). In the first half
of the 20th century, thousands of animals perished in
the region of the former Yugoslavia after mass attacks
by S. columbaschense, and Simuliidae-related damage is
reported from many European countries, e.g. AT, CH,
DE and IT. An investigation in a northern province of
Germany in 1987-88 revealed that 44 of I 587 diseased
cattle died. With improving water quality in many rivers,
considerable populations of Simuliidae can develop
again.
Adult black flies are found in temperate, endemic areas
ofEurope from March until November. The clinically
relevant populations are usually those that develop
with increasing temperatures in early spring from
overwintering larvae. Due to weather conditions, adults
then emerge largely synchronously from the pupae and
can occur in masses. Mass hatching is triggered after a
prolonged cool period when a warmer period of one
week or longer without precipitation occurs. Moreover,
if there are good flight conditions at this time with high
humidity and largely no wind, a mass attack on grazing
animals may occur. Continued changeable weather
14. Phylum Arthropoda (arthropods)
results in episodic emergence of smaller populations.
The abundance of Simuliidae as a consequence decreases
temporarily in June and July. Later, there is an increased
attack due to the emergence of new generations. In the
course of a year, l-5 generations can develop.
With the exception of some ornithophilic species, black
flies are preferably active in sunny, calm weather. At -
Q)
0.
high abundance, attacks can begin in the early morning 0
hours and last until just before sunset; maximum flight
activities are observed in the morning, at noon and in
late afternoon. With strong wind or rain, flight activity
virtually ceases. Black tlies do not tly into buildings and
rarely into shelters, but can be introduced into stables
on the animals. Pemalcs can actively cover distances of
>20 km per clay, and can be transported by wind over
long distances. Therefore. infestations of grazing animals
can also occur for away from breeding habitats. When
searching for a host, black tlies orientate themselves over
longer distances (with a favourable wind direction up to
a few km) olfactorlly (bovine odour), at a distance of a
few metres visually and prefer to land predominantly on
certain areas of the body, depending on the species, e.g. S.
lineatum on ears and S. erythrocephalum and S. ornatum
on the lower abdomen of the animals. Dark colours
(black, blue) are more attractive than brighter ones.
Diseases of cattle have been observed on pastures from
plains to altitudes of 1,300-1,500 m. Cases often occur
shortly after turnout to graze in April/May, but disease co
is also possible later (August/September), especially in -0
0
animals without previous pasturing.
e
a.
.c
t:'.
Pathogenesis. The painful bites of black flies can cause <(
a considerable nuisance for animals and humans, even at
low fly abundance. Simuliotoxicosis is caused by salivary
toxins, of which the toxicological and biochemical
characterisation is still pending. Symptoms suggest
that these toxins primarily cause vascular damage.
The pathological-anatomical picture is characterised
by numerous petechial haemorrhages in the skin that
are connected through the puncture channel with sub­
epithelial blood pools, from which the female black
flies suck blood (pools feeders) ( ► Figure 14.42).
Furthermore, it also often includes severe subcutaneous
oedema and oedema of organs (larynx, lung, abomasum,
(1)
brain), swelling of lymph nodes, petechial haemorrhages
·u
C
in the serous membranes, in the peri- and endocardium '6
in all parenchyma including the brain, and effusions in Q)
�
the pleural and peritoneal cavity. From the number of
skin lesions it was estimated that about 1 0,000 black
cco
C
flies can kill a cow. ·;;::
(1)
j
• Clinical signs in cattle. Approaching swarms of .s
black flies excite the animals, even to panic reactions. The >.
-
0)
bites cause pinprick-like bleedings in the skin, which are 0
0
conspicuous mainly at less hairy body parts (including ·u5
ears, udder, vulva, scrotum, tail, inner surface of the
co
Q
 Part Ill. Parasites and parasitoses: metazoa
Figure 14.42. Simuliotoxicosis: (a) skin reaction on udder of a cow that died; (b) puncture wound in skin of cattle (histological
section; blood pool see arrow) (Photo: IPZ, J. Eckert).
j,
hind leg). Through confluence of numerous petechial
haemorrhages, blood crusts may form.
In extreme cases, partly pronounced subcutaneous
oedemas develop, particularly at throat, dewlap, lower
abdomen, udder and scrotum. The oedema feel hot,
sometimes the animals have fever. Furthermore, there
are mucosa! swellings, oedema of internal organs (see
above), heart-lung symptoms with greatly increased
pulse rate and tachypnoea, accompanied by excitation,
unsteadiness, cessation of rumen activity and
recumbency. Death of animals can occur within a few
hours to 2 days after black fly attacks. Surviving animals
recover, depending on the severity of the disease, within
a few days or only after weeks.
In endemic areas, the continuous disturbance of
grazing animals and the painful bites are considered
as substantial factors that can affect weight gain and
especially milk production of the animals. Weather­
related mass occurrence of black flies in eastern Australia
temporarily decreased milk supply in the affected region
by approximately 15%.
• Clinical signs in other animal species. Simulio­
toxicosis is much rarer in other domestic species, e.g.
sheep, horse, pig and dog, than in cattle. Often, wild
ruminants are highly plagued by Simuliidae. The
observation that horses with summer eczema often have
high levels of lgE against salivary proteins of Simuliidae
gives rise to the suspicion that black flies are involved
in the genesis of this allergy.
Immunology. The reduced sensitivity of grazing cattle
to toxins of Simuliidae with progressive grazing periods
suggests that the animals develop immunity, possibly via
neutralising antibodies. However, proof for this has so far
not been provided (generally, there is little data available
with regard to the immune responses to Simuliidae,
and in particular their salivary components are largely
unexplored). Recent studies demonstrated complex
antihaemostatic factors and immunomodulatory
activities (inhibition of proliferation ofT-cells, induction
of apoptosis) of the saliva of Simuliidae.
Diagnosis. The clinical picture, especially the numerous
blood spots on the skin and the pathological findings,
together with the seasonally limited occurrence, secure
the diagnosis. From a differential diagnosis point of
view - also in view of the seasonal occurrence - grass
tetany has to be considered. Black flies can be collected
for diagnosis from the auricle of infested animals or
caught in their vicinity by netting (or in CO2-baited
traps). The typical larval and pupal stages are easy to
find in flowing waters. A diagnosis of the morphological
species is then a matter for the specialists.
Therapy and control. Diseased animals must be
put in stables and promptly treated symptomatically
(stabilisation of the circulation, anti-inflammatory
therapy, calcium infusions). One option for prophylaxis
in endemic areas, especially during the peak risk period
in spring, is night pasture or limiting day pasture to
rainy, chilly days. Predictions in spring provided by
agricultural weather services based on general weather
data or better after inspection of breeding waters are
helpful. The effect of pyrethroids (e.g. permethrin,
cypermethrin, spray or pour-on application) usually
only lasts a few days and offers also during this period
only partial protection against Simuliidae. Insecticide
ear tags do not provide sufficient protection.
Applying insecticides to watercourses is not feasible
because of potential environmental damage. Also,
interventions in the habitats, such as removal of water
plants, change of water flow, are often ecologically
questionable. A control of the aquatic stages by
introducing B. thuringiensis israelensis proteins to the
waters, as is successfully carried out for Culicidae ( ► p.
462), is in principle also possible for Simuliidae and is
indeed practised in some countries. However, since the
breeding habitats of black flies are flowing waters, the
effect is limited by the drift of the proteins. Moreover,
in the critical spring months, the usually low water
temperatures impair the effect of the B. thuringiensis
proteins.

Relevance to humans and vector role. In humans,
the bite of black flies leaves a small blood point on the
skin. Around the bite site there often develop 2-3 mm
large erythema with a central pustule and a larger
oedematous swelling. The painful reaction after the
bite can radiate far and continue for some days. General
reactions (fever, circulatory disorders) rarely occur.
Simuliidae transmit filaria, e.g. some Oncl10cerca spp.
of cattle(► p. 471) as well as Onchocerca volvulus, the
causative agent of river blindness in humans. Species
of the extensive S. damnosum complex are responsible
for the transmission of 0. volvulus in Africa, and local
species in the Americas. Protozoans of the genus
Leucocytozoon are transmitted among birds. Simuliidae
only play a minor role as vectors of viruses.
Selected references ==�=:::;:::::::::i=::::::i
Adler PH, C rosskey RW (2014) World black flies (Diptera:
Simuliidae): A comprehensive revision of the taxonomic and
geographical inventory 2014. Available at: http://tinyurl.com/
pux2zxu.
Adler PH, Cheke RA, Post RJ (2010) Evolution, epidemiology,
and population genetics of black flies (Diptera: Simuliidae).
Infect Genet Evol 10: 846-865.
Lechthaler W, Car M (2005) Simuliidae. Key to larvae and pupae
from Central and Western Europe (CD-ROM). Vienna, Austria:
Eutaxa; ISBN 3-9501839-3-0.
Family Ceratopogonidae (biting midges)
Disease: Sweet itch (summer eczema) of horses,
Keras(G): horn;pogon(G): beard. Refers to the fascicular
hirsute antennae of males.
Summary
• Morphology, species. Main genus: Cul/co/des. Very
small flies, length 1-4 mm, humped thorax, wings
brighVdark mottled and hairy. Antennae with 12 to 15
segments, in males fascicular hirsute.
• Life cycle. Oviposition in m1:1ddy places with large
amount of detritus. After four larval stages development
of a small mobile puf)a.
• Clinical signs and pathogenesis. Biting midges can
regionally be highly annoy img. Bites cause intense
itching, inflammatory reactions with blistering and
allergic skin diseases. The allergy manifests itself in
horses as localised, intensely itchy rash with pustules
and alopecia.
• Vector role. Some species of biting midges transmit
pathogens (viruses, bacteria, protozoa and nematodes),
e.g. Bluetongue virus and African Horse Sickness virus.
14. Phylum Arthropoda (arthropods)
Morph ology and species. The members of 4 of the
60 genera of the family suck blood from warm-blooded
animals. By far the largest (almost 1000 species) and
most important genus is Culicoides; about 50 species
of this genus act as vectors of pathogens. In Europe,
30-40 Culicoides species are believed to attack warm­
blooded animals. According to trap catches, species of cu
the C. obsoletus group dominate in the lowland, with <I,
Cl.
approximately 90% compared to the C. pulicaris group 0
species with about IO%; with increasing altitude in
alpine regions, this ratio is reversed. Biting midges of
grazing cattle in northern Germany from the C. obsoletus
group were C. dewulfi, C. obsoletus and C. scoticus,
each accounting for 20-30%; on horse C. chiopterus in
addition represented 20-25%. The other genera that
approach warm-blooded animals are Leptoconops,
Austroconops and Forcipomyia. Culicoides spp. are only
1-4 mm long. Most species have bright/dark mottled
and hairy wings that arc kept folded over the humped
thorax when resting. The 12-15 antenna segments of the
cJcJ are fascicular hirsute(► Figure 14.43 and 14.44).
Life cycle. Culicoides species breed in moist to muddy
habitats. Eggs are laid in a gelatinous mass in hidden
places. After four larval stages, which mostly live as
predators, the small pupa develops, from which, after 1-2
weeks, the adult midge hatches and survives 2-5 weeks.
Occurrence and epidemiology. The genus
Culicoides occurs worldwide in all climates and in areas (1j
up to high altitudes. The breeding habitats of different -0
0
species can vary widely, ranging from tree holes, muddy 0.
puddles, wet areas in marshland (the larvae of some .c
species are halophilic), rice fields, sandy b eaches and t
<t:
mangrove forests. Some European species (e.g. C.
dewulfi) use cattle and horse manure as larval habitats.
Figure 14.43. Scheme of a midge (Atrichopogon luteicollis)
(Source: J.-C. Delecolle and E. Gandolfi).
 Part Ill. Parasites and parasitoses: metazoa
Figure 14.44. Culicoides obsoletus (Photo: IPZ).
The development periods vary in different regions. In
temperate climates, there is usually only one generation
per year but there may be up to three generations in
some species (e.g. C. obsoletus). Overwintering occurs
in the larval stage. In areas with hot summers, 6 or more
generations develop per year.
In Europe, flight activities are observed, with species­
specific differences, in the months of April to mid­
December. The main activities range from July to
September. The flight radius of Culicoides spp. is just
a few 100 m around the breeding place. However,
long-distance drifts by wind are possible. Most species
are diurnal (late afternoon and early morning), some
also fly at dusk, all preferably with no wind and an
overcast sky. In autumn, the species C. obsolct·us and
C. dewulfi, in particular, also fly into stables when the
outside temperature drops. For host-Anding, olfactory
stimuli (CO2) are used. Females take blood at intervals
of 3-5 days.
Pathogenesis and clinical signs. Biting midges
can regionally be highly annoying. They are 'pool
QJ
T5
C feeders' and their bites cause intense, highly pruritic,
'6 inflammatory reactions with blistering. Cattle are
�
QJ
approached mostly on the back and abdominal areas
cco as well as on the limbs, horses preferably dorsally from
C the neck to the tail head.
·;::
QJ
�
A serious consequence of Culicoides attacks are allergic
-� reactions to saliva allergens. Originally described as
>,
0)
sweet itch in horses (Queensland itch in Australia),
0 this disease also affects other animal species (cattle,
0
·enco sheep). The allergy manifests itself in horses as localised,
intensely itchy rash with pustules and alopecia. Animals
co
0... often show severe scratching marks due to itching. The
locations usually correspond to the preferred body
regions of the regional Culicoides species, such as the
withers, back and dorsal tail or lower abdomen and legs.
According to studies in Scandinavia, eczema in horses
develops for the first time after 3-5 grazing seasons,
disappears at the end of the grazing period and relapses
with the occurrence of adult midges. In Europe, Icelandic
horses are particularly prone to suffer from summer
eczema. Significantly more often affected than horses
born in endemic areas are those born in Iceland, which
is Culicoides-free, and which later are imported into
endemic areas. The corresponding prevalences were 27%
compared to 7-8% in studies from Sweden and Norway.
The predisposition is also genetically inherited and is
associated with certain leukocyte antigens.
Immunology. Sweet itch of horses is an allergic disease
mainly of the immediate type. It is mediated by specific
IgE antibodies to allergens in the saliva of the biting
midges. In addition, specific IgG antibodies that sensitise
mast cells play a role. The spectrum of allergens is still
insufficiently investigated.
Diagnosis. First indications for biting midges are
their small size and their spotted wings. Morphological
species identification can be extremely difficult; as
alternatives, molecular biological (PCR) as well as
mass spectrometric methods (MALDI-TOF MS)
have been developed. In the differential diagnosis of
summer eczema, photosensitivity and mange have to be
considered. For allergy testing, commercial allergens,
usually crude extracts of C. variipennis, are available for
skin tests. Their specificity is valued differently.
Control and therapy. Horses can be protected
against biting midges with so-called eczema blankets
which cover most parts of the body. Prophylactic
weekly applications of pyrethroid solution can be used.
Summer eczema is treated with antihistamines and
corticosteroids. Attempts to desensitise allergic horses
with extracts of biting midges yielded conflicting results.
In cattle, a partial protection against biting midges is
possible through the use of insecticide ear clips or
insecticides in pour-on application. These measures
are insufficient to control biting midges as vectors of the
bluetongue virus (see below) (bluetongue disease can
be effectively controlled by vaccination of ruminants).
Vector role. Culicoides species transmit a broad
spectrum of pathogens (viruses, bacteria, protozoa and
nematodes;► Table 14.13). With the advent of the
economically important bluetongue disease in cattle and
small ruminants, caused by the bluetongue virus (BTV),
in Europe in 2006, the genus has attracted particular
interest. Virus DNA was found in C. obsoletus, C. scoticus
and C. dewulfi, but the epidemiological questions are
not yet entirely resolved. The main vector of BTV
in the Mediterranean, C. imicola, does not occur in
central and northern Europe. Recently, Schmallenberg
virus has been described in Europe as the cause of fetal
malformation; vectors are Culicoides species.
 14. Phylum Arthropoda (arthropods)

Table 14.13. Pathogen transmission (selection) by Culicoides spp.

Agent group

Bunyaviridae
Agent

Akabane virus
Affected hdste

domestic ruminants
-
I
Occurrence

Australia. parts of Asia, Middle

I
I
-- East, Africa
Schmallenberg virus cattle, sheep, goat _ __ __ many European coun_ tries
�
Reoviridae �ueto_r,gue vir_uJ _ - cattle, sheep, goat, wild ruminants worldwide \...
Q,
African Horse Sickness virus horse,
_.__ -- other equids - Africa, Middle East, Turkey. etc.
- -- - j[(ES. PTI 1 C

Epizootic Hemorrhagic Disease wild ruminants I North America, Israel Turkey,

I---
-- virus
- -- - - Africa. Australia
Haemosporina Hepatocystls spp. mostly tree-inhabiting mammals I Africa
-- (monkeys. bats)

.---- Haemop!!]leus spp. --- �oslly birds and reptiles I worklwide

Nematodes Onchoc�rca glbso.!!!._ cattle I Alrica, Asia, Australia
-- -
- cervlca/1s
Onchocerda - horse worldwide
Dlpetalonema perstans humans Africa, South America
Dipetalonema streptocerca humans West and Central Africa
1 Previous outbreaks.

·· Selected references i:....::::w:::c::;;;&a==m Kolm-Stark G, Wagner R (2002) lntradermal skin testing in

Carpenter S, Mellor PS, Torr SJ (2008) Control techniques for
Culicoides biting midges and their application in the U.K. and
northwestern Palaearctic. Med Vet Entomol 22: 175-187.
Carpenter S, Veronesi E, Mullens B, Venter G (2015) Vector
competence of Cullcoldes for arboviruses: three major
periods of research, their influence on current studies and
future directions. Rev Sci Tech 34: 97-112.
Carpenter S, Wilson A, Mellor PS (2009) Cul/co/des and the
Icelandic horses in Austria. Equine Vet J 34: 405-410.
Littlewood JD (1998) Incidence of recurrent seasonal pruritis
('sweet itch') in British and German shire horses. Vet Rec
142: 66-67.
Mathieu B, C�tre-Sossah C, Garros C, Chavernac D,
Balenghien T, Carpenter S, Set ier-Rio ML, Vignes-Lebbe
R, Ung V, Candolfi E, Delecolle JC (2012) Development co
and validation of IIKC: an interactive identification key for -0
0
Culicoides (Dlptera: Ceratopogonidae) females from the 0..

emergence of bluetongue virus in northern Europe. Trends
Microbiol 17: 172-178.
Gonzalez M, Lopez S, Mullens BA, Baldet T, Goldarazena A
(2013) A survey of Cul/co/des developmental sites on a farm
in northern Spain, with a brief review of immature habitats of
European species. Vet Parasitol 191: 81-93.
Hubalek Z, Rudolf I, Nowotny N (2014) Arboviruses pathogenic
for domestic and wild animals. Adv Virus Res 89: 201-275.
Kaufmann C, Steinmann I, Hegglin D, Schaffner F, Mathis
A (2012) Spatio-temporal occurrence of Culicoides biting
midges in the climatic regions of Switzerland along with
large scale species identification by MALDI-TOF mass
spectrometry. Parasit Vectors 5: 246.
Kaufmann C, Mathis A, Vorburger C (2015) Sugar-feeding
behaviour and longevity of European Culicoides biting
Western Palaearctic region. Parasit Vectors 5: 137. .c
t
Meiswlnkel R, Scolamacchla F, Olk M, Mudde J, Dijkstra <(
E, Van der Ven IJ, Elbers AR (2014) The Mondrian
matrix: Culicoides biting midge abundance and seasonal
incidence during the 2006-2008 epidemic of bluetongue in
the Netherlands. Med Vet Entomol 28: 10-20.
Rasmussen LD, Kirkeby C, Bodker R, Kristensen B,
Rasmussen TB, Belsham GJ, Botner A (2014) Rapid
spread of Schmallenberg virus-infected biting midges
(Cul/co/des spp.) across Denmark in 2012. Transbound
Emerg Dis 61: 12-16.
Wenk CE, Kaufmann C, Schaffner F, Mathis A (2012) Molecular
characterization of Swiss Ceratopogonidae (Diptera) and
evaluation of real-time PCR assays for the identification of
Culicoides biting midges. Vet Parasitol 184: 258-266.
Q)
·u
C

midges. Med Vet Entomol 29: 17-25.

Q) I
Koenraadt CJ, Balenghien T, Carpenter S, Ducheyne E, 2 I
Elbers AR, Fife M, Garros C, lbanez-Justicia A, Kampen
H, Kormelink RJ, Losson B, Van der Poel WH, De C
·;;::
Regge N, Van Rijn PA, Sanders C, Schaffner F, Sloet Q)

van Oldruitenborgh-Oosterbaan MM, Takken W, Werner

D, Seelig F (2014) Bluetongue, Schmallenberg - what is .£
next? Cul/co/des-borne viral diseases in the 21st Century.
BMC Vet Res 10: 77. 0
0
·u3
Part Ill. Parasites and parasitoses: metazoa

- Suborder Brachycera ('short-horn

flies')

Brachys (G): short; keras (G): horn. 'Short-horns' ; refers

to the short antenna with few segments.

Family Tabanidae (horse flies, deer

flies, clegs)
Tabanus (L): horse fly.

Tabanids belong to the Orthorrhapha whose adults

emerge from the pupa through a T-shaped seam in the
puparium (orthos [G]: straight; raphe [G]: seam). Figure 14.45. Tabanlds: (a) Haematopota sp. (length 9-12 mm);
(b) Hybomitra sp. (length 13-16 mm) (Photos: A. Liebisch).
Summary
• Morphology. Robust flies, 6-25 mm long, head
piercing, rasping and sucking. Males do not bite, they
nearly triangular as seen from above, compound eyes
remarkably large. Antennae with 3 clearly Identifiable
lack parts of the piercing tools (maxilla).
segments, project forward, the apical segment
enlarged with a ringed 'pen' from 4-8 fused segments. Worldwide, approximately 4,000 tabanid species are
Mouthparts adapted for cutting, piercing, rasping and known, of which about 165 occur in Europe (50-60
sucking. species in Central Europe). Common tabanids in Europe
• Species. Numerous species; Important parasites of include, in addition to the genera Heptatoma and Silvius,
domestic animals In Europe are mainly species of the following:
the genera Haematopota, Tabanus, Hybomitra and
Chrysops. Genus Haematopota
• Life cycle (egg ..... 5-11 larval stages --+ pupa --+ adult)
in mud or In soil; duration around 1 year, partly longer;
Haematopota p/uvialis (common horse fly,
usually only one generation per year.
• Occurrence. Worldwlde distribution, ubiquitous from
notch-horned cleg)
lowlands up to high mountain areas.
• Epldemlology. In Central Europe, flight activity from Most common species, medium in size, 8-12 mm
mid-May to mid-October with highest abundances In long, slender, grey-black. Wings with bright spots on
July/August. Tabanlds are diurnal; only females suck dark ground; in rest they are closed together above the
blood, especially on cattle, horses, wild ruminants, abdomen. Eyes with wavy bands, antennae longer than
and humans. the head, 'pen' with three segments ( ► Figure 14.45a).
• Pathogenesis, cllnlcs, vector role. Painful bites, Other species: H. italica, H. subcylindrica.
considerable annoyance for animals, blood withdrawal,
reduced performance. Tabanlds are mechanical or Genus Tabanus
biological vectors of viruses, rlckettsla, bacteria,
protozoa and helmlnths.
Tabanus bovinus (pale giant horse-fly)
• Control see Muscldae (► p. 478).

Large tabanid {10-24 m m long) with a brownish

Morphology and species. Tabanids are robustly
built flies, 6-25 mm long, grey-black, yellowish brown to
greenish in colour, some with coloured spots or stripes
( ► Figure 14.45 and 14.46). The head is wider than long
and approximately triangular when viewed from above.
Remarkable are the large, iridescent (only in the living
insect) compound eyes, which may have patterns. In
males, the eyes nearly touch, whereas in females there
is a greater distance between them. In some species,
additional 1-3 small frontal eyes (ocelli) are also present.
The antennae always project forwards and consist of
three clearly identifiable segments. The mostly enlarged
apical segment carries a striped 'pen', which is composed
of 4-8 fused segments. The short and strong mouthparts
project downward and are adapted in females for cutting,
abdomen, wings without pattern and slightly spread
at rest. Compound eyes dull green with yellow stripe
patterns, antennae shorter than the head, 'pen' with 4
segments; very similar to T. sudeticus ( 19-25 mm long).
Other, smaller species {10-16 mm long): T. bromius, T.
maculicornis.
Genus Hybomitra
Hybomitra spp.
Very similar in habitus to Tabanus, length 13-16 mm,
densely hairy, wings transparent, eyes large and without
pattern, 'pen' of the antennas with 3 segments ( ► Figure
14.45b).

Pupa
Figure 14.46. Life cycle of tabanids (Graphics: IPZ, S. Ehrat).
Genus Chrysops
Chrysops caecutiens (splayed deer fly)
Relatively small, 9-13 mm long tabanid, abdomen
strikingly black-yellow, wings with a broad stripe and
spread at rest (delta position). Bright green eyes and
iridescent with patterns; antennae much longer than
head, 'pen' with 4 segments. Other species: C. re/ictus,
C. viduatus.
Occurrence. Tabanids are cosmopolitan from
temperate climates to the tropics and from lowlands
up to high mountain areas (>3,000-5,000 m). Among
the many species that occur in Europe, Haematopota
and Tabanus species are the most predominant parasites
of domestic animals.
Life cycle and epidemiology. Development
proceeds from egg over several larval stages and a pupa
to the adults. Eggs are usually deposited in masses of
100-1000 in humid soil (Haematopota spp. and some
Tabanus species) or on plant parts at the edge of water
bodies (Hybomitra and Chrysops species). Larvae hatch
and moult twice within 3-6 days, then penetrate the mud
of water bodies or the soil where they remain for months,
overwinter, go through several more moultings and live
as predators of small animals (Tabanus, Haematopota)
or feed on plant material ( Chrysops). The total number
of larval stages varies from 5 and 11 (13) and is variable
even within the same species. The last larval stage is
cylindrically shaped and segmented; it has hooked
14. Phylum Arthropoda (arthropods)
� ��� Eggs (I)
o_
c5
mandibles at the front end and a reduced head capsule
(hemicephalic larva, ► Figure 14.46). In spring, the
larvae migrate into drier areas at the edge of water bodies
or moist locations and pupate (mummy pupae) there just co
below the surface. After a pupal period of 1-4 weeks, the -0
0
adults hatch. Development (egg to adults) takes about a.
I year, but can also extend over 2-3 years. .c.
t
<(
At favourable temperatures, males form swarms - usually
in the morning - and mate with females in the air or
on plants. The activity period of adults lasts in Europe
from mid-May to mid-October, but varies in length
within the individual genera. The majority of species
do not occur in larger population densities until June
and reach a peak in July/August. Most tabanid species
are diurnal, a few nocturnal. Daily activity is strongly
influenced by meteorological factors (temperature,
humidity, light intensity). In cool weather conditions
( < 13 °C), tabanids are inactive and remain at resting
places. Favourable conditions for many species are
Q)
sunny, warm (>20 °C), wind-poor days with low relative C
humidity (<60-70%). Horse flies (Haematopota spp.) can "c:5
'6
also be very active in overcast, humid thunderstorm and 2
Q)
light rain conditions. During the day, tabanids usually �
exert their main activities from late morning until early co
C
·;:::
afternoon, but some species can also be active in the Q)
morning and evening hours. Males and females are
obligately dependent on carbohydrate-containing juices -�
(nectar, tree sap) and water. Females of most species >,
CJ)
require a blood meal after mating because protein is 0
0
required for egg maturation. They approach a host every 'cii
2-3 days, and their life span is 3-4 weeks. Males are not co
co
haematophagous and die soon after mating. 0..
 Part Ill. Parasites and parasitoses: metazoa
Preferred hosts for the female tabanids are ungulates
(cattle, horses, wild ruminants) and other larger
mammals(► Figure 14.47); occasionally, they also attack
birds. Humans are mainly affected by Haematopota
and Chrysops species. Females rest during the day
in protected places in bushes, and locate their hosts
primarily visually, partly olfactorily. For blood feeding
they have a strong preference for the following body
parts: head, neck, back, lateral abdominal wall( Chrysops
species) or flanks, lower breast and belly, udder, limbs
(Tabanus and Hybomitra species); Haematopota species
often display no preference. Tabanids do not fly into
stables, and rarely into shelters of grazing animals where
they are hardly active.
Pathogenesis and clinical signs. Female tabanids
cut with their large, cutter blade-shaped mouthparts into
the skin, and inject anticoagulant saliva into the wound
where a small pool of blood forms on which the tabanids
feed ('pool feeders'). The deep and painful bites, which
may be accompanied by urtication, cause nuisance,
which in grazing animals can cause significant disorders
of feed intake and reduced productivity (reduced milk
production). The amount of blood ingested by a female
depends on the size of the insect and ranges from 20-200
mg ( extreme values 500-700 mg). With 50 tabanids per
hour on an animal as observed in Europe, up to 60 ml of
blood can be lost in 6 h. However, blood losses are often
C of the lid of brood and honey cells in which the larvae
>-
0)
0 honey. In differential diagnosis Acarapis and Varroa
0
·u5
Figure 14.47. Common horse flies (Haematopota sp.) (length
co
0.. 8-12 mm) on the neck of a horse (Photo: A. Liebisch).
lower and have no measurable impact on healthy cattle.
The blood that leaks from the biting sites attracts blood­
licking insects that are a further nuisance to the host.
Vector role. Tabanids are biological or mechanical
vectors of numerous pathogens under natural or
experimental conditions. Mechanical transmission is
favoured by the fact that defensive reactions of the host
cause part of the female tabanids to interrupt blood
feeding and then immediately continue on the same
or another host, mostly within a 100 m range. Upon
completion of the blood meal, a blood film adheres
to the mouthparts, in which pathogens present in the
host blood can survive for some time. The efficiency
of transmission depends on pathogen density in the
blood, survival period of pathogens and other factors.
The following paragraph lists a selection of pathogens
that are transmitted by tabanids.
• Mechanical transmission. Viruses: Virus of
equine infectious anaemia. Rickettsia: Anaplasma
marginale, causative agent of anaplasmosis in cattle
(principal vector: hard ticks). Bacteria: Francisella
tularensis, causative agent of tularaemia(vectors: ticks,
tabanids and other blood-sucking insects). Protozoa:
Trypanosoma brucei evansi, causative agent of surra, T.
vivax, causative agent of nagana(main vectors: glossinids;
tabanids and Stomoxys are mechanical vectors). Tabanids
and other blood-sucking insects transmit Besnoitia
besnoiti under experimental conditions, but the vector
role of these insects under natural conditions is still
unclear.
• Biological transmission. Protozoa: Trypanosoma
(Megatrypanum) theileri of cattle and Megatrypanum
spp. of wild ruminants. Helminths: Loa loa, causative
agent of human loaosis.
Diagnosis and control. Tabanids can be visually
distinguished from other flies by their habitus. Species
identification requires special knowledge. Control
measures are discussed in the Muscidae chapter(► p.
478).
Family Braulidae and Drosophilidae
• Braulidae. Braula coeca (so-called bee louse), the
causative agent of braulosis of honey bee, is a small, about
1.5 mm long, wingless, cosmopolitan fly (► Figure
14.48). Adults are commensals, living on the thorax
and abdomen of bees, and they ingest food from the
mouthparts of their hosts. Eggs are laid on the inside
develop. This can lead to a reduction in the quality of
mites must be considered.

Figure 14.48. Brau/a coeca (length about 1.5 mm) (Graphics:
IPZ, A. Seeger; after Hiepe and Rlbbeck 1982).
• Drosophilidae(fruit flies, vinegar flies) are 2-4 mm
long flies which use fermenting or acidifying substrates as
breeding substrates and which can sometimes become a
nuisance in households or in food processing companies.
Drosophila me/anogaster has achieved worldwide fame
as a study object in genetics. Phortica variegata, already
earlier known as the intermediate host of Thelazia
callipaeda ( ► p. 346) in East Asia also has this role
in Europe. Adults feed on fermenting plant juices and
lacrymal secretions of animals and humans.
Family Muscidae and Fanniidae
Musca(L): fly; morphe(G): form, shape.
Muscidae and Fanniidae belong to the group of
Muscomorpha in which pupae open by tearing a
circular seam and lifting a lid at the anterior pole(hence:
Cyclorrhapha; kyklos [G]: circle; raphe [G]: seam).
Summary
• Morphology, species. Mostly dark-coloured, medium­
sized flies. Mouthparts llcklng-sucklng or piercing­
sucking. The short antennae have on the third segment
a lilristle(arista), which Is differently shaped In the various
families(► Figure 14.49). Important groups: house and
stable flies: large house fly (Musca domestics) and
stalille fly (Stomoxys calcitrans); so-called 'pasture flies':
eye and face fly (Musca autumns/ls), sweat and head
flies (Hydrotaea spp.), horn flies (Haematobla lrrltans and
H. stimulans). Main harmful effect for animals especially
lily liliting flies.
• life cycle. Uniform basic pattern (egg - 3 larval stages
-+ Ji)upa -+ adult), larval development In very different
breeding substrates im and around stables or In the field.
Mostly high proliferation fi)Otential with three or mQre
generations per year; therefore partly high abundances.
• Occurrence, epidemiology. Widespread and common.
Flight activities species-specific, but usually from May
to October, in stables also all year round. Diurnal activity.
• Adverse effects, vector role. Nuisance pests of animals,
reeuced performance in case of severe infestations.
Stat>le flies (Musca, Stomexys) can spread various
pathogeras(e.g. Esclilerichia coli, Campylobacter jejuni,
Cryptosporidium oocysts, Ascaris eggs). Pasture flies
y
14. Phylum Arthropoda (arthropods)
are vectors of the causative agent of summer mastitis
(Hydrotaea species) and keratoconjunctlvitis (Musca
autumns/is) In cattle. In addition, stable and pasture flies
(Musca, Stomoxys) play a role as intermediate hosts for
helmlnths (Habronema, Parafllarla, Thelazia). Stomoxys
ca/citrans is suspected to transmit Besnoitia besnoiti �
(► p. 115)
• Control. With physical, biological, chemical and 0
integrated procedmes. f2roblem: lnsecticl�e-resistance.
Morphology and species. The family Muscidae
includes >4,000 species, the family Fanniidae .··J
approximately 260. These are mostly dark-coloured,
medium-sized nies with licking-sucking or biting­
sucking mouth parts ( ► Figure 14.49). They are of
considerable importance worldwide as nuisance pests
and vectors of different groups of pathogens. A selection
of important species is shown in ► 'fable 14.14. lt should
be noted that highly similar species exist that are difficult
to distinguish.
General description of development. Development
of the species of the two families follows a uniform
basic pattern(egg-+ 3 larval stages-+ pupa), which is
shown for Musca domestica as an example ( ► Figure
14.50). The larvae(Ll) emerge from the 1-2 mm long,
oval, yellowish white eggs that are laid by females into a
breeding substrate; these then develop by moulting into 2 co
other larval stages(L2-3)(length of L3: 8-13 mm). Larvae "O
0
are elongate and legless(= maggots). There is no head a.
capsule at the pointed apical end (= acephalic larvae), ..c:.
t:::
but a dark-coloured cephalopharyngeal skeleton that <C
bears retractable mouth hooks which serve to adhere to
substrates and to facilitate locomotion( ► Figure 14.50).
Closely behind the apical end are fan-shaped respiratory
openings(spiracles). At the posterior truncated end are
paired spiracle plates. These plates(► Figure 14.58, p.
486) are of importance for the identification of maggots.
The pupal stage develops within the L3, which creates a
special shell(puparium) by thickening, hardening and
darkening of its integument. The puparium is barrel­
shaped in M. domestica(► Figure 14.50). In other fly
species, there are variations of the morphology of the
larvae(e.g. rows of thorns or appendages) or the puparia
(which might bear structures of the L3).
In the following section, some fly species are described
and divided into the groups of stable/house flies and
pasture flies.
Stable and house flies
Life cycle and epidemiology. Stable and house
flies prefer to remain in buildings and their immediate
environments, but also invade apartments and other
spaces, e.g. kitchens, bakeries, slaughterhouses and
food processing plants, where they, especially Musca
 Part Ill. Parasites and parasitoses: metazoa

Antenna

b C

Figure 14.49. Musca domestica: (a) head; (b) antenna with arlsta; (c) labellum, SEM (Graphics: a, b: IPZ, M. Mathys; Photo: c:
H. Mehlhorn).

'., Table 14.14. Species (selection) of the families Muscidae and Fannlldae.
'l
., ,, " • ' •<, '" ,:fv �ll�
�.. 'I! '"' '.t'·i' a ;· . ".,;

�'F�mily, subfamily an� sp_ttcl•�

·-�
Oecumtnce
( l'f. ��. 1 .".•. Main habitats
J..? length of adults �- ··- ' :c
V.{�. '-' l.i;;i,'{i,; ,,._
I Family: Muscidae, subfamily: Muscinae
,-- Musc;-d�;�;tica (comm�n h�usefly) worldwide stables, houses and environments
L: -5-8-· mm
L- -·---
- - - - --
I
Musca sorbens (bazaar fly) subtropics and tropics: Africa, Asia, houses, stables and environments
Pacific region1
I
I L: 4-7 mm
- ·----- - ---- - -•- ---
' Musca autumnalis (face fly) Europe, USA pasture land
L: 5-7 mm ---· -·---
I.. - - --- --- .
Hydrotaea spp. (sweat flies, head flies) Europe pasture land
-- - -L: 3-6,_mm
- --- - - - --- -
Family: Muscidae, subfamily: Phaonllnae
... Oph;ra aenesce�� (garbage-or dump 110 t �rope, Nearctlc, Neotroplc, Pacific stables, flats, waste disposal sites
Le 6-6.6 mm raglans
�amll_y� M�scld�e! _subfaml!Y: Stomo�ylnae!>�tl�g flies)
�

Stomoxys ca/citrans (stable fly) worldwide stables, houses and en vironments

- L: 4-7 mm
----------------- -···-------
Haematobla stimulans (large horn fly) Europe, Asia, North America pasture land
L:-5-7
-- mm- --- - · · - ----- --
Haematobia irritans (horn fly) Europe, North and South America, North pasture land
L: 3-5 mm Africa, Middle East to East Asia
--
Family: Fanniidae
Fann/a canicularis (lesser house fly) worldwide stables, houses and environments
L: 4-7 mm
1 Not in Australia.

domestica (see below), are nuisance pests for animals and or stables ( ► Figure 14.51). Because some species prefer
humans and act as mechanical vectors of microorganisms to live in the environment of humans, they are called
of hygienic importance. Some species also occur on synanthropic.
g razing animals, especially in the close vicinity of farms
 14. Phylum Arthropoda (arthropods)

Imago

�
/ Eggs
Pupa, openad
�

��
�_
_ ___ � �Larva 1
...,
Larva 3
Larva 2

Figure 14.50. Life cycle of Musca domestica (Graphics: IPZ, S. Ehrat).

Genus Musca plant origin, silage, or on the floating layer of cow or pig ro
-0
manure. Further development requires high humidity 0
a.
Musca domestica (common housefly) (r.h. >90%)and appropriate temperatures(>12 to 35 °C). 0
During the warm season, the development time of a ..c
t
Black-grey, medium-sized fly with four black stripes on generation (egg - adult) is 2-3 weeks, but it can be <(
thorax and dark middle stripe on abdomen, wings spread shortened to one week at higher temperatures (33 °C)
when resting (► Figure 14.51a), mouthparts licking­ or extended to 4 weeks at low temperatures (16 °C).
sucking(► Figure 14.49). Female flies lay 100-150 eggs A female lays 500-2,000 eggs during its lifetime; 6-9
at intervals of several days onto the surface of a variety of generations can develop per year. In warm summers,
breeding substrates such as dung of cattle, pigs, horses, there are often 'explosions' of fly populations (up to
poultry and other domestic animals (but usually not 15,000 M. domestica larvae were counted in 1 kg of
human faeces), manure, compost and garbage heaps, pig manure). M. domestica adults are active during the
decaying left-over feed in stables, food of animal or day and at temperatures above 14-18 °C, the optimum

a C

Figure 14.51. Muscidae: (a) Musca domestica � (length 7 mm); (b) Fannia canicularis (length 5 mm); (c) Stomoxys calcitrans
(length 7 mm) (Source: B. Greenberg and Princeton University Press).
 Part Ill. Parasites and parasitoses: metazoa
temperature being 32 °C. Its activity radius is small
(500-800 m), but flights or passive transport by wind
over larger distances are possible. Adults survive under
favourable conditions for 1-2 months. M. domestica
overwinters primarily in the larval stage, rarely as adult.
Within rooms, adults prefer certain rest areas, which can
often be recognised by the faecal traces left by the flies.
Genus Fannia
Fannia canicularis (lesser house fly)
This species (► Figure 14.51b) is slightly smaller
than the housefly and differs in its morphological
characteristics and flight behaviour(striking zigzag
flight). It is mostly found in pig and chicken houses,
but also in cattle barns and homes. Populations reach
highest densities in spring and early summer. Breeding
substrates are various organic materials such as faeces
of animals and humans, decaying plants and animal
carcasses. Larvae are covered with conspicuous long
appendages.
Genus Stomoxys
Stomoxys calcitrans (stable fly)
Similar in habitus to M. domestica, but with projecting
biting mouthparts(proboscis); wings spread in a wide
angle at rest(► Figure 14.Slc). After multiple blood
meals, females search for suitable breeding places
outdoors or in stables and lay batches of 60-100 eggs(a
total of up to 800 eggs) into organic material, such as
horse and cattle droppings, manure, silage, rotting left­
over feed, etc. Conditions for pupation are favourable
in dark areas at high temperatures(around 27 °C).
Overall development takes about 3-7 weeks, and several
generations develop per year. Prom their breeding sites,
the flies actively invade buildings or they are passively
carried by animals into stables. Highest abundances are
recorded in early and late summer. Under favourable
conditions (e.g. insufficient removal of excrements,
high temperatures), explosive growth can occur, so that
up to 300 stable flies can be found per m 2 of stable
walls. S. ca/citrans is diurnal, its radius is only 40-150
m, but stable flies can follow their host animals over
(l)
C long distances. Grazing animals can be infested by S.
·c3
'6 calcitrans near farms, and usually only small numbers,
�
(l)
if any, of stable flies occur on more distant pastures.
c
co
Just a few hours after hatching, the adults(males and
females) are ready for biting. Preferred blood donors
C
·.:: are cattle and horses, but also sheep, pigs, other animals
(l)
j and humans. Predilection sites on the animal bodies are
-� limbs, lower body regions, but also parts of the back.
>,
CJ)
Stable flies sometimes take blood meals twice their own
0
0
weight. ln very warm weather, they take 2 blood meals
·u5 daily, in autumn at multi-day intervals. Larvae and pupae
co overwinter in frost-free niches.
co
a..
Genus Ophyra
Ophyra aenescens (garbage fly)
This fly species was probably introduced from America
and now belongs to the fly fauna of landftlls and animal
stables in Europe. It is used in the biological control of
stable flies(see below).
Adverse effects and vector role. House and stable
flies can greatly annoy their host animals and cause
reduction in performance. As a threshold of nuisance,
20 flies per animal were determined. In extreme cases,
massive infestation with Stomoxys causes a reduction in
feed intake and milk production of cows(up to 10%).
In stables and living areas, in food producing plants,
etc., some species of stable and house flies constitute a
hygiene problem, because they can mechanically spread
pathogens(viruses, bacteria, protozoa) that adhere to
their exoskeleton. The flies can also ingest pathogen­
containing feed and excrete the pathogens unaltered
by regurgitation or defecation, e.g. Cryptosporidium
oocysts. According to studies in Germany, flies (Musca,
Fannia, Stomoxys, Lucilia and others) from animal stables
were carriers of different species of bacteria(including
Campylobacter jejuni, Esch erichia coli [EHEC and
EPEC], Staphylococcus aureus), fungi(e.g. Aspergillus
and Candida species) and parasites(e.g. Ascaris eggs).
The pathogens were on the exoskeleton or in the gut.
Stomoxys species can act as vectors of trypanosomes
as already outlined in the tabanid chapter. House and
stable flies are also intermediate hosts for helminths(M.
domestica for Habronema muscae, Draschia megastoma,
Rail lietina tetragona, Choanotaenia infundibulum, S.
calcitrans for Habronema majus). Different species of
the families Muscidae and Fanniidae are facultatively
causing myiasis(► Table 14.16, p. 485).
Control. Control of stable and house flies requires an
integrated approach, in which several measures must
be combined and carefully coordinated under expert
guidance. Principally, physical, chemical and biological
methods are available. Particularly important are
technological and hygiene measures. Chemical agents
should be used sparingly and selectively. A significant
problem is the widespread insecticide resistance of stable
and house flies(see below). Control measures should be
launched in spring if possible, in order to affect the first
generation of flies and to impair population build-up.
• Physical processes. Technological and hygienic
measures:(a) installation of stable floors and manure
removal systems that offer as few niches for the
development of fly larvae as possible;(b) keep stables
dry, compress deep litter well, provide good stable
climate;(c) regular removal of droppings in buildings
and environment, thorough cleaning of stables, mangers,
calffeeders etc.;(d) prevent invasion offlies into stables

and homes by fly screens on windows and doors; (e)
stack manure well to achieve temperatures that are lethal
to larvae(>42 °C), repack upper layers(about 10 cm) of
the dung pile where fly larvae develop, destroy floating
layer on slurry by stirring.
Sticky flypaper. To control adult flies in stables, plastic
cords coated with glue are stretched under the ceiling
throughout the stable, or sticky tapes are spanned at
appropriate sites. These are particularly effective when
the glue surfaces contain both an attractant and an
insecticide. Caution: swallows may stick to large sticky
tapes, so keep them small and in locations that do not
endanger these birds.
Electric traps combine the visual attraction of flies by
UV light with death by electric contact. These devices
are not very effective in case of large fly populations,
but can be useful in rooms with low fly abundance, e.g.
anterooms of milk parlours.
• Biological control. The manure fly (Ophyra
11e11escens), which is widespread in the New World and in
other areas(►Table 14.14), was established in the mid-
1960s in Europe, mainly in landfills and in pig fattening
units. This fly species was first used in East Germany in
a state-approved procedure for the biological control of
stable flies. 0. aenescens develops in the same breeding
sites as stable flies(especially M. domestica) and can be
established in stables with slatted floors and slurry pit.
Their larvae are predators of stable fly larvae and they
control their own population through cannibalism.
An Ophyra larva can destroy up to 20 Musca larvae.
The nocturnal manure fly generally thrives in manure
pits and underfloor areas and does not usually annoy
animals or humans. For the establishment of manure
flies, several releases at intervals of 2 weeks are required.
After previous applications of insecticides or larvicides,
waiting times are to be observed. For biological control,
parasitic wasps (Nasonia vitripennis, Muscidifurax
zaraptor, M. raptor, Spalangia spp.) are also used, which
develop in larvae and pupae of the stable fly in litter
(e.g. calf stables) and in dry solid manure (e.g. poultry
droppings). In both cases, additional measures are
recommended in case of existing high fly abundances
(e.g. fly bait, see below). The above-mentioned species
of insects are used in various European countries and
are commercially available (e.g. MuscaMorte• manure
flies and parasitic wasps). Swallows should be offered
very favourable breeding and living conditions as they
consume large quantities of flies.
• Chemical measures. Chemical control of fly
larvae is done with larvicides which are spread, sprayed
or poured, especially in barns of calves and young
livestock(► p. 557). Most commercial larvicides contain
as active ingredients insect growth regulators, such as
cyromazine, diflubenzuron(= dimilin), hexaflumuron
and methoprene. These agents interfere with chitin
14. Phylum Arthropoda (arthropods)
synthesis and the moulting processes of larvae, but do
not harm adults or beneficial insects and are innoucuous
for warm-blooded animals. Their spectrum also covers
larvae of insecticide-resistant flies, but resistance can
also develop against growth regulators. In poultry flocks,
cyromazine (e.g. Larvadex") is used as an additive to
feed, which inhibits the development of fly larvae after
excretion in faeces. -
co
'-
<D
()_
cS
Insecticides ( organophosphates) or toxins of Bacillus
tlturingiensis are rarely used as larvicides.
For the control of adult flies in stables, insecticides
of different groups of active substances are available
(pyrethrins, pyrethroids, organophosphates, carbamates,
thiamethoxam, splnosad)(► p. 557). These compounds
are used as sprays and in paints as well as in other
formulations. Also well proven efficiencies have fly
papers that contain contact insecticides and attractants,
or baits(granulates, blocks) in which feeding poisons and
attractants are combined. They allow targeted, selective
fly control. Many factors arc to be considered when
applying these measures, such as type of application,
fish and bee toxicity of the active substances, possibly
legally required waiting periods for milk and meat, and
measures for the protection of people, e.g. when spraying
insecticides.
Resistances. A low or decreasing effect of insecticides
or larvicides may be due to faulty application or co
resistance of the fly populations. Such resistances are -0
0
known in Musca domestica to all major insecticide
groups(pyrethrum and pyrethroids, organophosphates,
e
()_
.c
t
carbamates) and to growth regulators. Alarming data <(
from a study performed in 2008 in Germany revealed
that 87% of 60 M. domestica populations from dairy
farms were fully and 10% partially resistant to the
pyrethroid deltamethrin.
Pasture flies
Life cycle and epidemiology. Grazing animals
are parasitised in Europe by up to 20 species of the
family Muscidae. Of these, the obligate haematophagous
biting flies of the genus Haematobia and non-biting
or facultatively haematophagous species of the genera
Musca and Hydrotaea have the greatest practical
significance(► Table 14.14).
Genus Musca
Musca autumna/is (face fly)
This fly species is very similar in habitus to the housefly.
Females lay their eggs in fresh cattle droppings in which
larval development takes place; pupation occurs i n
the soil. The entire development only takes about 10
days under summer conditions, and 4-5 generations
develop per year. Preferred hosts of M. autumnalis are
 Part Ill. Parasites and parasitoses: metazoa

cattle on which they mainly settle on the head(eyelids,

nostrils, muzzle), but also other parts of the body (teats,
legs) and wounds(► Figure 14.52). On horses, M.
autumnalis is also predominantly found in the head
region(eyes, nostrils, mouth opening). With small teeth
at its labellum, M. autumnalis can dab and rasp mucous
membranes and thus increase the flow of secretions.
The flies lick proteinaceous secretions as feed which
is needed by females for egg maturation. Blood drops
that reach the skin surface at biting sites of tabanids are
very sought-after and ingested by M. autumnalis and
Hydrotaea species. M. autumnalis is the most common
nuisance of grazing cattle and horses. The flight activity
period lasts under favourable conditions from mid-April
to early November, with the highest abundances In July Figure 14.52. Musca autumna/1s and other flies on the head
and August. In this period, 250-900 flies were counted of a cow (Photo: IPZ).
per head of cattle in southern Germany. M. autunmalis
can be active from early morning until the evening; at
temperatures below 12 °C and with light rain, activity is = Actinomyces pyogenes, Staphylococcus aureus, etc.) has
reduced, but not completely abandoned. M. autumnalis been confirmed experimentally; however, transmission
is an intermediate host of Thelazia(eye worms) in cattle was successful only to teats with skin lesions.
and horses, of Parafilaria bovicola of cattle and a vector
of Moraxella bovis, the main causative agent of infectious Genus Haematobia
keratoconjunctivitis in cattle.
Haematobia irritans (horn fly)
Genus Hydrotaea
This fly species is equipped with piercing-sucking
Hydrotaea spp. (sweat flies, head flies) mouthparts and is similar to Stomoxys calcitrans but
smaller in size and with long maxillary palps ( ► Figure
Hydrotaea species are Musca-like flies that are usually 14.53a). A noticeable feature of the flies is that they sit
smaller at only 3-4 mm in length, and they are close together and with their heads pointing downwards
conspicuous by their great mobility on animals. On on the hosts, the wings spread in a delta-shaped manner
cattle, 10-12 species were found in Germany, with Hy. (► Figure 14.54b). In Europe and elsewhere, H. irritans
irritans and Hy. albipuncta being the most common is an important parasite that is highly adapted to cattle
representatives. Oviposition of Hydrotaea species and, only occasionally and in small numbers, also infests
occurs in different breeding media; Hy. irritans prefers horses. Females lay their eggs in fresh cattle droppings
moist soil on pastures, especially along the skirts of in which larvae develop. Pupation also takes place in
forests, Hy. albipuncta in contrast cattle droppings. the faeces or in the soil below the cow dung; the pupae
The larvae of Hydrotaca species arc prcdal'ors of larvae overwinter. At low temperatures the entire development
of other species of flies or their own species. After in Europe takes about 3 weeks; 3-5 generations develop
overwintering of the larvae of the fall generation, flrst per year. During the flight season from May to late
adults hatch, depending on the species, in late May or October, highest abundances are to be expected f rom
June of the following year. Hy. irritans usually develops
one generation per year, Hy. a/bipuncta 3 generations.
The development of a generation of Hy. albipuncta
can be completed in just over I month under summer
Q)
C: temperatures. The activity period of Hydrotaea species
·13
'6 extends from May to October, with highest abundances
�
Q)
in August (Hy. irritans) or with several peaks over the
2:' year (Hy. albipuncta). Hydrotaea species, similar to M.
co autumnalis, live off secretions with low protein contents
C:
·;:::
Q) (tears, sweat, saliva, wound secretion) and facultatively
� blood. Therefore, they often aggregate in large numbers
C: around blood drops at biting sites of tabanids or small
>,
Ol
skin wounds. On cattle, Hy. irrilans can most commonly
0 be found on head, abdomen and teats; on horses and
0
·1n sheep on the head(sheep head fly). The long-standing Figure 14.53. Horn flies: (a) Haematobia irritans (length 3-5
co hypothesis that Hy. irritans may transmit causative agents mm); (b) Haematobia stimulans (length 5-7 mm) (Photo: A.
co
0.. of summer mastitis of cattle(Corynebacterium pyogenes Liebisch).

Figure 14.54. Haematobia irritans: (a) Crowd of flies on grazing cattle (arrows) (Photo: IPZ, J. Eckert); (b) Close-up of H. irritans
in typical sitting posture with head down (Photo: A. Lleblsch).
July to end of August. The adults live almost constantly
on cattle and can be found especially at the back and
at the horn base ( ► Figure 14.54a). Gravid females
only very briefly leave the host to lay their eggs within
about I min in freshly deposited cattle droppings. In
case of strong defence reactions of the host or other
disturbances, the flies briefly become air-borne and then
re-settle on the animal. In summer, high population
densities are reached in Europe with infestation numbers
of 200-500 flies per host animal. Males and females
are haematophagous and take blood every day about
20 to 40 times. In heavy infestations, the injection of
saliva antigens stimulates the formation of circulating
antibodies in highly variable concentrations. According
to data from the USA, the painful bites are a significant
nuisance for cattle, and reduction of milk and weight
was observed resulting from infestation rates higher than
SO flies per animal. Calves or suckler cows in which H.
irritans was controlled by insecticides had higher weight
gains than calves from untreated cows. A closely related
subspecies, H. irritans exigua, mainly affects buffalo and
cattle in subtropical and tropical areas. This subspecies
can cause milk losses of about 15 litres, assuming a
prevalence of 300 flies per animal in 20 days. H. irritans
is a mechanical vector of Anaplasma marginale and an
intermediate host for Stephanofilaria species of cattle, H.
atripalpis (not autochthonous in Europe) for Parafilaria
multipapillosa of equids.
Haematobia stimu/ans (syn. Haematobosca
stimulans; horn flies)
This fly species ( ► Figure 14.53b) is larger than H.
irritans (► Figure 14.53a). On cattle, H. stimulans sit
with the head upwards especially on the trunk. Horses
nearby are also affected. Development occurs in cattle
droppings; there are up to 4 generations per year, and
heavy infestations with about 100 flies per animal occur
only in late summer and autumn. Adults stay only during
the day on the hosts and suck blood; they spend the
night at resting places in the vegetation. Little is known
about adverse effects.
14. Phylum Arthropoda (arthropods)
Adverse effects and vector role. /-/. irritans
and other biting flies cause small tissue lesions and
haemorrhages in the skin with infiltration of eosinophilic
and mononuclear cells and oedema formation in
the dermis. It has been shown that these lesions are
responsible for a loss of quality in leather. The annoyance
caused by these flies and their vector roles have already
been mentioned above.
Diagnosis. Under practical conditions, some fly taxa
can be recognised visually because of their habitus and
the seating positions on the animal body and can thus
be distinguished from tabanids, namely M. autumnalis,
horn flies and Hydrotaea spp. The exact identification C'O
requires special knowledge. -0
0
e
Cl.
Control. A control of pasture flies is to be considered .c
t
if the nuisance for animals has reached a significant <x::
degree (animal protection) and if adverse effects are
to be expected. Fly control in cattle and horses is
still largely based on the use of insecticides. Control
measures are often omitted or neglected, so that flies
on grazing animals can be a significant nuisance. For
control options in cattle ► p. 584, for horses ► p. 596.
Family Glossinidae (tsetse flies)
Glossa(G): Tongue. Refers to the wings which are kept at
rest in a tongue-like shape over the abdomen; according
to another interpretation refers to the projecting
mouthparts. Tsetse (Bantu language): denomination of
the flies in imitation of their buzzing sound.
Morphology and occurrence. Glossinids exclusively
occur in tropical Africa south of the Sahara(latitudes 14
north to 20 south), and they are of particular importance
for the continent as vectors of the agents ( Trypanosoma
spp.) causing nagana in domestic and wild animals as
well as sleeping sickness in humans( ► p. 62). Glossinids
are usually brownish-dark, 6-14 mm long biting flies,
whose piercing apparatus is directed forward and
extends far beyond the head. The arista of the antennas
is very plumose. In resting position, the tongue-shaped
 Part Ill. Parasites and parasitoses: metazoa
folding of the wings ( ► Figure 14.55.) is characteristic
of tsetse flies and distinguishes them from other biting
flies of the genera Stomoxys and Haematobia (wings
spread). The family contains only the genus Glossina
with 4 subgenera and >20 species. Most of them can be
assigned to three main groups: the Glossina morsitans
group in savanna habitats, the Glossina palpalis group in
wetlands along rivers and lakes, and the Glossina fusca
group in rainforests. The G. morsitans group is most
important for transmission of nagana in cattle.
Life cycle and epidemiology. A special feature of
glossinids is that in females one larva (L3) develops at
a time; this is fed a milk-like secretion and deposited in
sheltered places when ready to pupate. Within hours,
pupation takes place in the soil ( ► Figure 14.55). Larval
development takes about 10 days, the pupal period about
30 days at 25 °C. Adults have a life span of 2-5 months,
a female produces in this period only 8-12 larvae.
Males and females are exclusively haematophagous.
They harbour symbiotic microorganisms, namely
Wigglesworthiaglossinidia (in specialised epithelia of the
midgut) and Soda/isglossinidius (in epithelia of midgut
and in various organs), which play a role in the supply
, .. of vitamins of the B complex. S. glossinidius is believed
to promote the development of trypanosomes in the
fly. Both species of bacteria are transferred to the larvae
with the milky secretions. Another symbiont with still
unclear significance is Wolbachia pipientis, which is
passed transovarially to the next generation.
Mammals, humans and reptiles, and occasionally birds,
serve as hosts of Glossinidae. Many species prefer one
or several host species, but basically have a broad host
range. Host finding occurs visually at greater distances,
and olfactorily at shorter distances.
Control. Glossinids are controlled by spraying low
quantities of insecticides (ultralow volume) and catching
in insecticide-treated traps to which the flies are attracted
by colour and olfactory stimuli. Urine of cattle, among
others, is a proven attractant. Furthermore, screens are
quite effective. They consist of large, rectangular cloths
(2x l m), which can be divided into a central black area
b caught at different rural locations in Germany. J Med Entomol
C (Dlptera: Muscidae): effects of direct exposure and
Figure 14.55. G/ossina pa/pa/is: (a) adult (length 11-13 mm);
(b) pupa (5-6 mm) (Photo: IPZ, J. Eckert).
and 2 blue side strips, impregnated with an insecticide
(e.g. deltamethrin), hung in a wooden frame and placed
in sufficient numbers in an area. The visually attracted
tsetse flies are killed upon contact with the insecticide.
The application of 1 m high, pyrethroid-impregnated
nets at fenced enclosures of cattle and pigs not only
protected the animals from tsetse flies and reduced the
risk of Trypanosoma infections, but also reduced the
tsetse flies population in the near environment ( ► p.
596). Treatment of cattle with pyrethroids in pour-on
applications against ectoparasites also kills glossinids,
but an effective control can be achieved with this method
only under limited conditions and with very considerable
effort. Regionally, the 'Sterile Insect Technique' is used
for control, and was successful in eliminating glossinids
on the island of Zanzibar (more details on this method
► p. 488). Often, several control measures are used
in coordinated integrated programmes. Humans can
protect themselves from the bites of the diurnal (!)
tsetse flies as follows: cover skin widely with clothes,
treat exposed areas with repellent, spray the interior of
vehicles with insecticides and inspect for tsetse flies.
Selected references
Baldacchino F, Desquesnes M, Mihok S, Foil LD, Duvallet
G, Jittapalapong S (2014) Tabanids: neglected subjects
of research, but important vectors of disease agents! lnfec
Genet Evol 28: 596-615.
Blaho M, Egri A, Szaz D, Kriska G, Akesson S, Horvath G
(2013) Stripes disrupt odour attractiveness to biting horseflies:
battle between ammonia, CO2 , and colour pattern for
dominance in the sensory systems of host-seeking tabanids.
Physlol Behav 119: 168-17 4.
Bauer B, Holzgrefe B, Mahama Cl, Baumann MPO, Mehlitz
D, Clausen PH (2011) Managing tsetse transmitted
trypanosomosls by Insecticide treated nets - an affordable
and sustainable method for resource poor pig farmers in
Ghana. PloS Negl Trop Dis 5: 1-9 (e1343).
DeRouen SM, MIiier JE, Foll LD, Gentry GT (2009) Control of
horn flies (Haematobla Irr/tans) and gastrointestinal parasites
and its relation with cow-calf performance . Vet Parasitol
162: 320-326.
Forster M, Klimpel S, Sievert K (2009) The house fly (Musca
domestica) as potential vector of metazoan parasites caught
in a pig-pen in Germany. Vet Parasitol 160: 163-167.
Forster M, Sievert K, Messler S, Klimpel S, Pfeffer K (2009)
Comprehensive study on the occurrence and distribution
of pathogenic microorganisms carried by synanthropic flies
46: 1164-1166.
Geden CJ, Devine GJ (2012) Pyriproxyfen and house flies
autodissemination to larval habitats. J Med Entomol 49:
606-613.

Guglielmone AA, Gimeno E, Idiart J, Fisher WF, Volpogni
MM, Quaino 0, Anziani OS, Flores SG, Warnke O (1999)
Skin lesions and cattle hide damage from Haematobia irritans
infestations. Med Vet Entomol 13: 324-329.
Krafsur ES, Moon RD (1997) Bionomics of the face fly, Musca
autumnalis. Annu Rev Entomol 42: 503 -523.
Llenard E, Salem A, Grisez C, Prevot F, Bergeaud JP,
Franc M, Gottstein B, Alzleu JP, Lagalisse Y, Jacquiet
P (2011) A longitudinal study of Besnoitia besnoiti infections
and seasonal abundance of Stomoxys calcitrans in a dairy
cattle farm of southwest France. Vet Parasitol 177: 20-27.
Malik A, Singh N, Satya S (2007) House fly (Musca domestica):
a review of control strategies for a challenging pest. J Environ
Sci Health B 42: 453-469.
Skovgard H, Nachman G (2012) Population dynamics of
stable flies Stomoxys ca/cltrans (Dlptera: Muscidae) at an
organic dairy farm In Denmark based on mark-recapture
with destructive sub-sampling. Environ Entomol 41: 20-29.
Taylor DB, Moon RD, Mark DR (2012) Economic Impact of
stable flies (Diptera: Muscidae) on dairy and beef cattle
production. J Med Entomol 49: 198-209.
Families Calliphoridae (blow flies) and
Sarcophagidae (flesh flies)
Disease: Myiasis (fly strike).
Calliphoridae: kalos(G): beautiful; phorein (G): to wear.
Refers to the mostly beautiful, shiny metallic colours
of the adults.
Sarcophagidae: sarx (G): meat; phagein (G): to feed, to
eat. Refers to the carnivorous larvae.
Myiasis: myia (G): fly.
Summary
The larvae of several fly species of the famllles (a)
Muscidae, Calliphoridae, Sarcophagldae and(b) Oestrldae
are causative agents of myiases in sheep, other domestic
animals, wildlife and humans. The following chapter deals
with myiases that are caused by flies of group a( ► Table
14.15). Of these, especially blowfly strike in sheep and
rabbits is significant in Europe. In addition, larvae of some
species can infest food and feed as storage pests and
render them unusable. Myiases caused by Oestridae are
discussed in separate chapters(► p. 485 ff).
Blowfly strike in sheep
Species. Lucilia sericata (mainly Central Europe),
L. caesar and L illustris (mainly northern Europe)
(Calliphoridae), Woh/fahrtia magnifica (mainly eastern
and southern Europe)(Sarcophagidae).
• Life cycle. Females of L sericata lay eggs in
breeding media (decaying plants, food, carcasses,
etc.), facultatively also on intact skin or in wounds.
T occurs in Europe, especially in sheep.
14. Phylum Arthropoda (arthropods)
Development of three larval stages (L 1-L3), L3 fall off
the artimal body and pupate in 1he soil; 3-4 generations
per year. In contrast to L. serlcata, W. magnifies is an
obligate ectoparaslte. Its females lay L 1 onto the hosts
where they develop to L3, and fall to the ground where
they pupate. (ti
• Epidemiology, occurrence. Mylasis caused by L
CJ
0.
serlcsta occurs in sheep in north-western and Central c5
Europe from spring to autumn. In the UK and NL, each
year around 80% and 50% of flocks of sheep and
approximately 1-3% of the animals are affected. W.
magnlflea cauHs myiasis In southern Europe In sheep
with herd prevalences up to >80%.
• Pathogtne1l1, cllnlcal 1lgn1. Larvae of L. seflcata feed
on superficial skin components, lymph exudates and
necrotic tissue in wounds. At affected areas 1here is
itch, wool loss, exudatlve dermatitis, extensive wounds,
tissue loss, necrosis, genertjJ symptoms, which can
lead to death. Larvae of W. magnifies penetrate the
skin, mucous membranes and wounds and from there
into deeper tissue layers; they also attack living tissue.
• Diagnosis. Identification of larvae detected by
adspectlon.
• Therapy and control. Wound treatment, fluid replace­
ment and other measures in severely diseased animals.
Treatment with insecticides(dips, spraying, parenteraQ.
In endemic areas, prophylactic use of insect growth
regulators.
More mylasls fonns in other animal species ► Table
14.16 and text. co
-0
0
Q.
The importance of fly species of this family is based .c
t::
on the fact that their maggots infest feed and food, �
rendering them unusable, or that they cause diseases
in animals and humans, known as myiasis. Adults play
a role as mechanical vectors of different pathogens,
especially the Calliphoridae. Larvae of Lucilia species
play a useful function in medicine in the treatment of
slow-healing wounds (see below).
Adults of Calliphoridae and Sarcophagidae are medium­
sized flies with licking-sucking mouthparts that resemble
the Muscidae in habitus. Calliphoridae are mostly
I:
metallic-shiny and bluish, violet, bronze or greenish; I
Sarcophagidae in contrast are grey-black(► Figure
I
(I)
14.56). A selection of species is given in ► Table 14.15.
·u
C I
'6
I
Traumatic myiasis I II
(I)
I
Myiasis is a collective term for the infestation of a co
�
C
·;;:: 11I
living organism with Brachycera larvae (maggots)
(after an extended definition with larvae of Diptera). I 11
Aetiologically, also species of other families in addition -�
to Calliphoridae and Sarcophagidae are to be taken into
account(► Table 14.16). An important form of myiasis 0
0
is traumatic myiasis of pet animals that causes disease
particularly in tropical and subtropical areas, but also
·en
 Part Ill. Parasites and parasitoses: metazoa

Genus Lucilia

Disease: Luciliosis (blowfly strike) of sheep

Species. Causative agents are larvae of various Lucilia

a b
species. The most important species in north-western
and Central Europe is L. sericata; further north occur L.
caesar and L. illustris. L. sericata has been spread from
the Palaearctic to other areas, e.g. Australia and New
Zealand. L. cuprina is endemic in many tropical and
subtropical areas and causes significant losses mainly
in sheep farming areas, e.g. Africa, Australia and New
Zealand. L. cuprina was detected for the first time in
northern Spain in 1994.

Occurrence. In endemic areas of UK, L. sericata was

C d
Figure 14.56. Blow and flesh flies: (a) Luci/la sericata 9
(length 8 mm); (b) Ca/liphora vicinia 9 (length 11 mm); (c)
Chrysomya megacephala 9 (length 1 O mm); (d) Sarcophaga
haemorrhoids/is 9 (length11 mm) (Source: B. Greenberg and
Princeton University Press).
the only pathogen species in 80-100% of myiasis cases
in sheep, other species (e.g. L. caesar, Calliphora species)
were rare. In the period 2003/2004, the proportion of
farms with at least one myiasis case in sheep varied
from 60% in Scotland to 81 % in South-west England.
On average 1.4 to 2.8% of sheep fell ill (at least 420,000
animals of the total 30 million sheep). In the Netherlands,
myiasis occurred in 52% of 349 sheep holdings, and 2.9%
of sheep were infested in 1999. No exact infestation rates

Table 14.15. Species (selection) of the families Calliphoridae and Sarcophagidae.

FamlllN,epeclN Other designation, occurrence

L: Length of Imago•

Family: Calllphortdae Blowflies

Luci/la sertcats 1
L: 5·10mm
Lucilla cuprlna 1
L: 5-14 mm
Cslliphors vlclna 1
L:5-12mm
CBl/iphors vomltorls1
L: 10-14 mm
Chrysomys Blblceps
L: 5-10mm
Chrysomys bezzians
temperate climate zones of the northern hemisphere (Europe, USA, etc.), introduced to
Australia, South Afrl�South America _ ___
mainly tropical and subtropical regions: Africa, Middle East, India, Australia, New Zealand,
also northern Spain
cosmopolitan
HolarQtle and othor areas
tropic!s, subtl'QPic;& (not Australia)
----------
screwworm of the Old Wood; tropics and subtropics of Africa ano Asia
____
_....,...

(I)
-
L: 5-12 mm-
Cordytobla anthropophaga Tumbu fly; Sub Sahar
- an Africa
·u
C
L:�to12�m
'6
(I) Cochliomyla hominivorax Syn: Callitroga americana. screwworm of the New World; Central America, over Caribbean
�
-
L: 5-Bmm -- to northem �. Uruguay, A!_gentina
___ _ __ -------1
cu Family: Sarcoph&'Jldae Flesh fllea
C
·c: Sarcophaga carnsria 1 large or grey flesh fly; Holarctic and some other areas
--- ------ --
L:10-14 mm

.s SarcophBgs haamoohoidalis 1 cosmopolitan

>,
O')
0
L:10-15mm
WohlfahrtiB magnilica 1
------------------=....----------,
Central and eastern Europe, Mediterranean, Asia Minor
0 L: 8-14 mm
·u;
ro 1 These species occur in Europe.
ro
0..
 14. Phylum Arthropoda (arthropods)

Table 14.16. Important forms of myiasis in animals (selection).

'fype of mylasis Infestation/lesions Causative agents (selection): Affected animals

f: facuttatlve parasitic larvae; o:
obligate parasitic larvae

Skin myiases
Traumatic m. infestation of dermal wounds by Lucilia sericata 1 (0, L. caesar1 (Q. L. lsheep,callle, r'

larvae illustris 1 (0, L. cuprina 1 (Q, Calliphora horse, dog, rabbit,

I
r

. vomitoria 1 (0, C. vicina 1 (Q. Chrysomya poultry, game

C
spp. • IQ, Musca oomesuca 1 IQ, Fannie mammals
canicularis 1 (0, Colchliomyfa homlnlvorax
- (o), Wohlfahrt/a magnifies 1 (o)
Creeping m.
Furuncular m.
--
tunnel formation in skin by larvae
bump formation in skin by larvae
- Q_asterophllus spp.1 (o)
1
Hypoderma bovis (o), H. 1/neatum (o)1
1 equids
cattle
r cervids .
Hypoderma diana 1 (o)
I dog, cat
�--
Cordylob/(J enthropophaga (o)
Sanguinivorous m.
Gastrointestinal m.
larvae suck blood on skin -
development of larvae In stomach
Protocalliphora spp. 1 (o)
Gasterophllus spp. 1 (o)
wild birds
I equids

Nasopharyngeal m.
or Intestine
development of larvae In
- I
I
Oestrus ov/s 1 (o), Cephenemyla spp. 1 (o) , sheep, goal,
-

Ocular, auricular, rectal,

nasopharyngeal cavities --
eggs or larvae deposited in eye, ear several species of Calllphorldae,
, cervlds
I domestic and wild
urogenital m. canal, rectum, etc. Sarcoe_hagidae, M�cldae animal species
Pseudomyiasis passage of larvae through the several species of Calllphoridae, domestic and wild
digestive tract without clinical Sarcophagidae, Muscldae animal species
relevance
1 These species or genera occur in Europe.

of Lucilia blowfly strike in sheep are available for other
European countries.
Development and epidemiology. In late spring,
females of L. sericata are active at temperatures above
9 °C, especially on sunny days. During its lifespan of
around one week, a female can deposit batches of ~200
eggs in the wool fleece of sheep every 2-3 days. From the
eggs, three larval stages develop, the last of which falls off
the host and pupates in soil. The development time from
egg to adult stage is 4-6 weeks; 3-4 generations develop
per year. In the cold season, larval stages in the soil enter
into diapause and overwinter. The occurrence of myiasis
cases depends on the activity of the flies and many other
factors, including temperature, humidity, breed of sheep,
flock size, condition of fleece and skin( e.g. pollution by
faeces or soil, skin lesions) and time of sheep shearing.
In the UK, most myiasis cases are observed in unshorn
ewes in spring and early summer; the number of cases
declines after shearing. The initially short-woolled lambs
are only affected later in the summer after weaning,
when longer wool and pollution of the fleece by faeces
originating from parasite-induced diarrhoea favours
oviposition of the flies(see also pathogenesis).
Pathogenesis and clinical signs. Gravid
Lucilia females are attracted by skin perspiration
of sheep. Factors that play a role include elevated
CO 2 concentration, ammonia, sulphur compounds
(mercaptans, alkyl sulphides), volatile organic acids,
and indole compounds. The latter three groups of
substances are produced by bacteria on the skin or in
wounds, e.g. Pseudomonas aeruginosa, Bacillus subtilis cu
and Proteus mirabilis. Females lay eggs in parts of -0
0
the skin in which sufficiently high moisture for the Q.
0
subsequent larval development prevails, e.g. areas of .c
t::
the fleece that are wrinkled or soiled with faeces or <(
urine, or into body openings. Promotive is bacterial
dermatitis, due to proliferation of Pseudomonas spp.
which can occur after prolonged wetting of the fleece and
which causes superficial inflammation and exudation
of plasma proteins.
Larvae can live on the skin over an extended period of
time without causing major changes, but they can also
penetrate the skin through small wounds. Predilection
sites are the hind parts of sheep, back and flanks. Lucilia
larvae that hatch from the eggs excrete enzymes that
degrade skin epithelial cells and proteins, promote
exudate production, cause inflammation and trigger as
antigens humoral and cellular immunological reactions.
Larvae feed on compounds of the epidermis, skin and
wound exudate as well as necrotic tissue.
Sheep infested with fly larvae are restless; they try to
bite into the affected area or beat it. Feed intake may
be impaired. The affected skin area is itchy and there
is hair loss, the fleece is wet and usually brownish in
colour, and wounds become visible(► Figure 14.57).
Fly larvae are present in varying numbers at the lesions
and under the detached skin. Consequences of initially
small changes can be: exudative dermatitis, necrosis
 Part Ill. Parasites and parasitoses: metazoa

Resistance and immunology. Various sheep breeds

have genetically fixed anatomical characteristics that
favour the emergence of myiasis, e.g. highly folded skin
parts in Merino breeds, or large and easily vulnerable
tails in fat-tailed sheep. On the other hand, certain
breeds are naturally resistant to infestation with maggots.
Efforts are therefore made to select sheep breeds with
increased resistance to myiasis. Calliphoridae induce
at most a weak immunity. The susceptibility of sheep
against L. cuprina maggots gradually decreases only after
repeated infestations, antibody titres in serum rise only
slowly over many infestations and are highly variable.
Attempts to develop a vaccine against L. cuprina have
shown that sheep develop antibodies after experimental
immunisation with an antigen from the peritrophic
membrane of larvae (peritrophin 95, a so-called hidden
antigen, ► p. 569), and the antibodies strongly inhibited
the development of larvae in cultures (about 84%). A
vaccine is not yet available.

Diagnosis. For the detection of myiasis, an accurate

Figure 14.57. Myiasis of sheep: lesions in the caudal area
(Photo: A. Llebisch).
adspection of the skin (after shearing the animals
or only affected areas) and of the body openings is
required. Larvae are visually identifiable and can be
sent, stored in 70% ethanol, to an institute for species
identification. They can be identified based on structures
of the cephalopharyngeal skeleton and the posterior
peritremes (► Figure 14.58). Also, molecular biological
methods are used for identification.

Therapy and control. In case of existing wound

of skin, secondary infections with bacteria and fluid
loss. Ammonia, formed by Lucilia larvae, plays an
important role. lt can be detected in the venous blood
of affected skin areas in high concentrations, and causes
intoxication. In cases ofsevere myiasis that were detected
too late, mortality rates over I 0% were observed In
Central Europe.
myiasis, individual animals or herds of sheep are treated
with insecticides. A dip treatment (e.g. phoxim 0.05%)
has the advantage that the active ingredient emulsion
penetrates the fleece and reaches all parts of the body.
In spray treatments (e.g. phoxim 0.05%), it should be
ensured that the drug is sprayed under high pressure and
as evenly as possible into the fleece. As an alternative,
parenteral treatment with doramectin (0.2-0.3 mg/kg
b.w, i.m.) can be considered, which is effective against

Cephalopharyngeal skeleton

Q)

·o
C

'6
Q)
�
c
co
Musca domestica Lucilia sericata
C
·c
Q)

j
_£;
>,
CJ)
0
0
·enco
ci:l
a.. Figure 14.58. Characteristics of fly larvae (Graphics: IPZ, A. Seeger).

larvae of L. cuprina and gives good protection against
reinfestation for about 3 weeks. At the same time, such
a treatment is directed against other ectoparasites and
gastrointestinal nematodes. Animals with pronounced
skin lesions and systemic symptoms require further
treatment measures (including wound disinfection,
removal of necrotic skin, manual removal of larvae,
fluid replacement, and antibiotic therapy).
Of prophylactic importance is the accurate observation
of the animals as frequently as possible during the grazing
period and the immediate treatment of wounds. In areas
where cases of myiasis repeatedly occur, insect growth
regulators can be used for prophylaxis, e.g. dicyclanil
(CJik• as spray application, which grants protection
of 4 months or longer, but which is not approved in
many countries). The timing of the application of these
active agents must ensure that the main risk period is
covered and that the withdrnwal periods for meat are
taken into account. In sheep, whose milk is intended
for consumption by humans, the use of these agents is
not approved. Nevertheless, untreated dairy animals
are less affected if kept together in flocks with treated
non-lactating animals. For biological control, fly traps
are commercially available that are equipped with a
specific attractant and adhesive strips. The manufacturer
recommends placing the traps from end of April in
sufficient numbers in the vicinity of the grazing land at
appropriate sites(e.g. grazing poles) and to check them
regularly. According to data from the UK, myiasis could
be prevented most effectively if adult sheep and lambs
were treated with long-acting insecticides and fly traps
were simultaneously used.
Genus Wohlfahrtia
■ Wohlfahrtiosis of sheep and other hosts
Species and occurrence. This myiasis caused by
Wohlfahrtia magnifica occurs in southern and south­
eastern Europe (including among others HU, the
Balkans), the Mediterranean(including GR, reES)
and Asia Minor( ► Table 14.16). Sheep are mainly
affected, but other farm animals (goats, cattle, pigs,
horses, camels), dogs, free-living wild animals or those
kept in zoos, poultry and humans are also attacked by
W. magnifica. According to data from the 1990s, the
local prevalence of Wohlfahrtia infestations in sheep
was 5-39% in Hungary and 0.7 to 17% in Spain. In a
more recent study in southern Italy, prevalences around
up to 6.3 % were recorded, and the number of farms
affected increased over the years. Wohlfahrtiosis can
cause severe suffering in flocks of sheep and cause
significant economic losses.
Life cycle and epidemiology. Females of W
magnifica are viviparous and 'splash' 120-170 L1 onto
the host, especially at body openings and wounds but
also onto intact skin. The larvae immediately begin to
14. Phylum Arthropoda (arthropods)
ingest components of the skin and deeper tissue layers
and thus create a focus that attracts more females to
oviposit. The development of the next 2 larval stages
is completed in 6-7 days, pupation occurs in the soiJ.
Adults that hatch from the pupae ingest nectar of flowers,
but also liquids from meat, faeces, etc.
Pathogenesis and clinical signs. Larvae of W. 2
0.
magnifica are frequently deposited on the genitals of 0
female and male sheep which might trigger problems in
reproduction. The infection can lead to large-scale and
deep tissue changes with similar symptoms as described
for Lucilia. In dogs, lesions were observed mainly on
limbs, genitals, ears, nose and neck.
Treatment and control. Por the treatment of sheep,
the same principles apply as for Lucilia. Oft he available
active agents, doramectin and eprinomectin have good
efficacy against larvae and a prophylactic effect that
lasts about 3 weeks. A single application of an insect
growth regulator(dicyclanil) can protect sheep for 6-7
months from Wohljahrtia infestation under favourable
conditions. Since the use of the product is not permitted
in lactating sheep, it is recommended to treat only the
non-lactating animals of a flock. Even if only 15-20%
of the animals of a herd are treated, a protective effect
of 50% can be expected. Dogs were successfully treated
with moxidectin(0.4 mg/kg b.w., 2x every 10 days) and
simultaneous administration of antibiotics.
ro
Traumatic myiasis and other forms of -0
0
e
0.
myiasis in other animal species and in
humans .c
t::
<(
Traumatic myiasis also occurs in other domestic
mammals, poultry, in many species of wild animals and
in humans, caused by larvae of various species of flies
( ► Table 14.16). L. sericata myiasis occurs, according to
an extrapolation from the UK, in 8% of domestic rabbits.
Affected are neglected animals, those with diarrhoea
(caused by Eimeria infection) or malnutrition as well as
animals with abnormal grooming behaviour(caused, for
example, by mouth infections or malpositioned teeth).
Of particular interest are the forms described below.
Genus Cordylobia
■ Furuncular myiasis caused by the Tumbu fly
Infestations with larvae of the Tumbu fly( Cordylobia
anthropophaga) occur in central Africa and occasionally
as imported cases in humans and animals elsewhere.
Part Ill. Parasites and parasitoses: metazoa
Genus Cochliomyia
■ Cochliomyia wound myiasis in subtropical
and tropical areas (screwworm infestation)
This form of traumatic myiasis is discussed here mainly
as a teaching example of successful biological control.
In subtropical and tropical regions of the Americas,
Cochliomyia hominivorax (syn. Callitroga americana),
the screwworm of the New World, is the most important
causative agent of traumatic myiasis, affecting domestic
ruminants, horse, pig, dog, wild mammals, and also
humans. Chrysomya bezziana is the screwworm of the
Old World(► Table 14.16). C. hominivorax penetrates
through larger(castration, dehorning) or smaller lesions
i n the skin and causes deep, baggy wounds, usually
containing several larvae.
Because of the huge economic losses that C. hominivorax
had caused in earlier years in the USA, an original
biological control programme was started in the late
1950s. In the southern USA, C. hominivorax was mass­
reared in dedicated industrial plants, where per week
20-100 million flies were bred. The flies were sterilised by
irradiation of the pupae (y-rays) and released by aircraft
at certain time intervals and numbers per area unit. The
most significant effect of this technique called Sterile
Insect Technique (SIT) is that the females that mate with
sterile males remain infertile (females mate only once)
and thus the fly population collapses after a certain
time. C. hominivorax was originally distributed from
the central USA to southern Brazil and is now limited to
areas south of Panama thanks to the successful control
measures. Through a series of measures, including the
control of animal transport and the release of sterile
males in a buffer wne of Panama, recolonisation of areas
free of C. hominivorax has been prevented.
C. hominivorax was introduced into Libya in 1988,
representing an enormous threat to this country and
the whole of Africa. By using SIT and accompanying
measures, the elimination of the fly was successful with
an approximately I-year control campaign led by FAO.
Genus Protocalliphora and others
■ Sanguinivorous myiasis
Another form is sanguinivorous myiasis, where fly larvae
feed on blood. The larvae of Protocalliphora species
develop in bird nests and suck blood on nest birds('bird
blood flies'). In West Africa, Auchmeromya senegalensis
larvae repeatedJy take blood meals from humans and
mammals, mostly in huts or houses.
Zoonotic importance. The various forms of myiasis
are usually considered zoonoses, since the same fly
species infest vertebrates and humans(► Table 14.16).
However, a reciprocal transfer of larvae (vertebrate H
man) does not occur.
Use of fly larvae for wound treatment ('maggot
therapy'}. Since 1931 it has been known that the
application of Calliphoridae larvae can accelerate the
healing process in persistent wounds. This method, also
referred to as maggot therapy, is now quite successfully
used in medicine in cases in which standard therapies
have failed, e.g. severe gangrene in diabetics. The
treatment is carried out with larvae of L. sericata reared
in sterile cultures and considered a medicinal product.
Selected references
Abo-Shehada MN (2011) The myiases. In: Palmer SR, Lord
Soulsby, Torgerson PR, Brown DWG, eds. Oxford Textbook
of Zoonoses. 2nd ed. Oxford, UK: Oxford University Press,
pp. 817-827; ISBN 978-0-19-857002-8.
Blsdorff B, Wall R (2006) Blowfly strike prevalence in domestic
rabbits In southwest England and Wales. Vet Parasitol 141:
150-155.
Farkas R, Hall MJ, Bouzagou AK, Lhor Y, Khallaayoune
K (2009) Traumatic myiasis in dogs caused by Wohlfahrtia
magnifica and its importance in the epidemiology of
wohlfahrtiosis of livestock. Med Vet Entomol 23 (Suppl 1):
80-85.
Giangaspero A, Brianti E, Traversa D, Hall, MJR (2014) A
retrospective and geographical epidemiological survey of
traumatic myiasis in southern Italy. Med Vet Entomol 28:
391-397.
Hall MJ (1997) Traumatic myiasis of sheep in Europe: a review.
Parassitologia 39: 409-413.
Orfanou DC, Papadopoulos E, Cripps PJ, Athanasiou LV,
Fthenakls GC (2011) Mylasls In a dog shelter in Greece:
Epidemiological and clinical features and therapeutic
considerations. Vet Parasltol 81: 374-378.
Robinson AS, Vreysen MJ, Hendrlchs J, Feldmann U (2009)
Enabling technologies to Improve area-wide Integrated pest
management programmes for the control of screwworms.
Med Vet Entomol 23 (Suppl 1): 1-7.
Rose H, Wall A (2011) Modelling the impact of climate change on
spatial patterns of disease risk: sheep blowfly strike by Lucilia
sericata in Great Britain. Int J Parasltol 2011 41: 739-7 46.
Sandeman RM, Bowles VM, Colwell DD (2014) The
immunobiology of myiasis infections - whatever happened
to vaccination? Parasite lmmunol 36: 605-615.
Sotiraki S, Farkas R, Hall MJ (2010) Fleshflies in the flesh:
epidemiology, population genetics and control of outbreaks
of traumatic myiasis in the Mediterranean Basin. Vet Parasltol
74: 12-18.
Wall R, Rose H, Ellse L, Morgan E (2011) Livestock
ectoparasites: integrated management in a changing climate.
Vet Parasitol 180: 82-89.
Zumpt F (1965) Myiasis in man and animals of the Old World.
London, UK: Butterworths; UDC number: 576-895-772.

Family Oestridae (bot flies, warble flies,
and other names)
Oistros (G): sting. Refers to the irritation caused by the
parasite.
Summary
• Larvae of fly species of this family an, obligate parasites
In mammals and live mainly In the nasopharyngeal
apace (Oestrlnae), the digestive tract (Gasterophlllnae)
or the akin (Hypodermlnae, Cuterebrtnae).
• Some species are monoxen, other euryxen. Humans can
bt accidental hosts for larvae from all four subfamilies.
• Adults are 8-17 mm long, partly densely brletled,
bumblebee-like, yellowlah-black coloured fllea with
reduced, usually non-functional mouthparte, and small
eyee.
• Subfamily Oestrinae (bot flies)
In Europe, pnrticularly Oestrus ovis, the bot fly of sheep
and goat, various genera (Cephenemyia, Pharyngomyia)
of nose or throat bot flies in wild ruminants, and
Rhinoestrus species (nose bot fly of equines) are to be
considered. In other regions more genera and species
parasitise in domestic and wild animals (including
camels, zebras, antelopes, giraffes, warthogs, hippos,
elephants, kangaroos, caribou).
Summary
Bot fly of sheep
Life cycle. Oestrus ovis. Females are viviparous and
deposit larvae (L1) during flight, especially onto nostrils;
L1 migrate to nasal and head cavities and mature to L3
(17-28 mm long); the latter leave the host and pupate
in the soil. Usually only one fly generation a year In
temperate regions.
• Epidemiology, occurrence. From August strong
increase in number of L 1, which overwinter In diapause
in the host. Prevalence of 0. ovis in sheep In south­
western Germany about 50%.
• Pathogenesis, clinical signs. Inflammatory reactions
in head and nasal cavities, partly also In larynx, trachea
and bronchi. Nasal discharge, sneezing, lacrimatlon,
cough, dyspnea, reduced feed Intake, emaciation,
impaired general condition.
• Diagnosis, therapy. Post-mortem detection of larvae
in nasal and head cavities, intra vitam clinically and
by detection of antibodies in serum. Treatment with
macrocyclic lactones or closantel.
Bot flies of wild ruminants
Larvae of Cephenemyia and Pharnygomyia species are
partly a considerable nuisance in cervids in Europe.
14. Phylum Arthropoda (arthropods)
Genus Oestrus
Oestrus ovis (sheep nostril fly, sheep nasal bot
fly)
Disease: Oestrosis in sheep and goats.
L.
r_
Morphology, life cycle and epidemiology. Adults
of Oestrus ovis are 10-12 mm long, slightly hairy,
brownish-grey nies with a broad head and small eyes;
mid-thoracic segment with small warts and yellow hairs,
abdomen wilh black spots. Mouthparts greatly reduced.
In Europe, depending on the climate, adults occur from
May to September or October; they do not feed during
their short lives (up to 4 weeks). After mating, eggs
develop into larvae (LI) in the females within 2-3 weeks.
The gravid females swarm, especially on hot, dry days
and deposit during flight batches of about 25 LI to the
nostrils of sheep, and partly to the mouth edges, the
eye area or to other parts of the body. A female can
produce 500-1000 larvae. The approximately 1 mm
long larvae migrate directly or after been licked from
the depositing areas into the nasal cavity and settle
later at the nasal conchae, accessory nasal sinuses as
well as frontal and maxillary sinuses, where they firmly
attach to the mucosa and feed on mucous secretions
and inflammatory products. Several proteases that
are secreted by the larvae play a role in liquefaction of
tissue and extracorporeal digestion of proteins. Through
growth and moulting the Ll develop into L2 (4-12 mm)
and then into L3. The 17-28 mm long, cylindrical L3 are
equipped with mouth and caudal hooks, and have rows
of spines and papillae on the ventral side; the annular
posterior spiracles have numerous pores. In spring and
early summer, the L3 that are ready to pupate detach
and leave the host actively or are discharged by sneeze
and cough. On the ground, the larvae pupate; the pupal
period usually lasts 2-6 weeks.
In the temperate climate zones, usually only one fly
generation arises per year because the development of
most Ll in the host is arrested (diapause) in autumn
for several months and continues afterwards. In this
way, overwintering of the parasite is secured in the
host. In warmer areas, e.g. the south-west of France,
the internal development can be completed already
in 25-35 days, and thus 2-3 fly generations per year
are produced. Under these conditions, Ll-L3 can be
found at the same time in infected animals throughout
the year. Almost throughout the year, L1 are the largest
part of the population; the proportion of L2 and L3 is
generally low throughout the year, especially in winter,
but strongly increases after April.
 Part Ill. Parasites and parasitoses: metazoa

Occurrence. 0. ovis is widespread in sheep-farming
areas around the world. In southern Europe (e.g. ES,
FR, IT, GR) high prevalences are still to be expected, e.g.
80% in 120 slaughtered sheep in north-eastern Spain. In
the south-west of France, the annual mean infestation
rates of 0. ovis were 43% in adult sheep (n=631) and
28% in goats (n=672). The mean infestation intensities
per animal were 11 Oestrus larvae in sheep and 5 in goats
(maximum in sheep 150 larvae/animal). In Germany,
0. ovis was detected in 55% of 59 sheep at slaughter;
serum antibodies against 0. ovis were present in 50%
of 1497 sheep older than 6 months.
Pathogenesis and clinical signs. The depositing of
L1 and their migration into the nasal cavities can cause
restlessness, rubbing the head on objects and shaking
the head. The first weeks of infestation are usually
unapparent. At their places of settlement, larvae cause
inflammatory changes, which can trigger ascending
bacterial infections and result in nasal discharge,
sneezing, lacrimation, cough, dyspnoea, impaired food
uptake, weight loss and deterioration in the general
condition. In case of strong infestation, colonisation
of the larynx, the trachea and the large bronchi with
related symptoms is possible.
Resistance and immunology. Sheep are more
susceptible to 0. ovis than goats. Experimental
immunisation of sheep with extracts of 0. ovis larvae
significantly reduced the proportion of surviving larvae
after challenge inoculation compared to non-immunised
controls. Polypeptides which are produced in the glands
of 0. ovis larvae are more immunogenic than antigens
from the cuticle. In the course of infestation, there is
a hypersensitivity reaction of the nasal mucosa with
infiltration mainly of lymphocytes, macrophages,
eosinophils, mast cells and other cells. Such reactions,
which can also occur on mucous membranes of the
upper airways and in the lung, are thought to play a
role in the elimination of larvae and thus in limiting
larval populations. A systemic Immune reaction leads
to the formation of circulating antibodies which con be
detected 2-4 weeks after a primary Infection.
after the end of the flight period of the adults. At that
time, L1 predominate and are killed by the above­
mentioned ML. The use of these ML for the control of
gastrointestinal nematodes at other times of the year
also affects 0. ovis larvae.
Genus Rhinoestrus
Disease: Rhinoestrosis in equids. I
Rhinoestrus purpureus and some other species of this
genus are specific parasites of equines and cause diseases
in horses and donkeys, especially in southern and eastern
Europe, Russia and parts of Asia and Africa.
Genera Cephenemyia and Pharyngomyia
■ Nasal bot flies in wild ruminants
In Europe, roe deer are quite often infested with larvae
of bot flies (Cephenemyia stimulator), red deer are
parasitised by C. auribarbis and Pharyngomyia picta.
The latter species also occurs in roe deer, moose, other
cervids and mouflon. The development cycle is similar
to 0. ovis but the up to 35 mm long larvae primarily
infest pharynx, larynx and tongue root(► Figure 14.59).
Such an attack can be a significant nuisance and cause
fatal diseases. Treatment is possible by administration
of macrocyclic lactones (e.g. ivermectin with feed).
Oestrinosis in red and roe dear was successfully
treated with ivermectin (e.g. 2x0.4 mg/kg b.w. p.o.),
administered at an interval of one week.
Zoonotic importance. Larvae of 0. ovis can establish
in aberrant hosts, such as dogs and humans. In certain
endemic areas, 0. ovis quite often causes various forms
of myiasis (pharyngeal, conjunctival, etc.) in exposed
persons, e.g. shepherds. Human infestations with larvae
of other Ocstrinae (Rhi110estrus, Cephenemyia spp.) are
rarely reported.

Diagnosis. Diagnosis is usually performed clinically.

An indirect serological diagnosis is possible by detection
of specific antibodies using an ELISA with E/S antigens
from 0. ovis larvae. Sensitivity and specificity of the
test are high (both around 97%). Larval stages can be
detected post mortem by adspection of nasal and head
cavities (use magnifying glass to detect the 1-3 mm
long LI).

Treatment and control. Macrocyclic lactones (ML),

such as ivermectin(0.2 mg/kg b.w. s.c.) and doramectin
(0.2 mg/kg i.m.) are very effective against 0. ovis larvae
(Ll-L3) in sheep. Moxidectin (0.2 mg/kg p.o.) is not
sufficiently efficient! The anthelmintic closantel (10
mg/kg p.o.) also has a good effect. A suitable time for Figure 14.59. Cephenemyia trompe: larvae 3 from the pharynx
treatment in temperate wnes is autumn or early winter of a wild ruminant (length 35 mm) (Photo: IPZ).

Selected references
Angulo-Valadez CE, Scholl PJ, Cepeda-Palacios R, Jacquiet
P, Dorchies P (2010) Nasal bots - a fascinating world! Vet
Parasitol 174: 19-25.
Angulo-Valadez CE, Ascencio F, Jacquiet P, Dorchles
P, Cepeda-Palacios R (2011) Sheep and goat immune
responses to nose bot infestation: a review. Med Vet Entomol
25: 117-125.
Bauer C, Steng G, Prevot F, Dorchles P (2002) Seroprevalence
of Oestrus ovis infection in sheep in southwestern Germany.
Vet Parasitol 110: 137-143.
Dorchies P, Bergeaud JP, Tabouret G, Duranton C, Prevot
F, Jacquiet P (2000) Prevalence and larval burden of
Oestrus ovis (Linne 1761) In sheep and goats in northern
mediterranean region of France. Vet Parasltol 88: 269-273.
Goddard P, Bates P, Webster KA (1999) Evaluation of a direct
ELISA for the serodiagnosls of Oestrus ovls Infections In
sheep. Vet Rec 144: 497-501.
Gracia MJ, Lucientes J, Perlbai'lez MA, Castillo JA, Calvete
C, Ferrer LM (2010) Epidemiology of Oestrus ovis Infection
of sheep in northeast Spain (mid-Ebro Valley). Trap Anim
Health Prod 42: 811-813.
Scala A, Paz-Silva A, Suarez JL, L6pez C, Diaz P, Diez­
Banos P, et a/. (2002) Chronoblology of Oestrus ovis (Diptera:
Oestridae) in Sardinia, Italy: guidelines to chemoprophylaxis.
J Med Entomol 39: 652-657.
Silva BF, Bassetto CC, Amarante AF (2012) Immune responses
in sheep naturally infected with Oestrus ovis (Diptera:
Oestridae) and gastrointestinal nematodes. Vet Parasitol
190: 120-126.
Yilma JM, Dorchies P (1991) Epidemiology of Oestrus ovis in
southwest France. Vet Parasitol 40: 315-323.
• Subfamily Gasterophilinae (stomach bots,
horse bot fly)
Disease: Gasterophilosls in equids.
Gaster (G}: stomach; philos (G}: loving, devoted. Refers
to the location of larvae in the stomach.
Summary
Morphology, species. Gasterophillnae are heavily
bristled flies with rudimentary mouthparts. Larval
stages live as obligate parasites in the digestive tract
of equine species (Gasterophi/us), rhinos (Gyrostigma)
or elept:tants (Cob'boldla, etc.). In Europe, several
Gasterophilus species occur in horses, with G.
lntestinalis being the most important.
• Life cycle, occun-ence, epidemiology. Oviposition
by Gasterophl/us spp. females in summer months
on hair of different parts of the body of horses or in
the case of G. pecorum on plants. Development of
L 1, which enter the oral cavity in species-specific
�
14. Phylum Arthropoda (arthropods)
manner, then penetrate the mllcosa and moult to L2;
L2 and L3 settle In the stomach or duodenum, and
partly also In the f'ICtum. GasteropHllus Infestation Is
common in Europe; regionally high prevalence with
strong seasonal fluctuations.
• l'athogenesis, cljntcal •lgns. MIid and moderate
Infestation Is asYmr:>totnatlc or associated with reduced
a.
peiformahce1 heavy infestation With lnappetenoe, oollo, 0
anaemia and cac:hexla.
• Diagnosis, Detection of �gs on hair; endoscopy of
atomaoh and proximal amlill lntestlne tor the detection
of� ahd L3: 11eot10n.
• Therapy, control. 1reatrnent with macrocycllc
laotonee (moxldeotin, lvermeotln) In autumn (Ootober
to November).
Species and morphology. The main characteristic
of this subfamily is the obligate parasitism of the larval
stages in the digestive tract of equine species (genus
Gasterophilus), rhinos (genus Gyrostigma) or elephants
(genera Cobboldia, Platycobboldia, Rodhainomyia).
Among the Gasterophilus species described in Europe
in horses, G. intestinalis is the most important ( ► Table
14.17).
The adults of Gasterophilus species are l 0-17 mm long
flies of different colours (black brown, yellowish brown,
rust yellow), with densely bristled head, thorax and
abdomen and with rudimentary mouthparts. Colour, ro
mottling of the wings and some other characteristics are "'O
0
0..
species-specific. The acephalic and legless larvae have a
spindle-shaped, segmented body. The front edge of most ..c
t
segments is covered with 1-3 rows of spines. All larval <l::
stages bear strong mouth-hooks. The posterior spiracles
are located in a closable wrinkle, the spiracles are slit­
shaped, straight or slightly curved. The 15-20 mm
long, brownish or flesh-coloured L3 can be identified
to species especially by using features of mouth hooks
and spines.
Life cycle. Adults of Gasterophilus species have a short
flight period from late June to August (occasionally to
October) in temperate regions and a life span of a few
days (usually <l week), during which they do not feed
(► Figure 14.60). Immediately after hatching from the
pupae, which are in horse manure or in the immediate
vicinity, the adults mate. After a short rest ( <20 h)
required for egg production, the females swarm on warm
and sunny days for oviposition. Host-fmding takes place
on the basis of visual (large silhouettes) and olfactory
signals (horse smell). They pursue horses over long
distances on the pasture, but do not fly into stables. For
oviposition they swarm around the horses and deposit
the eggs during flight on hair using an adhesive. The
preferred oviposition site is species-specific. G. pecorum
lays its eggs on plants. Gasterophilus females produce
a buzzing noise during flight which in the case of G.
intestinalis causes little disturbance in horses, but a strong
 Part Ill. Parasites and parasitoses: metazoa

Table 14.17. Gasterophi/us species.

Gasterophilus intestinalis forelegs (>70%, especially L 1 : tongue mucosa, distal migration in tongue -+ M L2
L: 12-17 mm inner surface of carpal region), (3-4 weeks)
0: cosmopolitan also flank, hind legs, shoulder, L2: pharynx, epiglottis (few days)
neck L2/L3: stomach (pars cardiaca)
Gasterophifus haemorrhoidafis hair of lips L1: skin of lips, mouth mucosa
L: 10-12 mm L2/L3: stomach
0: cosmopolitan L3: rectum and edge of anus (especially in spring)
Gasterophilus inermis cheek L1: migration in skin to corner of the mouth and to
L: 12-17 mm buccal mucosa
0: Palearctic, South Africa L2/L3: rectum
Gasterophilus nasalis mandibular space L1: migration in skin to lips and gingiva -+ M L2 (approx.
L: 12-17 mm 3 week p.i.)
0: Cosmopolitan L2/L3: proximal duodenum (ampulla duodeni)
Gasterophifus nigricornis cheek L1: migration in skin to corner of the mouth and to
L: 12-17 mm buccal mucosa _, M L2
0: southern regions of Palearctic L2/L3: duodenum
(southern Europe, Russia, ot11ers)
Gasterophilus pecorum plants, rarely on limbs L1: mucosa of lips, tongue, hard and soft palate -+ M L2
L: 13-14 mm L2: tongue, soft palate, pharynx
0: Europe, Palearctic regions in L3: stomach (pars cardiaca)
Asia, Africa
1 Localisation of moulting from L1 to L2 not yet known for all species.

one in the case of G. haemorrhoidalis and G. nasalis. It
is still unknown how the choice of the predilection
site on the animal body is made. The total number of
eggs produced by a female is high(~1,000-2,500) in G.
intestinalis and G. pecorum but lower(~150-500) in the
other species. Eggs are about I -1.5 mm long, oblong in
shape and golden yellow or black in colour(G. pecorum).
The embryonic development often takes only a few days,
but can take up to 4 weeks depending on abiotic factors
and the Gasterophilus species.
After exposure to stimuli (licking of oviposition sites
by horses on own body or by other horses) or after
oral ingestion of eggs(G. pecorwn), LI hatch from eggs
and penetrate the oral mucosa. The LI of G. incrmis,
G. nasalis and G. nigricornis leave the egg membranes
spontaneously and migrate from the deposition sites
in the skin to the corners of the mouth and then to the
mouth mucosa where different locations are preferred
Q)
depending on the species(buccal, tongue, palate, gingiva,
·u
C
different regions of central and northern Europe (e.g.
BE, CH, DE, PL, SE), G. intestinalis was recently the
predominantly reported species, sporadically in mixed
infections with G. nasalis. In horses in central and
southern Italy, G. intestinalis and G. nasalis dominated,
whereas G. inermis, G. pecorum and G. haemorrhoidalis
were rare. According to older data (before 2002),
observed average prevalences of G. intestinalis in
slaughter horses were 4-65% in DE, CH and SE. A recent
study (2015) from Sardinia revealed prevalences of G.
intestinalis and G. nasalis of 86% and 54%, respectively,
and of <4% for 4 other species. There was a marked
seasonality in prevalences with the highest values in the
winter months (for infestation intensities, see below).
Epidemiological data reveal that horses get infested
with larvae of G. intestinalis and G. nasalis mainly in
summer or late summer, shortly after the female flies
have deposited their eggs on hair. In the case of G.
intestinalis, minor infestations apparently are possible

'6 pharynx mucosa)(► Table 14.17). The LI remain 3-4 even later, since L l can survive in eggs on the fur for
(I) weeks in the oral cavity, moult to L2 and then move long periods of time (at + 10 °C ambient temperature
cco to their predilection sites in the gastrointestinal tract. up to 2 months, and winter temperatures are tolerated
C After 8-10 months (in spring/early summer), the L3 for long periods of time).
·c are excreted with the faeces. Pupation takes place in
(I)
horse manure or in the immediate vicinity in the soil; Pathogenesis and clinical signs. 70-90% of the
.£; the pupal period lasts 2-12 weeks. infested horses have a slight or moderate infestation
>,
0) (1-100 larvae per horse) of G. intestinalis, while the
0 Occurrence and epidemiology. Gasterophilus remaining have a heavy infestation with >100 larvae/
0
·u3 infestation is very common in equids worldwide. In animal(maximum values around 300-1000 per horse) as
co
a..

Oral uptake of
G. intestina/1s eggs
by licking deposition
sites
; fore limbs
-----
/:.:.,
Eggs of
G. pecorum
Female of
G. pecorum
laying eggs
on plant
Figure 14.60. Ufecycle of Gasterophllus spp. (Graphics: IPZ, S. Ehrat).
shown in studies in Europe. Low or moderate infestations
are usually unapparent, but reduced performance
is also attributed to such infestations. Symptoms in
severe infestations are inflammation of the oral mucosa
f
and tongue, dif iculties in chewing and swallowing,
erosion, inflammation and ulceration of the stomach
and small intestine (especially in the pars cardiaca of
the stomach and proximal duodenum; ► Table 14.17),
as well as inappetence, colic, anaemia and cachexia.
At the attachment sites of the Gasterophilus larvae in
the stomach and small intestine, crater-like lesions
(ulcers) of the mucosa and submucosa are produced,
with initial necrosis, inflammation, loss of glandular
tissue and subsequent fibrosis surrounding the focus
14. Phylum Arthropoda (arthropods)
ro
0
Egg deposition
by G. intestlnalls
predominantly on
Larva 2
Larva 3
co
-0
8.
e
of inflammation. Although the larvae penetrate deep
into the stomach or the intestinal wall, perforations
are very rare. The LI of different species ( G. inermis, G.
ll(ISt1lis, G. 11igricornis) that migrate in the skin toward
the mouth opening cause changes in the form of thread­
thin, hairless, slightly sinuous stripes covered with crusts
which stretch between the eye and cheek region and
throat towards the corner of the mouth ( ► Table 14.17).
Immunology. No effective immunity develops under
natural infestation conditions, not even with increasing
age of the horses; however, circulating antibodies are
formed. The larval stages produce specific proteins; L2
are more immunogenic than L3.
 Part Ill. Parasites and parasitoses: metazoa
Diagnosis. Eggs or egg shells that are detectable on the
coat of horses in summer (June/August) and partly until
February provide clues to Gasterophilus infestations in
a herd. The same applies to larvae that are occasionally
observed in faeces of horses in spring/early summer
or after treatment. Endoscopic examination allows for
the detection of lesions or larval stages (L2 or L3) in the
oral cavity, oesophagus and stomach. ELISA with E/S
antigen from L2 of G. intestinalis can prove circulating
antibodies against G. intestinalis and G. nasalis. In Spain,
the highest seroprevalences (100%) were found in horse
populations in winter (January/February), the lowest
(3%) in June. Older larval stages are easy to diagnose
by adspection post mortem.
Therapy and control. The drugs of choice for
treatment are macrocyclic lactones which are highly
effective against Gasterophilus larvae (L2 and L3) as
well as against strongyles and some other parasites; e.g.
moxidectin (0.4 mg/kg b.w. p.o.) or ivermectin (0.2 mg/
kg, b.w. p.o.). Control ► p. 597.
Zoonotic importance. Gasterophilus larvae are
occasionally causative agents of myiasis in humans
(► Table 15.3, p. 513).
Selected references
Agneessens J, Engelen S, Debever P, Vercruysse J (1998)
Gasterophilus intestinalis infections in horses in Belgium. Vet
Parasitol 77: 199-204.
Cogley TP, Cogley MC (2000) Field observations of the host­
parasite relationship associated with the common horse
bot fly, Gasteroph/lus lntestinalis. Vet Parasitol 88: 93-105.
Hoglund J, Ljungstrom BL, Nilsson 0, Lundquist H,
Osterman E, Uggla A. (1997) Occurrence of Gasterophllus
intestlnalis and some parasitic nematodes of horses In
Sweden. Acta Vet Scand 38: 157-165.
Niedzwiedz A, Borowicz H, Nlcpon JM (2013) Prevalence
study in horses Infected by Gasterop/1/lus sp. In an eastern
region of Poland. Vet Parasitol 191: 94-96.
Otranto D, Milillo P, Capelli G, Colwell DD (2005) Species
composition of Gasterophilus spp. (Dlptera, Oestridae)
causing equine gastric mylasis In southern Italy: Parasite
biodiversity and risks for extinction. Vet Parasitol 133:
Q)
·u 111-118.
C
'6 Pilo C, Altea A, Scala A (2015) Gasterophilosis in horses in
Q)
Sardinia (Italy): effect of meteorological variables on adult
egg-laying activity and presence of larvae In the digestive
cu
C tract, and update of species. Parasitol Res 114: 1693-1702.
·c
Q) Roelfstra L, Deeg CA, Hauck SM, Buse C, Membrez M,
Betschart B, Pfister K (2009) Protein expression profile
C of Gasterophilus intestinalis larvae causing horse gastric
>,
myiasis and characterization of horse immune reaction.
0)
0
Parasit Vectors 2: 6.
0
·u;
ro
ro
CL
Sanchez-Andrade R, Cortinas FJ, Francisco I, Sanchez JA,
Mula P, Cazapal C, Vazquez L, Suarez JL, Francisco
R, Arias MS, Diez-Banos P, Scala A, Paz-Silva A (2010)
A novel second instar Gasterophilus excretory/secretory
antigen-based ELISA for the diagnosis of gasterophilosis in
grazing horses. Vet Parasitol 171: 314-320.
• Subfamily Hypoderminae (warble flies,
cattle grubs)
Disease: Hypodermosis.
Hypo (G): under; derma (G): skin. Refers to the location
of larvae in warbles beneath the skin surface.
Summary
• Species. The most Important species are Hypoderma
bovls and H. 1/neatum, the causative agents of
hypodermoals of cattle.
• Life cycle. During the flight period in May and June (H.
1/neatum) or June to September (H. bovis) the female
flies attach eggs to the hair of grazing cattle. The
hatching larvae {L1) penetrate the skin and migrate
through the spinal canal (H. bovis) or the oesophageal
wall (H. llneatum) to the subcutaneous tissue of the
back. There, they develop into L3 and form from
January (H. lineatum) or February (H. bovis) warbles
with a breathing hole in the skin. The L3 leave the
warbles in spring or early summer and pupate in the soil.
• Occurrence, epidemiology. H. bovis and H. lineatum
occur in temperate regions in the northern hemisphere
(North America, Eurasia). Hypodermosis still represents
a problem in some countries of the distribution area,
whereas the disease Is eliminated or only focally
present with mostly low prevalence In most countries
of northern, western and Central Europe. Starting
from such foci, hypodermosls can spread rapidly if
no countermeasures are taken. Hypodermosls-.free
areas are vulnerable to Imported animals from endemic
regions.
• Adver1e effect. Hypoderma larvae damage the skin
and partly also the back muscles; they also can also
cause rl3Cluction in performance and suffering of the
hosts.
• Diagnosis. In apparent hypodermosls (visible warbles)
clinlcally, In unapparent Infestations by detection of
antibodies in blood serum or In milk.
• Therapy, control. In endemic areas, treatment of all
>3 month-old, pastured cattle In the period from late
September to late November with systemically active
Insecticides in usual therapeutic dosages, which are
highly effective against the migrating larvae. Treatments
from early December to mid-March hold the risk to kill
larvae of H. bovls that are located in the vertebral canal,
thereby causing damage to the spinal corc1. A proven
and cost-effective alternative Is the treatment of cattle
with a 'micro-dose' of lvermectln (2 micrograms/kg b.w.
s.c.) during the winter period.
'f
 14. Phylum Arthropoda (arthropods)

ng treatments only topically in cases of manifest
odennosls. Observe official regulations!
phylaxls. Important are measures to prevent
lhtroductlon of the parasites Into hypodennosls­
fr&t areas and for continuous monitoring of the
epldemlologlcal situation.
Hypodennosls In wild ruminants. Caused by other
species, e.g. H. actaeon.
In Europe, the genera Hypoderma and Przhevalskiana of
the subfamily Hypoderminae are ofparticular veterinary
interest. The adults are bumblebee-like flies whose
larvae develop in the body of ruminants and other
mammals and eventually settle in the subcutaneous
tissue. Occasionally, closely related or aberrant hosts
become infested. Ofspecial significance is hypodermosis
of cattle.
Genus Hypoderma
■ Hypodermosis in cattle
Morphology and species. Causative agent of
hypodermosis of cattle are 1-lypoderma bovis (northern
cattle grub) (13-15 mm) and H. lineatum (common
cattle grub (11-13 mm). They are bumblebee-like flies
0.
with dense bristles and rudimentary mouthparts. In 0
H. bovis, the yellowish and black bristles usually form
transverse bands on the dorsal thorax and abdomen,
whereas the white and yellowish bristles are rather
irregularly distributed in H. lineatum.
Life cycle. H. bovis and H. lineatum are adapted
to cattle but there are significant differences in their
development In the host. Only grazing animals are
affected by this infestation ( ► Figure J 4.61 ).

I
n of larvae 1

'
of the bacj<

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0
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<(

.;,
/. Sites of egg deposition on skin
/
I
I Larva 2
I
I
! _,_Larva� Q)

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I Eggs attached to a hair:

'
H. bovls (left),

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H. 1/neatr:Jm (right) �
!Larva 3 co
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0
Hypcx;Jerma SAP· female Pl!lpa, G>peneGl ·u5
co
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Figure 14.61. Development cycle of Hypoderma spp. (Graphics: IPZ, S. Ehrat}. Q..
 Part Ill. Parasites and parasitoses: metazoa

H. bovis. Adults are active from June until September on H. lineatum. Adult activity of this species begins in May
warm(>18 °C), sunny days. Mating occurs immediately and lasts until June. To lay their eggs, the females crawl
after emergence of adults from pupae. For oviposition onto lying cattle, without perturbing them, and attach
which may begin shortly thereafter, the females search up to 20 eggs (length 0.8 mm) in a row on a hair, mainly
for grazing cattle which often flee from the approaching in the distal body part. The hatched L1 penetrate the
warble flies ('gadding'). The flight radius of the females skin and migrate to the submucosa of the oesophagus.
can be up to 14 km. During the short lifetime of a few Possibly they may also be swallowed after cattle has
days, a female lays 300-600 eggs(egg length of~ 1 mm). licked oviposition sites and penetrate directly into the
Females lay their eggs through an ovipositor, preferably oesophageal wall. After several months of dormancy
on the distal parts of the body. The eggs are attached in the oesophagus, the larvae migrate - presumably
singly to hair by the pincer-like end of the ovipositor through the diaphragm, byp assing the spinal canal - to
by means of a pedicled adhesive apparatus. Within 3-7 the subcutaneous tissue of the back, where they form
days, first larvae(L 1) hatch from the eggs and penetrate warbles that are visible as early as January. L1 from
the skin into the animal body where they migrate along eggs that have been deposited in the caudal regions of
fascial and perineural tissue of larger nerve fibres to the the body may directly invade the subcutaneous tissue
spinal canal. They can be found between early December of the back. As with H. bovis, L3 leave the warbles after
and mid-March in the epidural fat tissue. Following a few weeks and pupate in the soil. The pupal period
this phase, the larvae migrate through muscle to the lasts 3-7 weeks.
dorsal skin, especially in the lumbar region, where
they form warbles (see below) which are connected Occurrence and epidemiology. H. bovis and H.
through a breathing hole with the outside world. Here, lineatum occur in temperate regions in the northern
moultings to L2 and L3 take place. The mature L3 are hemisphere (North America, Eurasia), with often
oval, up to 3 cm long maggots with fine dorsal and overlapping distribution areas, but H. lineatum prefers
ventral spines, yellowish and brownish to dark brown more southerly areas. In Switzerland for example, the
in colour (► Figure 14.62a). The cephalopharyngeal warble fly population was composed of approximately
skeleton is reduced, mouth-hooks are not visible 90% H. lineatum and 10% H. bovis. By applying control
externally. The warbles usually appear from February measures during the last decades, hypodermosis of cattle
to May (sometimes until August) (► Figure 14.626). has been eliminated in most countries of northern,
The L3 leave the warbles from April to June, rarely in western and Central Europe or reduced to focal
July, and pupate in the soil. The pupal period lasts 7-10 occurrence with mostly low prevalences (e.g. AT, CH,
weeks. Adults do not take any feed; their life span is CZ, DE, DK, FI, FR, IE, NO, NL, SE). After repealing
usually 3-5 days, rarely up to 4 weeks. regulatory control measures, increasing prevalences are
observed in some areas.

,•. . , h
Before implementing control measures, 40% to nearly
100% of herds were infested with warble fly larvae in

" , ..
.1.
� some countries.
p>_ •.}.
;.:.r �
'

,,.,'
' "t •
t" V.
• ·, •

-�(' .. ;;_ . -'�.•

t .11•··4.4

r_.f,.,
.· ,'l �· l '�
,,.- .-. �· . ,. ·L
.I . t
Because of the marked host specificity, warble flies of wild
,..I '
' I ·'· o-1•·
') • I
f
...
, C': • '
I -1 ii!
',, '
, '�I.( ruminants do not pose a threat to cattle. Rather, infected
'... . :i
I
'"' '. ' ,
',...,.. I imported cattle can be a source for re-colonisation of
a Hypoderma-free areas. Within Hypoderma-free areas,
unnoticed endemic foci with low to high prevalence
can persist and become starting points of a large-scale
spread. Therefore, continuous surveillance of the
situation is important.
Q)

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'5 Pathogenesis and clinical signs. The panic escape

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Q)
reactions of cattle('gadding') during the approach of H.
bovis can cause injury to the animals at fences and other
co
C obstacles. The migrating larvae in the animal body are
·;::
partly surrounded by gelatinous, greenish discoloured
reaction zones heavily enriched with eosinophils.
-� Occasionally, aberrant larvae invade other organs
>,
0)
causing different types of damage. In the subcutaneous
0 tissue of the back, inflammation develops around each
0
·u;
Figure 14.62. Hypoderma: (a) larva of H. bovis (Photo: IPH, larva with connective tissue encapsulation and a fistula
W. Ruhm); (b) cattle with warbles {Photo: IPZ). (breathing hole of the larva) to the outside (warble).
co
a.. The changes may radiate to the back muscles and cause

inflammation and oedema of considerable extent in
heavy infestations. In rare cases, migrating larvae can
cause damage to the spinal cord (recumbency). The
number of warbles per bovine animal varies greatly
(1-200) and is often between 5-20(► Figure 14.62b).
Hypodermosis causes suffering of animals, leather
damage(through holes and scars of warbles), meat loss
(unusable back muscles), lack of weight gain, decreased
carcass weights, reduced milk production(up 15%) and
costs for control measures.
Immunology. The fraction of surviving L1 decreases
by about 50% in the first or second reinfestations
compared to the first infestation. Accordingly, partial
immunity develops, which initially manifests as Th l
response(IgG2 and IFN-y) thereafter changes to a Th2
response(IgG I and IL-4). The formation of antibodies
is of diagnostic significance. Despite these immune
reactions, Hypoderma larvae can survive in the host for
many months because they have developed strategies
of immune evasion. They produce various trypsin and
chymotrypsin-like proteases, e.g. hypodermins(HA,
HB, HC), of which especially HA is associated with
causing immunosuppressive effects. It damages the
membrane proteins of lymphocytes and monocytes,
inhibits the early blastogenesis of lymphocytes as well
as the synthesis of IL-2 and IFN-y by T-cells and cleaves
bovine IgG. HA and HB cleave complement proteins.
A vaccination of cattle with soluble fractions of the fat
body, which originates from the interior of H. lineatum
L3 ('hidden antigens'), caused a marked reduction in
the number of warbles.
Diagnosis. Hypodermosis can clinically and post
mortem unequivocally be diagnosed based on the
characteristic warbles in the back skin and squeezed­
out warble fly larvae. L3 of H. bovis and H. /ineatum
can be distinguished by their spiracles and some other
characteristics. The identification of larval stages of
various Hypoderma species is also established with
molecular tests. Warbles occur from January to July,
rarely later. Important is the early diagnosis of infestation
before damage occurs in the dorsal skin. Approximately
3-6 weeks after infestation with Hypoderma larvae,
bovine IgG antibodies can be detected in serum,
reaching highest concentrations in natural infestation
during the winter months and then(after development
of L3 in the warbles) decreasing gradually. Antibodies
persist for 3-5 months after L3 have left the animal body
or the elimination of the infestation by chemotherapy.
For antibody detection, an ELISA with high sensitivity
(94%) and specificity(98%) is used. Sources for antigens
are L1 of H. lineatum. These antigens also react with
antibodies directed against other Hypoderma species
and Przhevalskiana silenus, but no cross-reactions
were observed with antibodies against Oestrus ovis,
Gasterophilus intestinalis, ticks, Psoroptes, Chorioptes,
helminths or protozoa. Because of the antibody
14. Phylum Arthropoda (arthropods)
dynamics, the time between end of October to March
is best for serological testing of herds. Serological tests
which are performed either with individual animal
samples or pooled samples of 10 animals quite reliably
detect infested herds. With bulk milk samples, reliable
ELISA results are obtained if the infestation rate is higher
than about 2%.
Q)
a.
Therapy and control. Hypodermosis is among the i:5
few parasites that can be eliminated with the currently
available control methods, as demonstrated with data
from different countries. Control of hypodermosis
is officially regulated in many countries; in CH, it is
classified as 'disease to be controlled: with mandatory
reporting of cases; in contrast, e.g. AT and DE have no
corresponding regulations. Control is based on the use of
systemically acting insecticides to kill Hypoderma larvae
in the animal body. In recent years strategic treatments
of young cattle with a microdose of ivermectin(off-label
use) and of dairy cattle with eprinomectin (pour-on)
have proven to be highly effective for sustainable control
of hypodermosis. For further information, ► p. 584.
■ Hypodermosis in wild ruminants
Causative agent of hypodermosis of wild ruminants in
Europe are H. actaeon in red deer and the euryxenous
H. diana especially in roe deer, but also red and fallow
deer, reindeer, elk, chamois and mouflon. In the north,
Hypoderma(formerly Oedemagena) tarandi has to be co
noted as a pathogen in reindeer(► Figure 14.63). 'O
0
a.
Genus Przhevalskiana
e
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<(
■ Przhevalskiana infestation of goat
In the Mediterranean region (southern Italy, Greece,
North Africa, etc.), the Middle East and southern Asia,
Przhevalskiana silenus is widespread and common in
goats(e.g. prevalence of 57% in southern Italy). This
species also infests gazelles and rarely sheep. P. silenus
causes a furuncular myiasis(warbles) in the back and
flank areas, similar to H. bovis in cattle. Recent findings
suggest that P. silenus does not migrate through the
Figure 14.63. Hypoderma (formerly Oedemagena) tarandi:
changes in the dorsal skin of a reindeer (Photo: IPZ, J. Eckert).
 Part Ill. Parasites and parasitoses: metazoa
body, but rather that the larvae penetrate the skin at the
oviposition predilection sites and settle in the subcutis.
Zoonotic importance. Occasionally, Hypoderma
larvae also infest humans and cause forms of furuncular
myiasis, but they cannot develop(► Table 15.3, p. 513).
• Subfamily Cuterebrinae
Larvae of Dermatobia hominis infest domestic animals
and humans in Central and South America and cause
similar warbles in the skin as H. bovis (furuncular
myiasis). The development has the peculiarity that
the females of D. hominis attach their eggs to other
insects (flies, mosquitoes) as transport hosts. If these
insects come in contact with a vertebrate, the L l of the
flies hatches and penetrates the skin, where they form
warbles. A migration of the larvae through the body
does not occur.
- Selected references c::.:==::cics.z::c::..J
Asbakk K, Kumpula J, Oksanen A, Laaksonen S (2014)
Infestation by Hypoderma tarandi In reindeer calves from
northern Finland - prevalence and risk factors. Vet Parasitol
200: 172-178.
Boulard C, Argenta M, Argenta G, Languille J, Paget L, Petit
E (2008) A successful, sustainable and low cost control­
programme for bovine hypodermosis in France. Vet Parasitol
158: 1-10.
Colwell DD (2011) Hidden antigens from third instar Hypoderma
tineantum: Impact of immunization on larval survival in artificial
infestations. Vet Parasitol 175: 313-319.
Hassan M, Khan MN, Abubakar M, Waheed HM, Iqbal Z,
Hussain M (2010) Bovine hypodermosis - a global aspect.
Trop Anim Health Prod 42: 1615-1625.
Otranto D, Puccini V (2000) Further evidence on the Internal
life cycle of Przhevalsklsns sllenus (Dlptera, Oestridae). Vet
Parasitol 88: 321-328.
Otranto D, Colwell DD, Traversa D, Stevens JR (2003) Species
Identification of Hypoderma affecting domestic and wild
ruminants by morphological and molecular characterization.
Med Vet Entomol 17: 316-325.
Pfister K, Charbon JL (2014) Control of hypodermosis in
Q)
Switzerland: looking back. Schwelz Arch Tiemeilk 156: 39-43.
Panadero R, Vazquez L, Colwell DD, L6pez C, Cacal V,
·u
C
'6 Morrondo P, Diez-Banos P (2007) Evaluation of an antigen
Q)
capture EUSA for the early diagnosis of Hypoderma lineatum
in cattle under field conditions. Vet Parasitol 147: 297-302.
cu Panadero R, Lopez C, Vazquez L, Diaz P, Perez A, Cabanelas
C
·;:::
E, Morrondo P, Diez-Banos P (2013) Effect of reinfestations
on systemic immune responses in cattle naturally infested
.!; by Hypoderma sp. (Diptera: Oestridae). Vet Parasitol 193:
>, 238-244.
Ol
0
0 of larvae that are ready to pupate (see glossinids, ► p.
'ui
cu
0...
Salaba 0, Vadlejch J, Petrtyl M, Valek P, Kudrnacova M,
Jankovska I, Bartak M, Sulakova H, Langrova I (2013)
Cephenemyia stimulator and Hypoderma diana infection
of roe deer in the Czech Republic over an 8-year period.
Parasitol Res 112: 1661-1666.
Vazquez L, Dacal V, Lopez C, Diaz P, Morrondo P, Diez­
Banos P, Panadero R (2012) Antigen-specific antibody
isotypes, lymphocyte subsets and cytokine profiles in cattle
naturally infested by Hypoderma sp. (Diptera: Oestridae). Vet
Parasitol 184: 230-237.
Webster K (1998) lmmunodiagnosis. In: Boulard C, Sol J, Pithan
K, O'Brien D, Webster K, Sampimon OC (eds.) Improvements
In the control methods for warble fly in livestock. Final
report, COST 811. Luxembourg, Luxembourg: European
Commission, pp. 71-77; ISBN 92-828-2604-X.
Family Hippoboscidae (louse flies,
keds, forest flies)
Disease: Hlppoboscidosis. I
Hippos (G): horse; boskein (G) to feed, to graze.
Summary
• Species, development. Hippoboscids are flies with
piercing-sucking mouthparts; they permanently or
temporarily have wings or are wingless. The most
common species Is Melophagus ovinus, the wingless
sheep ked, a stationary-permanent parasite in the fleece
of sheep. Females deposit larvae that are ready to
pupate; pupae remain in the wool fleece.
• Clinical signs. Symptoms of heavier Infestations are
restlessness, prurltus, wool loss, disorders of feed
Intake.
• Diagnosis Is visually.
• Therapy preferably with pyrethrolds by pour-on
appllcatlon,
• More species of Hlppobosclds In mammals and birds.
Hippoboscids are 2-10 mm long flies (► Figure 14.64)
with dorsoventrally flattened, bristled, brownish­
coloured body. The adults of some species permanently
carry wings, in other species the wings break off as soon
as the flies have reached their host, or they can also be
reduced or completely absent ( ► Figure 14.64a). The
abdomen has no distinct segmentation; the legs are large,
with serrated claws. The piercing-sucking mouthparts
are withdrawn at rest into a cavity of the front head. The
antennas are hidden in pockets. Hippoboscid species
which live permanently on their host have high host
specificity; other species are less host-specific. A special
feature of their development is the deposition by females
481). Hippoboscids are frequently confused with ticks.

Figure 14.64. Hippoboscidae: (a) Hippobosca equina, adult (length 8 mm) (Photo: IPH); (b) Melophagus ovinus: left: adults
(length 5 mm), right: pupae (Photos: IPZ).
Members of the family Hippoboscidae are parasites
of domestic animals (genera Hippobosca, Melophagus,
Lipoptena), of wild ruminants (Lipoptena, Neolipoptena),
domestic pigeon (Pseudolynchia, syn. Lynchia), wild birds
(Ornithomyia, Crataerina, Stenepteryx) and a number
of other animal groups. Of veterinary importance is the
species Melophagus ovinus.
Genus Melophagus
Melophagus ovinus (sheep ked)
Melos(G): fleece; phagein (G): to eat.
Morphology and life cycle. The body of the 3-6 mm
long sheep ked is dorsoventrally flattened, bristled and
enclosed in a leathery, very resistant chitinous cuticula.
The head is very close to the thorax, wings and halteres
are absent. The compound eyes are greatly reduced
(► Figure 14.64b).
Sheep keds parasitise sheep and mouflon, rarely also
goat. They live permanently on the host and prefer to
stay in the fleece of the neck and chest area and the
lateral abdominal wall. Both males and females are
haematophagous; blood meals of 3-15 mg are taken at
intervals of about 36 h. Similar to other haematophagous
insects (e.g. Glossinidae, fleas), hippoboscids harbour
microorganisms in a dedicated zone of the midgut that
provide them with additives (e.g. vitamin B). In the
uterus of the female Melophagus, a single larva develops
which feeds on the secretions of two glands, moults 2
times, reaching the L3 stage which is ready to pupate.
After being deposited in the wool fleece, the larva
develops within a few hours into a reddish brown, about
3 mm long pupa(► Figure 14.64b). T he pupal period
lasts 30-35 days. During a lifetime of about 4 months,
each female produces l 0-15 offspring.
Occurrence and epidemiology. M. ovinus is almost
cosmopolitan, but is absent i n very hot climates or
present only at higher altitudes. In Europe, keds are
common ectoparasites of sheep. In untreated sheep,
about 40 adults were counted on average, but there are
also reports of higher abundances (up to 400 adults per
sheep). The transmission of M. ovinus occurs via direct
14. Phylum Arthropoda (arthropods)
co
....
a.
Q)
i:5
animal contacts, when adults migrate from infested to
non-infested sheep. Adults of M. ovinus can survive up
to 7 days off the host.
Pathogenesis, clinical signs and vector role.
Signs of heavy infestation with M. ovinus are anxiety
and itching that causes the sheep to frequently scrub and
'gnaw' the affected skin areas. Wool loss, impairment of
wool quality, allergic dermatitis with formation of smaU
nodules, disorders of feed intake and possibly emaciation
are the consequences. After feeding on wool when
'gnawing' itchy areas, bezoars may arise in the stomach
and cause clinical symptoms. The economic losses
are considerable in some areas. M. ovinus transmits
Trypanosoma melophagium(non-pathogenic).
Diagnosis. Demonstration of adults and pupae by (lj
adspection of the parted fleece. Differential diagnosis "O
0
e
should take Psoroptes infestation into account in Q.
particular. .c
t
<{
Therapy and control. Today's preferred treatment of
infected sheep is the pour-on application of pyrethroids,
e.g. deltamethrin(0.75 mg/kg b.w.). The pupae survive
the treatment, but hatching adults are affected by the
drugs if a sufficiently high concentration persists in
the fleece for at least 30-35 days (duration of the pupal
period). Elimination of M. ovinus in sheep populations
may therefore be achievable with a single treatment. An
alternative is the laborious dipping method, e.g. with
phoxim (0.05% solution). Sheep shearing reduces the
I
ked population. I II
■ Other hippoboscid species Q)
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C
Of lesser importance are the following species: H. equina �
(forest fly)(7-10 mm)(► Figure 14.64a): cosmopolitan,
adults permanently with wings, good flyers, mainly cu
C
affects horses (perineum, areas between hind legs), and ·;::
Q)
occasionally cattle; pupate in the soil. H. variegata (7-9
mm): global occurrence, especially on cattle, also on .S
equids. H. longipennis: widespread in eastern Europe and >.
0)
in the Mediterranean; major host is the dog. Lipoptena 0
0
cervi (3-5 mm): frequent occurrence in Europe and ·u5
North America; young flies carry wings which are
discarded by the females(males only occasionally) once
cu
Part Ill. Parasites and parasitoses: metazoa

a host is found; hosts: wild ruminants (on cervids often

massive infestation) elk, reindeer, rarely on cattle and
goat (ear base). L. capreoli (3-4 mm): similar to L. cervi;
frequently on goats, rare in cattle. In mammals and birds,
other species, e.g. Crataerina pallida on swifts. In poultry,
infestations with louse flies are not important; on pigeons
rarely Pseudolynchia (syn. Lynchia) maura occurs. H.
longipennis transmits Dipetalonema dracunculoides in
carnivores; louse flies are vectors of Haemoproteus spp.
and Trypanosoma spp. in birds.
Zoonotic importance. In general, louse flies remain
on their preferred hosts. However, in the absence of
blood donors, they also attack other hosts. In humans,
they can cause painful, macular, nodulous and urticaria!
bite reactions.
Selected reference
Small RW (2005) A review of Melophagus ovinus (L.), the sheep
ked. Vet Parasitol 130: 141-155.
14.3.6 Order Siphonaptera (fleas)
Disease: Causative agents of flea Infestations.
Syphon (G): tube; a- (G): without; pteron (G): wing.
Refers to the piercing-sucking mouthparts and the lack
of wings.
Summary
• Fleas are periodic haematophagous ectoparasltes
of mammals, birds and humans: they are especially
Important as parasites of dogs and cats, and also as
peats In humans and as vectors of various pathogens.
• Morphology, apeclN. About , -8 mm In length, laterally
flattened, wlngleu lnHCtl with powerful legs adapted
to Jump: plerclng-aucklng mouthparts. Important
apeclee: Ctenocephalldea fells (cat flea), C. can/a (dog
flea), Ceratophyllu1 gall/nae (chicken flea) and aome
othn. C. fells Is the moat common flea speclee In
dogs and cats.
• Ute cycle. Only adult fleas live on the host, aome
species temporarily, other e.g. C. feJia constantly (on cat,
dog, etc.); males and femal88 suck blood. Deposition
of eggs on host, development of larvae (L1 ·L3) and
pupae In the environment. Development require& high
humidity (r.h.>60%) and suitable temperatures. Ufe
cycle duration 3-4 weeks, aometlmee several months.
• Occurrence, epidemiology. Flea Infestation of dogs
and cats la common. Fleas do not survive the cold
season outdoors, but part of the pop1.1latlon can
overwinter as adults on hosts (dog, cat, wild eamlvofes)
caves). In living areas, flea development Is possl
all year round.
Pathogenesis, immunology, clinlcal signs. In
•
and cats primarily skin reactions (pruritus, erytt,i
papules) at the site of bites, and secondary dam
by scratching, biting, rubbimg. Repeated flea
can cause flea allergy dermatitis (FAE>) (papulo
dermatitis, alopecla, ete.).
• Diagnosis. Evidence of fleas or flea faee
animal and In material obtained by combing
clinical diagnosis, possibly supported by an I
skin test.
• Therapy, control. Control must be direct
adults on all contact animals and against devel
stages In the environment. Options: use of lnsectl
or Insect growth regulators on animals and ln
environment, as well as hygiene measures.
• Zoonotlo Importance, vector role. Animal fleas a
Infest humans: fleas transmit Yerslnla pastis, Ricketts/a
typh/, Dlpylldlum canlnum and other pathogens.
Morphology and species. Fleas are light to
dark brown, 1-6 mm long insects with the following
characteristics ( ► Figure 14.65 and 14.66): body
laterally flattened, covered with numerous, rear-facing
bristles; boundaries between head, thorax and abdomen
indistinct; short antennas that lie in small pits at rest;
eyes (reduced compound eyes) usually present; biting­
sucking mouthparts facing downwards; no wings,
third leg pair particularly well developed (jumping
legs); diagnostically important combs (ctenidia) on
head (genal ctenidium) and first thorax segment (=
pronotum) (pronotal ctenidium); some species without
ctenidia or only with one.
Of the approximately 2,500 flea species, representatives
from three families are of the greatest veterinary
significance ( ► Table 14.18). Of these, only a few species
are considered here.
Figure 14.65. Ctenocephalides canis, adult (length 3 mm)
(Photo: IPH).

• and as pupae In protected habitats (e.g. In buildings,

 14. Phylum Arthropoda (arthropods)

Pronotal ctenidium
Sensilium (sensory organ)
/
Antenna
Eye

Genal ctenidium
co
C:
0
Palp .c
a
(ij
Mouthparts

Figure 14.66. Scheme of an adult Ilea (Graphics: IPZ, A. Seeger: oftur Smilh 1973).

Table 14.18. Flea species (selection).

Family and lpfflH Hom (Hlectlon)1

O:occul'Tlnce
,,. T -..
..
Family Pullclda!.._ - - -- - -- ---
Ctenocephalldes felis felis (cat flea)2 cat. dog, fox, other wild carnivores, also domestic ruminants, horse, rnbbit,
·-- 0:. cosmopolitan
- -· human and other hosts; broad spectru� or >50 host specios -
Ctenocephalides canis (dog flea) dog, fox and other canlds; also cat. weasel, ermine, polecat, hare, rat and
- - --
0: cosmopolitan
-- others, human; host_spectr.u� somewhat narrower than C. f. fells - -
Archaeopsylla erinacei (hedgehog flea) hedgehog, polecat, rat, human, dog, cat
� Europe, North America - - -- -
Pu/ex irritans (human flea) human, dog, cat, pig, fox, badger, wild and domestic ruminants a1
0: cosmopolitan -0
0
Spilopsyllus cuniculi (rabbit flea) rabbit, hare, mink, rodents
a.
0: Europe, other areas
Echidnophaga gallinacea (sticktight flea) gallifonnes, other bird species, also mammals and humans
0: cosmopolitan
Xenopsylla cheopis (rat flea) brown rat. other rodents, cat, sheep, goat. human
0: cosmopolitan
Family Ceratophyllidae
Ceratophyllus gallinae (bird flea) many wild bird species, chicken, cat and others, also human; broad
0: cosmopolitan spectrum, -80 host species
Family Tungidae
Tunga penetrans (sand flea) human, dog, pig, cattle
0: Neotropical and Afrotropical regions
1 Important species in bold.
2 Four subspecies are known from C. fells: C. felis felis (cat flea) (referred to as C. felis in this text), C. felis s/rongylus and C. felis damarensis
(Africa), C. felis orientis (India to Australia).
Q)

·u
C

Life cycle. Development of fleas is associated with other hosts and feed off their blood. Blood uptake from '5
a complete metamorphosis and progresses from egg alternative hosts allows survival of the adults, but can Q)
�
over three larval stages to pupae and to adult stages have a negative effect on egg production of females. i::'
(► Figure 14.67). Fleas are periodic ectoparasites, of co
C
which most species parasitise the hosts in their nest • Life cycle of C. felis. Females of C. felis on a host ·;::
Q)
habitats (e.g. wild carnivores, hedgehogs, birds). Only (e.g. cat, dog) start 24-48 h after the first blood meal
the adults stay on the hosts, some species permanently, and mating to lay eggs (~30 eggs per day), which can C

others temporarily. In contrast, the development stages last for 50-100 days, but is usually of shorter duration. >.
0)
(larvae, pupae) live in habitats in the vicinity of the The round-oval, whitish, O.Sx0.3 mm eggs fall off 0
0
hosts (resting places, nests, etc.). Flea adults also infest the host within a few hours and are deposited in the ·u;
other than their preferred hosts. Thus, flea species of nest or bedding of their hosts or are scattered in the
co
dog, cat, hedgehog, etc., can move on to humans and environment by roaming hosts ( ► Figure 14.67). CL
 Part Ill. Parasites and parasitoses: metazoa
Pupa
enclosed in "'
cocoon
�
Free pupa
Figure 14.67. Life cycle of Ctenocephalides fells (Graphics: IPZ, S. Ehrat).
Favourable conditions for the further development are
temperatures between 25 and 30 °C at a high r.h. of
80-90%. After about I week, 1-2 mm long, whitish,
eucephalic, legless larvae (LI) with chewing mouthparts
hatch from the eggs. The larvae live mainly from faeces of
adult fleas, which drop from the host and which contain
undigested blood, and from flea eggs (cannibalism).
Since larvae are extremely sensitive to desiccation (<50%
r.h.), they are able to live only in protected microhabitats
(I)
where they develop via two moultings to L3 (length
·u
C
'6 4-5 mm). Guided by their intrinsic behaviour (positive
(I)
� geotaxis and negative phototaxis), larvae crawl to
cco
hideouts, e.g. crevices in the floor, under cushions in
C resting places of cats, or under carpets. At 24 °C and
·c
(I) high r.h., larval development is completed in 7-11 days,
� but can take five weeks or more at low temperatures.
C The mature L3 produce a 5 mm long cocoon in which
>.
0)
pupation takes place. Particles from the environment
0 adhere to the sticky surface of the cocoon, serving as
0
"ui a peculiar camouflage ( ► Figure 14.67). The pupal
co period lasts 10-14 days at 24 °C. When the fleas are fully
co
CL developed, they hatch from the pupal case but remain
I
/
-- .,,.,,,,,
/
QEgg
/
Larvae 1-3
within the cocoon. At this stage, fleas can survive up to
12 months at low temperatures and sufficient humidity.
The entire development of C. felis in homes takes 3-4
weeks, but can be shortened to 2 weeks or extended
to several months. Under favourable conditions in the
summer months, development outside of the living
area is possible in shady and moist places, e.g. kennels,
at resting places of cats outdoors or in shady and moist
spots in the soil.
The hatching of adults from cocoons is triggered by
various stimuli (pressure, vibration, high temperature).
Newly hatched adults immediately search for a host; they
orient themselves towards light and respond especially
to sudden changes in light intensity as caused by passing
hosts. Also, body heat of hosts as well as CO2 in their
breathing air are important for orientation. The jumping
ability of fleas plays an important role in infesting a host.
Adults of C. canis can jump up to ~30 cm in distance
and up to ~ 15 cm high. This jumping performance
is made possible by a special protein (resilin), which
allows a faster reaction than ordinary muscle fibres and

works even at low temperatures. Once a suitable host is
reached (cat, etc.), adults of C. felis remain there. Both
sexes of fleas suck blood; a blood meal takes 2-10 min.
• Life cycles of other flea species. Development
of C. canis is similar to C. felis; it is possible in the range
13-32 °C and 50-90% r.h. Under these conditions, unfed
adults survive for some weeks, pupae for more than 1
year. At best, the life cycle can be completed in three
weeks.
Ceratopl1yllus gallinae is considered a 'generalist: which
has been demonstrated in a large number of wild birds
and some mammals and occasionally also in humans.
The preferred hosts of this species (primary hosts) are
wild birds breeding in caves, especially great tits and blue
tits. 60-90% of nests of hole-nesting birds are infested;
abundances per nest fluctuate between 50 and > 1,000
fleas. Prevalences and abundances are lower in open
nests. In contrast to C. felis and some other species,
adults of C. gallinae live mainly in the nests and infest
the hosts for only a short time for blood feeding. The
fleas overwinter in the pupal cocoons and emerge as
temperatures rise in spring. If the nest is not populated
with birds at this time, the fleas move to the entrance
of the cave and attempt to infest birds which inspect
the nest. The fleas might also further spread along
branches towards intense light and get ready to jump
when light intensity suddenly decreases, e.g. when a bird
approaches. This mode of searching a host inevitably
provokes erroneous jumps, the fleas fall to the ground
where they might encounter animals or humans which
they attack as secondary hosts. When migrating from
nests located in houses, C. gallinae and related species
occasionally enter apartments and become a nuisance
to the inhabitants.
The development of Spilopsyllt,s cuniwli (rabbit flea)
is closely adapted to the reproductive cycle of rabbits.
Rising levels of oestrogens and corticosteroids in the
blood towards the end of pregnancy stimulate egg
production of blood sucking flea females. After birth of
the pups, the fleas migrate from their preferred feeding
area on ears to the face of the dam from where they can
easily spread to the new-borns.
Tunga penetrans (sand flea) undergoes a special
development. Males and young females of this species
stay in sandy soil. Females penetrate the skin of a host.
Within 1-2 weeks, the abdomen of the female flea swells
up, sometimes up to pea size, due to egg production.
Eggs pass through a skin opening to the outside where
they fall to the ground and undergo a development
which basically corresponds to other fleas.
Occurrence and epidemiology. Information
on the geographical distribution is given in ► Table
14.18. Prevalences of flea infestations in dogs and cats
depend on the examined animal groups, the housing
14. Phylum Arthropoda (arthropods)
conditions and other factors, and they vary greatly,
ranging from < 1% to >90%. In many countries of the
northern hemisphere C. felis is the most common flea
species on cats and dogs, followed by C. canis on dogs
which is less common on cats. Dogs and cats can also be
carriers of other flea species. According to an extensive
Q)
study (2003/2004) of 1,922 dogs and 1,838 cats from 0..
three regions in Germany, 5.1% of dogs and 14.3% of cu
C
cats were infested with fleas on an annual average. The 0
..c
flea population on dogs consisted of C. felis (73.2%), C. 0..
u5
canis (17.6%), A. erinacei (4.3%), Pu/ex irritans (3.5%),
C. gallinae (0.4%), and other species (1%). In cats, C.
felis (89.8%), C. canis (7.3%) and A. erinacei (1.1 %) were
also the most common species; in addition S. cuniculi
(1.8%) was identified. Occasionally, flea infestations
caused by C. gallinae affect chickens and pigeons. Flea
infestations of other domestic species are rare. On the
other hand, infestation of farm animals (sheep, goats,
cattle) with the subspecies C. felis strongylus ( ► Table
14.18) poses a significant problem in Africa (e.g. Libya)
and in the Middle East. Dairy goats, sheep, cattle and
pigs in Greece were exclusively infested by P. irritans.
• Population dynamics and overwintering.
During the year, the populations of C. felis are subject
to fluctuations, with the highest abundances occurring
in the warm season. Fleas cannot survive the cold season
outdoors in northern areas, since all stages are very
sensitive to freezing temperatures. However, part of the
flea population can survive the winter, either as adults co
on their hosts (3-4 months) or as pupae in protected -0
0
microhabitats (e.g. in buildings, especially in residential a.
areas, in caves of wild mammals, e.g. foxholes). .c
t::
<(
• New or re-infestations of dogs or cats with C.
jelis or C. canis occur by newly hatched fleas f rom the
environment or, rarely, by adult fleas after contact with
infested conspecifics or wild carnivores. C. felis and C.
canis develop in homes, e.g. in resting places of animals,
under carpets or in dark, protected corners. In summer,
a development is possible in kennels, hunting cabins,
arbours, etc., as well as in stables or in shaded resting
places outdoors. Therefore, these 'breeding places' also
need to be considered for control measures.
Pathogenesis and immunology. Fleas are
nuisance pests whose bites cause itching, erythema
and papules in the skin. The reactions of the host to
flea bites are due to salivary components of the fleas.
Histamine and histamine-like substances are the cause
of the erythematous, oedematous areas that develop
within a few minutes around the fine haemorrhage
at the biting site. Different enzymes with proteolytic,
cytolytic and anticoagulant properties are responsible for
the lysis of tissues, the inhibition of blood coagulation
and inflammatory skin reactions. Higher molecular
weight antigens (>20 kDa) and a low molecular weight
hapten (in combination with dermal collagen) can cause
allergic reactions (immediate-type and delayed type).
 Part Ill. Parasites and parasitoses: metazoa
Animals with flea-bite allergy have increased levels
of circulating antibodies directed against flea antigens
(IgE, IgG), however, the allergy is rarely a pure type I
but rather a mixed type with hypersensitivity of the
delayed type(type IV). A few fleas can trigger an allergic
reaction; the allergens of different flea species cross­
react. Other possible pathogenic factors are blood loss
and presumably also inhibition of erythropoiesis in case
of mass infestation with fleas. Female fleas take each day
on average about 14 µl blood.
Mortality is significantly increased in young animals of
singing birds infested with C. gallinae. Eggs of tits which
were exposed to flea infestation showed an increased
level of anti-flea antibodies (IgG). Offspring of flea­
exposed mothers were less affected in their development
by fleas than progeny of unexposed mothers(presumably
by IgG transfer in the egg).
Clinical signs. Flea infestations primarily cause local
bite reactions (erythema, papules) and itching as well
as secondary skin damages due to self-traumatisation
(wounds by scratching, rubbing, biting, possibly
secondary bacterial infections). Fleas are capillary
feeders and repeatedly pierce the skin in search of
superficial blood capillaries. Repeated and intermittent
flea-bite exposure of dogs and cats may cause flea-bite
allergy and flea-bite allergy dermatitis(FAD). FAD is one
of the most common skin diseases in dogs and cats. It
occurs in all races and both sexes and is most prevalent
in the age group 3-6 years. Symptoms in the acute phase
include itching, erythema and papules, in the chronic
phase in the dog papulo-crusty, sometimes purulent
dermatitis, bacterial folliculilis, secondary seborrhoea
and alopecia, in cats miliary dermatitis with alopecia.
Enabling factors for the development of FAD include
among others atopy, other diseases, first infestation with
fleas at an older age and intermittent flea infestation.
Lasting flea infestations often induce a tolerance, so
symptoms are absent or attenuated.
Diagnosis. Diagnosis of tlea Infestation In animals
is based on clinical symptoms, the detection of adult
fleas and flea faeces when inspecting the fur, and the
investigation(hand magnifiers) of material which has
been combed or brushed out of the coat. The reddish
(l)
brown particles of flea faeces are often easier to find than
·o
C:
'6 the parasites. lf flea faeces are wetted with a drop of water
�
(l)
on filter paper, a red-brown discoloration appears due to
� the release of haemoglobin. Eggs or larvae adhering to the
co coat can quite frequently be found, especially in cats. In
C:
·;::
(l) case of a negative result, the environment(resting places,
bedding, carpets, upholstered furniture, etc.) should also
,!; be investigated for the presence of developmental stages
>,
0) of fleas (attach a fine mesh gauze behind the suction
0 nozzle of a vacuum cleaner to collect these flea stages).
0
·u5 1n case of an unclear origin of flea pests in apartments or
co houses, the identification of the flea species is important
co
0... because not only dogs and cats are suitable sources of
nuisances, but also other species, e.g. hedgehogs and
song birds. Species identification can be achieved based
on different morphological characteristics (including
ctenidia on head and bristles on legs)( ► Figure 14.68).
C. canis (dog flea) and C. felis both have genal and
protonal ctenidia. Although these species have subtle
differences on their genal ctenidium, differentiation can
be more easily carried out by structures on the dorsal
margin of the tibia( ► Figure 14.68): C. canis has 8 and
C. felis 6 bristle-bearing notches. C. gallinae has only a
pronotal ctenidium; the genal ctenidium of A. erinacei
contains only 3 spines and the protonal ctenidium only
one( ► Figure 14.68).
Diagnosis of flea-bite allergy dermatitis can be difficult
despite clear clinical pictures, as other allergies of
various origins (feed, medicines, other arthropods),
mange and other dermatoses must be considered in
the differential diagnosis. Other diagnostic possibilities
are intracutaneous tests with flea antigens and other
allergens as well as the detection of circulating, flea
antigen-specific IgE. However, results of such tests are
highly variable and their explanatory power dependent
on the quality of the antigen.
Therapy and control. Fleas of dogs and cats can be
controlled on host animals by the use of insecticides
or insect growth regulators (IGR) ► Table 19.16. For
control of flea stages in the environment, the same
substance groups are used and additional hygiene
measures implemented( ► p. 606). FAD requires special
treatment.
Zoonotic importance and vector role. Fleas of
dogs, cats, hedgehogs, other mammals and birds can also
affect humans and suck blood. The changes(punctate
haemorrhage, erythema, papule, pustule) caused by
flea bites almost always occur multiple-fold(rows of
flea bites}, especially on the extremities, but also on the
face, neck, neck, hips and shoulders.
Fleas are vectors of various infectious agents, as the
following examples demonstrate: Xenopsylla cheopis
(rat flea) and related species: Yersinia pestis(plague) and
Rickettsia typhi(humans: murine typhus}; Ctenocepha­
lides fe/is: Rickettsia felis(humans: fever with maculo­
papular skin lesions) and Bartonella henselae(humans:
cat scratch disease). Evidence of other Bartonella species
in rodent or cat fleas indicates their vector potential.
Feline mycoplasma (Mycoplasma haemofelis, Candidatus
M. haemominutum, M. turicenis) have been detected in
C. felis, but it is still unclear whether fleas are vectors of
these pathogens(see also ticks, ► p. 411 ff). C. felis and
C. canis are intermediate hosts of Dipylidium caninum,
Hymenolepis nana, H. diminuta and some other
Hymenolepis species as well as of Acanthocheilonema
reconditum.
 14. Phylum Arthropoda (arthropods)

a b
1
2
3
4
5 Cl:l
6
/' � 7
Q)

8
Ctenocephalides canis C
0

4
/' 9/�
Ctenocephalldes felis

Ceratophyllus gal/inae Archaeopsylla erinace/

Figure 14.68. Notes on the differentiation of flea species: (a) head structure of flea species; (b) tibia structure of C. canis and
C. felis (for explanations, see text; for details, see specialised literature) (Graphics: IPZ, A. Seeger).

Selected references
Beck W, Boch K, Mackensen H, W iegand B, Pfister K
(2006) Qualitative and quantitative observations on the flea
population dynamics of dogs and cats in several aeras of
Germany. Vet Parasitol 137: 130-136.
Bruet V, Bourdeau PJ, Roussel A, Imparato L, Desfontis JC
(2012) Characterization of pruritus in canine atopic dermatitis,
flea bite hypersensitivity and flea infestation and Its role in
diagnosis. Vet Dermatol 23:487-e493.
Coles TB, Dryden MW (2014) lnsecticide/acaricide resistance In
fleas and ticks infesting dogs and cats. Parasit Vectors 7: 8.
Eisen RJ, Gage KL (2012) Transmission of flea-borne zoonotic
agents. Annu Rev Entomol 57: 61-82.
ESCCAP (2015) Control of ectoparasites in dogs and cats.
Available at: www.esccap.org.
Gillespie JJ, Ammer man NC, Beier-Sexton M, Sobral
BS, Azad AF (2008) Louse- and flea-borne rickettsioses:
Lam A, Yu A (2009) Overview of flea allergy dermatitis. Compend Cl:l
Conlin Educ Pract Vet 31: E1-10. -0
0
Muller GC, Dryden MW, Revay EE, Kravchenko VD, Broce Q.
0
AB, Hampton K, Junnila A, Schlein Y (2011) Understanding .c
t
attraction stimuli of the cat flea, Ctenocephalides felis, in non­ <(
chemical control methods. Med Vet Entomol 25: 413-420.
Otranto D, Dantas-Torres F (2010) Canine and feline vector­
borne diseases in Italy: current situation and perspectives.
Parasit Vectors 3: 2.
Pampigllone S, Fioravanti ML, Gustinelli A, Onore G,
Mantovani B, Luchetti A, Trentini M (2009) Sand flea
(Tunga spp.) infections in humans and domestic animals:
state of the art. Med Vet Entomol 23: 172-186.
Rust MK (2005) Advances In the control of Ctenocephalides felis
(cat flea) on cats and dogs. Trends Parasitol 21: 232-236.
Q)
·o
C

biological and genomic analyses. Vet Res 2008 40: 12.

Q)
Halos L, Beugnet F, Cardoso L, Farkas R, Franc M, Guillot
J, Pfister K, Wall R (2014) Flea control failure? Myths and
Cl:l
realities. Trends Parasitol 30: 228-233. C
·;:::
Hornok S, Meli ML, Perreten A, Farkas R, Willi B, Beugnet Q)

F, Lutz H, Hofmann-Lehmann R (2010) Molecular

C
investigation of hard ticks (Acari: lxodidae) and fleas
>,
(Siphonaptera: Pulicidae) as potential vectors of rickettsial 0,
0
and mycoplasmal agents. Vet Microbiol 140: 98-104. 0
Kramer F, Mencke N (2001) Flea biology and control. Berlin, ·u5
Cl:l
Germany: Springer; ISBN 3-540-41776-1. Cl:l
0...
 15. Zoonoses and parasites in food
15.1 Zoonoses
Zoon (G): animal, living being; nosos (G): disease.
Definition and nomenclature. WHO defines
zoonoses as diseases and infections [the agents of]
which are naturally transmitted between vertebrate
animals and humans. The agents can be transmitted
directly or indirectly by vectors. It should be noted
that this definition refers only to 'vertebrate animals'
and not to animals in general (e.g. transmission of a
human-specific pathogen by an insect from one person
to another is not a zoonotic transmission, as a vertebrate
animal is not involved). Zoonoses can be divided into
different groups. Thus, the direction of transmission
(humans - other vertebrates or other vertebrates -
humans) is reflected in the terms anthropozoonosis
and zooanthroponosis, respectively. The transmission
routes are indicated inter alia in terms such as food­
borne, arthropod-borne, fish-borne, soil-borne
or w ater-borne zoonoses. In this book we refer
predominantly to the comprehensive term 'zoonosis'.
Some infections or infestations, usually dealt with in
the context of zoonoses, do not strictly fulfil the criteria
of the WHO definition, for example various forms
of myiases in humans and animals. For such cases a
somewhat wider definition is applicable, designating
zoonoses as infectious diseases which may occur both
in vertebrate animals and humans.
Significance of zoonoses. Zoonoses are regarded
as a global threat to human health. Approximately 60%
of human pathogens are zoonotic, including viruses,
bacteria, fungi and parasites (WHO). Of the 200
zoonoses described, at least 35% are caused by parasites.
In addition to their role as causative agents of zoonotic
diseases, parasites - especially arthropods - are of great
importance as vectors of zoonotic pathogens. A selection
of parasitic zoonoses is listed in ► Tables 15.1-15.3.
Socio-economic impact. Certain zoonoses have
Q)
C major socio-economic effects, due to impairment of
·c3
human and animal health, mortality, and the resulting
Q)
�
financial burden. In 2006, the WHO established a
� 'Foodborne Disease Burden Epidemiology Reference
(ll
C Group' (FERG) that is concerned with estimating the
·.::
Q) burden of zoonoses by evaluating various criteria and
j expressing the results in DALY (Disabi.lity Adjusted
Life Year) units. These units include the number of
C
>,
CJ)
years of human life lost due to premature mortality
0
0
·u;
(ll
(ll
and the years lived with a certain level of disability,
related to specific periods and populations. One DALY
corresponds to 1 year of healthy life lost. According to a
recent publication of the FERG (Torgerson et al., 2014),
the global burden of human congenital toxoplasmosis is
estimated at 190,000 new cases each year, resulting in 1.2
mi1lion DALYs. Foodborne trematode infections, due to
Clonorchis, Opisthorchis, Fasciola and other genera, are
responsible for approximately 665,000 DALY s a year. The
number of new human cases of alveolar echinococciosis,
caused by Echinococcus multilocularis, is estimated at
18,000 annually (more than 90% occurring in China)
and represents 660,000 DAY Ls. These estimates show
that some parasitic zoonoses may have enormous social
and financial consequences. On the other hand, the
burden of Trichinellosis is regarded as relatively low, but
EU countries still spend large amounts of money every
year on testing slaughtered pigs for Trichinella infections
(estimates between€ 220 and€ 570 million).
Epidemiological aspects and risk factors.
In previous periods, the significance of zoonoses
was widely underestimated, and some of them were
neglected. Recently, the WHO has included in a list
of 17 'neglected tropical diseases' the following 10
parasitic zoonoses (diseases or disease complexes; note:
not all of them are typical tropical diseases): Chagas
disease, human African trypanosomosis, leishmaniosis,
schistosomosis, food-borne trematodoses, cysticercosis/
taeniosis, echinococcosis, dracunculosis, lymphatic
filariosis, and soil-transmitted helminthoses. There is
increasing awareness that several epidemiological factors
may not only promote the persistence and spread of
zoonoses but also increase infection risks. Such factors
include the spread of pathogens and vectors by global
trade and travelling, urbanisation with invasion of cities
by wild animals (e.g. foxes), close contact between
humans and domestic animals (potential reservoirs of
pathogens), changing eating habits, and climate change.
It is evident that prevention and control of zoonoses
requires a multidisciplinary approach in the sense of the
'one health concept', involving veterinary and medical
specialists, epidemiologists, biologists, etc.
Table 15.1 to 15.3 contain an overview of parasitic
zoonoses, but do not claim to be comprehensive. For
more detailed information on the individual zoonoses
and zoonotic parasite species the reader is referred to
parts II and III ( ► p. 44 ff, ► p. 164 ff).
 15. Zoonoses and pmas1tes 1n food

Table 15.1. Zoonoses (selection) caused by Protozoa and M1crospondia (1n alphabetical order).
- - - - - - - � 1
--
Disease in humans Causative agent Principal Vectors I Parasite stage Transmission

I
D: distribution vertebrate transmitted to route to
animals involved1
- - humans humans

Protozoa -
Human African Trypanosoma brucei (pig, cattle, dog, Glossina spp. metacyclic tsetse fly bite
trypanosomosis gambiense some antelope form
(sleeping sickness) D: Sub-Saharan Africa: species)
West Africa, regions in
central Africa
T. brucei rhodeslense domestic Glossina spp. metacyclic tsetse fly bite
D: Sub-Saharan Africa: ruminants, several form
East Africa, regions in antelope species,
central Africa warthog, dog, lion,
hyena, etc.
American Trypanosoma cruz/ dog, cat, Guinea Trlatomlnae, metacyclic deposition of
trypanosomosis D: Latin America pig, opossum, family Reduvlidae form vector faeces
(Chagas disease) armadillo, etc. on skin
Babesioses B. dlvergens Cattle (wild lxodes spp. sporozoite tick bite
D: Europe ruminants)
B. venatorum2 roe deer lxodes rlclnus sporozoite tick bite
D: Europe
B. microti complex rodents lxodes spp. sporozoite tick bite
D: North America, Asia,
Europe
B. duncani unknown unknown the parasite has been identified in
D: North America humans after blood transfusion.
Natural transmission most likely
by tick bite
Balantidiosis Balantidium coli pigs, monkeys - cyst (faeces) per os
D: worldwide
Cryptosporidiosis Cryptosporidium spp. cattle, small - oocyst (faeces) per os
D: worldwide ruminants, (dog,
cat, birds)
Entamoebosis Entamoeba histolytica monkeys, (dog) - cyst (faeces) per os
D: Tropics, subtropics
Giardiosis Giardia duodena/is cattle, sheep, dog - cyst (faeces) per os
(various genotypes)
D: worldwide
Leishmanioses
• Visceral L. Leishmania infantum dog, wild Phlebotomes: promastigote Phlebotomus
D: southern Europe, carnivores, (cat), Phlebotomus bite
Mediterranean, Middle East, hare, rat spp.
Central Asia, China
Leishmania infantum (syn. dog, fox, opossum Phlebotomes: promastigote Lutzomyia
L. chagas1) Lutzomyia spp. bite
D: Central and South
America
L. donovani dog, (felids) Phlebotomes promastigote Phlebotomus
D: Asia, East Africa bite
• Cutaneous L. L. major rodents Phlebotomes promastigote Phlebotomus
D: North Africa, Sahel zone, bite
Middle East, western Asia
• Mucocutaneous L. L. mexicana complex rodents Phlebotomes promastigote Lutzomyia
D: southern USA, Central bite
America, northern South
America
L. peruviana dog Phlebotomes promastigote Lutzomyia
D: Peru bite
Malaria3 Plasmodium know/esi Macaques Anopheles spp. sporozoite mosquito bite
D: South East Asia
 Part IV. Zoonoses and parasites in food

Table 15.1. Contin ued.

Principal Vectors Parasite stage Transmission

vertebrate transmitted to route to
animais involved1 humans humans

Sarcocystiosis
• Intestinal S. Sarcocystis hominis cattle cyst peros
D: worldwide (musculature)
S. suihominis pig cyst peros
D: worldwide (musculature)
• Muscular S. S. nesbitti snakes sporocyst peros
D: South East Asia
Toxoplasmosis Toxoplasma gondii cat oocyst (faeces) peros
D: worldwide sheep, goat, pig, cyst peros
(cattle), birds, etc. (musculature)
Microsporidia
Encephalitozoonosis Encephalitozoon cunicu/1 rabbit, dog, spore peros
(various genotypes) monkeys
D: worldwide
E. intestinalis ruminants, pig, spore peros
D: worldwide dog, crow
E. hellem passerine birds spore peros
D: worldwide
1 Vertebrate animals as director indirect inf ection sources o
f r humans; animals of ow
l signif icance in parenthesis.
2 Formerly named Babesia EU-1.
3 Other Plasmodium species with zoonotic potential: P. simium and P. eylesl o ( ccasional natural transmission o
t humans); P. brasilianum,
P. cynomo/gi, P. inui, P. schwetzi (accidental and induced human infections).

Table 15.2. Zoonoses (selection) caused by heiminths (in alphabeticalorder).

Ro.ute of
hGSts� transmitted to transmission
IH: lntennedlate hosts2 humans to humans
PH: �ratenle hosts (I,,: larva)'

Trematoda
Alariosis A/aria spp. DH: wild canidae mesocercaria (in wild peros
D: North America, Europe IH 1: snails, 2: frogs boar meat)
Cer cariaJ dermatitis Bl/harzlella. Trlchobllharzla, DH: water birds cercaria active skin
Gigantobllharzla spp. IH: water snails invasion
D: worldwide
Schistosoma spindale and DH: mammals cercaria active skin
other species IH: freshwater snails invasion
D: Tropics
Clonorchiosis Clonorchis sinensis DH: dog, cat, pig, marten metacercaria (in fish) peros
Q) D: Asia (RU, China, Korea, IH 1: freshwater snails, 2:
C
·o Vietnam, etc.) freshwater fish
Dicrocoeliosis Dicrocoelium dendriticum DH: ruminants metacercaria (in ants) per os
Q)
� D: Europe, America, North IH 1: terrestrial snails, 2: ants
c:-
c,:l
Africa, Asia
D. hospes DH: ruminants metacercaria (in ants) peros
·c D: Sub-Saharan Africa IH 1: terrestrial snails, 2: ants
....,
Q)
Fascioo
l psiosis Fasciolopsis buski DH: pig, dog metacercaria (on peros
D: South East Asia, Japan IH: freshwater snails water plants)
.!;
>- Fascioo
l sis Fasciola hepatics DH: ruminants metacercaria o
( n peros.
0)
D: worldwide IH: freshwater snails plants)
...., F. gigantica DH: ruminants metacercaria o
( n peros
·u5 D: Subtropic, tropics IH: freshwater snails plants)
 15. Zoonoses ancJ parasites in food

Table 15.2. Continued.

- -- -- - -- - - - - ·- - - -- - --
f
Disease in humans Causative agent DH: Vertebrate definitive Parasite stage Route of
I transmitted to I
D: distribution hosts 1 transmission
IH: intermediate hosts2 · humans to humans

Metagonimosis3 Metagonimus yokogawai

PH: paratenic hosts
--- -- -
DH: dog. cat, fox. pig
.
· (L: larva)
- --
metacercaria (in fish) per os
-
D: Asia, Europe IH 1: freshwater snails. 2:
freshwater fish
Opisthorchiosis Opisthorchis felineus DH: cat, dog, fox, pig metacercaria (in fish) per os
D: Europe (Baltic states, IH 1: freshwater snails. 2:
northern PL, DE, RU), Asia freshwater fish
0. viverrlni DH: fellds, canids metacercaria (in fish) per os
D: South East Asia IH 1: freshwater snails, 2: fish
Paragonimosis Paragon/mus spp. DH: Dog, cat, fox, mink, etc. metacercaria (in per os
D: Asia, Africa, America IH: 1. freshwater snails, 2. crabs, crayfish)
crabs, crayfish
Schistosomosis Schistosoma japon/cum4 DH: cattle, buffalo, pig, dog, cercaria active skin
D: East Asia rodents, etc. invasion
IH: freshwater snails
Schistosoma mansoni DH: non-human primates, cercaria active skin
D: Africa, Middle East, South occasionally rodents, dogs, Invasion
America, Caribbean etc.
IH: freshwater snails
Schistosoma haematobium DH: occasionally non-human cercaria active skin
D: Africa, Middle East, primates, pigs, rodents, etc. invasion
Corsica
Cestoda
Coenurosis Taenia multiceps DH: dog, fox, other canids egg with oncosphere per os
D: worldwide IH: ruminants
T. serialis DH: fox, wolf (dog, cat) egg with oncosphere per os
D: worldwide IH: lagomorphs
Cysticercosis T. solium DH: human egg with oncosphere per os
D: Latin America, Asia, USA, IH: pig
Africa, (East & South Europe)
T. crassiceps DH: fox, other wild carnivores egg with oncosphere per os
D: northern Eurasia IH: rodents
T. martis DH: mustelids, wild cat egg with oncosphere per os
D: Europe IH: rodents
Diphyllobothriosis Diphyl/obothrium /atum DH: fox, dog, cat, etc. plerocercoid (in fish) per os
D: northern Eurasia, Europe, IH 1: copepods, 2: freshwater
North America fish
D. pacificum DH: seal, sea-lion plerocercoid (in fish) per os
D: American Pacific coast, IH 1: copepods, 2: marine fish
Japan
Dipylidiosis Dipylidium caninum DH: dog, other canids, cat cysticercoid (in fleas) per os
D: worldwide IH: fleas
Echinococcosis
• Cystic E. Echinococcus granulosus DH: dog, other canids egg with oncosphere per os Q)
C
s.l. IH: ungulates ·5
D: worldwide '6
Q)
• Alveolar E. E. multilocularis DH: fox species, other wild egg with oncosphere per os
D: North America, Eurasia canids, dog, (cat) C"
IH: rodents cu
C
·c
• Unicystic E. E. oligarthrus DH: wild felids egg with oncosphere per os Q)
D: Central & South America IH: agouti, paca, opossum
• Polcystic E. E. vogeli DH: bush dog, (domestic dog) egg with oncosphere per os _£;
D: Central & South America IH: paca, agouti >,
0)
Hymenolepiosis Hymeno/epis nana DH: rodents egg with oncosphere per os 0
0
D: worldwide
·u5
H. diminuta DH: rodents cysticercoid (in per os
D: worldwide IH: beetles, fleas insects) cu
Cl..
 Part IV. Zoonoses and parasites in food

Table 15.2. Continued.

�se in humans Causative agent DH: Vertebrate definitive Parasite stage I Route of
D: distribution hosts 1 transmitted to transmission
IH: intermediate hosts2 humans to humans
PH: paratenic hosts (L: larva)

Sparganosis Spirometra spp. DH: cat, dog, other carnivores plerocercoid (in 2nd IH per os
D: Europe, Asia, North IH 1: copepods, 2: frogs, or PH)
America, Australia reptiles, rodents
PH: wild pigs
Taeniosis
•Saginata T. Taenia saginata DH: human cysticercus (in per os
D: worldwide IH: cattle, buffalo musculature)
•SoliumT. T. solium DH: human cysticercus (in per os.
D: Latin America, Asia, USA, IH: pig musculature)
Africa, (East and South
Europe)
•Asiatica T. T. asiatica DH: human cysticercus (e.g. in per os
D: East and South East Asia IH: domestic & wild pig pig liver)
Nematoda
Ancylostomosis
•Intestinal A Ancylostoma caninum DH: dog, other canids L3 active skin
D: worldwide invasion
A. ceylanicum DH: dog, dingo L3 active skin
D: Asia, Australia invasion
Angiostrongylosis
•Cerebral A Angiostrongylus DH: rats L3 (in IH or PH) per os
cantonensis IH: snails and slugs
D: Asia, Australia, Pacific PH: shrimps, crabs, frogs, etc.
region, USA
•Intestinal A. A. costaricensis DH: cotton rat L3 (in IH) per os
D: Latin America, Africa IH: terrestrial snails
Anisakidos is Anisakis (A), Contracaecum DH: A: dolphins, whales, C: L3 �n fish) peros
(C) Poffocaecum (PO) seals, PO: birds, PS: seals,
Pseudotterranova (PS) sea-lions, walruses
species IH: crustaceans
D: Atlantic Ocean, North Sea, PH: marine fish
Baltic Sea. Pacific Ocean.
etc.
Ascariosis Ascaris suum DH: pig L3 (in egg) per os
D: worldwide
Capillariosls
•Hepatic C. Cspillaris hepatics DH: rodents. other mammals L1 (in egg) per os
D: worldwide
•Intestinal C. C. phllipplnensls DH: fish-eating birds Infect ive larva (in fish) per os
D: South East Asia, Pacific IH: freshwater and brackish
region water fish
Filarioses
Q)
T5
C •Lymphatic Brugia malayi, B. timori, B. I DH: cat, dog, wild carnivores L3 mosquito brte
filarioses pahangi IH: Culicidae
'6 D: South and East Asia
Q)

•Oirofilarioses5 Dirofilaria immitis DH: dog, cat. fox. other wild L3 mosquito bite
co D: Subtropics. Tropics, carnivores
C southern Europe IH: Culicidae
·;::
Q)
D. repens DH: dog. cat, fox, other wild L3 mosquito brte
D: Africa, Asia. Europe carnivores
C IH: Culicidae
>­
O'l Onchocercosis Onchocerca lupi DH: dog, cat L3 insect bite
0 D: southern and Central IH: Simulfidae (suspected)
·en Europe, USA

Ctl
a.
 15. Zoonoses and parasites in food

Table 15.2. Continued.

DH: Vertebrate deflnlth,e Par-aslte mage

hosts1 transmitted to
IH: Intermediate hoeta2 human•
PH: paratenlc hoets (L: larva)

Larva migrans Ancylostoma, Uncinaria, DH: dog, cat and other hosts L3 active skin
cutanea Strongyloides spp. of the involved species invasion
D: worldwide -�
Q)
>
Larva migrans Toxocara canis, T. cati, DH: dog, fox (T. canis), cat (T. L3 (in egg) per os
visceralis Baylisascaris procyonis cat,), raccoon (8. procyonis)
D: worldwide
Strongyloidosis Strongyloides stercoralis DH: primates, dog L3 active skin
D: mainly tropics & invasion
subtropics
Thelaziosis Thelazia callipaeda DH: dog, cat, wild carnivores L3 deposition of
D: Europe, Asia (fox, wolf, wild cat, etc.) L3 by vectors
IH: Phortica spp. to the eye
(Drosophilldae)
Trichinellosis Trichina/la splralls, T. britovl DH/IH: pig, wild boar, horse, L 1 Qn musculature) peros
& other species dog, fox, bear, etc.
D: worldwide
Trichostrongylidosis Trichostrongylus DH: ruminants L3 peros
colubriformis & other
trichostrongylid species
D: worldwide (regionally)
Acanthocephala
Moniliformiosis Moniliformis moniliformis DH: rodents larva Qn IH) per os
D: worldwide IH: beetles, cockroaches
Macracantho­ Macracanthorhynchus DH: pig larva Qn IH) peros
rhynchosis hlrudinaceus IH: beetles, cockroaches
D: Asia, southern& eastern
Europe
1 Vertebrates as direct or indirect infection sources for humans and other vertebrates.
2 1 : 1 st intermediate host, 2: 2nd intermediate host.
3 Example for a group of many other genera and species with similar life cycles.
4 The S. japan/cum species group Includes other zoonotic species, such as S. sli1ensium and S. ovuncatum. For other zoonotic schistosomes,
see cercarial dermatitis above.
5 Other zoonotic 0/rofitarla species: 0. lenuls, 0. ursi, 0. subdermata, etc.
 Part IV. Zoonoses and parasites in food

Table 15.3. Zoonoses (selection) caused by Arthropoda and Pentastomida (in alphabetical order).
•·
·- ,_,,., �;;;,,t· , .•rJ•.
Causative agent 1•Principal vertebrate animals Parasite stage Transmission route to
D: distribution lnvolved1 transmitted to humans
� humans2
(L: larva)

Flea Ctenocephafides fefis, cat, dog, hedgehog, other adult fleas skin infestation by fleas
dermatoses C. canis, Archaeopsyffa mammals from indoor or outdoor
erinacei, other species environments or rarely by
from mammals close contact with animals
D: worldwide
Ceratophyffus gaffinae poultry and many species of adult fleas skin infestation by fleas
D: worldwide wild birds from stables, outdoor
environments or invasion
of homes by fleas from
birds' nests
Mite Cheyfetieffa spp. dog, cat, rabbit adult and juvenile skin infestation by mites
dermatoses D: worldwide stages through close contact
with animals
Dermanyssus gaffinae chicken, pigeons, wild birds adult and nymph skin infestation by mites
D: worldwide from the environment,
adult and nymph predominantly stables
Ornithonyssus syfvlarum chicken, pigeons, wild birds
D: North America, Australia,
Europe
0. bacoti rat, hamster, other rodents, adult and nymph skin infestation by mites
D: worldwide dog, cat from the environment,
especially in homes and
pet stores
Sarcoptes spp. dog, pig, cattle, camel, etc. adult and juvenile skin infestation by mites
D: worldwide stages through close contact
cat adult and juvenile with animals
Notoedres cati
D: worldwide stages
Otodectes cynotis cat, dog adult and juvenile
D: worldwide stages
Trixacarus cavlae guinea pig adult and juvenile
D: worldwide stages
Myiases Various species sheep, etc., serve as reservoir egg deposition of eggs
of Calliphoridae, hosts for certain fly species: by female flies to skin
Sarcophagldae, Muscidae other fly species without folds, wounds, mucous
D: worldwide particular reservoirs membranes, body
openings
Oestrus ovls sheep, goat L1 deposition of L1 by flies
D: worldwide onto eye, nose
Rhinoestrus purpureus squids L1
D: worldwide
Gasterophlfus spp. equlds egg deposition of eggs onto
D: worldwide the skin
Hypoderma spp. cattle, other ruminants egg deposition of eggs onto
D: Central and eastern the skin, eyes
Europe
(I)
C Dermatobia hominis cattle, sheep, dog, etc. L1 deposition of eggs onto
T.i D: Latin America
'6 the skin by other diptera
(I) (transport hosts)
Coch/iomyia hominivorax cattle, sheep, dog, etc. egg deposition of eggs onto
co D: USA, Latin America wounds
C
·;::: Tungaosis Tunga penetrans dog, pig, rodents, other female flea penetration of female fleas
D: Tropical America, Africa, vertebrates into the skin
C
India, China l
Pentastomida
>- •
(
0)
0 Armilliferosis Armiffifer spp. snakes, lizards egg per os
0 D: Tropical Africa, South
"iii East Asia
co )
co Unguatulosis Unguatufa serrata dog, wild canids egg or nymph per os
a..
J
D: worldwide (organs of
ruminants, etc.)

Selected references a:::::====::::.-•
Aspock H (ed.) (2010) Krank durch Arthropoden. Denisia 30;
ISSN 1608-8700.
Bauerfeind R, Von Graevenitz A, Kimmig P, Schiefer HG,
Schwarz T, Slenczka W, Zahner H (2016) Zoonoses.
Infectious diseases transmittable from animals to humans. 4th
ed. Washington DC: ASM Press; ISBN 978-1-55581-925-5.
Chai JY, Murrell D, Ly mbery AJ (2005) Fish-borne parasitic
zoonoses: status and issues. Int J Parasitol 35: 1233-1254.
Colwell DD, Dantas-Torres F, Otranto D (2011) Vector­
borne parasitic zoonoses: Emerging scenarios and new
perspectives. Vet Parasitol 182: 14-21.
0eplazes P, Van Knapen F, Schwe iger A, Overgaauw
PAM (2011) Role of pet dogs and cats in the transmission
of helminthic zoonoses in Europe, with a focus on
echinococcosis and toxocarosis. Vet Parasitol 182: 41-53.
Kampen H, Werner D (2011) Arthropod vectors and their
growing importance in Europe. In: Mehlhorn H (ed.) Progress
in Parasitology. Parasitol Res Monographs 2. Heidelberg,
Germany: Springer, pp. 259-282; ISBN 978-3-642-21395-3.
Palmer SR, Lord Sou Isby, Torgerson PR, Brown DWG (eds.)
(2011) Oxford textbook of zoonoses. 2nd ed. Oxford, UK:
Oxford University Press; ISBN 978-0-19-857002-8.
Ramasamy R (2014) Zoonotic malaria - global overview and
research and policy needs. Front Public Health 2: 123.
T hompson RC (2013) Parasite zoonoses and wildlife: One
Health, spillover and human activity. Int J Parasitol 43:
1079-1088.
Torgerson PR, Macpherson CN (2011) The socioeconomic
burden of parasitic zoonoses: global trends. Vet Parasitol
182: 79-95.
Torgerson PR, De Silva NR, Favre EM, Kasuga F, Rokni MB,
Zhou XN, Sripa B, Gargouri N, Willingham AL, Stein C
(2014) The global burden of foodborne parasitic diseases:
an update. Trends Parasitol 30: 20-26.
Zinsstag J, Meisser A, Schelling E, Bonfoh B, Tanner M
(2012) From 'two medicines' to 'One Health' and beyond.
Onderstepoort J Vet Res. 79: 492.
15.2 Parasites in food
Parasites may occur in food of animal origin and have
to be regarded as potential risk and adverse factors for
the following reasons:
• Mammals, birds, reptiles, fish, crustaceans and
molluscs, serving as food sources for humans, can
contain pathogenic parasite stages. Transmission
of pathogens through the food chain to humans or
other susceptible hosts must be avoided.
• Parasites in food are disgusting.
• Parasites can impair the quality of animal carcasses
and organs so that they are unsuitable for human
consumption.
15. Zoonoses and parasites in food
• During production or storage, food may be
contaminated by eggs and larvae of blow and flesh
flies or other arthropods (e.g. mites, cockroaches,
beetles).
• Animal products (meat, organs, milk, eggs) may
contain residues of antiparasitic agents above the
threshold value if the compulsory withdrawal
periods are disregarded. This aspect is discussed in
Chapter 17 ( ► p. 556).
• Through contaminated drinking water parasite
stages can be transmitted to humans or animals,
e.g., Giardia cysts or Cryptosporidium oocysts. In
countries meeting high hygiene standards, the
risk for humans of acquiring water-borne parasitic
infections is low, if water treatment works perfectly
and secondary drinking water contamination is
prevented.
With the aim of avoiding risks for human health as far
as possible and ensuring a high quality standard for food
products of animal origin, legal rules for monitoring
food have been implemented in the EU and other
regions, which include inter alia ante-mortem and post­
mortem examinations ('meat inspection') of slaughter
animals for parasites and other pathogens.
The basis for this is an extensive body of laws, regulations
and instructions which are explained in teaching courses
on food safety. In Europe, EU regulations are adopted by
the member states in national legislation and sometimes
supplemented by special national rules. In EU-associated
countries, these regulations correspond to those of the
EU. Regulations of the EU and individual states are
constantly adapted to take account of new developments.
Of the large number of EU rules, only two examples are
mentioned here: (a) Regulation (EC) No. 854/2004 of
the European Parliament and of the Council of29 April
2004 laying down specific rules for the organisation of
official controls on products of animal origin intended
for human consumption, (b) Commission Regulation
(EC) No. 2075/2005 of 5 December2005 laying down
specific rules on official controls for Trichinella in meat.
In ► Table 15.4 parasites are listed, which may occur in
food-producing animals. This compilation of important
or frequently occurring parasites is not exhaustive. The
(I)
tables show that some parasites are not covered by official C
·c3
regulations, because they are neglected or there are no
efficient screening methods (e.g. Toxoplasma gondii, �
certain Sarcocystis species which are macroscopically c:-
co II
invisible). Therefore, the consumer should apply C
·;::
preventive measures under certain circumstances as (I) I
described in Part II of this book.
.£
0
0
·u5
co
co
 Part IV. Zoonoses and parasites in food

�·-
Table 15.4. Examples of important parasites in food-producing animals.
·-
· ·-,.
iPredilection sites of Transmission Examination Measures:

.... . .
r paraSites to humans 1 according to A: Advice

... legislation2
J$ .
L: Legislation3 '

1. Domestic animals: ruminants, pig, horse

Toxoplasma gondii sheep, goat, skeletal musculature per os: raw None A: heat treatment(>60 °C),
(cysts)(► p. 101) pig, etc. and muscular organs meat freezing -18 °c, 3 d
Sarcocystis cattle skeletal musculature per os: raw MA L: generalised infection:
hominis(cysts) meat whole carcass unfit for human
(► p. 116) consumption
muscular organs per os: raw MA L: affected4 organs: unfit
meat
Sarcocystis pig skeletal musculature per os: raw MA L: generalised infection: whole
suihominis(cysts) meat carcass unfit
(► p. 116) muscular organs per os: raw MA L: affected organs: unfit
meat
Sarcocystis, other ruminants, skeletal musculature none MA L: generalised infection: whole
species(cysts) pig carcass unfit
(► p. 116) muscular organs none MA L: affected organ: unfit
Fascia/a hepatica ruminants, liver: bile ducts, none MA L: affected organ: unfit
(adults, preadults) horse, pig parenchyma
(► p. 175)
Dicrocoelium ruminants, liver: bile ducts none MA L: affected organ: unfit
dendriticum horse, pig
(adults, preadults)
(► p. 191)
Taenia saginata cattle masseter muscles, per os: raw MA L:(a) generalised infection
(cysticercQ tongue, heart, meat with living or dead cysticerci:
(► p. 224) diaphragm, skeletal whole carcass unfit; (b) light
musculature infections with living or dead
cysticerci: fit for human
consumption after freezing
(e.g. -18 °C, 72 h)
Taenia solium pig tongue, diaphragm, per os: raw MA L: as with T. saginata
(cysticercQ skeletal musculature meat
(► p. 230)
Taenla ovis sheep, goat heart, diaphragm, none MA L: affected organs unfit,
(cysticerci) skeletal musculature otherwise as with T. saginata
(► p. 233)
Taenia hydatigena sheep, goat, omentum, liver, lung none MA L: affected organs: unfit
(cysticerci) (cattle), pig (subserously)
(► p. 232)
Echinococcus ruminants, liver, lung, spleen, none MA L: affected organs: unfit
granulosus s.l. pig, horse kidney, omentum A: cysts should not be
(hydatid cysts) opened!
{► p. 240)
E. multilocularis pig liver(often only small none MA L: affected organ: unfit
(small cysts) lesions)
Q)
C (► p. 247)
·c:; Ascaris suum pig liver('milk spots') none MA L: affected organ totally or
'6
Q)
(larvae)(► p. 327) partly: unfit
Toxocara canis pig liver('milk spots') none MA L: affected organ totally or
co
C
(larvae)( ► p. 333) partly: unfit
·c Dictyocau/us spp. cattle, sheep, bronchi, trachea none MA L: affected organ: unfit
Q)
(adults, preadults) goat
(► p. 303)
.£;
>, Protostrongylids sheep, goat lung parenchyma, none MA L: affected organ: unfit
Ol (adult, preadults, small bronchi I�
0
0 eggs)(► p. 313)
·v;
co
co
0..
 15. Zoonoses and parasites in food

Table 15.4. Continued.

Parasite species and Animal Predilection sites of Transmission Examination Measures:

stages in meat or species parasites to humans 1 according to A: Advice I
organs legislatlon2 L: Legislation3 I
- ---- --- - - - ·- - I
Trichinella spp. pig, horse musculature per os: raw Ml. note: L: whole carcass and blood:
(encysted larvae, meat special unfit
rarely without cyst) regulations5 (j)

(► p. 376)
Ectoparasites ruminants, skin, subcutis none MA L: affected parts (skin,
Chapter 14, pig, horse musculature): unfrt
(► p. 392)
Other causes associated with parasitoses, such as significant MA L: whole carcass and blood:
abnormalities of colour, consistency or odour of muscle tissue or organs, unfrt
emaciation, general or localised oedema
2. Domestic animals: domestic rabbits and poultry
Extensive domestic various organs none MA L: whole carcass and blood:
subcutaneous, rabbit, poultry unfit
muscular
or systemic
parasitoses
Parasite infection domestic parts of carcass or none MA L: parts of carcass or organs:
of parts of the rabbit, poultry organs unfit
carcass if other
parts are not
affected
3. Wild animals: wild boar, wild ruminants, other animal species
Trichinella spp. wild boar, musculature per os: raw Ml, note: L: whole carcass and blood:
(encysted larvae, bear, fox, meat special unfit
rarely without cyst) beaver, other regulations5
(► p. 376) potential
hosts
Other parasites: as with
cysticercosis, etc. domestic
animals
4. Fish and fish products
Diphyl/obothrium freshwater body cavity, body per os: raw MA L: apparently affected fish or
spp. and marine tissues fish parts of them: unfit
(plerocercoids) fish
(► p. 208)
Opisthorchis spp. various body tissues per os: raw none A: in endemic areas heat
(metacercariae) species of fish treatment of fish (>60 °C) or
(► p. 197) fresh-water freezing (-10 °C, 5 d)
fish
Anisakidae (larvae) numerous body cavity, body per os: raw MA L: apparently affected fish or
(► p. 339) species of tissues fish parts of them: unfit. Fish to
marine fish be eaten as 'natural finish'
product, has to be pretreated
by freezing (-20 °C, at least
24 h)
(I)
MA
Other parasites: marine and skin, musculature none L: fish unfit, if body tissues or
·u
C

various species freshwater skin are infected/infested with

of Protozoa, fish parasites
Trematoda,
Cestoda and
al
Arthropoda C
·;;::
1 Stages of some parasites occurring in food are not infectious for humans. For example, adult or preadult stages of F. hepatica occurring (I)

in liver do not infect humans, but metacercariae are infective.

2 MA= macroscopic examination includes visual inspection, palpation and, if necessary, incision; Ml= microscopic examination.
3 The abbreviated term 'unfit' stands for: unfit for human consumption. .s
>,
4 'Affected' means with lesions caused by parasites. O>
0
5 Microscopic examination after muscle digestion(► p. 535).
0
·u5
al
0....
 Part IV. Zoonoses and parasites in food

- Selected references---------•

Broglia A, Kapel C (2011) Changing dietary habits in a changing

world: emerging dn\ters for the transmission of foodborne
parasitic zoonoses. Vet Parasitol 182: 2-13.
Dorny P, Praet N, Deckers N, Gabriel S (2009) Emerging
food-borne parasites. Vet Parasitol 163: 196-206.
European Union - legislation. Available at: http://www.eur­
lex.europa.eu.
Hui YH, Sattar SA, Murrell KD, Nip WK, Stanfield PS (eds.)
(2000) Foodbome disease handbook. 2nd ed. New York, NY,
USA: Marcel Dekker; ISBN 0-8247-0338-3.
Murrell KO (2013) Zoonotic foodborne parasites and their
surveillance. Rev Sci Tech 32: 559-569.
Torgerson PR, De Silva NR, Fevre EM, Kasuga F, Rokni MB,
Zhou XN, Sripa B, Gargouri N, Willingham AL, Stein C
(2014) The global burden of foodborne parasitic diseases:
an update. Trends Parasitol 30: 20-26.

Q)

·o
C

Q)

co
C
·;::
Q)

_c;;;
>-
0>
0

·enco
co
a..
 16. Diagnostics
16.1 Laboratory procedures
16.1.1 Introduction
The principle 'an accurate diagnosis is the indispensable
basis for veterinary interventions' applies to all
diseases, including parasitoses. Case history, clinical
findings and epidemiological data provide important
information, but in most cases do not allow for a
definitive diagnosis of parasitic infections. Therefore,
a direct or indirect identification of the causative agent
must be achieved. For this purpose, different procedures
are available, which can be applied intra vitam or post
mortem (intravital or post mortem diagnosis). For
some parasitoses the detection of pathogens in the
environment is of diagnostic importance.
Direct detection of parasites. Macroscopic and
microscopic (rarely electron microscopic) examinations
are conventional procedures for the direct detection
of parasites. They are polyspecific, i.e. an experienced
diagnostician can identify a variety of parasite stages
present in a sample and thus might also discover an
unexpected infection. These procedures are still central
today, but new molecular methods are available that
complement, improve or replace them in many instances.
Parasite antigens (excretory/secretory antigens, shaded
surface antigens and antigens from dissolved parasite
stages) can be detected by immunological procedures
using specific antibodies. These assays are monospecific
(species- or genus-specific), determined by the specificity
of the employed antibodies. The sensitivities of such
assays are dependent on the metabolic activity and
biomass of the parasite as well as on the concentrations
of the antigens (e.g. in faeces or blood).
DNA analyses rely on DNA amplification by PCR (in
conventional or real-time format, in single-or multiplex
assays) or LAMP. If well desi.gned and evaluated, these
assays are highly specific, allowing an identification
Q)
C of parasites at the level of a species or subspecies
·c::; (strains or genotypes, usually requiring sequencing
i5
�
Q)
of PCR products). The sensitivity of DNA analyses is
i::' higher when targeting a repetitive genome sequence
co
C (multicopy gene or repetitive non-coding regions) but
·c might be impaired when using DNA isolated from
Q)
certain specimens (e.g. faeces, intestinal contents or
C environmental samples) due to the presence of co­
>,
CJ)
purified inhibitory substances. Such inhibition seems
0 less of an issue in LAMP assays.
0
·u5
co Mass spectrometry (MAL DI-TOF MS) has come
co
0.. of age for the rapid and low-cost identification of
microorganisms in clinical diagnostic laboratories.
Recently, the method has been successfully applied in
parasitology for the identification of arthropods ( ► p.
525). The method is polyspecific, i.e. all organisms
are identified, of which a reference mass spectrum is
available in a database.
In selected cases, in vitro cultivation is a useful aid
for diagnosing parasites after multiplication (e.g.
Tritrichomonas, Leishmania) or development (e.g.
larval culture for strongylids and trichostrongylids).
Experimental infections of animals for diagnostic
purposes have largely been replaced by in vitro and
molecular methods.
Indirect parasite detection. Indirect detection
is based on detecting immunological host reactions
against parasite antigens and includes the detection of
specific antibodies in blood, serum/plasma, milk, or
cerebrospinal fluid, but also allergy tests and delayed
hypersensitivity tests. The specificity of these tests is
dependent on the antigens used and their sensitivity to
the immunological reactions which may, for example,
appear 10 days after antigen exposure but can persist
for months after parasite elimination.
In the future, new approaches, particularly DNA­
based, largely automated methods, might also have a
huge impact in diagnostic parasitology. Diagnostic
metagenomics ( other equivalent terms include high
throughput sequencing, next generation sequencing),
the large-scale sequencing of DNA/RNA isolated from
specimens, is used in environmental and medical
microbiology to identify bacteria and viruses in
microbial communities, directly from the samples or
after enrichment. The method, so far rarely used in
parasitology, is demanding and currently expensive,
but apparently very promising and suitable for the
simultaneous detection of multiple pathogens (e.g.
viruses, bacteria, protozoa) in the same sample.
Diagnostic parameters remain to be determined.
Another trend is the development of rapid diagnostic
tests (RDTs) to identify antigens of pathogens, antibodies
directed against them or specific metabolic activities.
RDTs are easy to handle, provide rapid results and are
applicable in veterinary practice or in the field/stable.
Such tests should have features which can be summarised
under the acronym ASSURED (affordable, sensitive,
specific, user-friendly, rapid/robust, equipment-free
and deliverable to those who need it).
 16. Diagnostics

16.1.2 Diagnostic samples of the parasitological techniques are not performed

The accuracy of a diagnosis depends largely on correct
sampling as well as on conditions of storage and
shipping of the test material. Instructions on the type
ofsamples required for parasitological examinations are
summarised in► Table 16.1. Faecal, blood, skin samples
and organs are most often submitted for parasitological
examination, more rarely biopsies, other tissue samples
in a consistent manner, resulting in methodological
differences between laboratories. Examinations using
some of the parasitological procedures described herein
or using commercially available test kits can easily be
performed in laboratories of veterinary practices. In
addition to general safety regulations for laboratory ::J
work, special safety precautions have to be considered D
a.,
for handling parasite material. Environmentally toxic
e
()

or isolated parasites (e.g. ticks, fleas). For monitoring
of animal populations, representative samples should
be taken. Specimens should be collected in watertight
and tightly sealed containers (e.g. special vials for faecal
samples or blood tubes made of plastic) and sent by the
most expeditious means to the laboratory, observing the
official rules for the transport of potentially infectious
material. Of particular importance for sample submission
are: clear labelling of the samples, disclosure of patient's
data (species, breed, age, sex, number), case history
(clinical symptoms, type of pretreatment, possible stay
abroad) and the client's address (with telephone and
fax numbers or e-mail address for quick transmission
of the diagnostic report).
16.1.3 Diagnostic laboratories
Nowadays, parasitological examinations are mostly
performed in officially accredited laboratories that
provide specific guidelines for sampling and shipping
of material on request. It should be noted that some
substances, used for laboratory examinations, or 0..
infectious material must be disposed of or inactivated
properly.
16.1.4 Procedures for intravital
parasite detection
The following section provides an overview of some
laboratory procedures for intravital parasite detection.
Procedures that can be performed with simple equipment
in small laboratories are described here in more detail.
• Equipment. The minimum equipment for such
examinations comprises: compound microscope
(eyepiece lens lOx, objective lenses 4, 10, 40x and
oil immersion SOx or lOOx), centrifuge (centrifuge
tubes 15 ml, centrifugation up to 2,500xg), various
small equipment (see below) as well as chemicals and
consumables.

ble 16.1. Guide for submission of material required for parasite detection with a variety of methods (see also instructions
laberatories).

cation of ectoparasites: several parasites fixed In 70% ethanol or B: microscopy

ticks, lice, mosquitoes, flies, native In a container with a piece of wet A: DNA analyses, MALDI-TOF MS
e of flies, fleas filter paper
parasites living on skin surface: 3 transparent adhesive tapes on B: microscopy, where required KOH
Cheyletiella, lice, fleas microscopic slides per animal and procedure
brushed out hair and skin material
rasites living In deeper skin layers:
rect detection (e.g. Demodex, deep skin scrapes, preferably from B: microscopy, KOH procedure
,ptes, Psoroptes, several predilection sites, raative, in tightly A: DNA analyses
rioptes mites) sealed plastic vessels
rology (e.g. Sarcoptes in dogs 5 ml native blood or 2 ml serum/plasma B: ELISA; iridividual diagnosis in dogs,
pigs, Psoroptes In sheep and usually herd diagnosis in pigs, sheep
e, hypodermosis in cattle and cattle
sis in dogs and cats see 2.5
in cattle(► p. 115)
skin biopsy 8: microscopy
A: DNA analyses
2 rnl serum/plasma B: specific antibody detection (ELISA,
-lFAI,WB)
 Part V. Diagnostics
Table 16.1. Continued.
- .;-,\ J,}, •r � •< :.:
lnation fo� par:asltesl
• �•--,.,·
E
sftoses of org,-n SY$tems
2. Blood, haemopoietic or lymphatic organs
2.1 Trypanosomoses in horses, cattle, sheep, dogs, etc.
a) Direct detection
b) Serology(genus specific, possibly 2 ml serum/plasma
cross-reactions with Leishmania)
2.2 Babesiosis and Theileriosis in
horses, cattle, sheep, dogs, etc.
a) Direct detection
b) Serology
2.3 Filarioses in dogs and cats
a) Detection of microfilariae
b) 0. immitis antigen detection(dog, 2 ml serum/plasma
reduced sensitivity in cats)
c) Specific antibody detection(cats) 2 ml serum/plasma
2.4 Angiostrongylosis in dogs
a) Detection of laNae(L1)
b) Serology
2.5 Leishmaniosis in dogs and cats
a) Direct detection(► p. 76)
b) Serology(► p. 76)
3. Gastrointestinal tract
3.1 Faecal examination
a) Detection of oocysts and cysts
of protozoa, eggs of trematodes,
cestodes and nematodes and
nematode laNae
b) Faecal examination as in 3.1a,
Q) including vegetative forms
C birds: maximum 1 g faeces in 10 ml SAF
·c3 of protozoa (selected animal
species)
Q)
c) Copro-antigen detection
(Cryptosporidium, Giard/a, Taenia,
co Echinococcus, Fascia/a and other
C
·;:: parasites)
d) Total copro-DNA detection
C (Cryptosporidium, Giardia,
>, Echinococcus)
O> e) Differentiation of third stage laNae native faecal sample: horse, cattle, small
0
0 of gastrointestinal nematodes
.in
co
co
a..
.,.
Req1:1lrid material
3 thin blood smears(unfixed, air dried or
fixed in methanol) or 5-10 ml EDTA blood
see 2.1; 5 ml native blood, several thin B: microscopy after staining
blood smears(thin smears of lymph node A: DNA analyses
aspirate fixed in methanol for Theileria
spp. in ruminants)
2 ml serum/plasma
5 ml EDTA blood
4-10 g native faeces
2 ml serum/plasma
lymph node or bone marrow aspirate
(blood) in culture medium(order from
laboratory)
2 ml serum/plasma
native, fresh faecal sample: cattle, horse,
donkey: 20-30 g; sheep, goat, pig: 10-
20 g; dog, cat, rabbit: 5-10 g; poultry,
caged birds, reptiles, other small animals:
0.5-5 g
fresh faeces in SAF solution: dog, cat,
monkeys, amphibians, reptiles, caged
solution (order solution from laboratory)
native or buffered faecal sample: 2-5 g
native or buffered faecal sample: 2-5 g
ruminants: 15-30 g
Basic (B) and advanced (A) diagnostic
procedures 1 and remarks
B: microscopy after staining
A: DNA analyses
B: specific antibody detection(CFT,
ELISA, IFAT, WB); antigen detection
(ELISA)
B: specific antibody detection(CFT,
ELISA, IFAT, AT, WB)
B: isolation: filter technique or Knott test;
differentiation: size measurements,
staining for acid phosphatase activity
A: DNA analyses
B: ELISA, IC, RDT
B: ELISA, WB
B: Baermann procedure, FLOTAC
A: DNA analyses
B: Antigen detection(ELISA, RD1);
specific antibody detection(ELISA)
B: microscopy after staining(low
sensitivity)
A: DNA analyses, cultivation
B: detection of specific antibodies(ELISA.
IFAT, WB, AT, RD1)
B: eggs/cysts/oocysts: concentration
(sedimentation/flotation, sedimentation
methods); laNae: Baermann
procedure; all stages: FLOTAC(► p.
529)
A: DNA analyses
8: microscopy after SAFC procedure
(SAF not optimal for DNA analysis)
8/A: ELISA, ROT
8/A: DNA analyses
8: microscopy after recovery of larvae
from culture
A: DNA analyses
 16. Diagnostics

Table 16.1. Continued.

-
Examination for parasites/ Required material Basic (B) and advanced (A) diagnostic
parasitoses of organ systems procedures 1 and remarks

D Quantitative analyses: faecal egg native faecal sample: quantities as in B: usually McMaster counting procedure
or oocyst counts (epg, opg) or 3.1. For FECAT sampling before
U)
faecal egg count reduction test chemotherapy and 2 weeks thereafter Cl)
(FECAT ► p. 529) (► p. 529) ::::J
u
g) Cryptosporidiosis B: microscopy (staining; FATI, copra- Cl)
native faecal sample: all animal species: u
1-5 g ( ► p. 526) antigen detection 2
A: DNA analyses 0...

h) Tritrichomonosis in cats fresh faeces in culture medium (lnPouch®) B: culture, microscopy

or native faecal sample for immediate A: DNA analyses
examination: 1-5 g ( ► p. 526)
3.2 Eggs of Oxyuris (horse), Taenia, per animal 3 adhesive tapes from the B: microscopy
Echinococcus, Toxocara (dogs) perianal region on microscopic slides A: DNA analyses
often adhering to the coat (► p. 525) (/)
Cl)
4. Liver
:::; '·
"0'
4.1 Fasciolosis in sheep, cattle, horses and other species (I)
()
a) Egg detection In faeces native faecal sample as In 3.1 a B: microscopy after sedimentation
technique
C'
b) Copra-antigen detection native or buffered faecal sample A: ELISA, IC 0

c) Specific antibody detection 2 ml serum/plasma, milk and bulk tank A: ELISA, IC

d) Egg detection in bile
4.2 Dicrocoeliosis in sheep, cattle, New
World camelids
a) Egg detection in faeces
b) Egg detection in bile
5. Respiratory tract
5.1 Lungworm infection In cattle, sheep, equines and pigs
a) Direct detection of larvae
(dictyocaulosis in ruminants and
equines, protostrongylosis in
small ruminants)
b) Specific antibody detection (cattle 5 ml native blood or 2 ml serum, milk and A:ELISA
dictyocaulosis)
c) Egg detection in faeces
(metastrongylosis in pigs, 0.
arnfieldi in equines)
5.2 Lungworm infections in carnivores
a) Detection of larvae in faeces
(Crenosoma, Aelurostrongy/us,
Filaroides, Troglostrongylus)
Angiostrongylus, see 2.5)
b) Detection of eggs in faeces
(Capillaria aerophila and C.
boehml)
6. Urogenital tract
6.1 Neospora in cattle, goats and
others; Toxoplasma in sheep, pigs
and others as cause of abortion
6.2 Tritrichomonas fetus in cattle
6.3 Dourine in equids
a) Direct identification not sensitive
5 ml native blood or 2 ml serum; samples
b) Serology (Trypanosoma spp., not from genital tract ( ► p. 56)
species specific)
0
milk sample for herd diagnosis ..0
(\j
2-5 ml bile (obtained by guided gall B: microscopy after sedimentation _J
bladder punction or after necropsy) technique
native faecal sample as in 3.1a B: microscopy after sedimentation/
flotation procedure
see 4.1d
native faecal sample as In 3.1 a B: microscopy after Baermann procedure,
FLOTAC
A: DNA analyses
bulk tank milk sample for herd diagnosis
native fresh faecal sample as in 3.1 a B: microscopy after sedimentation/
flotation procedure
native faecal sample as In 3.1 a, native B: microscopy after Baermann procedure
tracheal and bronchial mucus or FLOTAC (faeces) or direct (mucus)
A: DNA analyses
as in 3.1a B: microscopy after sedimentation/
flotation procedure
A: DNA analyses
aborted fetus, placenta, serum from fetus B: Histopathology, immunohistology, DNA
and dam analyses, serology (see 7.1 and 7.2)
samples from genital tract ( ► p. 56) B:microscopy after cultivation
A: DNA analyses
CFT, ELISA, WB
 Part V. Diagnostics

Table 16.1. Continued.

ale (Bl and' . c

)Pr-G>c1:t1clurea1 an rcem 11

6.4 Capillaria p/ica and Dioctophyma
renale infections in carnivores
6.5 Microsporidia, (rabbits, cats, monkeys, rodents)
a) Direct identification
b) Serology (Encephalitozoon
cunicu/1)
7. Various or multiple organ systems
7.1 Toxoplasmosis in dogs, cats, other
species (persistent asymptomatic
infections)
7.2 Neosporosis
a) Abortions in cattle, goats (see
6.1)
b) Persistent asymptomatic
infections in ruminants and dogs
c) Clinical infections in dogs
7.3 Taenia saginata-cysticercosis of cattle
a) Parasite identification
b) Specific antibody detection
7.4 Detection of helminths in internal
organs, e.g. liver, gastrointestinal
tract, lung
7.5 Detection of Tr/chine/la spp. in
musculature
7.6 Examination for metacestodes
in muscles, liver, lung, etc, (If
macroscopic dia nosls is unclear)
1 Abbreviations: AT: agglutination test; CFT: complement fixation test; EDTA: ethylene-dlamlne-tetr aacetic-acld; ELISA: enzyme-linked
immunosorbent assay; FLOTAC: ► p, 529; IFAT: Indirect fluorescent antibody test; IC: lmmunochromatography; MALDI-TOF MS: matrix­
assisted laser desorption/ionisation time of flight mass spectrometry; ROT: rapid diagnostic test; SAF: sodium acetate-acetic acid-formalin;
WB: western blot.
urine: several ml
urine sediment, lens material
serum/plasma (0.5-1 ml)
5 ml native blood or 2 ml serum
2 ml serum/plasma
2 ml serum/plasma, muscle biopsy, (in
phys. saline), liquor, tissue samples after
necropsy
meat with lesions
2 ml serum/plasma, milk and bulk tank
milk sample for herd diagnosis
organs (or organ parts) packed
individually in tightly sealed containers or
plastic bags
muscle samples from pigs, horses or
other species; sampling sites and sample
quantities (► p. 535 ff)
whole cyst or suspected tissue material,
native
B: microscopy of urine sediment for eggs
B: microscopy after staining (low
sensitivity)
A: molecular analyses
B: specific antibody detection (IFAT)
B: specific antibody detection (ELISA,
IFAT, AT, other methods)
B: antibody detection (ELISA, IFAT)
B: as in b, histopathology,
immunohistochemistry, DNA analyses
B: macroscopic and microscopic
identification
A: DNA analyses
B: ELISA
B: macroscopic, microscopic, histologic
examinations
A: if indicated detection of parasite
specific antigens or DNA analyses
B: microscopy or latex agglutination test
after digestion procedure
A: DNA analyses
B: microscopy, histology
A: DNA analyses

• Microscopic magnification ranges. The For the identification of some parasites, microscopic
following microscopic magnification ranges are usually size measurements are necessary. For the evaluation
Q)
T5
C required for parasitological examinations: of the test results, sensitivities and specificities of the
'6 Small arthropods: low magnifications, 40x or I OOx procedures are important and have to be considered
Q)
� ( IOx eyepiece, objective 4x or IOx), for details 400x ( ► Glossary, p. 620).
C' (I Ox eyepiece, objective 40x). For examinations of
ro larger arthropods or skin samples a stereomicroscope
·.::
C
Q) is needed.
Eggs and larvae of helminths: as for arthropods.
-� Protozoa: medium to high magnification, 400x
>,
Ol
and 630x or l,OOOx (lOx eyepiece, objective 40x
0 and 63x without, and SOx or 63x and IOOx with
0
'iii oil immersion).
ro
ro
a..

16.1.4.1 Detection of skin parasites
(arthropods)
Smears
Homogeneous, greasy material can be obtained by
pressing folds of altered skin between two fingers
(detection of Demodex mites) or by removal with a
swab from the external auditory canal (detection of
Otodectes mites). The material is spread on a microscope
slide, covered with a drop of glycerol and a coverslip,
and examined microscopically.
Adhesive tape method
After spreading hairs, a transparent tape (about 4 cm
long and 1 cm wide) is pressed onto the skin, removed,
gently pressed with the adhesive side on a glass slide and
examined microscopically. Usually, several samples are
taken from different skin areas. Suitability: detection of
Cheyletiella mites in dogs, cats, etc.
Superficial and deep skin scrapings and hair
material
Sampling of skin scrapings. At the edge of
cutaneous lesions or predilection sites of ectoparasites
(e.g. mites), hair is sheared and the skin is scraped with
a sharp bone curette or a scalpel blade superficially or
more deeply until capillary haemorrhages occur. The
sample is transferred into a transparent plastic tube or
beaker with large opening which can be tightly sealed.
Direct examination. Examination of skin material
and the walls of the plastic container using a
stereomicroscope, as mites and other arthropods tend
to migrate out of the skin material.
Examination after processing. Place the material
into a Petri dish with 10% KOH solution and leave it to
stand for at least 2-3 h at room temperature (longer if
needed). Alternative: boil material briefly in a suitable
vessel(caution: risk of KOH splashing, wear protective
glasses!!) or heat in a microwave (some odour emission!).
The KOH solution macerates keratin substances of the
skin and sets arthropods free, leaving the chitinous
exoskeletons. Examination of the suspension in a
Petri dish under a stereomicroscope; for accurate
identification isolate the arthropods individually,
transfer them to a slide and examine. Suitability: hair
examination and superficial skin scrapings: detection
of biting and sucking lice, and mites ( Cheyletiella,
Trombicula, Chorioptes Psoroptes); deep skin scrapes:
additionally Demodex, Sarcoptes, Notoedres mites.
16. Diagnostics
Detection of specific antibodies
Various skin parasitoses can be diagnosed serologically
by detecting specific antibodies, including sarcoptic
mange in dogs {individual diagnosis), sarcoptic
mange in pigs, psoroptic mange in sheep and cattle, t',
hypodermosis in cattJe (herd diagnosis), oestrosis in
Ql
.._
:i
sheep and gasterophilosis in horses(► Table 16.2). 7"'
cl)
Commercial test kits are available for some of these 0
0
parasitoses, e.g. Sarcoptes-ELISN Dog (Afosa, DE), ci
Sarcoptes-ELISN Pig (Afosa, DE), Pourquier• ELISA
Hypodermosis (Institut Pourquier, FR).
Identification of arthropods using molecular
techniques and mass spectrometry
The identification of some arthropod species by
morphology may be difficult or even impossible
(damaged specimens, sister taxa, juveniJe stages), but
can be accomplished by various DNA-based techniques
(suitable samples: whole live arthropods, preserved in
70% ethanol or frozen). Recently, MALDI-TOF mass
spectrometry has been successfully applied for the
identification of arthropods (material: arthropods
preserved in 70-95% ethanol).
16.1.4.2 Detection of parasites in blood,
cerebrospinal fluid (CSF) and
aspirates
Detection of protozoa
Smears of blood, bone marrow, lymph node
aspirate, or sediment of CSF. Thin smears of a drop
ofnative or EDTA blood (or other material) are prepared
on clean microscope slides. The slides are allowed to air
dry at room temperature or at 37 °C for about 30 min,
are then fixed in methanol for 5-10 min and stained
with Giemsa staining solution or Diff-Quick solution
(Differential Quick Stain Kit•). The characteristics
of protozoa are usually easy to recognise in properly
prepared and stained thin smears.
Microhaematocrit technique (buffy coat
method). A microhaematocrit tube is filled with
EDTA blood, sealed at one end with haematocrit clay
and centrifuged in a haematocrit centrifuge for 5 min.
The zone between buffy coat layer and plasma is then
examined microscopically for motile trypanosomes or
microfilariae. After scratching the haematocrit tube
with a small glass cutter at the level of the buffy coat
and breaking it, the buffy coat layer and plasma can be
transferred to a slide, mixed with a drop of physiologic
saline and examined directly, or the material can be
used for preparing stained thin smears.
 Part V. Diagnostics
Culture methods. Culture methods are used
for detecting various parasites, such as Leishmania,
Tritrichomonas or Acanthamoeba. Suitable media are
supplied by specialised laboratories or are commercially
available, e.g. InPouch• test for Tritrichomonas.
Detection of specific antibodies, parasite
antigens and DNA
Many protozoal infections or other parasitoses can be
diagnosed by detecting specific host antibodies in
serum, milk, or CSF with different methods ( ► Table
16.1). The detection of circulating antigens in blood
by ELISA or by rapid diagnostic tests (RDT) has proven
reliable for some parasitoses, particularly for diagnosing
Dirofilaria immitis and Angiostrongylus vasorum
infections in dogs (commercial tests, e.g.: SNAP• 4Dx"
Plus, IDEXX, USA; Petchek" IDEXX, USA; DiroCHEK•,
Synbiotics, USA; Heartworm antigen Canine ELISA•,
Demeditec, DE; Angio Detect N Test, IDEXX , USA. RDTs
are also available, for example, for detecting specific
serum antibodies against Leishmania infantum in dogs,
Toxoplasma gondii in dogs and cats, Neospora caninum
in dogs and cattle (FASTest•, Magacor, AT). Protocols
for the identification of parasites by DNA amplification
(PCR, more recently also LAMP) are available for most
of the parasites.
Detection of microfilariae
Microfllariae circulating in blood can be detected
with a filter method (commercial test kit: Difil­
Tes�, Vetoquinol). At least l ml EDTA blood is first
haemolysed in a special solution and then pressed
through a membrane filter using a syringe. The filter
disc is stained with a staining solution, and examined
microscopically. In the Knott test, I ml blood is
haemolysed and centrifuged in 10 ml of 2% formalin.
The sediment contains a concentrate of microfilariae,
which are stained (Giemsa stain) for morphometrlc
analyses or histod1emicaJly for acid phosphatase activity.
DNA analyses allowing a species diagnosis can be
performed using commercial kits for DNA isolation
from whole blood or after concentration of microfilariae
by �ntrifugation of a blood sample in water (without
formalin).
Q)
C flotation solutions are used: saturated NaCl solution (sG
·o 16.1.4.3 Detection of parasites in faecal
'6
Q)
� samples
co The techniques for examination of faecal samples
C
·c described here are not standardised and can be classified
Q)
as semi-quantitative when performed with consistent
C methodology and defined quantities of faecal material.
>,
O'l Parasite identification is achieved by microscopy (copro­
0 antigen and copro-DNA detection ► Table 16. l ).
'iii
co
a..
Sedimentation technique (ST)
Principle. In a faeces-water suspension, parasite eggs
with a relatively high specific gravity (e.g. trematode
eggs) and heavy faecal particles sink rather quickly to
the bottom and concentrate in the sediment. By repeated
sedimentation and decantation of the supernatant, the
lighter faecal particles are removed, and the parasite
stages can be detected in the final sediment.
Method. The following quantities of faecal samples
are used for this method: cattle and horse at least 10 g,
small ruminants 3-10 g. Hard and dry faeces of small
ruminants can be soaked in water for 1 h. The various
steps of the method are shown in ► Figure 16.1.
Suitability. The ST detects with sufficient reliability
oocysts of Eimeria leuckarti, and eggs of Fasciola,
paramphistomes or schistosomes. In examinations
for schistosome eggs, physiological saline solution has
to be used instead of water (miracidia hatch in water,
empty eggs do not sediment). The analytical sensitivity
(► Glossary, p. 620) of the ST for detecting Fasciola
eggs is very high (close to 100%) if epg (egg counts per
g of faeces) are between l 0 and I 000; the lower limit of
detection is 3-4 epg. In examinations of animals naturally
infected with F. hepatica, not all parasite carriers are
detected, as egg shedding is highly variable and often
low, especially in cattle. Thus, diagnostic sensitivities
in cattle of 60-70% can be expected, whereas in sheep
>80%. Repeated examinations of each 10 g of faeces of
the same batch revealed an average sensitivity of 69%;
the examination of 3 samples increased the sensitivity
to 90%. The specificity is high because the most related
eggs of Paramphistomum spp. can be differentiated by
colour and size.
Flotation techniques (FT)
Prlnclple. Faeces are mixed with a flotation solution,
which has a higher specific gravity (sG) than water (sG
1.0), to give a suspension. Heavy faecal particles sink or
remain in suspension, while specifically lighter parasite
stages ascend and accumulate on the surface.
Flotation solutions. Among others, the following
at 20 °C: 1.2 g), NaNO3 solution (sG: 1.2), ZnC12 solution
(sG: 1.3 or 1.45), ZnSO4 solution (sG: 1.2 or 1.3), NaCl/
ZnC12 solution (sG: 1.3) and sugar solution (sG: 1.3).
• Method A. Flotation with saturated NaCl solution
and centrifugation.
Place 3-5 g of faeces in a suitable container (beaker,
mortar) with about 10 times the volume of the
flotation solution, mix thoroughly to a homogeneous
suspension. Hard faeces can be pre-soaked in water.
 16. Diagnostics

(/)
Q)
:.,
TI
OJ
(.)

1 . Mix 5-1 0 g faeces with water 2. Pour suspension through a 3. Wash the sieving residue
to make a homogeneous fine-meshed sieve (mesh with strong waler jet and
suspension (as shown In tt,e size 250-300 µm) into a fill beaker up lo -1.5 cm
diagram or using a mixer) 250 ml beaker below the rim

J
4. Let the suspension sediment 5. Add a few drops of 6. Transfer sediment to a
for only 3 min, decant the methylene blue (1 % Petri dish with counting
supernatant, fill the beaker solution) to the grid and examine
with water and repeat the sediment microscopically
procedure once or twice.

Figure 16.1. Sedimentation procedure (SP) (Graphics: IPZ, M. Mathys).

- Pour a portion of the suspension through a sieve
(mesh size 500-800 µm) and funnel into two 15 ml
, centrifuge tubes and centrifuge for 3 min at 300-
S00xg.
- Transfer with a bacteriologic loop 3-6 drops from the
liquid surface to a microscopic slide. The loop of 5-6
mm in diameter is bent at a 90-degree angle to the
wire rod; the loop is sterilised by heating it to glow.
- Microscopic examination initially without coverslip
at low magnification; if necessary, apply a coverslip
and examine at higher magnification.
• Method B. Direct flotation. Alternatively, the
entire suspension is transferred to a glass beaker (e.g. 50
ml). After 15-30 min flotation (depending on flotation
medium and size of the beaker), a coversllp is placed
on the meniscus of the fluid, gently transferred with the
adhering fluid film to a microscopic slide and examined.
Alternatively, some drops can be transferred by means
of a bacteriologic loop as described above.
Suitability. The FT with saturated NaCl solution
as flotation medium is suitable for detecting eggs of
Strongyloides, strongyles, ascarids, anoplocephalids,
oocysts of coccidia and similar parasite stages with a
sensitivity of around 70-90%. The technique is unreliable
for detecting eggs of Trichuris, Capillaria, pinworms,
Taeniidae and Eimeria leuckarti of horses; Giardia cysts
sp. are deformed, but can still be recognised.
Test kits. Several disposable plastic devices and flotation
solutions are commercially available, e.g. Fecalyser•
(Vetoquinol), Ovassay- Plus (Zoetis Synbiotics), and
Ovatec• Plus (Synbiotics). Advantages include improved
hygiene, convenience of shipping, ease of sample
processing as well as reduced work for cleaning. The test
procedure is based on the principle of direct flotation.
Since the amount of faeces applicable in these kits is
small (approximately 1-2 g), their sensitivity is often
lower than that of procedures using larger samples (FT,
CST /FT), especially at low egg or oocyst counts per g
of faeces.
 Part V. Diagnostics

Combined sedimentation-flotation technique
(CSFT)
Principle and method. This method combines
concentration of parasite stages by sedimentation
with the effect of flotation. The method is shown and
described in ► Figure 16.2.
Suitability. The CSFT is suitable for detecting eggs
of nematodes, cestodes and trematodes as well as of
sporocysts, cysts, and oocysts of protozoa; cysts of
Giardia spp. are usually deformed but can be identified.
Eggs of Fasciola hepatica and paramphistomids also
become deformed; they can be detected with higher
reliability with the ST. The sensitivity for detecting eggs of
strongyles and ascarids is slightly higher (approximately
7%) than that of the FT.

1 . Mix 5-10 g faeces with water 2. Pour suspension through 3. Wash the sieving residue
to make a homogeneous a wide-meshed sieve with strong water jet and fill
suspension (as shown in the (mesh size 500-800 µm) beaker up to - 1 .5 cm
diagram or using a mixer) into a 250 ml beaker below the rim

I
•
•
.
.

•
.

18 8 8 I
4. Let the suspension 5. Transfer 1-2 ml of the 6. Add ZnCl2 solution 7. Using a bacteriologic
sediment for 30 min sediment in each of two (specific gravity 1.3) loop transfer 3 drops
and decant the centrifuge tubes up to -1 cm below from the surface of the
supernatant the rim and centrifuge suspension of each tube
for 2-3 min (-300 xg) to a slide for microscopic
examination (note: loop
is bent at 90 degrees to
vertical axis)

Figure 16.2. Combined sedimentation-flotation technique (CSFT) (Graphics: IPZ, M. Mathys).


Quantitative faecal examination (modified
McMaster technique for egg and oocyst
counting)
Principle. Helminth eggs(especially nematode eggs) or
coccidia oocysts present in a defined amount of faeces
are floated in a chamber and counted under a marked
field microscopically. The counted number is related to
1 g of faeces and expressed as epg (egg count per g) or
opg(oocyst count per g), respectively.
Method
• Mix thoroughly an exact amount of faeces(4 g: cattJe,
horses, pigs, small ruminants) with approximately
30 ml of saturated NaCl flotation solution.
• The saline-faeces suspension is poured through a
sieve (mesh size 500 to 800 µm) and funnel into a
calibrated cylinder (100 ml). The sieve residue is
well squeezed out with a pestle; sieve and funnel are
removed, and flotation solution is added to 60 ml.
• This suspension is transferred to a beaker and mixed
well by continuous stirring. A sample is quickJy taken
with a pipette and used to fill the flrst compartment
of the counting slide which has two compartments,
each with a volume of 0.15 ml(► Figure 16.3).
• The suspension is thoroughly mixed again
before taking a second sample to fill the second
compartment of the slide.
• Leave the slide for 5-10 min in order to allow the eggs
or oocysts to float under the surface of the counting
field of the chamber.
• The counting slide is placed on the microscope
stage, and all parasite stages are counted within the
counting grid (magnification 40- to 100-fold).
Calculation of epg or opg
numbers of eggs from 2 counting grids (N) X
Epg=---------------,:-
amount of faeces (g) x counting grid area (cm2)
volume of faecal suspension (ml)
height of counting chamber x number of counting grids
Example: 4 g faeces were su_spended in 60 ml flotation
solution, and 15 eggs were counted in two counting
grids:
_ 15 x 60 _ 900 _
Epg 750
- 4 X 1 X Q.15 X 2 - 1,2 -
In the example presented here, the detection limit of 50
epg is reached when only 1 egg is found in 2 counting
fields. If 2 g faecal samples are used, the limit is 100/g.
Based on the original McMaster counting technique,
several modifications have been described, including
one with a 3-chamber counting slide.
Suitability and comments. The sensitivity is around
70% and is comparable with that of other flotation
procedures. By using flotation solutions with higher
specific gravity (e.g. ZnC12, sG: 1.3) specifically heavier
16. Diagnostics
1cmj
Counting grid ::J
�:
Faecal suspension a,
0
0
Fig ure 16.3. Modified McMaster counting chamber with two
compartments and counting grids (Graphics: IPZ, A. Seeger).
eggs can be detected. Egg counting has frequently been
used in field studies on drug resistance of gastrointestinal
nematode populations in ruminants and horses, such
that one egg count was performed before anthelmintic
treatment and another one 2 weeks later (faecal egg count
reduction test PECRT ► p. 563). This sampling scheme
was recommended in a guideline published by WAAVP
in 1992. However, recent studies revealed that several
sources of variability have been neglected, for example
the large inherent, time-dependent variability of egg
counts in individual animals, the distribution of eggs in
faecal samples conforming a Poisson process, differences
of egg production of various nematode species, and
variations in the technical performance of egg counting
procedures. As many of the previous resistance studies
may have been hampered by inadequate methodology,
proposals for improved approaches and procedures,
including statistical methods, have been described
in the recent literature and should be consulted (see
Torgerson et al., 2012). Consequently, there has been
a recommendation to re-evaluate the FECRT and to
re-define the WAAVP recommendations (see Calvete
and Uriarte, 2013). In control programs with 'targeted
treatments' (► p. 593) of adult horses(>4 years) only
animals with egg shedding exceeding a certain threshold
(e.g. >200 epg) are subjected to anthelmintic treatment
within a group of grazing animals. In this indication egg
counts provide information on the role of individual
animals for pasture contamination, but they do not
usually provide conclusions regarding the worm burden.
Test kits and devices. McMaster chambers
are commercially available (check for sources at
Cl)
c::
parasitological institutions)
·u
'6
Cl)
FLOTAC®. A special device (FLOTAC apparatus) �
allows a combination of flotation by centrifugation �
followed by counting of parasite stages in 2 chambers co
c::
·c:
that can accommodate more faecal suspension (5 ml per Cl)
chamber) than the usual McMaster counting slides(see
above). This method requires special equipment, but has c::
the advantage that coccidia oocysts, helminth eggs and >,
Ol
nematode larvae are detectable. In a recent evaluation 0
0
85-100% of faecal samples were found positive when ·u5
they contained at least 15 Ascaris, Toxocara or Trichuris co
co
eggs per gram. 0...
 Part V. Diagnostics
SAFC technique
Principle and method. This method is particularly
suitable for detecting encysted and vegetative stages
of protozoa (e.g. trophozoites of Giardia, Entamoeba),
but it also recovers stages of helminths. Faecal samples
are used, which are preserved in SAF solution (SAF:
sodium acetate-acetic acid-formalin; composition:
4.5 g sodium acetate, 6.0 ml concentrated acetic acid,
12.0 ml formalin [ = 3 7% solution of formaldehyde],
3 1 aqua dest.). Since the SAF solution contains 1.5%
formaldehyde, accompanying viruses, bacteria and
thin-walled protozoan cysts will be killed, but not
resistant parasite stages, such as Taenia and Echinococcus
eggs or Eimeria oocysts. By processing the sample,
fat components are removed, and parasite stages are
concentrated. The SAFC technique is primarily used
for faecal examinations of carnivores, other pet animals
(reptiles, etc.) and zoo animals (e.g. monkeys). The steps
of the procedure are shown and described in ► Figure
16.4.
Suitability. Vegetative and encysted stages of protozoa,
eggs and larvae of helminths (including eggs of
trematodes and taeniids). Unsuitable for detection of
Cryptosporidium oocysts and spores of Microsporidia.
Less quantitative efficient than ST and CSFT.
Comment. Caution: danger of explosion if diethyl
ether is improperly handled; observe special rules! Use
explosion-proof centrifuges! In some laboratories diethyl
ether is replaced by ethyl acetate.
Flotation and sequential sieving (FSS)
An efficient enrichment of helminth eggs from faecal
samples (2- IO g) can be achieved by a combination of
flotation in zinc chloride solution (sG 1.45) followed
by sequential sieving using sie. ves with decreasing
mesh sizes (21-200 µrn). By selecting an appropriate
mesh size of the last sieve, eggs can be concentrated
from faecal suspensions allowing more efficient and
cheaper isolation of DNA used for further analyses.
This procedure has become a standard for the isolation
of eggs of Toxocara and taeniid cestodes (Taenia spp.,
Echinococcus spp.) from faecal samples of carnivores
(dogs, wolves, foxes) collected in the environment or
soil samples(for details, see Mathis et al., 1996).
Baermann technique for detecting nematode
larvae (syn. Baermann-Wetzel technique)
Principle. Living nematode larvae move out from
faeces (soil, animal tissues) into surrounding water and
are concentrated in a funnel(► Figure 16.5).
Method
• The stem of a glass or plastic funnel (upper rim
diameter about 10 cm) is connected to a 10 cm long
piece of soft PVC or silicone tube. The tube is closed
with a pinch clamp, attached at an acute angle to the
tip of the tube.
• The funnel is placed in a holder (ring) of a stand (or
a device with several holders) and partially filled
with tap water.
• A faecal sample is placed on a piece of gauze
(approximately 15xl5 cm) and wrapped up. 10-30 g
faecal samples of large animals (cattle, horse) or 5-10
g of smaller animals (small ruminants, carnivores)
are used. Soft faeces are mixed beforehand with
sterilised sawdust to a crumbly mass. Alternatively,
the mixture can be applied to a fine mesh screen.
The gauze bag (or sieve) is transferred to the funnel
and immersed halfway into the water.
• The funnel is left to stand at room temperature for
12-24 h. The larvae move out of the faeces and sink
to the tube tip.
• By cautiously opening the pinch clamp, a few drops
of the liquid are allowed to drain into a plastic Petri
dish with engraved counting grid.
• Microscopic examination (and counting if
required) at low magnification (compound or
stereomicroscope), identification of larvae at
higher magnification. After addition of 1 drop of
diluted Lugo! solution, the larvae are fixed and
stained so that the main morphological features
are recognisable. (Caution: undiluted Lugo! solution
causes degeneration of internal larval structures).
Suitability. The technique is especially suited for
recovery of larvae of lungworms, Angiostrongylus and
Strongyloides stercoralis from faeces. If older faecal
samples are used, larvae hatched from eggs of other
Strongyloides species or strongyles may also be recovered.
Sensitivity strongly depends on the density of larvae in
the faecal sample and on larva.I activity.
Comment. The reliability of detecting larvae of
Dictyocau/us viviparus decreases significantly at
temperatures above 25 °C. Therefore, faecal samples from
cattle should be examined immediately after collection;
otherwise, they can be stored in the refrigerator (+
5-9 °C), but no longer than 24 h. Although larvae of D.
Ji/aria are less sensitive to higher temperatures, faecal
samples from small ruminants should be treated like
samples from cattle. As the larval density in the samples
is often low, sufficiently large faecal samples should be
examined (see above).

1. Sample tube with 10 ml
SAF solution
4. Decant the supernatant , add
8 ml of physiological saline
solution and stir the sediment
with a stick
7. Detach detritus layer from
tube wall and decant supernatant
Figure 16.4. SAFC method (Graphics: IPZ, M. Mathys).
16. Diagnostics
2. Add 1 g frosh faeces ond 3. Pour half of the suspension
agitate Intensively through gauze Into centrifuge
tube and centrifuge 2 min
(500xg)
SAF/NaCI
. ..
Sediment
5. Add 3 ml diethylether, close 6. Remove stopper and
the tube with stopper, and centrifuge 5 min (500xg);
mix the content by gentle several layers are formed
shaking after centrifugation
•0 0
8. Transfer two (or more drops) of the sediment to a slide.
Add to half of the drops mall drop of diluted (1:10)
Lugol's solution'. Cover drops with cover slips and examine
microscopically
·Lugol's solution: potassium iodide: 10 g, iodine crist. 5 g, aqua dest. ad 100 ml
 Part V. Diagnostics

Recovery of larvae from the culture

• Open the glass and press the faecal mixture down
slightly with a pestle or a spoon.
• Fill the glass very carefully with tap water close to
the brim, so that the culture mixture is not disturbed
Water level
and remains adhered to the bottom of the glass.
Gauze bag with • Press the lid of a glass Petri dish firmly to the opening
faeces/sawdust of the culture glass, then turn the culture upside
mixture (alternative: down (180 °) ( ► Figure 16.6).
faeces placed on • Fill the Petri dish halfway with water and let the
metal screen)
culture system stand for 12 h.
• Larvae pass below the uneven rim of the culture glass
into the fluid of the Petri dish and accumulate there.
The fluid in the Petri dish, containing the larvae, is
largely free of faecal particles; it can be aspirated
with a pipette and used for microscopic examination
(differentiation of larvae ► p. 541 and ► p. 546).

Suitability. The method is suitable for recovering third

PVC tubing stage larvae of gastrointestinal nematodes (including
Trichostrongylidae, Oesophagostomum, Chabertia,
Strongylus, Cyathostominae, Bunostomum) and
Strongyloides of cattle, sheep, goats, horses, pigs and
Diagonally other species, e.g. wild ruminants and several species
attached pinch clamp of zoo animals). Since fairly large amounts of faeces
are used, this method is often more sensitive than the
egg counting technique or the FT, especially at low
egg density in faeces. Not suitable for the detection of
lungworm larvae.

Figure 16.5. Baermann funnel for detecting larvae (Graphics: Agar plate method for detection of
IPZ, M. Mathys). Strongyloides and hookworm larvae

A small faecal sample is placed in the centre of an agar

Coproculture for recovering third stage plate and incubated at 26-33 °C for 48 h. The surface
larvae of gastrointestinal nematodes of the agar is then rinsed with physiological saline,
and drops of the fluid are transferred to a slide for
Principle. Eggs of many genera of gastrointestinal microscopic examination. This method is useful for the
nematodes (trichostrongylids, strongylids) are examination of samples from carnivores and monkeys.
indistinguishable in fresh faecal samples. Since
morphological characteristics of third stage larvae allow
a differential diagnosis at genus level, they are grown in
coprocultures (also referred to as faecal or larval culture).

Preparation of cultures Faeces/

• Faeces (at least 50 g from cattle and horses, 20-30 sawdust
Q) mixture
C g from smaIJ ruminants and pigs) are thoroughly
·5 mixed with sterilised sawdust to a moist crumbly
'6
�
Q)
mass; if appropriate, moisten with tap water, but be
c
co
careful that the water remains absorbed to the mass.
• The mixture is transferred to a screw-top jar (e.g.
Water

C
·.:: jam jar, 500 ml) which is fiUed halfway and loosely Water wrth
Q)
migrated
dosed with the lid. larvae
C • Cultures are incubated for 7-10 days in the dark at
>­ 25 °C. In diffuse light and with sufficient moisture,
CJ)
0 L3 may migrate upwards on the glass walls thereby
0
·u5
forming net-like trails. Figure 16.6. Coproculture turned upside down (Photo: IPZ).
co
co
a.

Adhesive tape method
Method. A transparent tape, about 4 cm long and I cm
wide, is pressed with the adhesive layer onto the dry anal
and perianal skin, removed and placed with the adhesive
side down smoothly on a glass slide and examined
microscopically. Prepare several tapes per animal.
Suitability. Detection of pinworms eggs in horses and
monkeys, eggs of Taeniidae (Taenia and Echinococcus)
in carnivores.
Detection of Cryptosporidium
Oocysts of Cryptosporidium can be detected in thin
faecal smears after staining or by immunodiagnostic
methods. In smears after modified Ziehl-Neelsen
staining(test kit commercially available), oocysts appear
as pink-coloured objects (4-6 µm in diameter) on a
greenish background ( ► Figure 5.20, p. J 26). After
carbol fuchsin staining according to Heine, oocysts are
visible as colourless structures on a reddish background.
Alternative methods include the immunodiagnostic
visualisation of oocysts in smears using monoclonal
antibodies(test kit: PARA-TECT ™ , Medical Chemical
Corp., USA) and copro-antigen detection(ImmunoCard
STAT-, Meridian Bioscience Inc., USA; FASTest•
Cryptostrip, Vet.Laboratory Supplies, UK). DNA
analyses are applied for typing species and strains.
Autofluorescence microscopy
Certain parasite stages(e.g. coccidia oocysts and cysts
of Balantidium) exhibit autofluorescence when excited
by UV light (filter: 330-385 nm) which facilitates the
microscopic identification of these pathogens.
Detection of Microsporidia
Spores of Microsporidia are detectable in smears of
faeces, urine sediment or other materials(e.g. CSF) by
light microscopy after trichrome staining or by UV­
microscopy after staining with fluorochromes (e.g.
Calcofluor •, Uvitex 2B •). Sometimes the concentration
of spores in samples is so low that they can only reliably
be detected by DNA amplification.
Immunological and molecular techniques
Copra-antigen detection in faecal samples is used for
diagno sing various intestinal parasites, such as Fasciola
in ruminants, cestodes (Taenia and Echinococcus in
carnivores) or Cryptosporidium and Giardia(► Table
16.1). For example, rapid diagnostic tests are available for
detecting copro-antigens of Giardia and Cryptosporidia
in various animal species(FASTest•, Megacor, AT). By
means of DNA analyses, protozoa, and various stages
of helminths or arthropods can be diagnosed at the
species, strain or genotype level.
16. Diagnostics
16.1.4.4 Detection of parasites in urine
In urine sediments, eggs of Capillaria plica and of
the renal worm Dioctophyma in carnivores as well as
eggs of Stephanurus gyrus in pigs can be demonstrated
microscopically(detection of Microsporidia see above).
16.1.5 Methods for post mortem
parasite detection
16.1.5.1 Parasitological dissection of the
gastrointestinal tract
Principle. The aim of the parasitologicaJ section is the
recovery of parasite stages present in the gastrointestinal
tract, qualitatively and preferably also quantitatively, as a
basis for assessing the role played by the parasite burden
in pathogenesis. Such examinations are performed most
often in ruminants for the detection of gastrointestinal
nematodes and other helminths. Lesions of the
gastrointestinal tract may be indicative of the severity
of a disease and the etiological role of parasites.
Examination of the gastrointestinal tract of
ruminants for nematodes
Material. A reliable estimation of the worm burden
is only possible if the entire gastrointestinal tract is
available for investigation. After removal of the gut at
necropsy, double ligatures are placed at the anterior and
posterior ends of the abomasum as well as the small and
large intestine to prevent leakage of contents.
Method
• Take a faecal sample from the rectum and process it
according to the combined flotation-sedimentation
technique.
• Remove mesentery and excess of fat from abomasum
and intestine with a sharp knife or scissors. Place
entire gut on the necropsy table, spread and
examine it for pathological changes(haemorrhages,
oedematous swellings, adhesions, etc.). Separate
abomasum, small and large intestine by cutting
through between the two ligatures and place the
organs separately into large pans.
• Open the organs with intestinal scissors. Examine
the mucosa, prepare swabs or smears of the mucosa
for direct microscopic examination if indicated( e.g.
for detection of Eimeria stages).
• Transfer each organ with contents separately into
a plastic bucket, rinse and wash the mucosa of
abomasum and large intestine thoroughly under a
slow running jet of water and squeeze the entire small
intestine twice between two fingers so that contents
and mucus are carefully removed and collected.
• Pass the washing fluid of abomasum and small
intestine separately through a fine mesh sieve under
a strong water jet(► Figure 16.7b)(metal sieves,
diameter 25 cm, frame height 5 cm; mesh size for
 Part V. Diagnostics

adult nematodes of abomasum and small intestine the animal and (f) other causes of disease. For example,
150-200 µm, for larval stages 38-50 µm; for adult in young cattle, infections with> 15,000 adult Ostertagia
nematodes of large intestine 600 µm ( ► Figure ostertagi stages or with >200 adult Bunostomum sp. per
16.7a). animal are considered as relevant infection intensities.
• Transfer the sieve residue into a dissecting pan and Lambs can already exhibit clinical signs when infected
remove the remains from the screen surface by with a few hundred adult Haemonchus contortus, while
reverse flushing with a water jet. worm burdens> 1000 of Teladorsagia or Trichostrongylus
• For quantitative determination of the worm burden, do not usually induce clinical symptoms.
transfer the entire sieve residue into a large vessel,
add water or physiological NaCl up to a certain Detection of mucosa! stages of
volume (e.g. 2 or 4 1), mix it thoroughly and take gastrointestinal nematodes in ruminants
several aliquots up to a volume of 5% or 10%
(abomasum and small intestine), and 20% (large The recovery of Ostertagia ostertagi stages from the
intestine) of the total volume with a kitchen ladle. abomasal mucosa requires special methods, either the
Larger aliquots may be needed if low worm burdens incubation or the digestion method ( details see Wood
should be recovered. et al., 1995).
• The samples can be stored for some days in a
refrigerator or preserved with formalin (final Examination of the gastrointestinal tract of
concentration 1-2%) for later examination. horses for nematodes
• Pour small portions of the samples into a plastic Petri
dish with counting grid, examine the fluid in a thin A detailed methodology has been recommended by the
layer using a stereomicroscope, count the parasites WAAVP (Duncan et al., 2002). Larval stages of small
and collect a representative sample for identification strongyles (cyathostomes) are detected by transmural
of genera and species using a compound microscope. illumination (mucosa pieces are stretched over a light
• Washing fluid of the large intestine is examined source and examined under a dissecting microscope)
in thin layer in a dissecting pan with dark bottom or by the digestion method (for details, see Eysker and
for macroscopically visible nematodes ( Oesophago­ Klei, 1999).
stomum, Chabertia, Trichuris).
• The recovery of mucosa! stages of nematodes Examination of the intestinal tract of
requires special methods (see below). carnivores for Echinococcus species

Assessment of parasitological findings. Hardly
any farm animal with a grazing history is free of
gastrointestinal parasites. Therefore, it is often difficult to
make a distinction between a subclinical and a clinically
significant parasitic infection. The following factors are
relevant for assessing the findings: (a) numbers of adult
and juvenile stages of each parasite species, (b) spectrum
of species in mixed infections, (c) pathogenicity of
involved parasite genera or species, (d) age and immune
status of the ruminants (animals of the I 51 grazing season
are highly susceptible, older animals are usually partially
immune), (e) general condition and nutritional status of
Special methods are needed for screening the small
intestine of carnivores for Echinococcus species because
of the small size of the parasite. Two techniques are
preferentially used: the intestinal smear technique
(1ST) or the more sensitive sedimentation and counting
technique (SCT) (Conraths and Deplazes, 2015, Craig
et al., 2015). Because of the infection risk for humans
during handling organs that potentially contain infective
Echinococcus eggs, special safety regulations have to
be observed. Echinococcus eggs can be killed before
dissection by deep-freezing the unopened intestines
for at least 4 days at -70 °C.

Figure 16.7. Parasitological dissection: (a) sieve and instruments for dissection of the gastrointestinal tract; (b) sieving of washing
fluid of the gastrointestinal tract, under strong water jet (Photo: IPZ).

6.1.5.2 Parasite detection in liver and lung
Fascio/a and Dicrocoelium infections in the liver can
be diagnosed by detecting eggs in the sediment of gall
bladder contents or by opening of bile ducts (detection
of juvenile and adult Dicrocoelium and Fasciola stages)
and cutting the liver into thin slices (detection of
migrating Fasciola stages). Recovery of juvenile Fasciola
stages is facilitated when thin liver slices (about 1.5 cm
thick) are incubated in physiological saline at 37 °C
overnight. The flukes tend to migrate out into the
medium, if not encapsulated.
Large lungworms (e.g. Dictyocaulus, Metastrongylus,
Crenosoma, Troglostrongylus) are detectable macro­
scopically after cutting open the trachea and bronchi
and/or in the washing fluid after rinsing the airways
with physiological saline.
Special perfusion techniques have been described for
effective recovery of Dicrocoelium from the liver of
ruminants, adult and juvenile stages of Dictyocau/us
viviparus from lungs of cattle, and A. vasorum
lungworms from carnivores (cats: Capillaria aerophila
and Aelurostrongylus abstrusus, dogs: A. vasorum and
C. aerophila).
6.1.5.3 Trichinella detection in
musculature
In the EU and Switzerland the officially prescribed
standard technique for post-mortem examination of
slaughter animals (pig, horse) and game (wild boar,
bear, badger, etc.) for Trichinella larvae is the digestion
method. The previously used trichinoscopy (more
precisely trichinelloscopy) was permitted in the EU until
2009. Serology has been proposed for surveillance but
up to now the technology has not been implemented
(► p. 380).
Digestion method
Principle and characteristics. The EU Regulation
2075/2005 (in force since 2005) considers the existence
of several Trichinella species which are infectious to
humans and a wide range of other hosts, including
carnivorous land mammals, marine mammals, reptiles
and birds ( ► p. 376). Therefore, all potential Trichinella
carriers, whose meat is destined for human consumption,
are subject to official control ('meat inspection'). Muscle
samples are artificially digested in pepsin-hydrochloric
acid solution, thereby releasing Trichinella larvae
which are detected microscopically in the digestive
fluid (in fluid sediment or on a filter membrane after
filtration). The EU regulations prescribe the magnetic
stirrer digestion procedure as reference, and list other
techniques as 'equivalent methods: Digestion methods
are suitable for mass screening; they recover both
16. Diagnostics
encapsulated and non-encapsulated larvae in fresh and
frozen meat.
Sampling. The following samples shall be taken for
examination:
• Pig. In case of whole carcasses of domestic pigs, a
sample of at least 1 g has to be taken from a pillar of (/)
-0
0
the diaphragm at the transition of the sinewy part. .c
For breeding boars and sows larger samples of 2 g
are prescribed. In the absence of diaphragm pillars,
samples of double weight have to be taken from a
rib part or a breastbone part of the diaphragm, or
from jaw muscle, tongue or abdominal muscles.
From cuts of meat and frozen meat, 5 g samples of
fat- and fascia-free muscle tissue are to be taken.
• Horse, wild boar and other potential Trichinella
carriers. Muscle samples of at least 10 g have to be
taken from predilection sites (horse: tongue and the
jaw; boar: foreleg, tongue, diaphragm; fox: foreleg,
diaphragm; bear: diaphragm, masseter muscle,
tongue; walrus: tongue; crocodiles: masseter muscles,
pterygoid and intercostal muscles; birds: head and
neck muscles).
6.1.5.4 Magnetic stirrer technique
The magnetic stirrer technique, considered as reference
for several variants of the digestion method, is described
briefly below (details in EU 2075/2005):
a. 16 ml of 25% hydrochloric acid are added to a 3
I beaker containing 2 1 of tap water, placed on a
magnetic stirrer preheated to 46-48 °C; a stirring
rod is added, and stirring is started.
b. 10 g of pepsin are added to the liquid.
c. A pooled sample of 100 g muscle tissue in total is
chopped in a blender (such a pooled sample may
be composed of 1 g samples from 100 pigs or 10 g
samples from 10 horses).
d. The entire chopped sample is transferred to the
3-litre beaker containing the pepsin-hydrochloric
acid solution (digestion fluid, see a), the beaker is
covered with aluminium foil.
e. Efficient stirring has to be ensured during the entire
digestive process at a constant temperature of 44-
46 °C.
f. Digestion of the sample until meat particles have
disappeared (about 30 min for diaphragm muscle,
other specimens (game) may require up to 60 min).
g. Pouring the digestive liquid through a stainless steel
sieve (external diameter 11 cm, mesh size 180 µm)
into a separatory funnel (capacity 21).
h. After 30 min, 40 ml of digestion fluid are drained
into a centrifuge tube or graduated cylinder. After
10 min, 30 ml of the supernatant are removed, and
the sediment is examined in a counting dish under
a stereomicroscope or a trichinoscope for Trichinella
larvae.
Part V. Diagnostics
i. Trichinella larvae are to be regarded as infectious.
Contaminated instruments must therefore be
disinfected by heat >80 °C.
The lower limits of detection (number of larvae per
gram of muscle =L/g) of different methods are recorded
as follows: trichinelloscopy: 3 L/g; digestion of 100
samples of 1-5 g: 1 L/g; digestion of lx 20 g sample:
0.05 L/g. Trichinella larvae isolated by digestion have
to be identified by morphological criteria considering
migrating larvae of ascarids (Ascaris, Toxocara) and
artefacts (hairs, plant fibres) in differential diagnosis.
Since 2011 the EU has approved a latex agglutination
test as a method equivalent to the microscopic detection
of Trichinella larvae in meat of domestic swine (EU No.
1109/2011). However, both methods do not allow a
species diagnosis. In case of positive results, the samples
are therefore to be sent to a reference laboratory (http://
www.iss.it/site/Trichinella/index.asp) for genetic species
determination.
Antibody detection and PCR
Trichinella infections can be diagnosed by serological
detection of specific antibodies in meat juice or sera from
slaughter pigs. The serological methods are not approved
in the EU. DNA analyses have become important for the
identification of Trichinella species and isolates.
16.1.6 Hints for microscopic
identification of parasite
stages
The following features are important in diagnosing
helminth eggs and cyst/oocysts of protozoa: shape (e.g.
round, oval, polygonal, lemon-shaped), size, features of
the envelope (=egg shell, cyst wall) (thick-walled, thin­
walled, surface smooth, rough, dented, etc.), colour and
characteristics of the wall (e.g. operculum, pole plug,
micropyle) and contents (helminth eggs: unsegmented
egg cell, blastomeres, embryo or larva; protowan cysts:
number of sporocysts and sporozoiles, other structures).
In assessing the contents of eggs and coccidia oocysts,
the time which has elapsed since collection of the fresh
sample has to be considered.
Living larvae of lungworms, gastrointestinal strongyles,
Strongyloides and hookworms are easy to recognise
in fresh native preparations due to their motility, but
only some of them exhibit structures for immediate
identification in the native state, for example lungworm
larvae. Other larvae have to be fixed for morphological
identification by heat (carefully heating a drop of fluid
with larvae over the flame of a Bunsen burner) or by
adding a drop of LugoI solution diluted I: I 0.
More information on the identification of diagnostic
stages of parasites in ► Figures 16.8 to 16.18.
16.1.7 Examination of environmental
samples
Special techniques are required to find parasite stages
in environmental samples, for example the detection of
strongyle larvae on pasture plants, of helminth eggs in
soil, wastewater or manure, of Cryptosporidium oocysts
and Giardia cysts in surface and drinking water. The
reader is referred to specialised literature in this matter.
Molecular methods are increasingly used for detecting
parasite stages in the environment with high precision,
such as Echinococcus eggs in faecal samples deposited
by wild or domestic carnivores.
16.1.8 Preservation of helminths
and arthropods
Trematodes and cestodes are rinsed with water or
physiological NaCl solution and fixed in 70% ethanol.
Living cestodes should be kept beforehand in water until
they are immobile. Thick specimens are gently pressed
between two glass plates held together by rubber bands,
and 70% ethanol is filled with a pipette into the space
between the plates. Dry cestode segments are soaked
in water before preservation. Nematodes are fixed in
70% ethanol, containing 2-5% glycerol. Fixation in hot
(70 °C) ethanol-glycerol achieves a better stretching
of nematodes. A suitable fixative for small nematodes
is 2-4% formalin solution. Arthropods are preserved
in 70% ethanol. The use of ethanol as fixative has the
advantage that the material is also suitable over long
periods for DNA analyses.
- Selected references------
Ballweber LR, Beugnet F, Marchiondo AA, Payne PA (2014)
American Association of Veterinary Parasitologists' review
of veterinary fecal flotation methods and factors influencing
their accuracy and use--is there really one best technique?
Vet Parasitol 204: 73-80.
Calvete C, Uriarte J (2013) Improving the detection of
anthelmlntlc resistance: evaluation of faecal egg count
reduction test procedures suitable for farm routines. Vet
Parasitol 196: 438-452.
Conraths FJ, Deplazes P (2015) Echinococcus multilocularis
epidemiology, surveillance and state-of-the-art diagnostics
from a veterinary public health perspective. Vet Parasitol
213: 149-161.
Craig PS, Mastin A, Van Kesteren F, Boufana B (2015)
Echinococcus granulosus: epidemiology and state-of-the­
art of diagnostics in animals. Vet Parasitol 213: 132-148.
Cringoli G, Rinaldi L, Maurelli MP, Utzinger J (2010) FLOTAC:
new multivalent techniques for qualitative and quantitative
copromicroscopic diagnosis of parasites in animals and
humans. Nat Protoc; 5: 503-515.
 16. Diagnostics

oemeler J, Knapp F, Corte GM, Katzschke 0, Steininger Wood 18, Amaral NK, Bairden K, Duncan JL, Kassai T,
K, Von Samson-Himmelstjerna G (2012) Recovery Malone JB, Pankavich JA, Reinecke RK, Slocombe
of strongylid third-stage larvae from herbage samples: 0, Taylor SM, Vercruysse J (1995) World Association
standardisation of a laboratory method and its application for the Advancement of Veterinary Parasitology (WAAVP)
in the field. Parasitol Res 110: 1159-1164. second edition of guidelines for evaluating the efficacy of
Duncan JL, Abbott EM, Arundel JH, Eysker M, Klei T R, anthelmintics in ruminants (bovine, ovine, caprine). Vet
Krecek RC, Lyons ET, Reinemeyer C, Slocombe JO Parasitol 58: 181-213.
(2002) World Association for the Advancement of Veterinary Van Wyk JA, Cabaret J, Michael LM (2004) Morphological
Parasitology (WAAVP): second edition of guidelines for identification of nematode larvae of small ruminants and
evaluating the efficacy of equine anthelmintics. Vet Parasitol cattle simplified. Vet Parasitol 119: 277-306.
103: 1-18. Vidyashankar AN, Hanlon BM, Kaplan RM (2012) Statistical
Eckert J, Gemmell MA, Meslin F-X, Pawlowski ZS (eds.) and biological considerations in evaluating drug efficacy in
(2001) Manual on Echinococcosis in humans and animals: equine strongyle parasites using fecal egg count data. Vet
a public health problem of global concern. Paris, France: Parasitol 185: 45-56.
World Organisation for Animal Health. Available at: http://
tinyurl.com/olwancf.
European Commission (2005) Commission Regulation (EC) No.
2075/2005 of 5 December 2005 laying down specific rules
on official controls for Trichinella In meat. Official Journal of
European Union, 22.12.2005, L 338: 60-82.
European Union (2011) Regulation (EU) No. 1109/2011 of 3
November 2011, amending Annex I to regulation (EC) No.
2075/2005 as regards the equivalent methods for Trichlnella
testing.
Eysker M, Klei T R (1999) Mucosal larval recovery techniques
of cyathostomes: can they be standardized? Vet Parasitol
85: 137-144.
Kaufmann C, Steinmann IC, Hegglin D, Schaffner F, Mathis
A (2012) Spatio-temporal occurrence of Culicoides biting
midges in the cllmatlc regions of Switzerland, along with
large scale species Identification by MALDI-TOF mass
spectrometry. Parasit Vector 5: 246.
Kochanowski M, Karamon J, Dc1browska J, Cencek T (2014)
Experimental estimation of the efficacy of the FLOTAC basic
technique. 1. J Parasitol 100: 633-639.
Mathis A, Deplazes P, E ckert J (1996) An Improved test
system for PCR-based specific detection of Echlnococcus
multilocularis eggs. J Helmlnthol 70: 219-222.
Pallen MJ (2014) Diagnostic metagenomics: potential applications
to bacterial, viral and parasitic infections. Parasitology 141 :
1856-1862.
Rinaldi L, Levecke B, Bosco A, Ianniello D, Pepe P, Char lier
J, Cringoli G, Vercruysse J (2014) Comparison of Individual
and pooled faecal samples in sheep for the assessment of
gastrointestinal strongyle Infection intensity and anthelmlntic
drug efficacy using McMaster and Mini-FLOTAC. Vet Parasitol
205: 216-223.
Stothard JR, Adams E (2014) A preface on advances In
diagnostics for Infectious and parasitic diseases: detecting
Parasites of medical and veterinary importance. Parasitology
141: 1781-1788.
Torgerson PR, Paul M, L ewis Fl (2012) The contribution of
sim ple random sampling to observed variations in faecal egg
counts. Vet Parasitol 188: 397-401 .
 Part V. Diagnostics
16.2 Diagnostic plates
Diagnostically significant parasite stages occurring
in different host species are depicted in the following
diagnostic plates. It should be noted that in this book
only a selection of stages can be presented, not the
complete spectrum. Often different dimensions of
various parasite stages are recorded in the literature
(e.g. oocysts of protozoa and helminth eggs). This is due
to the fact that size measurements are often performed
on small numbers of parasite stages by different authors
with inconsistent fixation methods. Therefore, data
on sizes are usually regarded as approximate values.
To describe the egg envelope of helminths, the terms
shell, wall or egg capsule are used. We apply here the
uniform term 'wall' to both envelops of eggs and cysts/
oocysts of protozoa.
16.2.1 Ruminants
Characteristics of parasite stages (selection)
of ruminants
► Figure 16.8.
Explanations:C: cattle; G: goat; L: larva; 0: occurrence;
S: sheep; range: size range of several species.
• Trematode eggs
Fasciola hepatica: large (130-145x70-90 µm), thin­
walled, with operculum (lid) at one pole, golden­
yellow, completely filled with granular material
(zygote and yolk cells). 0:C, S,G.
Paramphistomum cervi: large (140-180x76-95 µm),
thin-walled, on average slightly larger than F.
hepatica eggs, with operculum at one pole, light
grey, completely filled with granular material (zygote
and yolk cells). 0:C (S, G).
Dicrocoelium dendriticum: small (38-45x22-30 µrn),
slightly asymmetrical, with operculum, dark brown,
with miracidium containing 2 spherical structures
(germ cells). 0: C, S, G.
• Cestode eggs
Moniezia spp.: medium-sized M. expansa (60-78
µm), M. benedeni (70-90 µm) irregularly rounded/
rectangular-shaped, thick-walled, contains
an oncosphere, surrounded by pear-shaped
embryophore (pear-shaped apparatus). 0:C, S, G.
• Nematode eggs
Nematodirus spp.: very large egg, wall of medium
thickness, contains fewer than I 6 blastomeres.
• N. battus (152-182x67-77 µm): almost parallel
side walls, brownish, poles rounded. 0: S (C, G).
• Nematodirus spp. (range I50-200x75-IO0 µm):
curved side walls, poles more tapered. 0:C, S, G.
Trichostrongyles, Oesophagostomum, Chabertia:
medium-sized eggs (range 70-98x30-50 µm),more
than 16 blastomeres, thin-walled, oval with equal
poles or one more tapered pole, colourless. Eggs
very similar,differentiation by identification of L3.
O:C,S,G.
Bunostomum spp.: medium-sized eggs (range
75-104x45-60 µm), thin-walled, elliptical with
slightly flattened poles, contents: in fresh faeces
4-8 dark blastomeres. B. phlebotomum eggs often
with adhering particles on surface; in advanced
embryonic development not reliably identifiable.
Differentiation from trichostrongyle eggs, etc. by
identification of L3. 0: C, S, G.
Strongyloides papillosus: small eggs (40-55x30-40
µm),thin-walled,wide ellipsoid with flattened poles,
colourless, with embryo. 0:C, S, G.
Toxocara vitulorum: medium-sized (70-95x60-
77 µm), spherical, thick pitted shell (golf ball
like), greyish or with yellowish tinge, contents
unsegmented, grainy. 0: C.
Triclmris spp.: medium-sized (70-80x30-42 µm),
thick-walled,lemon-shaped, curved side walls,with
2 transparent polar plugs,dark brown, unsegmented
contents. 0: C,S, G.
Capi/laria spp.: small (45-50x22-25 µm) thick walls,
side walls almost parallel, with 2 transparent, flat
polar plugs, dark brown, unsegmented contents.
O:C,S,G.
• Protozoan oocysts
Eimeria spp. ( ► Figure 16.9)
♦ E. zuernii: small (15-22x 13-18 µm), almost
spherical, thin-walled, colourless, contents:
spherical sporont. 0: C.
• E. bovis: small (23-24xl7-23 µm), oval, thin­
walled, orange brown, indistinct micropyle,
contents: spherical sporont. 0: C.
Cryptosporidium spp.: very small ( 4-5 µm),
spherical. 0: C, S, G.
• Nematode larvae
Dictyocaulus spp.: LI, length >300 µm, unsheathed,
oesophagus indistinct,midgut granulated.
• D. viviparus: 315-370 µm posterior end short and
pointed. 0:C.
♦ D. Ji/aria: 490-520 �un, anterior end with button­
like protrusion of the cuticle ('head knob'},
posterior end truncated. 0: S, G.
Protostrongylidae: L l, length 250-450 �1m,
unsheathed, entire body usually transparent
(oesophagus indistinct, midgut without or only a
few granules). Posterior end with genus-specific
structures ( ► Figure I 6.8).
 16. Diagnostics

µm
150

-�

100 .E

50

Fasc/ola Paramphlstomum Nematodlrus Nematodirus spp.

hepatica cetVI battus
µm
100

50

Dicrocoe/ium Moniezia spp. Trichostrongylids, Bunostomum Bunostomum Strongyloides

dendriticum Oesophagostomum, trigonocephalum phlebotomum papillosus
Chabertia
µm
100

'
50

@ � •
Toxocara Tr/churls spp. Cap/Ilaria spp. Eimeria Eimeria Cryptosporidium spp.
vitulorum zuernli bovis

b D (ctyocou/us viviparus , laiva 1 (315_370 µm) Protostrongylid a Protostrongylus rufescens b Mue/lerius copilloris
0tctyocou/us
f,lorio, larva (490 laJVa 1 (250-450 µm) c Cystocoulus ocreotus d Neostrongylus lineoris
1 _520 µm)
Figure
16·8• Cop rosc opically detectable parasite stages in ruminants (Source: IPZ, S Ehrat).
Part V. Diagnostics

Key for identification of sporulated Eimeria

oocysts of cattle

Using Eimeria spp. of cattle as an example, it is shown � ·-· ·. ·"' .,-- .,,,. . ,·•

here that species determination is based on the RQoeysts wl:th micropyle

morphology of sporulated (partly also unsporulated) maximumdimension <45 µm
oocysts and the sporulation time, determined under Oocysts ovoid or subspherical, E. bovis
constant conditions(► Figure 16.9). The recognition of orange-brown, micropyle indistinct,
fine features requires expertise. Some coccidia species, with OR and SR, 23-34x17-23 µm
for example most of the Eimeria species of chickens, can (27.7x20.3 µm), ST: 2-3 d
only be identified on the basis of biological or genetic Oocysts ovoid, colourless or pale E. canadensis
characteristics. For information on coccidia of other yellow, without OR, SR of some
granules, 28-37x20-27 µm (32.5x23
animal species, see specialised literature.
4 µm), ST: 3-4 d
Oocysts ovoid, thick-walled, yellow E. wyomingensis
brown, without OR without SR,
wide micropyle, 37-45x26-31 µm I
maximumdimension <15 µm
(40.3x28.1 µm), ST: 5-7 d I
Oocysts elongated oval, yellowish- E. auburnensis
Oocysts round or subspherlcal, E. subspherica brown, wall smooth or finely
colourless, without OR and SR,
granulated surface without OR, SR,
9-14x8-13 µm (11 x10.4 µm), ST:
32-46x20-25 µm (38.4x23.1 µm),
4-Sd
ST: 2-3 d
maximumdlmen
Oocysts ellipsoid, yellow-brown, E. brasiliensis
E.zuemll mlcropyle with a clear plug, without
OR, SR, 33-43x24-30 µm (37x27
µm), ST: 12-14 d
E. elllpsoldalls Oocysts oval, thick brown wall with E. pellita
without uniformly distributed protuberances,
(23.4x15, without OR, SR, 36-41 x26-30 µm
Oocysts oblong, 00lourless, without E. cytindrica (40x28 µm), ST: 10-12 d
OR,SR, 16-27x12•16 i,nt(23i{3x12.3 maximumdimension >45 µm
µm,ST:2d Oocysts pear-shaped or oval, one E. bukidnonensis
Oocysts ovoid, oolourfees, without E. alabamensis pole tapered, thick, radially striated,
OR without SR, 13-24><11-16 µm yellowish-brown wall, 4 7-50x33-38
,ST: 5-8d µm (48.6x35.4 µm), ST: 4-7 d
Abbreviations: d = day; OR = oocyst residual body; SR = sporocyst
residual body; ST = sporulation time; dimensions in brackets =
average.

40µm

E. subspherica E. zuernil E. ellipsoidalis E. cylindrica E. a/abamensis E. bovis E. canadensis

E. wyomingensis E. auburnensis E. brasi/iensis E. pellita E. bukidnonensis

Figure 16.9. Eimeria species in cattle: sporulated oocysts (Source: IPZ, J. Eckert).
 16. Diagnostics

Simplified key for the differential diagnosis Larvae with 16 intestinal celJs
of third larvae of gastrointestinal nematodes • Tail ofsheath short, larvae usually not longer than
of sheep 760 µm: Trichostrongylus.
♦ Tail of sheath short, but larva >780-900 µm:
Teladorsagia.
♦ Tail ofsheath ofmedium length, slightly flattened en
Explanations: L: length oflarva including tail ofsheath; anterior end, with refractile globules (arrow) (L: +-
c
ro
tail ofsheath: distance from posterior end oflarval body 710-850 µm): Cooperia curticei. C
to end ofsheath. ♦ Tail ofsheath ofmedium length, front end rather .E::::,
tapered, without refractile globules (L: 650-790 a:
• Larvae without sheath µm): Haemonchus.
- Larvae slender, oesophagus almost halfas long as the Larva without clearly identifiable intestinal cells
whole body, L: 520-655 µm: Strongyloides. ♦ Oesophagus divided into two parts, quite small
larva (L: 515-670 µm): Bunostomum.
• Larvae with sheath
- Larvae with 8 intestinal cells, usually large larva ( L:
>750 to 1,130 µm), tail ofsheath long: Nematodirus
(L3 rarely appear in coprocultures because their
development takes longer or they do not develop
in culture).
- Larvae with 32 intestinal cells, medium and large
larvae (L: 720 to >800 µm), tail of sheath long:
Chabertia or Oesophagostomum. These two species
are difficult to distinguish.

1mm

Stongy- Haemon- Cooperia Buno- Tricho- Telador- Nematodirus Chabertia

loides chus stomum strongylus sagia

Figure 16.10. Gastrointestinal nematodes of sheep: third stage larvae (L3); arrow: retractile bodies (Source: IPZ, J. Eckert).
 Part V. Diagnostics

,......____Spiculum

� i
�::u�:m

Ostertagia ostertagi Cooperia oncophora

Ostertagia lyrata Cooperia zurnabada

Trichostrongy/us axei Cooperia punctata

Distal end of spicula

Q)

tapering to a jointed
C
Nematodirus he/vetianus Cooperia pectinata
·5
tip
'5
Q)
�
�
co
C
·;::
Q) Figure 16.11. Trichostrongyles of cattle: features of posterior ends of the males (Bursa copulatrix, spicules, and gubernaculum,

j if present) (Graphics: IPZ, A. Seeger; after Skrjabin 1954, and other sources).
.£
>,

-
0)
0
0

-co�
a..
 16. Diagnostics

Spiculum
Gubernaculum--ttc+a1

C
co
C
.E
::i

Haemonchus contortus Trlchostrongylus co/ubrlformls

a:

Te/adorsagia circumcincta Trichostrongy/us vitrinus

Te/adorsagia trifurcata Cooperia curticei

Trichostrongylus axei Nematodirus fi/icollis Distal end of spicula

(ventro-dorsal and
lateral view)

Figure 16.12. Trichostrongyles of sheep: characteristics of posterior ends of males (Bursa copulatrix, spicules, and gubernaculum,
if present) (Graphics: I PZ, A. Seeger; after Skrjabin 1954, and other sources).
Part V. Diagnostics

16.2.2 Equidae • Protozoan oocysts

Characteris tics of parasite stages (selection)
of equines
► Figure 16.13.
Explanations: size range: values for several species;
L: larva.
• Trematode eggs
Fasciola hepatica: large(130-145x70-90 µm), thin­
walled, with operculum (lid) at one pole, golden­
yellow, completely filled with granular material
(zygote and yolk cells).
Dicrocoelium dendriticum: small (38-45x22-30
µm), slightly asymmetrical, with operculum, dark
brown, with miracidium containing 2 spherical
bodies(germ cells).
Eimeria leuckarti: large oocyst(7 l -8Sxs 1 _63 )
very thick wall, ovoid, brown, granular outer ��
1•
micropyle at the tapered pole, contents· sphe . '
nca l
sporont.
Cryptosporidium spp.: oocysts very sma ll(4- 5 µm)
spherical( ► Figure 16.8). '
• Nematode larvae
Dictyocaulus arnfieldi: LI , _len?t � 420-480 µm,
not sheathed, oesophagus md1stmc t, intestine
granulated, posterior end with thorn-like tip.

• Cestode eggs
Anoplocephala spp.: medium-sized (range 65-80
µm), irregularly rounded/rectangular-shaped, thick­
walled, contain oncosphere, surrounded by pear­
shaped embryophore(pear-shaped apparatus).

• Nematode eggs
Trichostrongylus a.xei: medium-sized(70-98x30-48
µm), more than 16 blastomeres, thin-walled, oval,
somewhat unequal poles. Eggs resemble strongyle
eggs. Differentiation by identification of L3 ( ► p.
546).
Large and small strongyles: medium to fairly large
eggs (range 70- I 40x40-65 µm), genera and species
not distinguishable; differentiation of species or
groups by identification of L3( ► p. 546).
Parascaris equorum: medium-sized (90-100 µm),
thick-walled, spherical, yellowish-brown, slightly
irregular surface; after loss of the outer layer the wall
appears smooth, bright and transparent, contents:
unsegmented, grainy.
Oxyuris equl: medium-sized (85-95x40-45 µm),
one side wall somewhat flattened, one pole with
transparent plug, contents: embryo or Ll.
Dictyocaulus amfieldi: medium- ized (74-96x46-58
µm), thin-walled, ellipsoidal, content: LI. LI hatched
from eggs are also found in fresh faeces and are
detected by the Baermann technique (see below).
Strongyloides westeri: small (40-52x30-40 µm),
thin-walled, wide ellipsoid with flattened poles,
colourless, contents: embryo.
Habronema sp.: small (40-55x8- J 6 µm), elongated
oval form, content LI.
 16. Diagnostics

µm
150

_.!_ 1.tt."'1'"(;� ... �

100 cc
(I)
' ,
-0
'}� .�-.,_
·.i;, ·5
CJ'
:'
\·
w
,, ,..-�r
50 ?'· -.;
- ;�.!t(
r
,·;i.•1:
·r,;;
· - r ..
,i;;•·•.'.,.,i,J'
t_.t<,,..�•,t,,�.l:..i.-
•., ·-,.....·, ''i· ,"'fl, ..\o-�"'�·t'f-
'.-1.�\.�tt-�,i::;�t�
�

Fasciola hepatica Dicrocoelium Anoplocephala sp. Trlchostrongylus

dendrltlcum axe/
µm
100

50

Strongylid: Parascaris equorum Parascaris equorum Oxyuris Oictyocaulus

Strongylus spp. without external layer equi arnfieldi
Cyathostominae, etc.
µm
100

I
50

Strongyloides Habronema sp. Eimeria leuckarti Dictyocaulus arnfieldi:

westeri larva 1 (length 420-480 µm)
and posterior end of the larva

Figure 16.13. Equines: coproscopically detectable parasite stages (Graphics: IPZ, S. Ehrat).

Q)
C
·c3
'5
Q)
�
c
(\:l
C
·;:::
....,
Q)

�
.s
>,
0)
0
0
·u5

8:
�
Part V. Diagnostics

Simplified key for differential diagnosis of Tail of sheath shorter than larval body.
third larvae of gastrointestinal nematodes of ♦ Larvae with 16 intestinal cells:
horses + Larvae very long, slender, L about 1000 µm:
Strongylus equinus.
► Figure 16.14. + Larvae smaller, L 610-780 µm, tail of sheath
very short: Trichostrongylus axei.
Explanations. L: length oflarva including tail of sheath; ♦ Larvae with 20 intestinal cells:
tail of sheath: distance from posterior end oflarval body + Larva large about 850 µm: Strongylus edentatus.
to the end of tail of sheath. ♦ Larva with 32 intestinal cells:
+ Larva large, L about 1000 µm: Strongylus
• Larvae without sheath vulgaris.
Larva slender, oesophagus almost half as long as the
whole body (L: 520-655 µm): Strongyloides.

• Larvae with sheath

Tail of sheath very long: about length of the larval
body.
• Larvae with 8 intestinal cells, L about 850 µm:
Cya thostominae (except Poster iostomum). In
addition to the frequent Cyathostominae there
are rarer small strongyles, having L3 with 12-20
intestinal cells.

1 mm

Strongyloides Trichostrongyfus Cyathostominae Strongylus Strongylus Strongylus

westen· axei vulgans equinus edentatus

Figure 16.14. Gastrointestinal nematodes of horses: third stage la,vae (L3) (Graphics: IPZ).
 16. Diagnostics

16.2.3 Pig Trichuris suis: medium-sized ( 47-71x27-34 µm),

thick wall, lemon-shaped, curved side walls, with
Characteristics of parasite stages (selection) 2 transparent, prominent pole plugs, dark brown,
of pigs granulated content, unsegmented.

► Figure 16.15. • Protozoan oocysts and cysts

Explanation: L: larva.
• Nematode eggs
- Hyostrongylus rubidus: medium-sized (70-82x34-
38 µm), elJiptical, thin wall, almost paralJel side walls,
contents: in fresh faeces>16 blastomeres; similar to
eggs of Oesophagostomum spp. Reliable differential
diagnosis by identification of L3.
- Oesophagostomum spp.: medium-sized(50-80x26-
46 µm), elliptical, thin wall, side walls slightly
arched, contents: in fresh faeces 8-16 blastomeres.
Differential diagnosis by identification of L3.
- Ascaris suum: medium-sized (56-87x46-57 µm),
round-oval, with very thick walls, surface with
irregular protrusions, content: almost completely
filled by granular zygote, unsegmented.
- Metastrongylus spp.: medium-sized(55-60x45-50
µm), ellipsoid, thick wall with wrinkled surface,
contents: Ll. Ll hatched from eggs are also found
in fresh faeces and are detected by the Baermann
technique.
- Strongyloides suis (syn. S. ransomi): Small eggs
(40-55x28-32 µm), thin wall, wide ellipsoid with
flattened poles, colourless, with embryo.
Cystoisospora (lsospora) s11is: small (17-25x16-22
µm), almost spherical oocysts, thin wall, in fresh OJ
0:::
faeces with round sporont (unsporulated). In
unsporulated state, the oocysts of this pathogenic
species differs from some of the less pathogenic
Eimer/a species morphologically by size and shape,
e.g. frorn E. scabra. Reliable differentiation is possible
with sporulated oocysts. /. suis: 2 sporocysts, each
with 4 sporozoites, Eimer/a spp.: 4 sporocysts, each
with 2 sporozoites.
Bala11tldlum coli: vegetative forms large(50-100x40-
75 µm) surface covered with cilia. Cysts( 40-65 µrn),
spherical, contents: filled with parasite stage(among
other structures a nucleus may be visible in stained
preparations).
Giardia spp.: trophozoite: small (9-21xl5-12 µm)
with 8 flagella and 2 nuclei. Cysts: small(8-15x17-10
µm)(► Figure 16.17).
Cryptosporidium spp.: oocysts very small(4-5 µm),
spherical(► Figure 16.8).

µm
100

50

/-lyostrongylus Oesophagostomum spp. Ascaris suum Metastrongylus spp. Strongyloides

rubidus suis

µm
C
100 ·c3

50 C
·;::

�
_!;
� �
0
Trichuris suis Cystoisospora suis Eimeria scabra Balantidium coli Balantidium coli 0
vegetative form cyst
·u5
Figure 16.15. Pig: coproscopically detectable parasite stages (Graphics: IPZ, S. Ehrat).
 Part V. Diagnostics

16.2.4 Dog and cat Trichuris vulpis: medium-sized (70-8Sx36 -4 0 µm)

Characteristics of helminth stages
(selection) of dogs and cats
► Figure 16.16.
Explanations: range: Range of values for several species;
L: larva; 0: occurrence.
• Trematode eggs
Opisthorchisfelineus: small (26-30x11-15 µm), oval,
slightly asymmetrical, with a slightly protruding rim
('shoulder') on the tapered pole where the operculum
fits, dark brown, contents: miracidium. 0: cat (dog).
• Cestode eggs
Diphyllobothrium latum: medium-sized (55-76x37-
56 µm), thin-walled, with operculum at one pole,
golden yellow, contents: granulated (zygote and yolk
cells), similar to Fasciola eggs. 0: dog, cat.
Dipylidium caninum: egg packets: large
(approximately 200x 120 µm), often slightly reddish,
with multiple (up to 30) eggs. Eggs: small (30-50 µm),
round, thin-walled, with oncosphere. 0: dog, cat.
Taenia spp. and Echinococcus spp.: eggs small
(about 30x40 µm), round, thick-walled outer layer
striped radially, with oncosphere that fills the egg.
Morphological differentiation of taeniid eggs not
possible. 0: dog, cat.
thick-walled, lemon-shaped, curved side walls, with
2 transparent, prominent pole plugs, dark brown,
contents: unsegmented , grainy. 0: dog.
Capillaria aerophila: medium-sized (62- 73 x35_40
µm) thick walls, side walls almost parallel, with 2
transparent, flat pole plugs, dark brow n, conte nts:
unsegmented, grainy. 0: dog, cat.
• Nematode larvae
The unsheathed LI of lung and vascular worms of
carnivores are similar to LI of Protostrongylidae of
ruminants ( ► p. 539). Larval body mostly transparent,
in part slightly granulated. Differential diagnosis based
on structure of posterior ends.
Crenosoma vulpis: L1 (270-330 1-1111), posterior end
pointed. 0: dog.
Troglostrongylus spp.: L1 (300-520 µm), posterior
end without notch ( ► Figure Ae. abstrusus), with
spine (not shown). 0: cat.
At1giostrongylus vasorum: LI (310-400 µm),
posterior end with notch and spine. 0: dog.
Aelurostrongylus abstrusus: Ll (360-400 µm),
posterior end with notch and thorn-like projections.
0: cat.

• Nematode eggs
Uncinaria stenocephala and Ancylostoma spp.:
thin-walled, with blastomeres.
• U. stenocephala: medium-sized (7 I -92x35-
58 µm), elliptical, almost parallel side walls,
poles ilattcncd, contents: in fresh faeces several
large blastomeres. Difficult to distinguish from
Ancylostoma eggs, which are usually slightly
smaller. 0: dog, cat.
♦ Ancylostoma spp.: medium-sized (45-78x34-57
µm), elliptic, slightly curved side walls, poles
flattened; content: in fresh faeces 2-8 large
blastomeres. 0: dog, cat.
Toxocara spp.: medium-siud eggs thick-walled,
spherical, greyish in colour, surface pitted (golf ball­
li.ke), contents: dark, unsegmented, grain)'·
• T. canis: 80-94x65-83 µm. 0: dog.
• T cati: 68-85x58-75 µm 0: cat (often gut passage
in dogs).
The eggs of these two species are morphologically
similar but distinguishable morphometrically.
Toxascaris leoniua: medium-sized (76-95x63-
C 76 µm), thick-walled, spherical, smooth surface,
>- contents: brighter than in Toxocara, contents:
0>
0 unsegmented, grainy. 0: dog, cat.
'in Spirocerca lupi: small (25x 15 µm), elongated oval
....
Ctl
(tl
contents: Ll. 0: dog.
►

16. Diagnostics

µm
150

100

so

Opisthorchls Dlphyllobothrlum Dlpylldlum canlnum, egg capsule

(elineus /atum
µm
100

50

Dipylidium Taenia spp. Uncinaria Ancylostoma spp.

caninum, egg Echlnococcus spp. stenocephala

µm
100

50

ij
Spirocerca Trichuris
Toxocara spp. Toxascaris Capillaria
/eonina lupi vu/pis aerophila

Crenosoma Angiostrongylus Aelurostrongylus

vu/pis vasorum abstrusus
Crenosoma vu/pis
larva 1 (length 270-330 µm) Posterior ends of larvae 1 from nematodes of the respiratory tract

table stages of helminths (Gr aphics: IPZ, S. Ehrat).

Figure 16.16. Dogs and cats: coproscopically detec
 Part V. Diagnostics

Characteristics of protozoan stages Sarcocystis spp.: usually excretion of sporocysts,

(selection) of dog and cat more rarely, very thin-walled oocysts. Sporocysts:
small (13-16x8-ll µm), contents: 4 sporozoites.
► Figure 16.17. 0: dog.

Explanations. 0: mean, 0: occurrence. • Cat

• Dog
Giardia spp.: trophozoite: small (9-2lxl5-12 µm)
with 8 flagella and 2 nuclei. Cysts: small(8-15 x17-10
µm). 0: dog, cat.
Cystoisospora (Isospora) oocysts: small, round-oval,
thin-walled, without micropyle, content: sporont in
fresh faeces. 0: dog.
♦ C. canis: 36-44x29-31µm(0 39x32 µm).
♦ C. ohioensis: 19-27x15-25 µm(0 24x2Oµm).
♦ C. burrowsi: 16-23xl5-22µm(0 2lxl8 µm).
Hammondia heydorni: oocysts oflsospora type, small
(1O-15x9-13, 0 ll.9xll.l µm), morphologically
indistinguishable from N. caninum oocysts (see
below). 0: dog.
Neospora caninum: oocysts of Isospora type,
s m al l (1O-13xlO-ll µm), morphologically
indistinguishable from H. heydorni oocysts (see
above).
Giardia spp.: (see above).
Cystoisospora (Isospora) oocysts: small, round-oval,
thin-walled, without micropyle, content: sporont in
fresh faeces. 0: cat.
♦ C.felis: 39-48x23-37 µm (0 45x33µm).
♦ C. rivolta: 22-3Ox21-27 µm(0 26x24µm).
Toxoplasma gondii: oocysts of Isospora type, small
(1O-14x9-ll, 0 12xlO µm), morphologically
indistinguishable from H. hammondi oocysts (see
below). 0: cat.
Hammondia hammondi: oocysts of Isospora
type, small (ll-13x1O-12, 0 ll.4xlO.6 µm),
morphologically indistinguishable from T. gondii
oocysts(see above). 0: cat.
Sarcocystis spp.: (see above). Sporocysts: small
(10x8-9 µm), contents: 4 sporozoites. 0: cat.
Cryptosporidium spp.: 0ocyst very small(4-5µm),
spherical.

Dog
µm
50
40

' '
30
20
10

Giard/a Giard/a Cystolsospora Cystolsospora Cystolsospora Hammond/a Sarcocystls spp.

trophozoite cyst cants ohloensls burrows/ heydomil sporocyst
Neospora
canlnum
Cat
µm
50
Q) 40
C
T5

I '
'5 30
Q)

20
co
C 10
·c
Q)

C Giardia Giardia Cystoisospora lsospora Toxoplasma Sarcocystis spp.

>,, trophozoite cyst felis rivolta gondii, sporocyst
0)
0 Hammondia
0 hammondi
·u5
co Figure 16.17. Dogs and cats: coproscopically detectable protozoan stages (Graphics: IPZ, S. Ehrat).
11.
 16. Diagnostics

16.2.5 Poultry Raillietina spp.: eggs of medium size (93x74 µm),

Characteristics of parasite stages (selection)
of poultry
► Figure 16.18.
Explanations. Range of several species; D: duck; G:
goose; C: chicken; L: larva; P: pigeon; T: turkey; 0:
occurrence.
• Cestode eggs
Eggs of cestodes rarely appear in faeces; however, they
can be isolated from excreted proglottids and be used
for diagnosis at the genus level.
round-oval, contents: oncosphere surrounded by
large, oval layer of the yolk envelope. 0: C, P, T.
Davainea spp.: small (55x36 µm), rounded, smooth
surface, contents: with oncosphere. 0: C, P, T.
Choanotaenia spp.: small (54x47 µm), oval,
outer shell with typical long processes, content:
oncosphere. 0: C, T.
Ecl1i11olepis (syn. Hymenolepis) spp.: eggs of
medium size (76x62 µm), egg envelope of many
layers, envelope of oncosphere ellipsoid. 0: C, T.
Amoebotaenia spp.: small (47-42 µm), surface
smooth, contents: with oncosphere, oncospheral
envelope relatively thick. 0: C, T.

µrn
100

so

Raillietina sp. Davalnea sp. Chaanataenia sp. Echlnolepls sp. Amoebotaenia sp.
µrn
100

so

Syngamus Amidostomum Trlchostrongylus Ascaridia Heterakis

trachea anseris tenuis galli gallinarum
µrn
100 Q)
T5
C

I
'6
Q)

so �
ro
C
·.::::
Q)

C
>-
Capi/laria Capi/laria Spirurid egg Eimeria Eimer/a 0)
caudinflata obsignata maxima tenella 0
0
·u5
Figure 16.18. Poultry: coproscopically detectable parasite stages. Shown are stages that can occur in one or more species of
ro
poultry(► Table 19.18, p. 608 and ► Table 19.19, p. 609) (Graphics: IPZ, S. Ehrat). 0...
Part V. Diagnostics
• Nematode eggs
Syngamus trachea: medium-sized (74-125x36-55
µm), el1ipsoid, often curved side walls equal, both
poles with transparent pole plug, contents: 8-16
blastomeres. 0: C, P, T.
Amidostomum anseris: large (80- lO0xS0-82 µm),
ellipsoid, flattened poles, thin wall, contents with
many blastomeres. 0: G.
Trichostrongylus tenuis: medium-sized (65-75x35-
42 µm), thin-walled, oval, somewhat unlike poles,
contents: more than 16 blastomeres. 0: C, P, T, D, G.
Ascaridia spp.: medium-sized (range 60-90x40-55
µm), ellipsoid, slightly curved side walls, surface
smooth, thick and transparent wall, contents: zygote
with granular appearance, unsegmented; easily
confused with Heterakis eggs (see below). 0: C, P,
T,D,G.
Heterakis spp.: medium-sized (range 60-75x36-
48 µm), ellipsoid, poles flat, smooth surface, thick
and transparent wall, contents: zygote with granular
appearance, unsegmented; easily confused with
Ascaridia eggs (see above). 0: C, T, D, G.
Capillaria spp.: medium-sized (range, 50-65x20-35
µm), thick-walled, lemon-shaped, sometimes slightly
asymmetric with 2 transparent pole plugs, species
differences in size, curvature of the walls and type
of pole plugs, contents: completely ftlled, granulated.
0: C, P, T, D, G.
Spirurids: small (30-40 µm), ellipsoid, with LL
• Protozoan oocysts
Eimeria spp.: oocysts of Eimeria species of chicken
are small (range I 5-30x 13-20 µm); they are non­
sporulatcd when excreted in faeces. Oocysts of
most species usually differ only slightly (except the
large oocyst of E. maxima). Therefore, a reliable
morphological differential diagnosis is not possible.
Species differential ion is based on different criteria
(► p. 88).
16.2.6 Characteristics of tick gen era
Together with descriptions of different genera of ticks
(► p. 396) the illustrated key should be an aid for the
identification of tick genera (► Figure 16.1 9). Howev er
the key contains only a general overview of importan�
features.Details can be found in the specialised literature
(see references).
Selected references
Berry C, Wall R, McGarry J (201 2) Guide to the identification of
ticks of veterinary Importance. Available at: http://bristoltickid.
blogs.ilrt.org/.
Burrows RB (1965) Microscopic diagnosis of the parasites of
man. New Haven, CT, USA: Yale University Press; Library of
Congress No. 65-16818.
Estrada-Pena A, Bouattour A, Camicas JL, Walker AR
(2004) Ticks of domestic animals in the Mediterranean region.
Houten, the Netherlands: Atalanta: ISBN 84-96214-18-4.
Hendrix CM (1998) Diagnostic veterinary parasitology, 2nd ed.
St. Louis, MO, USA: Mosby; ISBN 0-8151-8544-8.
Kassal T (1999) Veterinary helmlnthology. Oxford, UK:
Butterworth/Heinemann; ISBN 0-7506-3563-0.
Thienpont D, Rochette F, Vanparijs OF (1979) Diagnose von
Helmithosen durch koproskopische Untersuchung. Beerse,
Belgium: Janssen Research Foundation.
I /txodes
Medium-sized,
Rhipicephalus
Medium-sized, L 1.2 -
R. (Boophilus)
Small, pale, L 1.2-3mm,
Dermacentor Haemaphysalis
Large, L 3-6 mm, scutum Medium-sized. pale to
Hyalomma
Large, L 4-7 mm,
Amblyomma
Large, L6-7 mm, scutum
I
/Habitus
L 2-4 mm, dark scutum 4 mm, scutum pale scutum without with ornamentation reddish-brONO. L 2-4 mm, darl< brown, legs with with ornamentation, legs
L: length of unfed adult ticks and legs to dark brown ornamentation scutum wrthout palenngs with pale rings
omamentallOn

ee
Mouthparts Much longer than Short, palps shorter than Short, palps with sharp Short, basis capituli wider Short, 2"' palp article Longer than basis Longer than basis
basis capituli width of basis capituli, ridges than long, nearly with lateral projection. capitull, 2"' palp article capituli, 2"' palp article
the latter hexagonal with rectangular basis capitui short With longer than 1 • and longer than the others
lateral, pointed straight lateral margins 3"' articles
protrusions

Hypostome -�\
Palp-

v
Basis capituli
� � �
�

Eyes Absent Present Present Present Absent Present Present

Festoons(► Glossary) Absent Present Absent, males with Present Present Present. often ,ndlst,nct Present, indistinct In
(usually indistinct in fully caudal appendage fed females

\:!J \V \2) \2)

fed females)

� � �
Anteriorly and posteriorly Posterior to anus Posterior to anus, Posterior to anus Posterior to arus
Anal groove to anus indistinct
Posterior to anus Postenor to anus

Coxae Coxa I with long internal Coxa I with paired spurs Coxa I with small external Coxa I with large, Coxa I with sngie, Coxa I with large, Coxa I with unequal
spur and internal spurs paired spurs; coxa r./ la'ge internal spu-) equal paired spurs paired spurs

Lr
in males very large

�
Figure 16.19. Characteristics of ticks genera (Graphics: IPZ, M. Mathys).
[j � �
�

Parasitology in Veterinary Medicine Diagnostic plates Tick genera

 oc y c\i c \a ctones
Macr
Prophylaxis
 17. Therapy

Therapy (G: therapeia: cure, healing) of parasitic diseases

essentially refers to specific chemotherapy against the
causative parasites, partly combined with symptomatic
treatment. The term control comprises all measures
targeted at prevention (prophylaxis), containment or
elimination (eradication) of parasitoses. Preconditions
for any treatment or control measures include an exact
aetiologic diagnosis, assessment of the clinical status of
the involved animals, and a precise knowledge of the
epidemiological situation.

17.1 Categories of therapy

Depending on the indications for specific interventions,
Summary different categories of antiparasitic chemotherapy can
be distinguished:
• Concerning the treatment of parasitic diseases, a • Curative treatment to heal animals which are
distinction Is made between curative, prophylactic,
metaphylactlc (= mesophylactic) and strategic (=
diseased by parasite infections (remember:
planned) therapy. The latter Includes selective targeted
'prevention is better than cure').
treatments(see below). • Metaphylactic (= mesophylactic) treatment to
• For the treatment of parasltoses In animals, numerous eliminate or reduce parasite burdens at a time when
effective and mostly well-tolerated antlparaaltlc no symptoms or major damages have yet occurred.
drugs (• antlparaaltlcs) are available In different • Prophylactic treatment with the aim of suppressing
application forms(► Tables 17.1 to 17.5): Drugs the development of parasites in or on the animal
against ectoparasltes(ectoparasltlcldes or ectocldes, body and preventing or reducing the production
Insect growth regulators OGR) and repellents), against of infectious stages and thereby also decreasing the
helmlnths (anthelmlntlcs) and protozoa(antlprotozoals).
infection risk.
Ectaparasltlcldes and IGR are also used to control
• Strategic (= planned) treatments at certain time
arthropods In the environment.
• Most antlparasltlcs require a prescription and are
points, which are to be chosen according to the
approved for use in defined animal Sli)ecles amd parasite's biology, the epidemiological situation,
indications. The use of drugs for indications ether than the properties of the antiparasitics and other
those approved(off-label use) can be allowed by the criteria (e.g. treatment of grazing animal groups
regulatory authorities If no other drugs are available. against strongyles at certain times of the grazing
• When using antlparaaltlca the following must be period). These treatments are usually metaphylactic,
noted: spectrum of activity, possible drug resistance rarely prophylactic. To reduce the selection of
of parasites, doaage and application, species-specific drug-resistant strains of nematodes of ruminants,
pharmacoklnetlc (e.g. In goats, C811), tolerablllty(safety new strategies involving targeted and targeted
Index), drug raeldu• In the animal body and l'llpectlve selective treatment (TT/TST) are currently being
withdrawal periods (► Glollary, p. 620) 11 well as
evaluated. The TST concept proposes treating only
tolerabUlty for the environment and l8flty for the user.
• Acquired tNlm� ol .,.,..,.. popul,tlon1 to
those animals that are particularly vulnerable or
antipsa11t1c druge II I g,owlng l'JR')bllm wor1dwlde, Of epidemiologically important, for example since
partla,llar Importance n: l'8llatance of f/mtrla epeoles they shed large numbers of parasite eggs. In this
Q)
TC:
5 of poultry to various antlp,otoi.oal �. and the way, a smaller proportion of the parasite population
'5 benzlmldazole flllittanoe of trl� of lheep comes into contact with the antiparasitic agent, as
Q) and goat and of 1ffl811 etrongyl• O.t. oyJthgetomlns) compared to the treatment of whole grazing herds or
�
of the holN (► Table 17.8), Drug nlllltlnoi(DR) also groups. Whether TST provides sufficient protection
Ctl plays a role fn some ectoparultet. against harmful infections and concurrently helps
C:
;;::
·Q) • DR has a genetlo bull and dlVlloPt by telectlng reducing the development of resistance remains
naturally resistant Individual, within a parasite
an open question. Furthermore, methods for the
population followlng repeated trwatmenta and long�
C: identification of animals that require treatment need
term use of antiparasltlc agents. Development of DR
>, to be improved.
...
0) depends on and is favoured by many factors (e.g. in
0
0
·u5
Ctl
Ctl
(L

17.2 Antiparasitic drugs
Antiparasitic drugs (=antiparasitics) can be categorised
based on their efficiency against groups of organisms:
protozoa (antiprotozoals), helminths (anthelmintics),
arthropods (ectoparasiticides = ectoparasitics or
ectocides) or drugs against endo- and ectoparasites
(endectocides). Further groups are insect growth
regulators and repellents ( ► Tables 17.1 to 17.5). The
World Association for the Advancement of Veterinary
Parasitology (WAAVP) publishes international
guidelines that outline the standard procedures for
evaluating the efficacy of antiparasitics. Drug efficacy
is usually defined as the difference between parasite
burdens of infected and treated versus infected and
untreated control animals, expressed as a percentage.
For example, an efficacy of 98% means that the drug in
the recommended dose has the potential to eliminate
almost the whole parasite burden from an individual
animal or a group of animals. In the EU and many other
countries most antiparasitics are subject to authorisation.
The products may only be used in the target animal
species for which they are officially registered. As an
exception, an off-label use ( ► Glossary, p. 620) can be
allowed by the regulatory authorities if no other drugs
are available. Information on veterinary drugs, including
antiparasitics, which are authorised at European or
national levels can be obtained from various data banks
(► p. 576).
17.2.1 Use of antiparasitics
When using antiparasitic agents in defined indications
various factors must be taken into account, such as
need for treatment (according to the clinical condition
of the host animals, the pathogenicity of the parasite
species or the epidemiological requirements), spectrum
of activity, dosage and application, tolerability,
persistence of active substances in the animal body
as well as environmental tolerability and safety for
the user.
Tolerability and drug persistence. An indicator
for the tolerability of antiparasitics is the safety index
(SI) ( ► Glossary, p. 620). Drug residues in the animal
body have a twofold significance. On the one hand,
such residues can be active for longer periods against an
existing parasite population (e.g. against mange mites)
or they can provide protection against new infections or
infestations (e.g. against trichostrongyles). The residual
effect should be taken into account when setting the
intervals for repeated treatments. On the other hand,
drug residues may pass to food products (meat and
organs =edible tissue, milk, eggs) derived from treated
animals. Therefore, for antiparasitics approved for use
17. Therapy
in food-producing animals, the withdrawal periods are
defined by the authorities. They indicate the interval
between the application of an antiparasitic drug and the
permitted use of food products, derived from treated
animals, for human consumption. (/)
0.
::J
17 .2.2 Chemical groups of 0
CJ)
antiparasitic drugs co
l)
Today, highly effective and usually well-tolerated
.E
Q)
.c
drugs are available for the treatment of many parasitic 0
diseases. However, there are still specific therapeutic
shortcomings, e.g. in the chemotherapy of babesiosis,
leishmaniosis, cysticercosis or filarioses. Increasing
problems are caused by drug resistance of parasites.
The most important antiparasitic drug classes are listed
in ► Tables 17.1 to 17.5.
Antlparasltics against arthropods
Chemical substances active against arthropods can be
divided into the following groups: (a) ectoparasiticides
(= ectoparasitics, ectocides), ( ► Table 17.1); and (b)
insect growth inhibitors and repellents ( ► Table 17.2).
Application of ectoparasitics on the animal.
There are various pharmaceutical forms of ectoparasitics
which are suitable for bathing, washing or spraying
treatments and for spot-on or pour-on applications.
The cutaneous application of some ectoparasitics is
associated with a systemic effect. Various ectoparasitics
or endectocides can also be administered parenterally
or orally. Furthermore, ectoparasitics are used as
active ingredients in insecticide ear tags for cattle or
insecticide/acaricide collars for dogs and cats. In both
cases the drugs are released from a support matrix over
a long period and spread widely on the coat and skin.
Means for environmental treatments. To control
flies in cattle stables insecticides are usually used as a spray
or in bait form ( ► p. 479). The licensed products contain
pyrethrins alone or in combination with synergists,
pyrethroids (cypermethrin, deltamethrin, permethrin
and others), organophosphates (cythioate, fenthion,
phoxim, etc.) or mixtures of different active compounds
from these groups. For the control of fly maggots in
Q)
stables, mainly insect growth regulators are being used
·u
C
in different application forms (solid or liquid), rarely '6
Q)
organophosphates or Bacillus thuringiensis toxin. For flea �
control in dogs and cats spray or misting preparations
co
('Fogger') containing mixtures of a fast-acting pyrethroid C
·;::
and an insect growth regulator are particularly suitable Q)
for the treatment of the environment.
C
>,
CJ)
0
0
'in
al
Cl..
 Part VI. Principles of therapy and control of parasitoses
Table 17.1. Drugs(selection) used against arthropod parasites in animals .
i;.hemlcal' group� and ' drugs
genirle names)
,,,,-
Pyrethrins: pyrethrum-extract
(contains pyrethrins, cinerins, and
jasmolins)
Pyrethroids: cyhalothrin, cyfluthrin, C: substances derived from pyrethrins; with prolonged
cypermethrin, deltamethrin,
flumethrin, permethrin
Organophosphates: coumaphos,
cythioate, dimpylate(= diazinon),
fenthion, phoxim
Carbamates: bendiocarb,
propoxur
Macrocyclic lactones:
Avermectins: abamectin,
doramectin, eprinomectin,
ivermectin, selamectin
Milbemycins: milbemycin
oxime, moxidectin
Amidines: amitraz
Phenylpyrazoles: fipronll, pyriprole C: Insecticidal and acarlcldal effect
Neonicotinoids: nitenpyram,
imidacloprid, thiamethoxam
Oxadiazine: indoxacarb
Semicarbazone: metaflumizone
Tetracyclic macrolldes: spinosad
lsoxazolines:
afoxolaner, fluralaner
Organic acids: formic acid, lactic
acid, oxalic acid
1 In bold.
2 Gamma-aminobutyric acid.
.
- 'W'",,p} ·
,r.:;.1.
·
Characterlstles (e) and fields of application (A) Mode of action in
arthropods
C: herbal remedies from Chrysanthemum species; fast neurotoxic contact toxins, keep
initial effect('knock down effect'), short residual action, Na+ channels in the neuronal
with repellent effect; readily biodegradable; usually membrane open -+ , influx of
used with a synergist (piperonyl butoxide) to prolong Na+ -+ delay of depolarisation,
the action agitation, paralysis, death
A: arthropods living superficially on the skin, insects in the
environment (e.g. flies)
like in pyrethrins
activity, greater stability and repellent effect
A: arthropod control on animals and in the environment
C: phosphoric esters; lipophilic properties allow their insecticides with contact
absorption through the skin and the digestive tract of action, partially with respiratory
host animals(-+ systemic effect) action, or acting as feeding
A: arthropod control on and in the skin, in animals and poison:
the environment inhibition of choline esterases
-+ disorder of neuromuscular
transmission -+ paralysis,
death
C: like organophosphates contact and feeding poisons:
A: control of arthropods on animals and In the inhibition of choline esterases
environment
C: lipophilic fermentation products of the ground-dwelling feeding poisons: selective
actinobacterium Streptomyces avermitilis, partly binding to glutamate and
chemically modified; long residual action, systemic GABA2-controlled chloride
action, broad activity spectrum against arthropods and channels -+ influx of chloride
nematodes ions, hyperpolarisation,
A: control of blood-sucking athropods (ticks, lice) and paralysis, death
arthropods which live in the skin (mites) and of insect
larvae and nematodes in animals
C: lipophilic fermentation products of Streptomyces- similar to avermectins
cyanogriseus with properties similar to avermectins
A: similar to avermectins
C: formamidine derivatives from the group of presumable effect on
triazapentadienes octopamine receptors in the
A: control of mites, ticks, etc. nervous system-+ hyper-
excitability -+ paralysis and
death
binding to GABA-gated
A: small animals: ticks, certain mites (Cheyletiella, chloride channels -+
Tromblcula), lice, fleas overstimulation, paralysis,
death
C: substances with high selective activity against Insects blocking of nicotinic
A: flea control In dogs and cats acetylcholine receptors
(cholinergic agonists)
C: insecticide prodrug, active metabolite:
A: flea control in carnivores antagonist at voltage-gated
Na+ channels
C: insecticide contact poison: sodium
A: flea control in carnivores channel antagonist -+ disorder
of impulse conduction -+
paralysis
C: insecticide agonist of nicotinic
A: flea control in dogs acetylcholine receptors -+
hyperexcitation-+ paralysis
C: insecticidal and acaricidal effect GABA-gated chloride channel
A: flea and tick control in dogs antagonists -+ paralysis
A: Varroa mites of bees unknown
 17. Therapy

Table 17.2. Insect growth regulators and repellents.

Mode of action In arthropods

Insect growth regulators en

0.
Juvenlle homione analogues ::,

S-methoptene, pyr proxyfe

flea control bn animal: dog, cal
i n juvenile hormone analogues,
- --------- c
-+-'-( u
_ _ tan_..;. eou s ap � pl cai ·�tlo n ____ d sturbance
i of development ro
1----- :...;__: ..: !::...: :...
:... ,__ _, (.)
Feno carb fleas; application to the environment .E
Q'.)
Chitin synthesis Inhibitors .c
0
Urea der vat
i ves:
i

Lufenuron flea co n trol: dog, cat (per os) I n terference with chitin s ynthe s is
i----------------+------=--...._-..:....__--1
Dlflubenzuron fly larvae; appllcatlon to IM
environment
iriazlne derivative s :
Cyromazlne fly larvae; application to the disturbance of moulting and pupation;
environment no direct Influence on chit ni tliesi s
rm
i ldlnamlnes:

Dlcyclanll proph laxls of wound m lasls In shee Interference With chit n_

i mefabOlism

Repellents
Pyrethro ds
i (► Table 17.1) repellent s against tick s and Insects; combination of repellent and rap di
cutaneous or a s agent s of collar s and knock-down effect
ear tags
Ethylbutylacetylam noproprionate (IR3535) repellents aga nst t cks and In s ect s ; repelle n t effect on insects for a few
i-----------------
i i i
cutaneous hours, less on ticks
lcar d n i i repellent effect on Insects for a few
hours, less on ticks
Vegetable oils or der vat
i ves:
i c tronellol,
i weak a n d short-term (<1 h) repellent
eucalyptus o l,i coconut oil, among other s effect
1 In bold.

Antiparasitics against helminths intra-ruminal bolus(► Table 19.3, p. 581).(Note: the

(anthelmintics) term 'bolus' is also used for large tablets.)

According to the respective indications the following Antiprotozoal agents (antiprotozoals)

main groups of anthelmintics can be distinguished:
Drugs against trematodes (trematocides), cestodes
(cestocides), nematodes (nematocides) ( ► Table
17.4) and drugs that are effective against endo- and
ectoparasites (endectocides) ( ► Table 17.l and 17.4).
Application forms of anthelmintics. Anthelmintics
can be administered orally, cutaneously or by injection.
For this purpose, different application forms, adapted to
the needs of the individual animal species, are available.
For example, for sheep and goats anthelmintics are
frequently applied per os as suspension using special
application(drench) devices. In cattle injection or pour­
on products are usually preferred. T he latter can be easily
applied to the skin and are used accordingly to spot-on
in cats and dogs; after absorption the active ingredients
develop their effect in the body. For oral application to
horse, dog and cat, pastes work well; in pigs or poultry
anthelmintics are primarily administered through
the feed and also via the drinking water. Additional
application forms include tablets, powders or granules
as feed additives. A special application form mainly
used in cattle for long-term medication is the so-called
Of all the antiprotozoal agents, those used against
Eimeria species to combat chicken coccidiosis have a
high relevance worldwide( ► Table 5.2, p. 89 and ► Table
17.5). T hese anticoccidials include several ionophore
polyether compounds which are natural products
produced by fermentation from actinobacteria(genera
Streptomyces, Actinomadura). In addition, chemical
compounds from different groups are used, including
triazine derivatives. These substances are effective against
different stages of coccidia (sporozoites, merozoites,
schizonts, gamonts) and inhibit their development
(coccidiostatic effect) or kill them(coccidiocidal effect).
Since it is often difficult to distinguish between the
two modes of action, drugs acting against coccidia are
collectively referred to as anticoccidials. In 2008, the
EU stated that the use of anticoccidials for controlling
coccidioses in poultry and rabbits is essential, and this
is still valid today. For details on anticoccidials, ► Table
5.2, p. 89, and ► Table 17.5. Approved drugs are still
unavailable for some protozoa! infections of domestic
animals. This treatment gap can be bridged in part by
off-label use of medicines( ► p. 57).
Part VI. Principles of therapy and control of parasitoses

Table 17.3. Drugs (selection) used against trematodes and cestodes in animals.

loat group 1 and compounds Main Indication (applleatlon)2 !Mede of action llil cestodes or trematodes
�rlc names)

Drugs against trematodes (trematocides)

Benzimidazoles:
1, Albendazole, netobimin3 Fasciola (p.o.) inhibition of microtubule polymerisation
Triclabendazole Fasciola (p.o.) inhibition of microtubule polymerisation .....
disruption of tegument, osmotic imbalances,
1; decreased ATP production
Halogenated benzenesuifonamides:
"
Clorsulon Fasciola (p.o., s.c.) inhibition of enzymes involved in glycolysis .....
,. energy loss
( Pyrazinoisoquinolines:
·...
Praziquantel Schistosoma, Opisthorchis, tegument damage, increase of Ca++
Paragonimus: man, also in animals permeability, fast muscle contraction,
(p.o.) dysregulation of metabolism -+ death of
. parasite; primary mechanism unknown
Salicylanilides:
Closantel Fasciola, also Haemonchus and uncoupling of oxidative phosphorylation ......
Oestrus (p.o.) inhibition of ATP synthesis
1, Oxyclozanide Fasciola (p.o.)
Drugs against cestodes (cestocldes)
I< Benzimidazoles:
Albendazole, fenbendazole and cestodes: ruminants (p.o.) inhibition of polymerisation of tubulin to
others microtubuli
Pyrazinolsoqulnolines:
Praziquantel cestodes: sheep, dog, (horse) (p.o.), see above (trematocides)
·•
cat (p.o. or dermal)
Epsiprantel cestodes: dog, cat (p.o.) presumably similar to praziquantel
laothlocyanates

'\• Nitroscanate cestodes and nematodes: dog (p.o.) presumably uncoupling of oxidative
phosphorylation
1 lnbold.
2 Data do not refer to the Individual agents but to application possibilities within the group of active Ingredients.
3 Pro-benzimidazoles: the active Ingredients arise only after the substanc e has been metabolised in the body.
 17. Therapy

Table 17.4. Drugs (selection) used against nematodes in animals.

Chemical group 1 and compound Main Indication (appllcatlon)2 Mode bf action In nematodes
(generic name)

Amino-acetonitrile derivatives: gastrointestinal nematodes sheep agonist of nematode-specific, nicotinergic acetyl (/)
0.
monepantel (p.o.) choline-receptors ..... depolarisation, paralysis :::;

CJ)
Benzimidazoles: gastrointestinal, lung and other inhibition of polymerisation of tubulin to microtubuli
albendazole, fenbendazole, nematodes, partially adult Fascia/a co
()
flubendazole, mebendazole, and cestodes (p.o.)
oxfendazole, oxibendazole Q)
.c
Pro-benzimidazofes : 3
gastrointestinal, lung and other see benzimidazoles 0

I
febantel, netobimin nematodes, partially adult Fascia/a
and cestodes (p.o.)
Cyclooctadepsipeptides: nematodes, cat (spot-on); dog presumably several mechanisms, including binding
emodepside (p.o.) to calcium-activated potassium-channels in the
nerve- and muscle cell membrane ..... flaccid
paralysis of nematodes; presumably further
mechanism
lmidazothiazoles: gastrointestinal and lung reaction with nlcotinic acetyl choline-receptors .....
levamisole nematodes (p.o., s.c., dermal, depolarisation, paralysis (cholinergic agonists)
bolus)
lsothiocyanates: nematodes, cestodes (p.o.) interference with glucose transport and glycogen
nitroscanate synthesis
Macrocyclic lactones:
Avermectins: nematodes, ectoparasites (p.o., selective binding at glutamate-gated chloride ion
abamectin, doramectin, s.c., dermal) channels ..... influx of chloride ions, hyperpolarisation
eprinomectin, ivermectin, of nerve cell membrane, inhibition of signal
selamectin transduction, flaccid paralysis, death
Milbemycins: nematodes, ectoparasites (p.o., see avermectins
milbemycin oxime, moxidectin dermal)
Piperazines: intestinal nematodes (p.o.) opening of GABA4-gated chloride ion channels .....
piperazine paralysis
Pyrimidines: nematodes (p.o.), reaction with nicotinergic acetyl choline-receptors .....
pyrantel depolarisation, paralysis (cholinergic agonist)
Salicylanilides: Fasclola, Haemonchus, Oestrus uncoupling of oxidative phosphorylisation .....
closantel (p.o.) Inhibition of ATP-synthesis
Spiroindoles: nematodes (p.o.) antagonist of nlcotinergic acetyl choline-receptors .....
derquantel inhibition of muscle cell depolarisation ..... paralysis
1 In bold.
2 Data do not refer to tile individual agents but to application possibilities within the group of active ingredients.
3 Pro-benzimidazoles: tile active Ingredients arise after the substance has been metabolised In the body.
4 GABA: gamma-aminobutyrlc acid.
 Part VI. Principles of therapy and control of parasitoses

Table 17.5. Drugs (selection) used against protozoa in animals.

Mode of action in protozoa

Quinazolinones: Eimeria: chicken (p.o.) unknown

halofuginone Cryptosporidium: calves (p.o.)
Quinolones: Eimeria: chicken (p.o.) inhibition of mitochondrial respiration
decoquinate, methylbenzoquate
Guanidines: Eimeria: chicken (p.o.) inhibition of oxidative phospho ry1ation
robenidine Eimeria: rabbits (p.o.)
lonophore polyethers: Bmeria: chicken (p.o.) increased influx of cations (Na+, K+) into
lasalocid, maduramicin, monensin, narasin, the cell -. H 20 influx -> cell death
salinomycin
Thiamine analogues: Eimeria: chicken (p.o.) inhibition of thiamine transport
amprolium
Triazine derivatives: Eimeria: chicken (p.o.) interference with DNA synthesis
clazuril, diclazuril, toltrazuril lsospora: pig (p.o.)
Coccidia: various hosts (p.o.)
Sulfonamides: Bmeria: various hosts (p.o.) inhibition of folic acid and thus of DNA
sulfadimidine, sulfaquinoxaline, sulfadiazine + synthesis
trimethoprim, sulfaquinoxaline + pyrimethamine
and others
Drugs against other protozoa (antiprotozoals)
Antimony compounds: Leishmania: dog O.v.) interference with energy metabolism
N-methylglucamine antimoniate
Benzimidazoles: Giardia: dog, cat (p.o.) inhibition of microtubuli polymerisation
fenbendazole
Carbanilides: Babesia: various hosts (s.c., unknown
imidocarb i.m.)
Diamidines: Babesia, Trypanosoma: various interference with DNA synthesis,
diminazene aceturate, phenamidine isethionate hosts (s.c., i.m.) probably inhibition of synthesis of
biogene amines and aerobic glycolysis
Nitroimldazoles: carnidazole, dimetridazole, Trichomonas in carrier pigeons inducing the formation of free radicals
ronidazole (p.o.), Tritrichomonas in cats, -. inhibition of nucleic acid and protein
Giardia in dogs synthesis
Nitrothiazole salicylamides: Sarcocystis neurona: horse interference with anaerobic
nitazoxanlde (p.o.) metabolismus
Triazine derivatives: Sarcocystis neurona: horse interference with DNA synthesis
ponazuril (p.o.)
Hydroxynaphthoquinones: Theileria: various hosts (i.m.) probably blockade of mitochondrial
buparvaquone,parvaquone electron transport
Pyrazolopyrimidines: Leishmania (dog) (p.o.) purine analogue; as such disruption of
allopurinol nucleic acid and protein synthesis
Alkylphosphocholines: Leishmania (dog) (p.o.) DNA fragmentation among other effects
miltefosine -+ damage to the Leishmania
1 In bold.
Q) 2 Data do not refer to the individual agents but to application possibilities within the group of active ingredients.
C
·u 3 ► Table 5.2, p. 89.
'5
Q)

co
C
·c
Q)

C
>,
0)
0
0
·u5
co
0..

17.3 Drug resistance
Definitions. Populations of parasites (protozoa,
metazoa) that were originally sensitive to an antiparasitic
substance can develop drug resistance (DR). Thus, the
efficacy of antiparasitics in parasite control is limited or
lost. DR is defined as the ability of a parasite population
to tolerate a dose of an antiparasitic which would be
lethal to the vast majority of individuals at the same
developmental stage in a normal sensitive population.
Side resistance is directed against a chemically related
drug, whereas cross-resistance concerns an active
substance not chemically related. Multiple resistance is
defined as resistance to several different chemical groups
of antiparasitics. Tolerance is the natural property of a
parasite or parasite population to withstand the effect
of an antiparasitic when it is first used. Thus, a newly
introduced antiparasitic can be highly effective against
certain parasite species but of a lesser or no effect in
other species. Various parameters serve to assess the
degree of resistance, including the resistance factor
(ratio of LC50 for a sensil'ive population to the LC50 of
the resistant population; LC50 is the concentration of an
antiparasitic which is lethal for 50% of the individuals
of a population).
Prevalence and distribution of drug resistance.
Drug resistance of parasites and vectors is a worldwide
problem and plays a significant role. In some areas,
DR has reached unprecedented levels. An overview
of DR in important parasites of animals is provided
in ► Table 17.6. In Europe, DR is currently mainly a
problem in Eimeria species of chicken, small strongyles
(cyathostomins) of the horse, trichostrongyles of
sheep and goats, and stable flies. Multidrug resistance
is particularly problematic. For example, in Scotland,
England, Italy, Greece, Switzerland and in Germany, cases
of multiple resistance to benzimidazoles, macrocyclic
lactones and/or imidazothiazoles have been detected in
trichostrongyles of sheep and goats.
Dev elopment and mechanisms of drug
resistance. DR has a genetic basis and develops
from individuals in a parasite population that have
a higher natural tolerance to the relevant agent than
other individuals and that survive and propagate under
the effect of an antiparasitic. The repetition of such
treatments in a group of animals over a certain period
of time increases the proportion of drug-tolerant
individuals in the total population thus giving rise to
a resistant parasite population (selection of resistant
individuals). The development of DR is promoted by
various factors, including high frequency of treatments,
long-term use of the same drug group, sub-therapeutic
doses, parasites with short generation times and limited
availability of refugia of the parasite population.
Refugia are sites where parasites are not exposed to
drugs. Thus, in the case of partial treatment of a herd,
the parasites in the untreated animals are not exposed to
17. Therapy
the selection pressure of the anthelmintic in an animal
refugium. The environment can also represent such a
refugium, in which large amounts of sensitive parasite
stages persist. The maintenance of such refugia may be
a useful measure for the prevention of DR.
It Is also important whether the resistance is encoded
by only one or by several genes and whether it is
dominantly or recessively inherited. According to model
calculations, DR develops fastest when it is caused by
only one gene and follows a dominant trait. DR is thus
a complex phenomenon. The development of DR can
occur very quickly (e.g. in flies) or only after years of
use of an antiparasitic (usually in helminths). A well
understood example of resistance mechanisms is the
case of benzimidazole resistance in trichostrongyles (e.g.
Haemonc/111s contort us, Teladorsagia circumcincta). Here
resistance is based on the selection of specific �-tubulin
isotype l alleles that confer a reduced binding affinity
on benzlmidnzoles. In most resistant field isolates the
�-tubulin lsotype I differs from the sensitive isotype
I only by a single amino acid exchange at position
200 (phenylalanine to tyrosine). Additionally, in these
nematodes and other parasites there are also other,
non-specific resistance mechanisms. According to the
current state of knowledge these include especialJy
transmembrane efflux pumps such as P-gJycoproteins
of parasitic nematodes, for which an association with
resistance to multiple anthelmintic drug groups was
confirmed.
Diagnosis of drug resistance. To diagnose DR
different methods have to be used according to the
respective parasite species. The most important methods
for the diagnosis of anthelmintic resistance (AR) in
nematodes of the order Strongylida are the faecal egg
count reduction test (FECRT), the egg hatch test
(EHT), larval development test (LDT) and the larval
migration test (LMT). The latter three methods are in
vitro methods that allow AR of parasite populations to
be diagnosed in living host animals. For the qualitative
and quantitative detection of alleles associated with
benzimidazole resistance in H. contortus and other
ruminant trichostrongyles, PCR and special molecular
methods (e.g. pyrosequencing) have recently been
applied. Genetic markers that mediate DR of other
Q)
origins have been identified and may be used for DR T5
C
diagnosis. '6
Q)
�
In the FECRT, the average number of helminth eggs �
per gram of faeces (faecal egg count, FEC) is compared ro
C
in a group of animals pre-treatment and 2 weeks post­ ·.::::
Q)
treatment, and the achieved reduction is calculated (the �
time ofinvestigation after treatment may vary depending .!:;
on the examined parasite species and the anthelmintic >.
CJ)
tested; see special literature). An anthelmintic applied to 0
0
sheep is considered completely effective if the reduction ·u5
in egg numbers is greater than 95% and the lower limit
ro
of the 95% confidence interval is below 90%. However, Q
 Part VI. Principles of therapy and control of parasitoses

Table 17.6. Examples of antiparasitic drug resistance (DR) in animal parasites.

Animal species and parasites Resistance to

Sheep or goats
Fascio/a hepatica triclabendazole2 , albendazole, closantel
Haemonchus contortus 1 benzimidazoles 1 , levamisole, ivermectin, doramectin, moxidectin, closantel,
monepantel2
Teladorsagia/Ostertagia spp. benzimidazoles, levamisole, ivermectin, moxidectin
Trichostrongylus colubriformis benzimidazoles, levamisole, ivermectin
Nematodirus spp. benzimidazoles
Psoroptes ovis organophosphates
Bovicola bovis pyrethrolds
Lucilia cuprina organophosphates, pyrethrolds
Cattle
Fascia/a hepatica triclabendazole2
Trypanosoma spp. (Salivaria) quinapyramlne, isometamidium, homidium, diminazene aceturate, suramin
Ostertagia ostertagi benzlmidazoles, levamlsole, doramectln
Trichostrongylus axei benzimidazoles
Cooperia spp. benzlmldazoles, lvermectln, doramectin
Rhipicephalus (Boophilus) microplus organophosphates, amitraz, pyrethroids
Chorioptes bovis organophosphates
Haematobia irritans organophosphates, pyrethrolds
Horse

II
Cyathostomins 1 benzimidazoles 1 , pyrantel2
Parascaris spp. ivermectin, moxidectin, pyrantel3 , fenbendazole3
Pig
Oesophagostomum spp. benzimidazoles 2 , pyrantel2 , levamisole2
Dog or cat
Dirofilaria immitis macrocyclic lactones3
Ancylostoma caninum pyrantel3
Ctenocephalides felis organophosphates, carbamates, pyrethroids, pyrethrins, phenylpyrazoles
Chicken
Eimer/a spp. 1 many anticoccldial drugs 1 ( ► p. 89)
Others
Musca domestlca 1 pyrethrlns 1, pyrethrolds 1, organophosphates 1, phenylpyrazoles (fipronil), insect
growth reaulators (cyromazlne)
1 Parasites with frequent DR In Europe and the corresponding drugs.
2 No/limited importance of DR In Europe.
3 Not yet reported in Europe.

there are no commonly agreed values for this limit or for Reversion of drug resistance. Generally, a reduction
the details of the procedure/evaluation of the tests for the (reversion) of AR cannot be expected in strongyles, even
Q)
T5
C different host and parasite species. In recent publications after the responsible anthelmintic has not been used
'o a revision of the limits has been discussed. The FECRT is for several years. In various countries it was possible
Q)
::;E
generally suitable for examining the efficacy of all groups to displace drug-resistant strains of trichostrongyles
of anthelmintics and provides important evidence for of sheep by experimental dissemination of sensitive
co
C the existence of AR. Alternatively, or in addition to strains of the same species. This method offers new ways
·c the FECRT, the above-mentioned laboratory methods to control AR of trichostrongyles of ruminants, but it
Q)
(including EHT, LDT, LMT, PCR, pyrosequencing), in is still debatable whether this can ever be a practical
C some cases also by animal experiments, can contribute solution for the field. A prerequisite for this approach
>,
0)
to an improved quantification of the degree of resistance. is the availability of drug-susceptible strains of different
0 trichostrongyle species, which in principle is feasible
0
.iii
since infective trichostrongyle larvae can be stored for
co many years frozen in a viable state.
co
a..
 17. Therapy

Measures against drug resistance. To control • Prevention of introduction and spreading of

resistant parasite populations active substances of other
che mical groups, drug combinations or alternative
methods must be used. For the prevention of AR, there
are several recommendations that have not as yet been
sufficiently tested. Here, this is illustrated by the example
of sheep trichostrongyles.
• Reducing the selection pressure on nematode
populations. The selection pressure on nematode
populations can certainly be reduced by minimising
the number of treatments, adhering to dosage regimens
and choosing epidemiologically based time points for
targeted treatment. Furthermore, it is anticipated that
the selection pressure is lower if a part of the parasite
population is not affected by the treatment. This is, for
example, the case when parasites survive in 'refugia',
e.g. in untreated animals (when in a herd only selected
animals are treated, ► p. 593) or in the larval stage on
pasture (see above). The use of a range of treatment
indicators (e.g. pooled FEC, automatically registered
live weight gain, body condition score, FAMACHA,
Ostertagia bulk tank milk ELISA) has been studied for
different ruminant species and age groups, providing
evidence that TT/TST approaches may be beneficial
and practical solutions for maintaining drug efficacy
and productivity.
resistant strains. Reports exist from several European
countries on the introduction of resistant trichostrongyle
strains by sheep or goats imported from abroad. For
example in Switzerland, a Haemonchus contortus
strain resistant to a benzimidazole and ivermectin was
identified in a herd to which Boer goats from South
Africa had been introduced. Such introductions can
be prevented by quarantining imported animals and
treating them with one or several drugs that completely
eliminate the existing worm burden. In sheep, goats and
horses especially, it has to be taken into account that
drug-resistant strains of nematodes can be spread by
animal transport or by keeping animals from different
herds on common pastures. In the USA, spreading of
drug resistance of Dirofilaria immitis to macrocyclic
lactones in dog populations has been identified as an
emerging problem.

• Change of drug classes. Previously, the annual

change of the drug class in regular treatment regimens
has been considered advantageous for preventing DR
development. However, according to recent studies,
this measure is not particularly suitable to delaying the
development of anthelmintic resistance. The conditions
for a useful and successful rotation strategy are dependent
on a number of factors, such as the respective treatment
frequency, the environmental conditions, the specific
efficacy characteristics of the respective drugs and the
prevailing parasites species.

• Alternative measures. Measures such as pasture

management (strategic pasture change, pre-use of
pasture, mixed grazing of different age groups or species,
et€,) and possibly in the future also biological control
meth ods (e.g. nematophagous fungi) are other options
for reducing the risk of AR.
 18. Control
18.1 Control methods
18.1.1 Technical and operational
control methods
These include all measures that can help prevent
or reduce parasite infections/infestations, such as
appropriate construction of stables and stable hygiene,
disposal or recovery of waste from livestock production,
type of animal husbandry (stables, paddock, grazing,
intensive husbandry, organic farming), grazing systems,
pasture hygiene and pasture management, feeding and
water supply, animal care and welfare (grooming, good
attitude, etc.). This list is not exhaustive.
18.1.2 Legal and regulatory
measures
In some cases, legal regulations and actions based thereon
represent components of parasite control. According
to OIE some parasitic diseases are internationally
notifiable, including parasitoses of: (a) multiple host
species (surra, echinococcosis, trichinellosis, screwworm
infestations), (b) cattle (African trypanosomosis,
trichomonosis, babesiosis, theileriosis), (c) equines
(dourine, piroplasmosis), (d) bees (acarapiosis,
Tropilaelaps infestation, varroosis, small hive beetle
infestation), and fish (gyrodactylosis). For some
parasitoses further regulations exist on national or EU
levels. The use of antiparasitics and parasite control
on organic farms is subject to special EU and national
regulations (for more information see chapters on
individual parasitoses). Finally, it should be taken into
account that severe parasitoses may be a matter of animal
welfare legislation if necessary treatment and care of the
animals are neglected.
18.1.3 Physical measures
These measures include techniques to protect against
fly strike (cattle ► p. 478, horse ► p. 596). Physical
measures also play a role (see below) in cleaning and
disinfection.
18.1.4 Use of antiparasitics
Together with the technical and operational methods
the use of antiparasitics currently forms the main pillar
of parasite control. The antiparasitic agents are used
against external or internal parasites in animals or for
the control of vectors within prophylactic, metaphylactic
or therapeutic measures ( ► p. 556 ff).
18.1.5 Biological parasite control
'Biological control' is defined as a limitation of pathogen
populations by any means other than chemical methods,
e.g. by using competitive organisms, breeding parasite­
resistant host animals or by technical and operational
measures. After a somewhat broader definition chemical
agents that are biologically favourable may be included.
Some of these options are discussed here.

Use of competitive organisms. Organisms that
compete for development and growth with other
organisms are used for the biological control of a very
limited nwnber of parasites. Examples include the
use of the manure fly Ophyra aenescens to reduce the
populations of stable flies ( ► p. 479) and the autocide
procedure (sterile insect technique) to control the
screwworm fly (Cochliomyia hominivorax ► p. 488) and
tsetse flies(Glossinae ► p. 481). By using the autocide
procedure, the screwworm fly was successfully eliminated
in large areas. In numerous studies predacious fungi,
especially the species Duddingtonia jlagrans, have been
used to reduce strongyle populations in grazing animals.
Grown in an artificial nutrient medium, Duddingtonia
fungal spores(chlamydospores) are produced and orally
administered to the grazing animals. After intestinal
transit of the spores, the fungus develops in the faeces
a network (mycelium) in which larvae of parasitic
nematodes are trapped and killed. Although this method
can cause a significant reduction in trichostrongyle or
strongyle larvae on pastures of cattle, sheep or horses,
it has not found its way into practice. Commercial
preparations with Duddingtonia spores are not available.
Use of substances with favourable biological
properties. In order to control mosquito and blackfly
larvae ( ► p. 468) in the field and insect pests in
agriculture, Bacillus thuringiensis(Bt) or toxins derived
from Bt are used. Bt is a bacterium which grows in the
soil and occurs in about 30 subspecies, which produce
potent toxins during sporulation(delta-endotoxin and
cytolysins). The toxins are similarly effective against
certain insect groups and stages (e.g. larvae of Diptera
or beetles) as organophosphates. In the environment Bt
toxins are rapidly degraded, and they are well tolerated
by vertebrates. After oral intake of Bt or Bt toxin by an
insect, toxin fractions (i.e. crystal protein) are released
in the midgut which, after activation by proteases of
the epithelial cells, bind to specific receptors and insert
into the cell membranes. These pore-forming proteins
first cause cell damage and eventually death. Insects
can become resistant to Bt, as laboratory results and
individual cases of plant pests show. Recently, it has
been shown that Bt crystal(cry) proteins are also highly
effective against parasitic nematodes.
The biologically favourable compounds further include
insect growth regulators which specifically act on insects
and are used e.g. in the control of fly larvae in stables
(► p. 479) or for flea control on animals or in the
environment( ► p. 606).
Bioactive fodder plants. Various fodder plants
contain enzymes (e.g. cysteine proteases), alkaloids,
glycosides or tannins with antiparasitic properties.
For example, in several studies the uptake of tannin­
containing plants(e.g. legumes) by sheep led to reduced
trichostrongyle burdens and a better development of the
animals. However, in other studies this effect did not
18. Control
occur. Possible reasons for this discrepancy are anti­
nutritional properties of plants which may adversely
affect feed intake. fn order to make clear what the effects
of forage plants are, it is necessary to isolate the active
substances and examine their antiparasitic properties
C
and their potential side effects. 0
(.)
co
Phytotherapy. The use of drugs of plant origin for (.)
'6,
parasite control is recommended if their efficacy and 0
0
safety are proven, as is the case for pyrethrum extracts. C
::,
Unfortunately, various herbal commercial preparations E
which have not undergone an authorisation procedure E
(including testing for efficacy, quality and safety) are
commercially available as antiparasitic agents.
Physical and chemical dysregulation of
parasites. Biological control options already used in
practice include the disorientation of insects by visual
or olfactory signals causing aversion or attraction.
Aversion can be induced by repellents ( ► Table 17.2),
attraction for example by sex pheromones. Insects
attracted by pheromones to baits or traps can then
be killed chemically or physically. Examples of such
applications are used to control stable flies ( ► p. 4 79)
or tsetse flies( ► p. 481).
Resistance breeding. For many years, attempts
have been made to breed sheep, cattle and chicken
lines with increased innate resistance to certain parasite
species. One example is the successful selection of
Merino sheep with increased resistance to the stomach
worm Haemonchus contortus, which was associated
with decreased excretion of parasite eggs and lower
incidence rates of diseased sheep. Similar efforts to
breed cattle or sheep with increased resistance have
also been made for other parasitic diseases, including
trypanosomosis, tick infestation and myiasis. Extensive
genomic, transcriptomic and proteomic research to this
end has been performed in an attempt to expedite the
selection of parasite-resistant lines of livestock.
18.1.6 Immunological control of
parasites (vaccination)
Immunoprophylactic measures play a crucial role in the
control of many viral and bacterial infections, but their
significance in controlling parasitic diseases is still very
limited. The reasons are diverse: the complexity of the
composition and metabolism of eukaryotic pathogens
and the resulting diversity of antigenic structures, the
differentiated host-parasite relations with efficient
mechanisms of immune evasion of parasites, and
difficulties in obtaining parasite antigens. Only a few
parasites can be grown in sufficient quantity in vitro,
and recombinant vaccines have not always been as
successful as expected. However, there are currently
various promising approaches in the development of
vaccines against parasites.
 Part VI, Principles of therapy and control of parasitoses
The requirements for an antiparasitic vaccine to be
used in veterinary medicine can be very diverse. In an
animal with a high intrinsic value, a vaccine, e.g. against
Babesia spp. in dogs, must confer a higher degree of
individual protection than, for example, a vaccine against
gastrointestinal nematode infections in ruminants. In
the latter case a major objective of vaccination is the
maintenance of herd health and improved productivity.
According to model calculations concerning infections
with gastrointestinal nematodes in sheep, a substantial
success could be achieved by vaccination even if just
a 60% protection against test infections were reached
in only 80% of the animals of the flock. In cases where
the pathogen - as in gastrointestinal helminths of
ruminants or coccidia infections of chicken - can never
be completely eliminated, re-infections will be taken into
account as booster effects, i.e. to strengthen immunity
or to maintain an infection-based immunity.
Antiparasitic vaccines, either already authorised and
in use or still in the experimental stage, are based on
approved technologies and include as antigens virulent
or attenuated organisms, native or recombinant antigens
or nucleic acids ( ► Table 18.l ).
Live vaccines
Vaccines containing virulent pathogens. Since the
dawn of immunoprophylaxis against parasites and to this
day, virulent pathogens are used in vaccines. Amongst
the first vaccinations were those against the causative
agent of cutaneous leishmaniosis in humans, Leishmania
tropica. The infection with this pathogen causes ulcers
in which parasites are present (leishmanioms); they
leave disfiguring scars, often in the face. Based on the
observation that: humans develop such ulcers only once
in a lifetime, healthy persons have been immunised in
endemic areas for centuries by scarification of their skin
on a less conspicuous location and rubbing material
from Leishmanioms into the wound of infected patients
(so-called leishmanisation). Using special vaccine strains
this process was used in the Middle East until the late
20th century and is still practised to a great extent in
Asia (Uzbekistan).
Q)
In veterinary medicine virulent parasites, like Babesia
bovis and B. bigemina, were also used for vaccination
·o
C
'5 at the end of the I 9th century, but vaccines based on
Q)
� this approach have meanwhile become less prevalent,
although some are still i.n use.
co
C
·;;::
For many years, virulent strains of Eimeria species
have been used in the form of sporulated oocysts in
,!:; commercial vaccines, such as Coccivac• and lmmucox•,
>, to control chicken and turkey coccidiosis in some
0)
0 countries (USA, Canada) ( ► Table 18.1). These
0
·u5 vaccines are sprayed over the chickens in a special
co chamber ('Spraycox') or administered to 1-3-day-old
co
a. chickens with the feed. Thus, in the first days of life
the chickens experience a subclinical but sufficiently
strong infection and get immunised. Subsequently, the
immunity is enhanced by additional weak infections
through the uptake of oocysts from the environment.
Another approach is the injection of live Eimeria oocysts
into incubated eggs prior to hatching of the chickens
(embryonic immunisation) using large machines in
hatcheries. In the USA a vaccine is approved for this
indication (Inovocox"').
An essential precondition for the safety of live vaccines is
an exact dosage. If there is a risk that virulent pathogens
in the vaccine can cause clinical disease, attempts can be
made to control the infection in time by chemotherapy.
Such an approach is used when vaccinating cattle
against East Coast fever, caused by Theileria parva,
by injecting live and virulent sporozoites of T. parva
and simultaneously administering a long-acting
oxytetracycline.
Vaccines containing attenuated parasites. With
attenuation techniques the virulence and viability
of pathogens can be reduced, while maintaining the
highest possible degree of immunogenicity, so that the
organisms can be used in vaccines without great risk.
T he methods applied for attenuation are diverse.
In protozoa attenuations were successfully achieved
by in vitro passages. Thus, the in vitro passaging of
Theileria annulata results in an attenuation which
allows the use of macromeronts as vaccine stages. Strains
of Eimeria species with reduced virulence were obtained
by passages in embryonated chicken eggs (Livacox•)
or by selection from natural Eimeria populations
(Paracox•). A prerequisite for the use of attenuated
pathogens in vaccines is that certain properties remain
stable. For example, a strain of Toxoplasma go11dii,
originally isolated from an aborted lamb, lost the ability
to form tissue cysts and oocysts after repeated passages
in mice. Live tachyzoites of this strain are used in a
vaccine for the immunisation of ewes against abortion
caused by natural infections with T. gondii oocysts.
The important property of this strain is that injected
tachyzoites multiply locally for some time without cyst
formation and are eventually eliminated. However,
this vaccination induces cell-mediated protective
immunity and prevents abortion. Also, the selection
of precocious lines of different Eimeria species can be
regarded as attenuation. Precocity is due to the lack of
one or more merogonies resulting in shorter prepatent
periods. Therefore, the number of highly pathogenic
stages of the last merogony and of gamonts is essentially
smaller than in wild strains, while the immunogenic
early merogony stages are not affected. Vaccines on this
basis are commercially available (Paracox•, Hipracox•,
Livacox•) and mainly used i.n the rearing of laying hens
and broilers in organic farming.
 18. Control

cattle: Babesia bovis, B. bigemina no commercial product

0
chicken: 3-8 Bmeria species of chicken Coccivac®-D2. lmmucox® I & II (for u
chicken), lnovocox® (for injection in �
u
--------- ------1-h_a _tc_h �ing�gs_) ·5i
1 ________� 0
turkey: 2-4 Bmeria species of turkeys lmmucox® T Coccivac-� (for turkeys) 0
C
Virulent pathogen under cattle: Theileria parva no commercial product :::,
chemotherapeutic control2 E
E
, attenuated vaccines
chicken: Eimeria species:
E. acervulina, E. maJCima (two strains). Paracox 5® (for broilers)
E. mltis, E. tenella
E. acervullna, E. brunettl, E. maxima Paracox 8® (for hens)
(2 strains), E. mltis, E. necatrix,
E. praecox. E. tenells
E. acervullna, E. maxims,£. m/11s, Hipracox ® (for broilers)
E. praecox, E. tenella
E. acervulina, E. maxima, E. tenella Llvacox T® (for broilers)
E. acervulina, E. maxima, E. necatrix, Livacox QI!> (for hens)
E. tenella
rabbit: Eimeria species of rabbits experimental vaccines
enuation by in vitro passages turkey, chicken: Histomonas no commercial product
me/eagridis

sheep: Toxoplasma gondii Ovilis Toxovax®

cattle: Dictyocaulus viviparus Bovilis Dictol®
· e and recombinant subunit vaccines
Fucose mannose ligand of Leishmania dog: Leishmania infantum Leishmune®
donovani
Excretory/secretory proteins dog: Leishmania intantum CanI Leish®
Native, purified gametocyte antigen chicken: Eimeria maxima CoxAbic®3 (for maternal immunisation
of E. maxima of laying hens)
Native, intestinal membrane sheep: Haemonchus contortus Barbervax®
glycoproteins (= 'hidden antigens') of
H. contortus adult stages
Antigens from in vitro-cultures dog: Babesia canis Plrodog®
Recombinant antigen (A2 stress protein) dog: Leishmania infantum Leish-Tec®
Recombinant Tae111a oncosphere · _o_vs_i _______ use in pilot control programs
.._ s_ h e_ _ep:_� Tc_a_e _m_a _.
antigens (TSOL family) cattle: T. saginata
pig: T. solium
Recombinant Echinococcus oncosphere sheep, cattle: Echinococcus EG95 vaccine registered in Argentina
antigen (EG95) granu/osus s.s., metacestodes and China Q)
C
Recombinant antigen (BM86 intestinal cattle: Rhipicephalus (Boophilus)
microplus
TickGard®4, Gavac® ·u
wall antigen = 'hidden antigen')
Q)
DNA-vaccines various parasites· experimental vaccines �
1 In bold: vaccines used in Europe.
�

-
2 Simultaneous inoculation of live T. parva sporozoites and a long-acting oxytetracycline. C
3 Precocity: lack of one or more merogonies results in shorter prepatent period. ·;;:
4 At time commercially not available.

.!;
>,

-
0)
0
0
·u5
�
a..
 Part VI. Principles of therapy and control of parasitoses

In helminths attenuation of infective stages by radiation against homologous and heterologous Eimeria species.
is considered as a safe method after an effective vaccine Subsequently, light natural infections induce active
against Dictyocaulus viviparus(Dictol•) was developed immunity.
in this way in the 1960s. This vaccine is still in use
today. In principle, the method is suitable for various The situation is more difficult for the Haemonchus
helminth species; only the radiation dose has to be contortus infection in sheep, since this infection is
varied. Thus, for attenuation of the L3 of D. viviparus associated with slow development of immunity, especially
or trichostrongyles about 400 Gy are needed, while in lambs. In 2014, the first vaccine(Barbervax") against
for metacercariae of trematodes one tenth of this dose H. contortus in sheep was registered and released in
is sufficient. A vaccine based on radiation-attenuated Australia(► Table 18.1). The vaccine is based on
infective larvae was developed against Ancylostoma H. contortus native intestinal membrane antigens
caninum in dogs, but the commercial product was (glycoproteins), most of them being 'hidden antigens'
not successful on the market. In other parasites such (► Glossary). To achieve immune protection in lambs
as Fasciola hepatica the production of metacercariae (up to 92%), three injections are required at intervals
for such a vaccine is not economical. In protozoa, the of 3-4 weeks. Since natural exposure to Haemonchus
radiation attenuation has not proven successful. infections does not stimulate the immunoprotection
mechanisms, boosters given at 6-week intervals are
Attenuation can also be achieved by targeted genetic required to maintain immunity during a risk period
manipulation. With the production of auxotrophic following vaccination. However, the level of immunity
mutants(organism which are incapable of synthesising a may not be sufficient to prevent clinical haemonchosis
specific organic compound) the risk of reversion to full under all conditions.
virulence can be excluded. Mutants may be produced
with gene targeting, which can proliferate no longer Recombinant antigens(► Glossary) are now being
or only to a limited extent, but still induce sufficient tested on a relatively large scale and already used to
immunity. some extent in practice. One recent example is a vaccine
against Plasmodium falciparum, one of the causative
Native and recombinant subunit vaccines agents of human malaria. It contains a fusion protein
of hepatitis B surface antigen and a fragment of a P.
A subunit vaccine against Babesia canis infection in falciparum(circumsporozoite) protein, together with an
dogs(Pirodog•) contains concentrated B. canis antigens adjuvant. In a large trial in Africa(published 20 l 5), only
and saponin as adjuvant.(► Table 18.1). This vaccine 28% of young infants(6-12 weeks) and 36% of children
may not fully protect against infection but usually (5-17 months) were protected from clinical malaria.
prevents clinical disease. A vaccine based on killed This result illustrates the limitations of developing
Giardia duodenalis to be administered subcutaneously vaccines against parasitic diseases particularly when
to dogs(GiardiaVax•), is on the market in the USA using recombinant antigens..
(not registered in Europe!) but its efficacy has not
yet been satisfactorily documented. Similar simple Nevertheless, recombinant vaccines have been developed
vaccines containing inactivated Neospora caninum or in veterinary medicine. In Australia, a commercially
Tritrichomonas foetus are authorised for cattle and available vaccine was developed that contained a
in use in some countries, but their value is disputed. recombinant antigen(Bm 86) from the intestinal wall of
A vaccine approved in Brazil(Leishmune•) against the one host tick Rhipicephalus (Boophilus) microplus.
Leishmania infantum infection in dogs contains a Vaccination of cattle with this antigen induces circulating
purified antigen fraction(glycoprotein) of L. donovani antibodies that are taken up by blood-sucking ticks. The
and saponin as adjuvant. This vaccine is intended to antibodies bind to antigens of the ticks' intestinal cells
protect 80% of the dogs from visceral )eishmaniosis and damage the intestinal wall. This vaccine was used
and to reduce the density of parasites in the skin of the as an additional component in the integrated control of
(I)
animals, thus impairing their uptake by vectors. The R. microplus, especially in situations of high acaricide
·u
C:

'5 European Medicines Agency has recently approved a resistance of this tick species. However, the vaccine
�
(I)
vaccine(CaniLeish•) that contains E/S antigens of L. does not confer sufficient protection against various
� infantum and QA-21 saponin as adjuvant. This vaccine populations of the tick species, and thus current work
co
C:
has been documented to reduce the risk of progressing aims at improving it by using mixtures of antigens.
·;:::
(I) infection or overt disease by 68%. Affinity-purified
gametocyte antigens of Eimeria maxima are part of a Far advanced is the development of recombinant
£ vaccine(CoxAbic", no longer available) for the so-called vaccines against infections with larval cestodes
>-
0>
maternal immunisation: laying hens are immunised (metacestodes) in sheep and cattle. In Taenia ovis,
0 intramuscularly leading to a high accumulation of T. saginata, T. solium and Echinococcus granulosus,
'iii specific IgG antibodies(in chicken called IgY) in protective antigens were identified in the oncospheres
co the egg yolk. The antibodies are transferred to the and characterised. Vaccines containing recombinant
co
a.. chickens which thus gain transient passive protection antigens confer a high degree of antibody dependant

immunoprotection (>90%) against infections with
metacestodes in the respective hosts. For example, a
vaccine (EG95) against ovine cystic echinococcosis is
registered in Argentina and China.
DNA vaccines
DNA vaccines were expected to become the 3 rd
generation vaccines (following native and recombinant
proteins). The principle of such vaccines is that DNA,
coding for parasite antigens, is injected in the body
an d taken up by certain host cells. These cells then use
the parasite DNA as a template for producing parasite­
specific antigens which stimulate immune responses.
Though such vaccines are promising, results that can
be applied in practice are still lacking in the field of
parasitology.
18.1.7 Sterilisation and disinfection
Sterilisation is defined as elimination (destruction
or removal) of all infectious agents (pathogenic and
apathogenic) from objects (e.g. surgical instruments)
or products, fluids, culture media, etc. Disinfection
refers to specific measures targeted at the elimination
or inactivation of certain pathogens from an object
(macroorganism, room, stable, equipment, materials)
so that the respective object can no longer be a source
of infection. The clearing of rooms, warehouses, and
goods from animal pests (mostly arthropods) is called
disinfestation.
Sterilisation. Stages of parasites can be removed due
to their size by sterile filtration from liquids (e.g. cysts
of Giardia, Cryptosporidium oocysts) or killed by heat
(>70 °C, 5-10 min).
Disinfection. In veterinary practice, there are several
areas where disinfection measures against stages of
parasites are required. The available disinfection means
and methods are, however, very limited.
• Paddock and pasture disinfection. Disinfection
of soil in pens or grazing areas is generally not possible.
Exceptions are smaller outlets (e.g. enclosures in zoos
or kennels) where the top 10-15 cm soil layer can be
removed and replaced by non-contaminated material.
Fortified outlet surfaces ( concrete, stone, heat-resistant
plastic) are best thoroughly cleaned using high-pressure
cleaners with hot water containing a detergent. Cleaning
and hot water can achieve only partial disinfection. Using
hot water/vapour mixtures (e.g. 130-140 °C) produced in
high-pressure cleaners improves the disinfection effect.
However, a high disinfection effect is only obtained by
long exposure times (~1 min/m2 ) due to the strong and
immediatelcooling of the hot water/vapour mixture
when making contact with the ground surface (e.g. from
140 to about 90 °C).
18. Control
• Stable disinfection. Thorough mechanical
cleaning and the subsequent use of hot water high­
pressure cleaners are important prerequisites for stable C
0
disinfection. In addition, chemical disinfectants with :.-::;
()
activity against parasite stages should be used. Such Q)
C
agents are included in a list of the German Veterinary 'in
Medical Society (DVG, 2011) given that an evaluation '6
according to DVG guidelines demonstrated that they 'O
C
co
kill at least 95-98% of the highly resistant test organisms C
(Eimeria oocysts, Ascaris eggs) at an exposure time of 0
:g
2 h. This concept of evaluation is based on the justified -�
assumption that stages from other parasite species with ·;::
Q)
similar or lower tenacity (e.g. oocysts of lsospora, eggs if)
of 'foxocara or other ascarid species, eggs of strongyles)
are also killed under these conditions. However, it has
to be stressed that this does not apply to Taenia and
Echinoccus eggs (see below).
Most antiparasitic disinfectants contain methyl phenols
(= cresols) as active substances, predominantly 4-chloro­
m-cresol (= p-chloro-m-cresol). Some are based on
peracetic acid or other substances (see below OO­
Cide•). They are usually applied in concentrations of
2-4% with exposure times of 2-3 h. This group includes,
for example, Neopredisan• 135-1 (active ingredients:
25% 4-chloro-m-cresol, 5% organic acids) and Endosan
Forte• S New (active ingredient: chlorocresol), which are
effective against Ascaris eggs, oocysts of coccidia and
Cryptosporidium and against viruses, bacteria and fungi
with slightly different exposure times. Germicidan• KOK
(active ingredients: 15-30% phenols and halogenated
phenols, 5-15% surfactant) is effective against
coccidia oocysts. OO-Cide• has a similar spectrum to
Neopredisan• and Endosan Forte•, and consists of 2
separate components: ammonium chloride and sodium
hydroxide. Dissolved in water the two components
come into contact only on the surface to be disinfected
and release ammonia gas as active ingredient. Taenia
and Echinococcus eggs are resistant to the mentioned
disinfectants. However, sodium hyp ochlorite (NaOCl)
is effective in a concentration of at least 3.75%
(concentrated solutions containing approximately
13% NaOCI), which can be used for the disinfection of
concrete or stone floors and stables at exposure times
of at least 30-60 minutes. Due to various disadvantages
(caustic, corrosive, low penetration depth) NaOCl is
Q)
however a stopgap and not an optimal disinfectant.
·u
C
'6
Q)
In general, chemical disinfectants may only be applied �
in empty stables and in strict accordance with the C'
instructions regarding usage and protection of the co
C
·;::
user. Furthermore, measures must be taken to avoid the
J
Q)
outflow of disinfectants in the wastewater. The volatile
ammonia is not a problem for wastewater. C
>.
0)
According to an EU directive (889/2008), among the 0
0
agents that may be partially effective against parasitic ·u5
stages, only (hot) water, steam and sodium hypochlorite �
co
(caution: aggressive!) are approved for use on organic 0...
farms.
 Part VI. Principles of therapy and control of parasitoses
• Disinfestation of stables and other rooms.
Measures for the elimination of mites and their
developmental stages in stables are required in the
control of mange of domestic animals (sheep, cattle,
pigs, etc.) or the infestation with Dermanyssus in
chicken. To this end, the common cleaning measures
(hot water/steam) are taken and the stables sprayed
with an acaricide if necessary. Special measures against
Dermanyssus are described on ► p. 611. Environmental
treatments may be required for flea control in dogs and
cats. For this purpose, insecticides and insect growth
regulators alone or in mixtures are used.
• Disinfection in the laboratory. Working with
parasites in the laboratory requires special safety
precautions which may include disinfection measures.
Special guidelines should be consulted.
18.2 Control strategies
The term scheduled (= strategic) control refers
to the use of effective control measures at certain
epidemiologically appropriate and diagnostically backed
times in order to sustainably disrupt the life cycles of
the parasites and achieve the maximum benefit to the
host animals. An important issue is the targeted, limited
(with regard to the amount necessary), economical and
environmentally friendly use of antiparasitics. Special
attention requires the prevention of introduction
and elimination of parasitoses. In Europe, the latter
is currently only possible for a few parasitoses, under
the condition that the necessary funds are available
(examples: mange in swine and ruminants, hypodermosis
of cattle, Echinococcus granulosus infection in dogs and
intermediate hosts).
The measures for strategic control can be divided into
several categories:
• Prophylaxis. This term summarises all measures
aimed at the protection of individual animals and
livestock against parasites and parasitic diseases.
This includes general measures (also referred to as
prevention), which have already been mentioned
on ► p. 556. The aim of infection prophylaxis
is to prevent infection with pathogens and their
(J.)
C establishment or reproduction in animals or reduce
·c3
'6 it to an acceptable level. Contamination prevention
(J.) aims to reduce or prevent the contamination of the
�
environment with developmental stages of parasites
Ctl and thus to reduce the risk of infections.
C
·.:::: • Metaphylaxis (= mesophylaxis). Metaphylactic
measures, e.g. treatments with antiparasitics, affect
C the parasite cycle at an epidemiologically appropriate
>, time when a parasite infection in individuals or in
0)
0 herds already exists, but strong infections or adverse
0
·u5 effects have not yet occurred. An example is the
treatment of cattle against migratory warble fly larvae
Ctl
a..
in fall before they have reached the spinal canal and
the dorsal skin thus avoiding damage in these sites.
• Therapy. In strategic control, treatments to cure
disease should be exceptions, but they cannot always
be avoided.
• Integrated control. Programs for integrated control
combine all necessary measures for the sustainable
control of one or more parasites in a strategic
plan. An example is the simultaneous control of
gastrointestinal nematodes and lungworms in cattle
(► p. 582).
• Parasite control in organic farms. Although the
organic animal sector has been developing rapidly
in Europe in recent years, it is still limited compared
to total animal production. In the EU the share of
organic production within total production varies
between about 3% each in cattle and sheep, 0.33%
in pigs and 0.95% in poultry (EU 2013). However,
in some EU member states the shares are much
higher, for example for bovines in AT 19%, in SE
17% and in DK 10%.
The legal framework for organic farming is set in EU
regulations (Regulations no. 834/2007 and no. 889/2008)
which are adopted, unchanged or in a modified form,
by the EU member states and Switzerland. Furthermore,
there are numerous private law rules of organic
associations that in part define conditions beyond the
EU rules (e. g. negative lists of drugs which may not be
used in organic farms). Comprehensive information
about the 'organic farming' can be found on the Internet
(e.g. EU: http://ec.europa.eu/agriculture/rural-area­
economics/index en.htm; DE: www.oekolandbau.de,
AT, CH: www.fibl.org).
The above mentioned EU regulations contain, inter alia,
the following rules for 'disease prevention' in livestock:
• Choice of suitable breeds and strains of animals
and application of animal husbandry procedures
ensuring that the developmental, physiological and
ethological needs of the animals are met. Respective
measures include appropriate stocking densities,
access of the animals to open air, preferably to
pasture, hygienic conditions, and high quality of
organic feed.
• Diseases shall be treated immediately to avoid
suffering of the animal. According to Regulation
889/2008, phytotherapeutic and homeopathic
products, trace elements and 'other products' (which
are listed in annexes) 'shall be used in preference
to chemically synthesised allopathic veterinary
treatment or antibiotics' , provided that their
therapeutic effect is warranted for the animal
species and the condition for which the treatment
is intended.

• Products from animals that have been treated more
than 3 times with 'chemically synthesised allopathic
veterinary medicinal products or antibiotics' within
one year, may not be sold as organic products.
Excluded are treatments for parasites, vaccinations
and compulsory eradication programs.
I The withdrawal period prescribed for an 'allopathic
veterinary medical product' must be doubled in
organic farms.
• Use of 'coccidiostats' is not permitted, but rather
the use of 'immunological veterinary medicinal
products' (EC 834/2007).
• For deaning and disinfection only means permitted
in organic production may be used ( ► p. 571 ).
• Further regulations relate to bees and aquaculture.
From a parasitological point of view, the intentions
of organic farming to ensure animal health primarily
through preventive measures and minimal use of
medicines correspond with the 'classical' concepts
of parasite control (see strategic control). However,
the means that are recommended to achieve these
objectives in organic farming are partly inadequate or
questionable. For phytotherapeutic and homeopathic
products there are hardly any scientific examinations
concerning their effect, tolerability, residue behaviour
and environmental toxicology. Thus, an objective
assessment of the suitability of such agents for the
treatment of certain diseases is often not possible.
Therefore, the EU's general recommendation that
such remedies should be employed in preference to the
'chemically synthesised allopathic' veterinary drugs is
not rational. The distinction between synthetic chemical
and herbal ingredients is scientifically incorrect since
it does not matter whether chemical active substances
are derived from plants or from chemical synthesis. Of
more importance are their properties regarding efficacy,
etc. Also, the general doubling of the withdrawal periods
when using 'allopathic' veterinary medicinal products
is scientifically unjustified.
• Selected r,;;1ferences l'Dllaa.aam..aal!lm:m
Therapy
Campbell WC, Rew RS (eds.) (1986) Chemotherapy of parasitic
diseases. New York, NY, USA: Plenum Press; ISBN 0-306-
42029-5.
Knox MR, Besier RB, Le Jambre LF, Kaplan RM, Torres­
Acosta JF, Miller J, Sutherland I (2012) Novel approaches
for the control of helminth parasites of livestock VI: Summary
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Mehlhorn H (ed.) (2008) Encyclopedia of Parasitology. 3 rd ed.
Berlin, Germany: Springer; ISBN: 978-3-540-48994-8.
Vercruysse J, Rew RS (eds.) (2000) Macrocyclic lactones in
antiparasitic therapy. First edition, New York, NY, USA: CAB
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18. Control
Drug resistance
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Acaricide resistance in cattle ticks and approaches to its
management: the state of play. Vet Parasitol 203: 6-20.
Charlier J, Morgan ER, Rinaldi L, van Dijk J, Demeler J,
Hoglund J, Hertzberg H, Van Ranst B, Hendrickx G,
Vercruysse J, Kenyon F (2014) Practices to optimise
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Coles GC, Jackson F, Pomroy WE, Prichard RK, Von
Samson-Himmelstjerna G, Silvestre A, Taylor MA,
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Dobson RJ, Hosking BC, Jacobson CL, Cotter JL, Besier
RB, Stein PA, Reid SA (2012) Preserving new anthelmintics:
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Geurden T, Hoste H, Jacquiet P, Traversa D, Sotiraki S,
Frangipane di Regalbono A, Tzanidakis N, Kostopoulou
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Hanna RE, McMahon C, Ellison S, Edgar HW, Kajugu PE,
Gordon A, Irwin D, Barley JP, Malone FE, Brennan GP,
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Kotze AC, Hunt PW, Skuce P, von Samson-Himmelstjerna G,
Martin RJ, Sager H, Krucken J, Hodgkinson J, Lespine
A, Jex AR, Gilleard JS, Beech RN, Wolstenholme AJ,
Demeler J, Robertson AP, Charvet CL, Neveu C,
Kaminsky R, Rufener L, Alberich M, Menez C, Prichard
RK (2014) Recent advances in candidate-gene and whole­
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Matthews JB (2014) Anthelmintic resistance in equine
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Moussavou-Boussaougou MN, Silvestre A, Cortet J, Sauve
C, Cabaret J (2007) Substitution of benzimidazole-resistent
nematodes for susceptible nematodes in grazing lambs.
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Prichard RK, Geary TG, Chappell LH (eds.) (2007) Markers
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Schnyder M, Torgerson PR, Schonmann M, Kohler L,
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 Part VI. Principles of therapy and control of parasitoses
Voigt K, Scheuerle M, Hamel D, Pfister K (2012) High perinatal
mortality associated with triple anthelmintic resistance in a
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Von Samson-Himmelstjerna G (2012) Anthelmintic resistance
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Wolstenholme AJ, Evans CC, Jimenez PD, Moorhead AR
(2015) The emergence of macrocyclic lactone resistance in
the canine heartworm, Dirofilaria immitis. Parasitology 142:
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Biological control
Githiori JB, Athanasiadou S, Thamsborg SM (2006) Use
of plants in novel approaches for control of gastrointestinal
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Stear MJ, Doligalska M, Donskow-Schmelter K (2007)
Alternatives to anthelminthics in the control of nematodes
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Vercruysse J, Dorny P (1999) Integrated control of nematode
infections in cattle: a reality? a need? a future? Int J Parasltol
29: 165-175.
lmmunobiological control (vaccination)
Bassetto CC, Picharillo ME, Newlands GF, Smith WD,
Fernandes S, Siqueira ER, Amarante AF (2014) Attempts
to vaccinate ewes and their lambs against natural Infection
with Haemonchus contortus in a tropical environment. Int J
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Bethony JM, Cole RN, Guo X, Kamhawl S, Llghtowlers MW,
Loukas A, Petri W, Reed S, Valenzuela JG, Hotez PJ
(2011) Vaccines to combat the neglected tropical diseases.
lmmunol Rev 239: 237-270.
Gradonl L (2015) Canine Leishman/a vaccines: still a long way
to go. Vet Parasitol 208: 94-100.
Hiszczynska-Sawlcka E, Gatkowska JM, Grzybowski
MM, Dtugonska H (2014) Veterinary vaccines against
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Jarrett WFH, Jennings FW, McIntyre WIM, Mulligan W,
Sharp NCC, Urquhart GM (1960) Immunological studies on
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Jayashi CM, Kyngdon CT, Gauci CG, Gonzalez AE,
Ughtowlers MW (2012) Successful immunization of naturally
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C Jonsson NN, Matschoss AL, Pepper P, Green PE, Albrecht
·c.3
'6 MS, Hungerford J, Ansell J (2000) Evaluation of TickGARD
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in Rio Negro, Argentina: second study of impact. PLoS Negl
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crl
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Lightowlers MW (2013) Cysticercosis and echinococcosis. Curr
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19. Parasitoses of different animal species
and organ systems, antiparasitic drugs
and strategic control
This chapter offers tabular overviews of parasitoses
structured by host species and organ systems,
including diseases that occur predominantly in Europe.
These sets are intended to facilitate the orientation for
animal species- or organ-related teaching and studies.
Page references provide quick access to the previous
text sections with detailed information. Selections
of antiparasitic drugs (= antiparasitics) that are
currently (at the time of writing the book) registered
internationally in all EU member states by the European
Medicines Agency (EMA) or nationally in at least one
EU country or in Switzerland are also presented.
Registration and labels of approved drugs may differ in
various countries and may change at any time. Therefore,
every user is requested to observe the official national
regulations and to examine the labels of each drug
carefully. The spectra of efficacy of antiparasitics refer
- unless otherwise indicated - to the adult stages of
the parasite. The listed dosages are indicative dosages;
in addition there may be other feasible dosage and
administration options. Withdrawal periods will vary,
depending on the active substance, dosage, application
form and country, as the exemplary data show in the
tables. In Chapter 20 a variety of commercial products
of the active ingredients is listed for each species or group
of animals. The authors expressly point out that the
provided lists of active ingredients and the commercial
products do not claim to be complete. For 'off-label use'
(► Glossary, p. 620) of drugs the national legislation
has to be observed.
More information about antiparasitic drugs can be
found in Parts II and Ill and in Chapter 17 ( ► p. 556)
of this book, as well as in pharmacology textbooks
and databases (box below). Antiparasitics used as feed
Information on veterinary drugs, Including antiparasitics, which are authorised at the European or national level can be
obtained from:
European Medicines Agency (EMA) (htpp://www.ema.europa.eu/ema).
National data banks, for example:
• CH: Tierarzneimittelkompendium (http:/www.
tierarzneimittel.ch)
• DE and AT: Vetidata (http://www.vetidata.de)
• ES: Spanish Agency of Medicines and Medical Devices
(AEMPS) (https://www.aemps.gob.es/en/home.htm);
• FR: MED'VET - La reference sur les medicaments
veterinaires (www.med-vet.fr)
Above listed data bases usually provide detailed information on active ingredients, dosage, tolerability, etc., and also on
product names which often differ in various countries.
additives and some antiparasitic ectocides are in part
outlined in separate EU or national lists.
The measures described here for the strategic control
( ► Glossary, p. 620) refer to some important parasites
of various species of domestic animals. These measures
represent epidemiologically based and verified methods,
but also in part recommendations whose effectiveness
have yet to be further evaluated. Control measures
against various parasite species in one host species (e.g.
gastro-intestinal nematodes and lungworms in cattle)
should be combined into an integrated programme.
19.1 Parasitoses of cattle, sheep
and goats
19.1.1 Parasitoses of organ systems
and antiparasitics
Parasitoses of cattle, sheep and goats are presented in
► Table 19. l, and selected anthelmintics, ectocides and
endectocides in ► Tables 19.2 to 19.6. Antiprotozoals
are not listed here, because these drugs must be used
relatively rarely in ruminants in Central Europe and are
mentioned in the chapter on protozoa. Regarding drug
resistance (DR), the reader is referred to Chapter 17.
19.1.2 Strategic control of important
parasitoses of cattle
19.1.2.1 Fasciolosis
Diagnosis on farm level and investigations of the
local epidemiological situation are prerequisites for
an effective control of fasciolosis. The control is based
on preventive measures and strategic anthelmintic
• IT: Prontuario dei Medicunali Veterinari: (https://www.
vetinfo.sanita.it/j6_prontuario/public/)
• NL: FIDIN repertorium (http://repertorium.fidin.ni/)
• UK: NOAH: Animal Office of Animal Health (http://www.
noah.co.uk/) and UK Veterinary Medicines Directorate
(http://www.vmd. defra.gov.uk)
 19. itos s of different animal species and organ systems, antlparasitic drugs and strategic control

'llble 19.1. Parasitoses(selection) of organ systems of cattle, sheep and goats. 1

Tick infestation(► p. 396) lxodes ricinus, Oennacentor marglnatus, 0. ret/culatus, Haemaphysa/1s

punctat a , Rhipicephalus turanlcus and others
Demodicosis( ► p. 426) Oemodex ovis(S), Oemodex bovis
1------------+---------------1-- Dem
_ --'- ( ___
o _de_x_capcae �
Trombiculosis( ► p. 431) Trombicu/a spp. Trombicula sp .(S/§1._ _____.
Raillietiosis(► p. 424) Raillietia auris
Chorioptic mange( ► p. 439) Chorioptes bovis, Ch. texanus Chorioptes bovls (SIG)
Sarcoptic mange( ► p. 442) Sarcoptes sc a biei var. bovis Sarcoptes sc a b/el var. ovls(S),
S. scabiel var. rup/ca rae(G)
Psoroptic mange( ► p. 435) Psoroptes ovis Psoroptes ovls(S)
Ear mange( ► p. 435) Psoroptes cunicu/1 (SIG) 0
Chewing lice infestation Bovico/a bovis Lepikentron ovis(S), 0)

Bovicola caprae (G)

-0
(► p, 450) C

Unognathus ovillus(S),
<U
Biting lice infestation( ► p. Haematopinus sp., Unognathus sp., Q_
453) Solenopotes sp. Unognathus stenopsis (G) (l)
(l)
.r::.
Blackfly infestation( ► p. Simulium spp. Simulium spp.(SIG) (/)

465)
Fly infestation(► p. 472 ff) Tabanlds, Musca spp., Stomoxys Tabanids, Musca spp., Stomoxys ro
spp., Hydrotaea spp.,Haematobia spp., etc. (SIG) u
spp., etc.
Myiasis( ► p. 483) Lucilia spp., Cal/iphora spp., as In cattle
l--------·---t-Wi_oh_lfa_hrtla sp�_.,_etc _ _. ___ ___ _ _ __ _
Warble fly infestation( ► p. Hypod e rma bovis, H. lineatum Przhevalski8na sllenus(SIG), southern
494) Eur�e_e_ _
Louse fly infestation( ► p. Hlppobosca varlagata Melophagus ovinus(S),
498) Upoplf?!!B cap<�/(0)
Parafilariosis( ► p. 353) Parolllarlo bovlcola
Onchocercosis( ► _p. 357)_ (?!lcho_cerc� g!!.!_IU!.._0 8,P:!?_ li0fl_!!�S
Stephanofilarl�sis( ► e.:_ 356)_ s_rephano(llarla spp.
------i-Besnoltiosis( ► _p. 115)____ Bosnolt/FJ lx1snoltl
r
Musculature Toxoplaamoala( ► p, 101) ► p. 107 Tc»,opkJs,n�_Q!Jndti(SI�)
Neosporosia( ► � 1-2)_- tyooswra conlnu,n NooslX)ra can,n�!:'2JSI�)_________.
Sare� stlosls(� P:�6) _ Sar�ocystls spp. Sarcocystls spp. (SIG)
---- --Cysticercosls( ► p. 224) __ Taenla 5.ogl11ata, lurvol Tt.lonla ovis, larval(SIG)
r-- 1
I Respiratory Dlctyocaulosis(► p. 303) Dl£1Y!!C!'ulus v'!'iPD!)JS_ CJ!<:_tJOC(Jufus fifarl_a (S/_Q) _ _
1
organs Protostrongylidosls( ► p. Protostrongylus spp.. Mueller/us sp.
313) and others(SI_G)'- __
Echinococcosis, cystic( ► p. Echinococcus granulosus s.l., larval Echinococcus granulosus s.l., larval
240) (SIG)
Taenia hydatigena, larval (SIG)

l
Cystlcercosis( ► p. 232)
fBlood Trypanosoma theileri infection Trypanosoma theileri Trypanosom a melophaglum(S)

::�:i:�is( ► p. 129) Babes/a divergens, 8. bovis, 8. major, Babes/a motasi, Babesia ovis (SIG)
8. bigemina
·o-=s.c.::
is...,__
( ....2P:..:·_1_4.c.:: Th ei·,en=a a n nu
0),__- ---1-.:..:. a . :.:..T. bu�'·-comp vis ( SIG_
---+-Th_e_ila_n...c -= :::...:..:. = l=at=:... -=-=.:..:.=-.:::.::.:.: � -=le x:.._-i-.:....Th.:.::::.
ei/er, 1a:..:s:!:p:.:... 1:(S::...
IG=)!..:., ...:..Th...:..e:= il.=:...;r:
e iao _
-.: .::.. _,_ _ )
► -=.:..:. :..: = :.....,
!Rumen Paramp histomatidosis ► ( p. P a ramphistomum spp., Galicophoron Paramphlstomum spp. S ( )
I 189) daubneyi
Abomasum Trichostrongylidosis(► p. Ostertagia ostertagi and related H a emonchus contortus, Teladorsagia
I 287) species, Trichostrongylus axei, rarely c/rcumclncta, Ostertagia spp.,
Haamonchus contortus Trichostrongyfus axei (SIG)
 Part VII. Parasitoses of different animal species and organ systems, antiparasitic drugs and strategic control

Table 19.1. Continued.

,( � l , ,) I�. f-'1_,�,-jl; i.itlLTfit:n

. I
I
.. . ..

'!��\��Q)
\ 1' 1

Small Cryptosporidlasis ,Q ► I!).
intestine Eimeriasis ( ► p. 91)
Giardiosis ( ► p. 47)
Monieziosis ( ► p. 215)
' Stron9yloidosis ( ► p. 259)
Bunastomosis ( ► p. 285)
Trichostrongylldosis ( ► p.
287)
I Toxocarosis ( ► p. 338)
Capillariosis ( ► p. 373)
Large Eimeriosls ( ► p. 82)
intestine Chabertiosis ( ► p. 275)
Oesophagostomosls ( ► p.
276)
Trichuriosls ( ► p. 368)
Uver Dlcrocoellosls ( ► p. 191)
Fasclolosls ( ► p. 175)
Echinococcosis, cystic ( ► p.
240)
Cysttcercosls ( ► p, 232)
Genital tract/ Trltrlchomonosls ( ► p. 54)
fetus Neosporosls ( ► p, 110)
Toxoplasmosls ( ► p. 101)
CNS Toxoolasmosls ( ► p. 101)
NeoSDOroslS ( ► p. 110)
Coenurosls ( ► p, 234)
Elaphostrongytosls ( ► p. 317)
Eye Thelazloels ( ► p. 346)
1 The list is not exhaustive, the data predominantly relate to parasites occurring In Europe.
2
Bold: parasitoses of particular Interest.
0:.N
122) Oryptosporidiurn spl!).
EifiFleria alabamMsis, E el/ipsoidalis,
and others
Giardia dvodenalis
Moniezia benedeni
Strongy/oides papil/osus
Bun(!)stomum phlebotomum
Cooperia oncophora, Cooperia spp.,
Nematodirus spp.
Toxocara vltu/orum
Capillaria spp.
Elmeria bovls, E. zuernil
Chabertla ovina
Oesophagostomum radiatum
Trichuris globulosa, T. discolor
Dicrocoelium dendriticum
Fasciola hepatica
-�--
Echinococcus granu/osus s.l., larval
Taenia hydatigena, larval
Tritrlchomonas foetus
Neospora caninum
Neospora caninum
Taenla multiceps, larval
711elazia gulosa, 711. rhodesl,
711. skr/ablnl
,(Jr,yptospof:idium spp. (S/G)
Eimeria spp. (S/G)
Giardia duodena/is (S/G)
Moniezia expansa (S/G)
StrongyJoides papillosus
Bunostomum trigonocepha/11m (SIG)
Tric"1ostrongylus colubriformis,
T. vitrinus, Cooperia pectinata,
Nematodirus filicol/is, Nematodirus
battus and others (S/G)
Capillarla spp. (SIG)
Elmer/a spp. (SIG)
Chabertla ovlna
Oesophagostomum venulosum (S/G)
· Tr/churls ovls and others (S/G)
Oicrocoellum dendritlcum (SIG)
Fasclola hepatlca (S/G)
Echinococcus granulosus s.l., larval
(S/G)
Taenia hydatlgena, larval (SIG)
Toxoplasma gondi/ (S/G)
Toxoplasma gondii (S/G)
Neospora caninum (SIG)
Taenla multiceps, larval (S)
Elaphostrongylus cervi (G)
'

treatment. Due to epidemiological factors given in
Central Europe (main infection period in late summer
and autumn, prepatent period 8-10 weeks) the housing
period is an adequate time for treatment.
Prevention. The use of G. truncatula-free areas for
grazing of cattle and other susceptible hosts can limit
fasciolosis problems on a farm. Grassland inhabited by G.
truncatula and contaminated with Fasciola eggs (by liver
fluke carriers or slurry) should be used for production
of silage or hay. Access of cattle to permanent habitats of
intermediate hosts (e.g. localised damp patches, ponds
on pastures, creeks, etc.) can be prevented or restricted
by fences. This measure is particularly effective when
there are only a few habitats of G. truncatula in a pasture
area (e.g. in CH in 57% of 70 cattle farms). Artificial
watering places established on pastures contribute to
reduce the infection risk, but secondary snail habitats
(e.g. damp patches around these places) must be avoided.
Strategic treatment. In diagnostically confirmed
cases of fasciolosis all cattle (>3 months old) on the
farm and other potential Fasciola carriers (sheep, goats,
etc.) that have been exposed to an infection risk must
be treated with a highly effective fasciolicide ( ► Table
19.2) after housing (October to December). Unexposed
animal groups should be excluded from treatments.
Whether a second treatment during the housing period
is indicated depends on the choice of the fasciolicide (see
below). Treatments of cattle during the grazing period
are usually not indicated. In herds with a faciolosis
problem the control programme is initially performed
and monitored for 2-3 years. Thereafter, it should be
evaluated whether strategic treatments every 2nd year
 .,-,,,. 1fl.ll. Anthe/mint/cs (selection) for use In cattle (boll ► Table 19.3) (select/on of commercial products ►Chapter 20, p. 615).

wig !D

I i I i :�.H
6'
I
r
-:z (J)

� (!)

IIt f f fI
(J)

i
Ill 12.
i §
I:I f I
Cl

I ·!
: .. i .. i- ..
i
=I:
0 (!)
::a 0 I
: a
::I cil
IQ
iii
-! IQ g.
C c! C
3 f.. ( 3
§
C
i
0
•r: C
3
C
•• •
C I:
;r
0)
Ill ii ii'
Albendazole (BZ) 7.5 p.o. • () • • • • • • • • 21-28DE 5DE l!1.
•
7.5-10
• •
()

•
() () ()

Febantel (PBZ) 7.5 p.o. () • • • • 14DE 4DE

(J)

•
>40
•
()

•
()

• •
()

Fenbendazole (BZ) 7.5 p.o. () • • • • I • 7 DE

�°:_____) iR
•
>67
•
()

•
()

• •
()

Netobimin (PBZ) 7.5 p.o. • • • 4-10 5CH

• • •
1<JCH
•
()

•
()

•
()

• •
()

•
()

• • �
Oxfendazole (BZ) 4.5 p.o.
• 120 14DE 5DE
•
()

Levamisole (11) 10.0 spot-on • • • • • - I - • 6 22DE nLDE

---, �
�
Doramectin (MW 0.5 pour-on • • • • • • • • • • • • nLDE �
!
25 35DE
0.2 i.m. • • • • • • • • • • • • DE nlDE
-,
Eprinomectin (ML) 0.5 pour-on • • I • • • • • • • • • •
70
I 10-15 DE
-1

• • • • •
10
•
iI
lvermectin (ML) 0.5 pour-on • • • • • • 15DE
I nl
()DEE
D
• • •
>4
0.2 s.c. • • • • • • • • • � nlDE
• • • • • •
20
lvermectin (ML) + Closantel (VO) 0.5+20.0 pour-on • • • • • • • 2ace
• • • •
>4
• • • • • • • •
I[
Moxidectin (ML) 0.5 pour-on 140E
• • • •
+
0.2 s.c. • • • • • • • • 55DE nlDE
•
+
Closantel (VO) 10.0 p.o. • 6 28DE LDE
Oxyclozanide (SA) 10.0 p.o. • =f

I
2 .µa
oe 30&
Triclabendazole (BZ) 12.0 p.o. • 16 5().56DE nLDE
1 Chemical group: BZ = benzimidazoles; ML = macrocyclic lactones; IT = imidazothiazoles; PBZ = pro-benzimidazoles; 4 SI (safety index) calculated rl pert for sheep; GT: general tolerabllrty ♦ • good.
�-

SA= sallcylanilides; VO= various other chemical groups; registration of drugs (► p. 556).
2 Selection of recommended doses; additional information: see labels or databases (► p. 576).
3 Efficacy: • = good to very high; C> = partially effective or effective in increased dose or with repeated application; - =
insufficient effect; empty fields = not documented or drug not recommended in this indication.
i
5 Withdrawal periods: tissue: meat and other edible tissue: nL: do not use In laciating animals
producing milk for human consunptlon; use of some ML only allowed up to 60 days before C11Mng;
withdrawal periods may vary depending on country and commen::lal product; therefore note the
latest information (labels, databases).

Parasitology in Veterinary Medicine . = • Strategic control

 Part VII. Parasitoses of different animal species and organ systems, antiparasitic drugs and strategic control
would be sufficient. Monitoring by coproscopy (possibly
including detection of specific antibodies) is necessary to
verify the treatment success and to exclude the presence
of anthelmintic resistance.
Fasciolicides. Products should preferably be used
(► Table 19.2.) with high efficacy against adult and
juvenile F. hepatica stages (triclabendazole is highly
efficacious against juvenile stages from the 2nd week
p.i., closantel from about the 6th week p.i.). Albendazole
and netobimin (in increased dosages of 10 and 20
mg/kg b.w., p.o., respectively) and oxyclozanide (10
mg/kg b.w., p.o.) are effective against adult Fasciola.
.l Drugs affecting juvenile stages can be applied shortly
after housing, whereas adulticidal drugs should be
administered about 8 weeks later. A single treatment
during the housing period is usually sufficient. If,
however, persisting infections have been revealed
by coproscopic examinations a second treatment (in
March) is necessary.
The treatment of lactating cows producing milk for
human consumption is problematic. In this indication
albendazole, netobimin and oxyclozanide with efficacy
against adult Fasciola stages are often used, because of
their relatively short withdrawal periods for milk of 3-5
days (triclabendazole is not allowed for use in lactating
cows or has a withdrawal period of 12 days for milk,
► Table 19.2). Alternatively, cows can be treated during
the non-lactating period (disadvantage: not all cows on
a farm can be treated at the same time).
19.1.2.2 Trichostrongylidosis
Control measures against cattle trichostrongyles
(especially Ostertagia and Cooperia species, ► p. 287),
which are essentially present in all grazing cattle herds,
are generally restricted to young animals in their first
grazing season. AnimaJs in their 2nd grazing period and
older cattle are usually protected from clinical disease
by acquired immunity. The measures aim to prevent
heavy infections (typically occurring in the 2nd half of
the grazing period), disease and significant impairment
of performance. The available control measures include
several components.
Q)
C • Pasture and farm management. Pasture and
·c3
'6 farm management measures are commonly taken in
Q)
�
addition to other methods of control; they are not usually
C' sufficient on their own to control trichostrongylidosis
ro in intensive grazing systems. These measures include:
C
·;::
Q) avoidance of overuse of pastures, late turnout of calves
to pasture (mid-May/early June and additional feeding
.£ on pasture), use of pasture land in the first weeks of the
>- grazing season for hay or silage production, alternative
0)
0 grazing programmes (e.g. grazing by horses or sheep,
0
rotationaJ grazing of cattle on 'clean' pastures in intervals
'in
ro of 3 weeks; very laborious!). On organic farms with
ro
CL a low or moderate infection risk adequate control of
trichostrongylidosis can be achieved without strategic
use of anthelmintics by extensive grazing (not >2
livestock units/ha), pasture management and particular
types of farming (see below).
• Application of long-acting anthelmintics.
Young cattle (> 100 kg b.w.) may be provided with a
so-called bolus(► Glossary, p. 620) at the beginning
of their 1st grazing period (early application) ( ► Table
19.3). The bolus remains in the rumen and releases
defined doses of an anthelmintic over a longer time
thus controlling the worm burden for 3-5 months,
and keeping egg shedding at a low level. Therefore,
the contamination of the pasture with infective larvae
remains low and a greater infection potential cannot
build up in the 2nd half of the grazing period. In mixed
grazing groups with young (1st grazing season) and older
animals (2nd season), it may also be useful to provide the
older animals with a bolus to maintain egg shedding at
the lowest possible level. In mountainous regions, a late
application of the bolus early June/July is particularly
suitable when the animals are moved to higher alpine
pastures where they graze during summer. At the end
of the 1st grazing period an anthelmintic treatment is
recommended for the pasture groups (so-called housing
treatment). For this an anthelmintic should be used that
is also effective against hyp obiotic stages of Ostertagia
ostertagi (and if indicated of Dictyocaulus viviparus)
(► Table 19.2). When using macrocyclic lactones for
housing treatment various arthropods (mange mites,
lice, migrating larvae of Hypoderma) are affected in
addition to nematodes (s. corresponding chapter).
Recently long-acting (= extended-release) injec­
table anthelmintics (macrocyclic lactones) have
been developed preventing the establishment of
gastrointestinal nematodes and lungworms up to several
months (e.g. ivermectin: 2.5, eprinomectin: 5 months)
after a single application. Long-acting anthelmintics
raise concern regarding the development of anthelmintic
resistance. Therefore, this potential problem should be
addressed and monitored.
• Strategic treatments at or after turn out
to pasture. As with the long-term medication, the
objective of such treatments is a reduction of worm
burdens and egg excretion in the 1st half of the grazing
period to prevent severe infections later on. There are
several options including targeted treatments (TT)
and targeted selective treatments (TST) (► Glossary:
treatment).
Targeted treatments with macrocyclic lactones
(ML). ML not only act against the nematodes
established in the digestive tract (or in the lungs),
but also inhibit the establishment of newly ingested
larvae due to their long persistence in the animal
body for about 2-4 (5) weeks (residual= persistent
effect). The duration of the residual effect depends
on the anthelmintics and the nematode species
 19. Parasitoses of different animal species and organ systems, antiparasitic drugs and strategic control

Table 19.3. lntraruminal boli for parasite control in cattle.

iubstance (genertc name), amount of Mode of reteue of

eubetance per bolua, (product name), IUbstance (MR), doN tD) and
bolus structure
acaw.
duration of activity (DA)
........
�of

Levamisole (18.8 g)
(Chronomintic® Bolus)
MR: diffusion
D: 2.0 g in 24 h post application, then
GIN. Oictyocaulus IE: 140CH
M: nLCH
-
0

0
Drug matrix with hardened top layer -220 mg/day (.)

DA: 90 days
(.)
·a,
Fenbendazole (12 g) MR: corrosion, continuously GIN. Oictyocaulus E:200°E
(Panacur SR® Bolus) D: 0.2-0.4 mg/kg b.w. M: nLDE
10 fenbendazole tablets in corrodible DA: 120-140 days
(/)

magnesium shell
Oxfendazole (3.75 g) MR: corrosion, at intervals of -23 days GIN. Oictyocautus. E: rnoDE
(Systamex Interval Bolus®) D: per release 750 mg Monlezia M: nLDE
Metal part in conjunction with corrodible rod on DA: 125 days
which 5 containers are lined with 1 anthelmintic
tablet
Oxfendazole (7 .5 g) MR: corrosion, at intervals of -23 days GIN, Oictyocaulus, E: 18QDE
(Systamex Interval! Bolus forte®) D: per release 1,250 mg Moniezia M: nLDE
l«l Systamex Interval Bolus, but with 6 tablets DA: 150 days
1 GIN: gastrointestinal nematodes.
2 E: edible tissue: M: milk; nl: do not use the bolus in animals producing milk for human consumption; withdrawal periods specified by the
manufacturer in weeks or months were converted into days.

involved. After the residual effect has subsided
and a reinfection has occurred it takes another 2-4
weeks (prepatent period) until the resumption of
egg shedding. Based on these facts the following
treatment intervals have been recommended for
ML with long residual effects (e.g. doramectin,
moxidectin): first treatment at turnout in spring
and second treatment 6 or 8 weeks later (so-called
0-6 or 0-8 system). All I st season grazers are treated,
sometimes also older animals (especially in mixed
grazing systems). Such treatments can provide
nematode control throughout the whole grazing
season. Additionally, the 1 st season grazers and,
if necessary, also older animals in problem herds
should be treated at housing. Special precautions
and withdrawal periods have to be observed if
pregnant or lactating cattle are involved in such
treatment programmes. In alpine pasture systems, a
treatment of 1 st season grazers with an ML at turnout
to alpine pastures (June) and a second one at housing
represents an effective control measure.
- Targeted treatments with short-acting anthel­
mintics. The use of short-acting agents (e.g.
benzimidazoles, levamisole) requires shorter
treatment intervals, e.g. 3, 6 and 9 weeks after turnout
and in addition a further treatment at housing in
autumn (see above). Frequencies and intervals
of treatments should be based on the results of
diagnostic monitoring.
• Strategic treatment with change of pasture
(Weybridge system). Treatment of young cattle in
mid-July and moving the animals to a 'clean' pasture
(not yet grazed by cattle in the same year) 1-2 days later
has proven to be successful. However, the system has
been considered as likely to favour the development of
anthelmintic resistance in sheep. Although, anthelmintic
resistance of cattle nematodes is currently not a problem
in Europe, there are reservations against this control
method, which can be replaced by other options.
• Targeted selected treatments (TST}. The
occurrence of anthelmintic resistance (AR) in sheep
and horse nematodes has stimulated the development
of control options with the potential to confine the
resistance problems and to promote the sustainable use
of anthelmintics. Whereas targeted treatments comprise
the whole pasture group, targeted selective treatments
are confined only to those animals of a pasture group
which are identified as mainly responsible for pasture
contamination (for details, see parasites of horses, ► p.
590). Animals to be treated are selected based on a single
or a combination of treatment indicators, such as faecal
egg counts, plasma pepsinogen levels, weight gain or
body condition score. A recent comparative study in
Ireland suggests that the performance of dairy calves
can potentially be maintained in a TST system with
much lower use of anthelmintics compared to the T T
system. However, lungworm control was not satisfactory.
Currently, several TST approaches are under evaluation
with the aim of optimising the system. TST incurs more
cost for diagnostics and labour but less for anthelmintics
as compared to TT.
• Control in special husbandry systems. In cow­
calf enterprises suckler calves start to graze relatively
late and gradually. In contrast, the cows consume large
amounts of grass thus ingesting infective trichostrongyle
larvae ('vacuum cleaner effect'). As a result, the infection
risk for calves and for development of disease is lower
 Part VII. Parasitoses of different animal species and organ systems, antiparasitic drugs and strategic control
than on pasture used only by young stock. A similar
effect can be achieved by mixed grazing of 1 st season
grazers with 2nd season beef cattle and the additional
feeding on pasture.
19.1.2.3 Dictyocaulosis
As with trichostrongylidosis the heaviest Dictyocaulus
infections happen in the 2nd half of the grazing period
(► p. 303). Outbreaks of disease occur most often
from July to September but also partly very late in
the grazing period. Because of the high pathogenicity
of lungworms, pasture contamination even with low
numbers of lungworm larvae can lead to serious disease
at the end of the grazing season. It should be noted
that not only young cattle in their 1 st grazing season
can suffer from dictyocaulosis, but also older cattle if
they weren't pre-exposed to any lungworm infection
(e.g. cows transferred from lungworm-free herds to
endemic areas). The strategic control consists of the
following options:
• Pasture and farm management. The causative
agent of dictyocaulosis, Dictyocaulus viviparus, can be
introduced into uninfected stocks or pasture groups
by lungworm carriers and cause heavy losses due to
disease outbreaks. This should be taken into account
when purchasing cattle and when merging animals
from different herds. As a precaution cattle acquired
from potentially infected herds should be treated in
quarantine stables with an anthelmintic ( ► Table 19.2).
• Oral vaccination. Calves from a minimum
age of 2 months are immunised orally 6 weeks before
their I st grazing period and 4 weeks later. In this
case, all susceptible animals i.n a pasture group must
be vaccinated. Older cattle are to be included in the
programme if they have not been vaccinated/exposed
during their I st grazing season or if they are transferred
into stocks where there is a risk of infection (see above).
The method has proven very useful in endemic areas;
however, the vaccine (BoviJis• Dictol) is only available
in a few countries.
• Application of long-acting anthelmlntics,
TT and TST. The measures used to control
Q)
C trichostrongylidosis (see above) are usually also
·c:;
'5 effective in control of dictyocaulosis. However, since
�
Q)
severe clinical disease can occur at the end of the grazing
period, a late application of an anthelmintic bolus in
co
C the 2nd half of the grazing period will result in a better
·c control of the infection.
Q)
C 19.1.2.4 Infestation with ticks
>,
0)
0 In Central Europe tick control in grazing cattle is usually
0
'ci)
not necessary, but in some farms where heavy infestations
with Ixodes ricinus occur, the use of acaricides may
co
CL be indicated (e.g. pour-on treatment with flumethrin
at turnout with repeated treatments several times at
intervals of 2-3 weeks).
19.1.2.5 Mange
Sarcoptic, psoroptic and chorioptic mange are known
to occur in European cattle. For strategic treatments
the beginning of the housing period in autumn is an
appropriate time. The goal of strategic control should
be the elimination of mange on a herd level, rather than
just a therapeutic intervention. Elimination is possible by
the strategic and consistent use of macrocyclic lactones
(ML).
Sarcoptic and psoroptic mange. The animals are
treated with injectable ML, e.g. with doramectin(i.m.),
ivermectin (s.c.) or moxidectin (s.c.) ( ► Table 19.4).
The treated animals are protected from re-infestations
with mites for 1-7 weeks. The efficacy spectrum of ML
also includes gastrointestinal nematodes, lungworms
and lice. Pour-on formulations of ML are less effective
in these forms of mange. However, flumethrin applied
pour-on twice at an interval of 10 days is effective against
psoroptic mange(► Table 19.4).
Chorioptic mange. Known as 'tail mange' quite
commonly causes significant problems in dairy herds.
Drugs of first choice for control are products without
prescribed withdrawal periods for milk (e.g. moxidectin
or eprinomectin for pour-on application, ► Table 19.4).
Cleaning and disinfection. Stables and vehicles
used by infested animals and all equipment must first
be cleaned and then disinfected with hot water (steam
jet cleaners) and by spraying with an acaricide.
19.1.2.6 Infestation with chewing and
biting lice
Chewing and biting lice ( ► p. 450) occur frequently in
cattle, often in mixed infestations of several species. The
highest infestation intensities are observed in winter and
early spring. Control measures are indicated because of
the harmful effect of the parasite and the harassment
of cattle.
Treatments with pour-on formulations of pyrethroids
or ML are easy to perform and highly effective against
chewing and biting lice ( ► Table 19.4). Due to the
long residual activity of the ML the larval stages of the
parasites, which might emerge from the eggs (nits), are
affected even by a single treatment, and re-infestation
of the animals is prevented for several weeks.
In cases of massive infestations a second treatment may
be required after 7 -10 days. All cattle of the holding must
be included in the treatment programme. For lactating
cows ectoparasiticides without a withdrawal period
for milk are available (eprinomectin, moxidectin; in
 �

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Cytluthrin (PY) C 0.2 mg/kg b.w., pour-on •C 1o□e
Cypermethrin (PY) C ear tag •C i0DE 0□E
Deltamethrin (PY) c.s C, S: 0.75 mg/kg b.w., pour-on • • •S •C 1ac□e QCD E ;r
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• • • • • 'C
C/l

Flumethrin (PY) C 2.0 mg/kg b.w., pour-on ()

I 5DDEE 8o e �-
Permethrin (PY) C ear tag • •C 0 �
Phoxim (OP) s spray/dip (see leaflet) • • • • • • •S 35DE
Doramectin (ML) C 0.5 mg/kg b.w., pour-on () • () • • • I •C I •Ce 350E
c.s 0.2 mg/kg b.w.. i.m.7 • () • () • •S •C 7ocs0e
Eprinomectin (ML) C 0.5 mg/kg b.w., pour-on () • () • • •C •Ce 15DE 0□E
lvermectin (ML) C 0.5 mg/kg b.w., pour-on () • () • • •C •Ce 2 5DE nL DE
c,s 0.2 mg/kg b.w., s.c. • () • () • •S •C 49COE nLDE !"
Moxidectin (ML) C 0.5 mg/kg b.w., pour-on () • () • • •C •C6 j 14DE 00E �
C 0.2 mg/kg b.w., s.c. • () •
1 Chemical group: ML = macrocyclic lactones; OP = organophosphates; PY = pyrethroids; VO = various other active substances.
() • •C •C6 55DE nL
l
en
2 Registration of drugs(► p. 556). Approved for cattle (C) and/or sheep(SJ and/or goat (G). c'i'
3 Selection of recommended doses; additional information see labels or databases(► p. 576). a.
4 Efficacy: • = good to very high; o = partially effective or in increased dose or with applications; empty fields = not documented or drug not recommetICled in this indication.
5 Withdrawal periods: tissue: meat and other edible tissue; nL: do not use in lactating animals producing milk for human consumption. Wrthdrawal periods may vary depending on country and commercial product; therefore
tEen
note the latest information(labels, databases). �
a.
8 Effective against Haematobia Irr/tans(► p. 480). �
7 In CH in sheep 0.3 mg/kg b.w., withdrawal period for tissue 35 days.

o·

Parasitology in Veterinary Medicine Strategic control

 Part VII. Parasitoses of different animal species and organ systems, antiparasitic drugs and strategic control
AT withdrawal time for moxidectin: 6 days)(► Table
19.2). By using ML in pour-on applications for housing
treatment against nematodes in the fall (see above),
chewing and biting lice are also covered. Injectable
ML are effective against biting lice, but not sufficiently
against chewing lice.
19.1.2. 7 Flies in grazing cattle
Comprehensive measures introduced at the beginning of
the grazing season aim at hindering the development of
strong fly populations also in neighbouring populations.
In practice, such measures are usually only performed
when the fly strike has become a significant and
recurring plague. Recent studies indicate a widespread
occurrence of insecticide-resistant fly populations.
• Insecticide-impregnated ear tags (ear cli ps).
All animals of a pasture group (young animals, cows)
are equipped at the beginning of the grazing season
with insecticide-impregnated ear clips(► Table 19.4).
Pyrethroid-containing ear clips have both repellent and
insecticidal effects. T he efficacy may last a few weeks,
but is often variable. Withdrawal periods for meat or
milk are not prescribed.
• Pour-on method. Special pour-on formulations
of pyrethroids (► Table 19.4) are available. Since
the residual efficacy lasts up to 1-2 months, several
treatments are often required during the grazing season.
After pour-on application of ML, the development of
the larvae of Musca autumnalis and Haematobia irritans
in cattle dung is affected for 1-6 weeks by drug residues
excreted by the treated animals in faeces.
• Other methods. In areas with high fly abundance
further control measures are employed, such as
insecticide impregnated back or face rubbers and walk­
through fly traps (see references: Townsend).
19.1.2.8 Hypodermosis
T he key measure of hypodermosis control in Central
Europe is the targeted systemic treatment of cattle in
autumn in order to kill the warble fly larvae migrating
in the body before they have caused skin damage
(preventive treatment in autumn). Treatment in spring
is only indicated when warbles have been formed in the
skin (spring treatment of manifest hypodermosis). T his
treatment is not systemic but local. The control options
summarised in ► Table 19.5 may vary according to
governmental regulations in each country. An alternative
option is the winter treatment using ivermectin in a
'micro-dose' of 2 µg/kg b. w., s.c. (I/ 100 of the normal
dose) which has been successfully tested in France in
a national programme. T his medication is inexpensive
and has the advantage that withdrawal periods for meat
and milk are not needed.
Table 19.5. Control of hypodermosis in cattle.
,Autumn treatment end of Withdrawal periods
September until end of (days) (details for DE)\
November E: edible tissue, M: milk1
Dairy cows
Eprinomectin: E: 15; M: 0
0.5 mg/kg b.w., pour-on 2
Moxidectin: E: 14; M: 0
0.5 mg/kg b.w., pour-on 2
Cattle, mother cows, calves >3 months (if already grazed)
Doramectin: E: 35; M: nl
0.5 mg/kg b.w., pour-on 2
Eprinomectin: E: 15; M: 0
0.5 mg/kg b.w., pour-on 2
lvermectin: E: 28; M: nl
0.5 mg/kg b.w., pour-on 2,3
Moxidectin: E: 14; M: 0
0.5 mg/kg b.w., pour-on 2
1 nl: do not use the drug in lactating animals producing milk for
human consumption.
2 Spectrum of efficacy► Table 19.4.
3 Not for use in dry cows within 60 days before calving.
Important note. When treating cattle with systemically
acting insecticides in doses as indicated in ► Table 19.5
during the period from early December to mid-March,
there is a risk that migrating warble fly larvae are present
in the spinal canal and are killed thus causing spinal cord
injuries with paralysis and recumbency. In the French
programme using micro-doses of ivermectin(see above)
clinical disorders were observed in 0.8% of cattle in the
first year of control, which decreased after 2 years to 0.2%
and were subsequently no longer observed(probably due
to the decrease of the warble fly infestation).
Strict control programmes have eliminated cattle
hypodermosis from many European countries and some
other areas( ► p. 494 ). Important measures for preventing
the spread or re-introduction of hypodermosis into free
areas include continuous monitoring (serology, etc.),
control of animal trade, and - if indicated - preventive
treatment of export and import animals.
19.1.3 Strategic control of important
parasitoses of sheep and
goats
19.1.3.1 Fasciolosis
The control of fasciolosis of sheep and goats is based on
the same principles as in cattle ( ► p. 175). Since sheep
are more susceptible to F. hepatica as cattle, subacute
or even acute forms of fasciolosis can already occur
in late summer. Such cases can be prevented by early
treatment(August to mid-September) with a fasciolicide
highly effective against juvenile Fasciola stages(► Table
19.6). During the housing period sheep are to be treated
according to the same schedule as cattle.
 ...�

I [ l !,
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en
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en
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3.85 p.o. • • • • • • • • • () ()
I
• ()6 5-10 I 10-14
□E 5DE 3.
Febante\ (PBZ) 5.0 p.o. • • • • • • • • • • • • 14DE 4DE
;r�
•
8 () () +
Fenbendazo\e (BZl8· G 5.0 p.o. • • • • • • • • () • • 42__!_ - () () >50
�
E 7DE �
en
Monepante\ (AC)8 2.5 p.o. • • • • • • • • >10 7D E n LDE �ar
Netobimin (BZ)8 7.5 p.o. • • • • • • • () • • () () 4-..!..9_ 1CJAT 5CH, 4AT
Oxfendazo\e (BZ)8 5.0 p.o. • • • • • • • • • • • 20 _@-
10CH nLCH �
• • C.
() ()

Levamisole (11)8 8.0 s.c. • • • • • • • • I 6-8 8oe nL□E

c§
Levamiso\e (11)8 7.5 p.o. • • • • • • • • • • • • 21DE nLDE, JOI �

1
() 6-8
Doramectin (ML}8 0.2 i.m. • • • • • • • • • • • • () + 700E nLDE
Eprinomectin (ML}G 1.0 pour-on • •
• •
•
•
•
• • • • • • • • •
() + 15CH -- QCHD --

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lvemiectin (ML)S 0.2 nL E
•
s.c. ()
30 42DE !I'
Moxidectin (ML) 8
0.2 p.o. • • • • • • • • • • • () + 14De 5DE
Triclabendazole (BZ)stG 10.0 p.o. • 20 5QDI!, 2SCH nL DE, 7CH
Closantel 0/0) 8 10.0 p.o. • • i 42DE nLDE _
• - 25DE j ?'5.
;::i:

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Oxyclozanide (SA) 15.0 p.o. _n�

.•_ --==-1 .·-

2
Trlclabendazole (BZ)8 + Moxidectin 10.0 + 0.2 p.o. • • • • • • • • • • • 1 () >5 - ---- ��E
31DE
-
Closantel 0/0) 8 + Mebendazole (BZ) 10.0 + 15 p.o. • • • • • • • • • • - 4 55DE nl□E
[
()

Praziquantel (ISO)5 3.75 p.o. • >5 rpE ()DE

1 Chemical group: BZ = benzimidazoles; ML= macrocyclic lactones; ISO= isoquinolines; IT= imldazothiazoles; PBZ 4 Wrthdrawal periods: tissue,. meal lRi other edible bssues; nL,. do not use In lactating animals producing
= pro-benzimidazoles; SA= sallcylanilides; IVO = various other chemical groups; registration of drugs(► p. 556). milk for human con5lXll)tion; withaawal periods may vary depending on countrv and commercial product;
2 Efficacy: • = good to very high; ()= partially effective or effective in an Increased dose or with repeated applications; therefore note the latest inlormation (labels. databases). ?'5.

I
- "' Insufficient effect; empty fields = not documented or drug not recommended In this Indication. 5 For goats a slightly higher dose is required.
3 SJ: safety index; GT: general tolerability: + = good. e Partial effect: BZ and PBZ often cause only reduction of larval shedding.

Parasitology in Veterinary Medicine Strategic control

 Part VII. Parasitoses of different animal species and organ systems, antiparasitic drugs and strategic control
19.1 .3.2 Monieziosis
Sheep acquire the infection with Moniezia expansa
(► p. 215) by uptake of infected intermediate hosts
(moss mites) during the first months of the grazing
season (April-June). Lambs in their pt grazing period
are mainly clinically affected. Co-infection with Eimeria
species or trichostrongyles should be considered in
differential diagnosis.
Treatment of lambs. Treatment is usually performed
late June/early July with praziquantel or a benzimidazole
with efficacy against Moniezia (► Table 19.6) (some
benzimidazoles act against Moniezia only in an increased
dosage). Gastrointestinal nematodes are also affected
by the use of benzimidazoles. Lambs born later during
the grazing period are treated at the beginning of the
yd month of life. Effective methods of prophylaxis are
not known.
19.1.3.3 Gastrointestinal strongyles (GIS)
GIS infections of sheep and goats ( ► p. 287) usually
represent mixed infections including different species
of trichostrongylids and other strongyles, such as
Bunostomum, Oesophagostomum and Chabertia.
Depending on the geographic region, certain species may
play a dominant role in epidemiology and pathogenicity
( e.g. Teladorsagia circumcincta and Cooperia species in
sheep in mountainous areas, Haemonchus contortus
and Trichostrongylus species or Nematodirus battus
in lowland and hill areas). Haemonchus contortus is
particularly prevalent in southern European countries.
As with the trichostrongyles of cattle, the greatest risk of
infection exists in Central Europe in the 2nd half of the
grazing period (except N. battus). It is epidemiologically
important that H. contortus overwinters primarily in the
form of hypobiotic stages in the host and that the greatest
risk of N. battus infections is in spring. It should be noted
that anthelmintic resistance in trichostrongyles of small
ruminants may exist, especially against benzimidazoles,
in part also against levamisole and macrocyclic lactones
(► p. 564). Because of the very different forms of
sheep farming and grazing systems no comprehensive
recommendations but only some hints for control can be
given here. For specific measures in goat herds reference
Q)
C must be made to the specialised literature.
·c3
'5
�
Q)
• Pasture and farm management can help reduce
C' the risk of infection in sheep, for example through
a:l
C extensive grazing (see cattle).
·;::
Q)
• A ho using treatment of all sheep (young and
C old animals) in late autumn or beginning of winter is
>- common practice, using a highly effective anthelmintic
0)
0 ( ► Table 19.6) to relieve the animals of the worm burden
0
·u5 and to keep egg shedding the following spring as low as
possible (preventing the 'spring-rise' in Haemonchus!).
a:l
a..
• Spring treatment of the older sheep is only
indicated if significant egg shedding is demonstrated
by quantitative coproscopy.
• Treatments during the grazing season. In
intensive sheep farming lambs or the whole herd are
routinely treated with an anthelmintic at least once, but
often several times during the grazing season. In view
of the drug resistance problem new options of targeted
selective treatments (TST) have been introduced and
are currently being evaluated in more detail in several
countries (see cattle, ► p. 580). In this system faecal
nematode egg shedding should be quantitatively
measured a few weeks after the start of the grazing
season (June/early July). Animals with egg counts
exceeding a threshold level (e.g. 200 epg) are treated with
an anthelmintic. Sometimes it might be sufficient to treat
only the young animals of the flock. After treatment, the
animals should not immediately be moved to a 'clean'
pasture ( ► 19.1.2.2), as this might increase the risk of
development of resistance, especially when the whole
flock has been treated.
• Measures against Nematodirus battus.
Massive infections causing diarrhoea and severe disease
in lambs may occur a few weeks after the start of the
grazing season in spring. In this case, all lambs should
promptly receive adequate anthelmintic treatment
(► Table 19.6).
19.1.3.4 Infestation with ticks
In sheep flumethrin acts against Dermacentor
marginatus (treatment in spring), but is not licensed
for this indication. In warm countries regular strategic
treatments against ticks in cattle and sheep are often
required (dips, sprays, pour-on applications).
19.1.3.5 Sheep mange
In some countries control of sheep mange is governed
by legal regulations. T he traditional method for
strategic control against psoroptic mange in sheep is
the application of acaricides (e.g. phoxim) in plunge
dips or by spraying. Dipping is particularly expensive
and also associated with problems concerning the
environmentally safe disposal of used dipping fluid.
Therefore, increasingly injectable ML with long
persistence in the animal body are used (e.g. doramectin
0.3 mg/kg b.w., i.m. or ivermectin 0.2 mg/kg b.w., s.c.),
which affect also mite stages that hatch from the eggs
after application of the acaricide (► Table 19.4). In cases
of clinically manifested mange or for herd sanitation two
treatments at intervals of 7 -10 days are recommended,
since one treatment is usually not sufficient to eliminate
all parasites. Another advantage of this treatment
is its simultaneous effect against sucking lice and
gastrointestinal nematodes. T hrough intensive therapy
 19. Parasitoses of different animal spe cies and organ systems, antiparasitic drugs and strategic control
with ML, the risk of developing anthelmintic resistance
in nematodes may increase, particularly if sheep are
moved to a 'clean' pasture after treatment ( ► 19.1.3.3).
It is advantageous to use ML before mixing animals
originating from various farms on common grazing
land, for example on alpine pastures, or after the
grazing period before the animals are integrated into
other flocks. In Switzerland the selective treatment of all
seropositive herds and the limitation of transhumance
to animals from mange-free herds have resulted in a
reduction in outbreaks of psoroptic mange over several
years in a highly endemic region. Specific measures
are important for preventing the introduction of mites
into mange-free stocks: monitor animal transport
and movement of persons in the stock; keep recently
introduced animals (e.g. breeding rams) in quarantine;
examine serologically and treat if necessary. Methods
of cleaning and disinfection are described on ► p. 571
19.2 Parasitoses of pigs
19.2.1 Parasitoses of organ systems
and antiparasitics
Parasitoses of pigs are summarised in ► Table 19.7.
The most important parasitic diseases include cystoiso­
sporosis and strongyloidosis of piglets, and infections of
the digestive tract with Ascaris suum or other nematodes,
as well as sarcoptic mange and lice infestation affecting
different age groups. Depending on the type of husbandry
(indoor, outdoor pen, or free-range) the various parasite
species in swine herds have different relevance, which
has to be taken into account in control programmes.
An indication for the use ofantiprotozoals is cystoiso­
sporosis of piglets which can be effectively treated
with toltrazuril. For the treatment of nematode
infections anthelmintics of various chemical
classes (imidazothiazoles, (pro-)benzimidazoles and
macrocyclic lactones) are available in application
forms suitable for pigs ( ► Table 19.8). Anthelmintic
resistance has been found in Oesophagostomum spp. to
benzimidazoles, levamisole and pyrantel ( ► p. 564).
Main indications for ectocides in pigs are sarcoptic
mange and lice infestation.
19.2.2 Strategic control of important
parasitoses of pigs
19.2.2.1 Cystoisosporosis (syn.
lsosporosis)
Cystoisospora suis the causative agent of cystoisosporosis
(► p. 98), is an important pathogen causing enteritis in
new-born piglets aged 5-15 days, which become infected
in the first days of life by ingestion of sporulated oocysts.
Over 80% of piglet litters may be infected regionally in
Central Europe.
Control measures include thorough cleaning and
disinfection of farrowing pens before restocking and
a single treatment of all piglets in the first week of
life (3 rd -6 th day) using toltrazuril (20 mg/kg b.w. p.o.) 0
{)
(► Table 19.8). {)
·a,·
Q)
19.2.2.2 Strongyloidosis
Thorough cleaning and disinfection of farrowing
pens before restocking and keeping stable floors
dry are components of control. In problem herds
treatment of piglets between the ycl and 15 th day of
life is indicated using an anthelmintic highly effective
against Strongyloides (► Table 19.8). The lactogenic
infection of piglets can be prevented or greatly reduced
by treatment of pregnant sows with ivermectin (Ix 0.3
mg/kg b.w. s.c.) 8-16 days prior to farrowing or 0.1 mg/kg
b.w. in feed from 92-99th day of pregnancy.
19.2.2.3 Ascariosis
In pigs Ascaris suum is a common parasite (► p. 327)
which can cause substantial economic losses if not held
at low infection levels. For control, hygiene measures are
combined with the strategic use of anthelmintics. Broad­
spectrum anthelmintics also cover other gastrointestinal
nematodes (Oesophagostomum, Trichuris) (► p. 276 and
► Table 19.8). Anthelmintics are usually administered
in divided doses in feed over several days because this
ensures a more complete drug uptake by the animals
than a single treatment.
• Piglet rearing farms. Pregnant sows are treated
about 2 weeks before farrowing. After treatment (at least 4
days prior to farrowing) sows are washed (claw columns,
mammary glands, etc.) and transferred into cleaned and
disinfected farrowing pens. Piglets are treated during the
last IO days before they are transferred to the fattening
unit. Boars receive anthelmintic treatments 2 to 4 times
per year.
• Fattening units. Before restocking, the stables
have to be cleaned and disinfected. Only those piglets
or weaners that have previously been treated against
Ascaris (see above) should be transferred to a fattening
unit. A further treatment is indicated about 6 weeks after
the first treatment. Purchased animals should originate
from herds where control measures against ascarids (and
other intestinal nematodes) are carried out regularly.
Otherwise, all introduced pigs are to be treated i n a
separate stable, and transferred a few days later into a
cleaned and disinfected fattening unit.
• Outdoor and free-range husbandry. I n this
type of farming the control of gastrointestinal nematodes
is difficult because infective eggs or larvae can persist
 Part VII. Parasitoses of different animal species and organ systems, antiparasitic drugs and strategic control

Table 19.7. Parasitoses (selection) of organ systems in pigs.1

. ·- -- - - -- - ,.-·
Parasitosis2 Parasites

��"-
em

Skin Sarcoptic-mange ( ► p. 442) Sarcoptes scabiei var. suis

Lice infestation( ► p. 453) Haematopinus suis
Simulium infestation( ► p. 465), rarely and only in free-range pigs Simulium spp.
Fly infestation( ► p. 472 ff) Musca domestica, Stomoxys ca/citrans, etc.
Wound myiasis( ► p. 483) Larvae of different fly species
Musculature Toxoplasmosis( ► p. 101) Toxop/asma gondii
Sarcocystiosis( ► p. 116) Sarcocystis spp.
Cysticercosis( ► p. 230), sporadic in parts of Europe Taenia solium, larval
Trichinellosis( ► p. 376) Trichinel/a spiralis, T. britovi, larval
Respiratory Metastrongylosis( ► p. 312) Metastrongylus spp.
organs Echinococcus granulosus s.l., larval
Echinococcosis( ► p. 240)
Cysticercosis ( ► p. 232) Taenia hydatigena, larval
Stomach Hyostrongylosis( ► p. 300) Hyostrongy/us rubidus
Small Cryptosporidiosis ( ► p. 122) Cryptosporidium spp.
intestine Eimeriosis( ► p. 98) Eimeria spp.
Giardiosis( ► p. 47) Giard/a duodena/is
Cystoisosporisis (syn. lsosporosls)( ► p. 98) Cystoisospora suis
Ascariosis( ► p. 327) Ascaris suum
Strongyloidosis( ► p. 259) Strongyloides suis
Large Balantidiosis( ► p. 147) Balantidium coli
intestine Oesophagostornosls( ► p. 276) Oesophagostomum spp.
Trichuriosis( ► p. 368) Trichuris suis
Liver Dicrocoeliosis( ► p. 191) Dicrocoelium dendriticum
Fasciolosis ( ► p. 175) Fascia/a hepatica
,� Echinococcosis, cystic( ► p. 240) Echinococcus granulosus s.l., larval
Echinococcosis, alveolar( ► p. 247) Echinococcus multilocularis, larval
Cysticercosls( ► p. 232) Taenia hydatigena, larval
Milk spots(► p. 327, p, 333) Ascaris suum, Toxocara spp., larval
Kidney Stephanurosls(► p, 280) mainly in tropics and subtropics Stephanurus dentatus
CNS Toxoplasmosls( ► p. 101) Toxoplasma gondii
1 The list is not exhaustive; the Information relates mainly to parasites occurring in Europe.
2 In bold: parasitoses of particular Interest.

a long time in soil thus representing a reservoir of 19.2.2.5 Oesophagostomosis and

infection. To relieve the animals of the worm burden
anthelmintic treatments may be performed in spring
and autumn. Changes of outdoor runs and pastures are
recommended, but this is not expected to influence the
parasite populations for a sustained period.
19.2.2.4 Trichuriosis
Trichuris suis occurs in indoor systems more rarely
than Ascaris suum. When keeping pigs exclusively
indoors, anthelmintic treatments against T. suis may
not be required, while they may be necessary in free­
range systems. The rotation of grazing areas or runs at
intervals of 1-3 years is not an appropriate measure for
preventing severe infections because of the longevity of
T. suis eggs (and A. suum).
hyostrongylosis
Infections with Oesophagostomum species (nodular
worms) occur mostly in sows maintained in indoor or
pasture systems. Hyostrongylus rubidus (red stomach
worm) is primarily a parasite of older pigs (sows).
Infections with both parasites occur by ingestion of
infective larvae (L3 ). Contamination of pasture plants
with L3 is highest in the warm season(July to September)
when the plant cover is intact and not damaged by
burrowing. Oesophagostomum infections(► Table 19.8)
are also covered by measures against Ascaris as long
as correspondingly effective anthelmintics are used. It
should be noted that Oesophagostomum populations may
be resistant to benzimidazoles and levamisole(estimated
to occur in approximately 2% of breeding stocks, based
 Table 19.8. Antiparasitics (selection) for use in pigs (selection of commercial products ► Chapter 20, p. 615).

Active substance /oose:

I
Application Spectrum of efficacy of drugs3 Sl4 or Withdrawal periods5 (days) l
(generic name) and mg/kg b.w. or ppm in GT
chemical group 1 feed2 Stomach Small intestine
I
Large intestine Lung Skin Examples
d: days of application (0

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Febantel (PBZ) 5.0mg p.o. • - - () • • () () - - xi 5DE

15-30ppm x 5-6 d p.o. • () • • • • - -

Fenbendazole (BZ) 5.0mg p.o. • - - () • • () • - - xiOO 3CH 5DE

• • • • • �-
0

0.3-1.0mg x 5-15d p.o. - - () - -

Flubendazole (BZ) 5.0mg p.o. • - - () • • • • - - >40 5CH 0 14DE
fl!

30ppmx10d p.o. • - - • • • • • I - - >40 5CH, 14DE

§l
a.

Levamisole(IT ) 7.5mg • - - • • • • - - 14DE

0

I
p.o. () -2

Doramectin(ML) 0.3mg i.m. • - - • • • () • i • • >25 49CH 77DE

• • • • • • •
0

lvermectin (ML) 0. 3mg s.c . - - () >50 14DE, 25CH

0.1 mgx7d p.o. • - - • • • () • • • + 12DE

Phoxim(OP) 0.05% spray - - - - - - - - • • + gCH, 19DE

Toltrazuril(VO) 20. 0mg po

. . - • • - - - - - - - + ]QCH, 77DE

1 Chemical group: BZ: benzimidazoles; IT: imidazothiazoles; ML: macrocyclic lactones; OP: organophosphates; PBZ: pro-benzimidazoles; PY: pyrethroids; VO: vanous other chemical groups; registration of drugs( ► p . 556).
2 Selection of recommended doses (for additional infonnation, see labels).
3 Efficacy: • = good to very high; «l= partially effective or effective in increased dose or with repeated application; - = insufficient effect; empty fields= not documented or drug not recommended in this indication . 5·
a.
4 SI: safety index; GT: general tolerability: + = good .
5 Withdrawal periods may vary depending on country and commercial product; therefore note the latest infonnation (labels, databases). (/l
m
�
a.

5·
g
a
Q_

Parasitology in Veterinary Medicine Strategic control

 Part VII. Parasitoses of different animal species and organ systems, antiparasitic drugs and strategic control
on examination of 144 farms in DE). Earlier data on
pyrantel resistance described more than 25 years ago
in Denmark were thus far not corroborated in other
countries.
19.2.2.6 Sarcoptic mange
In some countries and regions Sarcoptes scabiei var. suis
( ► p. 442) is still a frequent parasite and a heavy burden
for the animals. The mites are transmitted from animal
to animal or infest new hosts from a contaminated
environment (stables, vehicles, etc.). Occasional and
unplanned treatments of pigs are not sustainable.
Therefore, the establishment of mange-free farms should
be pursued since this approach is not only cost-effective
in the long term but also animal- and user-friendly.
Eradication of sarcoptic mange in swine herds may
already be achieved by treating all animals twice with
a macrocyclic lactone (e.g. ivermectin, 0.3 mg/kg b.w.
s.c., doramectin 0.3 mg/kg b.w., i.m.) at an interval
of about 2 weeks, but this is not always the case. The
following eradication program recommended by the
Swiss Pig Health Service has proven successful: (a)
treatment of all animals of the herd with ivermectin
or doramectin;(b) after 3-4 days cleaning of all stables
and equipment with a steam cleaner and spraying with
an acaricide (e.g. organophosphate); washing of the
pigs with water, spraying them with an acaricide (e.g.
organophosphate) and transferring them into clean and
disinfected stables;(c) second treatment of all animals of
the herd with ivermectin or doramectin 14 days after the
first treatment. Mange-free animals must not be mixed
with treated animals for at least 7 days after the end of
treatment;(d) piglets born after the first herd treatment
are treated 3-4 days post-partum with doramectin or
ivermectin. Similar sanitation programs were also
successful in some other countries(DK, NL, DE). The
above-mentioned programmes comprise measures
for monitoring and prevention of reintroduction
of Sarcoptes mites (including serological surveillance,
acquisition of pigs only from mange-free holdings,
otherwise quarantine and treatment of purchased
animals twice with ivermectin or doramectin, animal
transports only in decontaminated vehicles).
Q)
19.2.2. 7 Lice infestation
·u
C
'5
Q)
� Haematopinus suis, the pork louse (► p. 453), is
transmitted through contact from animal to animal.
co
C Recent data on the prevalence in pigs are scarce. In
·;::
Germany, 15-40% of farms are suspected of being
infested. Pigs in SPF (specific-pathogen-free) systems
C must be Haematopinus-free.
>-
0)
0 For lice control in pigs several insecticidal drugs are
0
'in approved, such as the organophosphate phoxim(spray
co or pour-on) or the macrocyclic lactones ivermectin
co
a.. and doramectin in various application forms( ► Table
19.8). A single application is usually sufficient as the
residual activity of these drugs is long enough to affect
juvenile stages hatched from eggs after drug application.
In a farm all infested and contact animals should be
treated. The preventive measures against importation
of lice from another farm are similar to those applied
in mange control.
19.3 Parasitoses of horses
19.3.1 Parasitoses of organ systems
and antiparasitics
In Europe, protozoa play a minor role among the
parasites of the horse( ► Table 19.9). Accordingly, the
use of antiprotozoals is rarely necessary and primarily
required to treat Babesia or Theileria infections( ► p.
129 and p. 140). Anthelmintics ( ► Table 19.10) are
used in most of the individual animals and in horse
populations, especially for the control of strongyles and
Parascaris spp., often too frequently ('overtreatment').
One consequence is the worldwide distributed and
increasing anthelmintic resistance (AR) of small
strongyles (cyathostomins) mainly to benzimidazole
compounds, much less often to other drug classes( ► p.
564). In contrast, AR currently does not play a role
in large strongyles. Locally and apparently especially
in studs there are Parascaris populations resistant
to macrocyclic lactones. Since only a few ectocides
are registered for use in horses, off-label use is often
necessary to treat ectoparasitoses. Drugs effective against
Gasterophilus larvae are shown in ► Table 19.10.
19.3.2 Strategic control of important
parasitoses of the horse
Parasite control in horses requires as a base regular
diagnostic examinations or a routine parasite monitoring
(especially in studs and other groups of horses) to
determine the relevant parasite species and to adapt
control plans to the specific situation in the stocks.
Actions against various groups of parasites should be
coordinated in integrated control programmes.
19.3.2.1 Anoplocephalidosis
In Europe, the most common tapeworm species of the
horse is Anoplocephala perfoliata( ► p. 218). Infection
occurs on the pasture by ingestion of moss mites
containing infectious larvae (cysticercoides) of the
parasite. In Central Europe, one treatment each in June/
July and autumn with praziquantel is recommended(LO
mg/kg b.w. p.o.). There are currently no data concerning
the sustainability of this approach. For simultaneous
treatment of Anoplocephala and nematodes combination
products are available( ► Table 19.10).
 19. Parasitoses of different animal species and organ systems, antiparasitic drugs and strategic control

19.9. Parasitoses (selection) of organ systems of the horse.1

Paraeltolle2 --- "

-�
nck infestation ( ► p. 396) lxodes ricinus. Dermacentor marginatus.
D. reticulatus. Rhipicephalus turanicus,
' Haemaphysalis spp. and others
Chorioptlc mange ( ► p. 439) Chorioptes bovis
Chewing or biting lice infestation ( ► p. 450) Wernec/Qella equi equi, Haematopinus spp.
.,
1
Fly infestation( ► p. 472 ff) tabanids. Musca spp.. Slomoxys spp. and
others.
Culicoides infestation ( ► p. 469) Cul/co/des spp.
Simulium Infestation( ► p. 465) Slmulium spp.

t Gasterophllosls( ► p. 491)
Wound myiasis( ► p. 483)
Gasterophilus spp.. larval
larvae ol different fly species
Hfppobosca infestation( ► p. 498) Hippobosca equina

r 11'/ Habronematidosis( ► p. 350)

Onchocercosis( ► p. 364)
Habronema spp.. Draschfa megastoma
Onchocerca spp.
Parafilariosis( ► p. 355) Parafilaria multipapillosa
Musculature Toxoplasmosis( ► p. 101) Toxoplasma gondii
Trichinellosis( ► p. 376) Trichinella spiralis, T. britovi, larval
Respiratory Dictyocaulosis ( ► p. 303) Dictyocaulus arnfieldi
organs Echinococcosis( ► p. 240) Echinococcus granulosus s.l.. larval
Blood, blood Babesiosis( ► p. 129) Babesia caballi
vessels Theileriosis( ► p. 140) Theileria equi
Strongylosis( ► p. 264) Strongylus vulgaris, larval
Stomach Gasterophilosis( ► p. 491) Gasterophilus sp., larval
Habronematidosis( ► p. 350) Habronema spp., Oraschia megastoma
Trichostrongylosis( ► p. 300) Trlchostrongylus axei
Small Cryptosporidiosis( ► p. 122) Cryptosporidium spp.
intestine Eimeriosis( ► p. 95) Eimeria leuckarti
Giardiosis( ► p. 47) Giardfa duodena/is
Anoplocephalldosls( ► p. 218) Anoplocephala perfoliata and others
Parascariosis ( ► p. 330) Parascaris equorum, P. univalens
Strongyloidosis ( ► p. 259) Strongyloides westeri
Large Oxyuriosis( ► p. 343) Oxyuris equi
intestine Strongylidosis( ► p. 264) Cyathostominae, Strongylus spp. and others
Liver Dicrocoeliosis ( ► p. 191) Dicrocoelium dendriticum
Fasciolosis( ► p. 175) Fascia/a hepatica
Echinococcosis, cystic( ► p. 240) Echinococcus granulosus s.l.. larval
Kidney Halicephalobus infection( ► p. 263) Halicephalobus gingivalis
Genital tract Dourine, southern and eastern Europe( ► p. 67) Trypanosoma brucei equiperdum
Eye Thelaziosis( ► p. 346) T helazia lacrymalis
CNS Neosporosis ( ► p. 114) Neospora hughesi (North America)
Sarcocystiosis ( ► p. 116) Sarcocystis neurona (North America)
Nematode infection larvae: Strongylus vulgaris, Setaria equina;
Halicephalobus gingivalis
1
This list is not exhaustive. The data refer mainly to parasites occurring in Europe.
2 In bold: parasitoses of particular interest.
 Parasitology in Veterinary Medicine

Table 19.10. Antlparasitics against helmlnths and Gasterophilus larvae (selection) for use in horses (selection of commercial products► Chapter 20, p. 615).

S14 or Withdrawal period-5 (days)

andahanllll ���ij:.,js�.-.-�poi!ill!l!'..,_______,,,_.��----IGT

hDl"Ne--­
Dnlp Liver, lung Examples
llPPft'Rd
anclaloaaillll

III
Ii'
I
i'
tI
i
:,
t
i
ii l
�
o'
Ii"
�

• • • •
,I

Febantel P
( BZ) 6.0 p.o. 40 20DE nLDE
Fenbendazole BZ
( ) 7.5 p.o. I) • • • • 75 20DE nLDE
Mebendazole BZ
( ) 10.0 lp.o. • • • • 40 23DE nLDE
Oxlbendazole BZ
( ) 10.0 !p.o. • I) • • • • + 3CH n s.
( L)
lvermectin M 0.2 [p.o. • • • • • • • • • 10 3 5DE nL DE
lvermectin M ( SO) 02 + 1.5
( L) +Praziquantel I
I
p.o. • • • • • • • • • • 1 01>5 3 0DE nLDE
Moxidectin (ML) '0.4 p.o. • • • • • • • • • + 32DE nLDE
( L) +Praziquantel (ISO) 0.4 + 2.5
Moxidectin M lp.o. • • • • • • • • • • + 54DE nLDE
Praziquantel (ISO) ,.o p.o. • >5 o DE nLDE
Pyrantel-base P
( Y) 6.6 p.o. • I) • • () 20 oDE nLDE
Triclabendazole BZ
( ) 12.0 p.o. • + n.s. n.s.
Closantel SA( ) 10.0 p.o. • + n.s. n.s.
1 Chemical group: BZ = benzimidazoles: ML= macrocyclic lactones; ISO= isoquinolines; PBZ = pro-benzimidazoles; PY= pyrimidines; SA= salicylanilides; registration of drugs(► p. 556).
2 Selection of recommended doses; additional information see labels or databases(► p. 576).
3 Efficacy: • = good to high; ll= partially effective or only in an increased dose; -= insufficient effect.
4 SI: safety index; GT: general tolerability; + = good; n.s. = not specified.
5 Withdrawal periods: tissue = meat and other edible tissue; nL = do not use in lactating mares producing milk for human consumption; withdrawal periods may vary depending on country and commercial product, therefore
note the latest information Qabels, databases).
 19. Parasitoses of different animal species and organ systems, antiparasitic drugs and strategic control
19.3.2.2 Strongyloidosis
Strongyloides westeri may cause diarrhoeal diseases in
foals that acquire the infection initially by lactogenic
transmission of infective larvae in the mare's milk ( ► p.
259). Therefore, foals in problem stocks are treated at the
age of 3-6 weeks with one repetition, if needed. ( ► Table
19.10). It should be noted that repeated anthelmintic
treatments may impair the development of immunity
against this parasite. However, control measures are
rarely necessary because infections are usually weak
and do not cause clinical symptoms.
19.3.2.3 Strongylidosis
The control of horse strongyles is based on strategic
anthelmintic treatments in combination with other
measures, such as pasture management, pasture hygiene,
and monitoring systems. Due to the great variety of horse
keeping and different epidemiological conditions, it is
necessary to adjust any control option to the specific
situation of the individual stocks.
Pasture management. Overstocking of pastures
must be avoided. Wherever possible, horses should be
grazed successively on several plots that are temporarily
also grazed by ruminants or are used for hay production.
The alternating or joint use of pastures by ruminants and
horses can reduce the risk of infection for both groups
as their respective nematode species are quite host­
specific. An exception is Trichostrongylus axei which
may pass from ruminants to horses, but such infections
are usually negligible. The potential risk of infection of
horses with Fascia/a on sheep and cattle pastures should
be considered.
Pasture hygiene. The cleaning up of all faeces from
pastures at least once or better twice a week reduces the
densities of infective larvae on pasture plants. For larger
areas, various types of appropriate vacuum cleaners are
available.
Treatment of horses with anthelmintics.
Scheduled anthelmintic treatments of horses eliminate
existing intestinal worm burdens and reduce shedding
of strongyle eggs. This results in lower pasture
contamination with infective larvae and thus in
decreased infection risks for the horses. For several
decades targ eted (strate g ic) treatments have been
internationally recommended and practiced for
horse strongyle control. In view of the wide-spread
drug resistance of small strongyles, targeted selective
treatments were proposed as an alternative control
approach.
• Targeted treatments (TT). Strategic treatments
at certain epidemiologically justified time points are
performed with the objective to restrict the number
of treatments to the bare essentials, but to disrupt the
development cycle of the parasites as sustainably as
possible. Since it is anticipated that mostly all animals of a
pasture group harbour strongyles, all animals are treated.
This control method was directed particularly against
the highly pathogenic Strongylus species, which have
been effectively controlled by this approach and are now
rare or absent in most herds in which regular treatments 0
0
are carried out. There may be, however, differences in the 0
prevalence of S. vulgaris depending on the geographic a,
Q)
region and the control systems. This treatment approach
results in the reduction of intestinal worm burdens (J)
of the animals and, in case macrocyclic lactones are
used, has also an effect on somatic larval stages. The
increasing dominance of small strongyles, whose
prevalences were not effectively reduced (presumably
due to their relatively short prepatency periods), led in
recent years to a focus on control measures against this
group of strongyles and to a modification of the control
recommendations.
These recommendations take into account that in the
majority of farms in many countries cyathostomins
occur which are resistant to benzimidazoles (BZ), and
less frequently to pyrantel but are essentially susceptible
to macrocylic lactones ( ► p. 564). Despite this resistance,
according to experts, the number of clinical cases caused
by cyathostomins did not increase in the last decades,
which may be attributed to the low pathogenicity of the
cyathostomins. In order to limit the risk of development
of anthelmintic resistance, the concept of targeted
selective treatments has been proposed.
• Targeted selective treatments (TST}. This
approach is recommended only for adult horses (e.g.
at least four years old), since younger animals are
considered as not having sufficient immune protection
thus requiring regular removal of the acquired worm
burden by anthelmintic treatment. The concept for
these treatments is based on the fact that in a group
of horses pasture contamination with strongyle eggs
is predominantly due to only a few animals with high
egg excretion (e.g. >200 epg). Identifying these high
egg shedders by performing egg counts and subsequent
treatment of these animals will substantially reduce
pasture contaminations and the risks of infection for all
animals. As a result, only a portion of the cyathostomin
Q)
population existing in a pasture group gets into contact C
with the anthelmintic. The other part of the population ·5
'6
Q)
in non-treated animals as well as the developmental 2
stages in the environment are in a 'refugium: i.e. they �
are not exposed to the anthelmintic and thus not subject co
C
·c
to selection pressure. A preventive effect against the Q)
development of anthelmintic resistance is expected
by this approach, however, long-term experiences are C
currently lacking. >,
O')
0
0
In this context it is important to note that there is no ·u5
direct relationship between egg count and worm burden
co
of an animal. This means, for example, that horses with CL
 Part VII. Parasitoses of different animal species and organ systems, antiparasitlc drugs and slraleglc control
an egg count of < 100 epg might harbour more than
100,000 cyathostomins. Accordingly, when only horses
with values>200 epg are treated (a cut-off often used in
selective treatment programmes) some of the animals
with high worm burdens are left untreated.
TT versus TST and current recommendations.
Although the principles of TST were first published
more than a decade ago, experiences with this system
are still limited. In some countries, e.g. DE and CH,
the TST system is currently applied on a broader basis.
A recent study in DE comprising 1,887 horses in 192
farms revealed that over a period of one year there was
no significant statistical difference in the distribution
of faecal egg counts between two groups treated either
according to the TT or the TST system. Furthermore,
using coprological examinations, a re-emergence of S.
vulgaris in the TST group was not detected. In contrast,
S. vulgaris has been found to occur more often on farms
in DK where TST was applied compared to those using
the TT approach. Though these studies are not directly
comparable, monitoring systems should always include
large strongyles. One potential risk of the TST strategy is
that heavy, non-patent infections with small strongyles
may remain undetected and untreated, eventually
resulting in disease. However, respective data are lacking.
Generally, neither the potential long-term effects of TST
on the incidence of cyathostominosis nor the influence
on development of drug resistance are currently known.
Selective treatments reduce the use and the costs of
anthelmintics but require a high expenditure for
diagnostic examinations, at least initially.
� mentioned above, the TST system is recommended
only for older horses. The American Association of
Veterinary Practitioners (AAVP) recommends basic
treatments of all horses consisting of one or two yearly
treatments against (large) strongyles, tapeworms,
spirurid nematodes and Gasterophilus bots. All
further treatments should be targeted to horses with
a high strongyle contamination potential. Similar
recommendations published in 2011 by an expert group
in DE are briefly summarised below.
Monitoring. Monitoring of the parasitological situation
(I)
C in any control programme is important, including the
·c3
'6 following measures:
(I) • Initial identification of the parasite spectrum in the
�
cco horse stock (large and small strongyles, Strongyloides,
C Parascaris, Trichostrongy/us, cestodes, Gasterophi/us,
·.:::::
(I) etc.), regular examination of faecal samples of each
of the different age groups present on a farm, and
C specific testing for S. vulgaris either by larval culture
>­ or DNA analysis.
CJ)
0 • Testing whether anthelmintic-resistant cyathosto­
0
·en mins are present in the respective stock using the
co faecal egg count reduction test (FECRT). The
co
a.. pre-treatment epg values of groups of animals (if
possible at least 6 animals each) are compared with
the values 10-14 days after treatment. For BZ and
pyrantel a mean epg reduction of ::::90% and for
macrocyclic lactones of::::95% are currently regarded
as indicators of non-resistant populations. However,
these threshold values are currently discussed. This
test requires a critical evaluation (and the indication
of statistical confidence intervals) since egg counts
are subject to large fluctuations. The FECRT should
be repeated at annual intervals (according to AAVP
at least every three years).
Selection of anthelmintics and plans for control.
Anthelmintic treatments are usually performed based
on the results of monitoring.
• For selecting the anthelmintics and setting the
treatment intervals the duration of anthelmintic
activity of the drugs is to be taken into account.
Indicators for this are the Egg R eappearance
Periods (ERP: time between successful treatment
and subsequent rise of the epg values, e.g. to an
average of> 200 epg in more than half of the horses
of the herd).
• Control plans should aim at reducing the number
of annual treatments to the minimum necessary.
Macrocyclic lactones with long-term efficacy are
preferably to be used at the beginning and end of
the grazing season, while pyrantel and BZ without
any residual efficacy should be chosen during the
grazing period. Animals newly introduced in the
stock are subject to a quarantine treatment and a
monitoring of its success.
Currently, there are no standard recommendations for
the drug-based control of horse strongyles. On page 595
( ► Table 19.11), an integrated model is presented as an
example, which takes into account not only nematodes
but also other parasites.
The control concepts described above as TT and TST
are illustrated by the following examples:
Option 1: Targeted treatments (TT). Exemplary
initial situation: Large stock of horses with different
age and use groups (i.e. including broodmares), regular
grazing with the usual seasonal risks of infection by
strongyles (initially by overwintering larvae and later
increasing risk by larvae from eggs excreted by grazing
horses).
• Objectives. Reducing the excretion of strongyle
eggs and thus the pasture contamination with minimum
use of anthelmintics, protection of all animals of
the stock against disease and negative impact on
performance caused by strongyles as well as control
of other relevant parasites on the farm (especially
Parascaris, Anoplocephala, Gasterophilus). The latter
can be achieved by the use of antiparasitics with activity
against the respective spectrum of parasites.
 19. Parasitoses of different animal species and organ systems, antiparasitic drugs and strategic control

Table 19.11. Scheme of a trea tment plan1 •2 f or different age groups of horses of grazing herds.

'·:ii'
\ • •l • • - •

I :J, . , ·I· 1 • 1 � 'I , • ',1.........<--=-._

h
, -!t��
,I 'j .• l 1_i,.. ��,·):,• •·:�•1r
1 � 1 �1.'\'\,,, -t•� ,,
.. .:,:'i...jl
_,,\ • (, ,,j,. --U t-- ., .
►
- I. , I I
,I ' I., ·-'. . :-I(
j

-, \ �.... , � -:_ -�,. i� •

. -.. ,:f' ,._ - _ ;'I> .. Jr,o- �.... -
l\1,t11ir• fl''IIIJII

e
� -

!=oals X(4 W) X(2M) X(5M) X(BM) X (11 M)

(age, W: weeks,
M: months)
Str3 S,P S, P,
A3
s, P,
A3 ,G
s c0
u
Yearlings and X Mo (X) X Mo(X) u
horses up to 5 s S, P, s, P. ,, s '5>
years A3 A ,G3
�
Horses >5 years X Mo(X) X Mo (X) cl)
s S,A3 S,A3 ,G s
1 Treatment plans need to be adapted specifically to the farm and region. X: time of treatment: (X): treatment only after positive monitoring
results: Mo: monitoring {see text).
2 Targeted parasites: A= Anoplocephala, G = Gasteroph/lus, P = Parascaris, S = small strongyles, Sir= Strongyloides.
3 Treatment only if the parasite is detected on farm,

• Measures. Treatment of all animals of the stock, Option 2: Targeted selective treatments (TSTI.
but according to age at different frequencies ( ► Table Exemplary initial situation as in option 1, but only
19.11). Foals: first treatment at 2-Yd months of age, adult horses are the target group.
then at intervals of about 3 months until housing, and
during the winter. Yearlings and young horses (up to • Objectives. By treating only horses with high egg
and including 4 years): (a) 1-2 months after turn out shedding (e.g. >200 epg) (a) the contact of the parasite
to pasture; (b) about 3 months later; (c) at housing; and population with anthelmintics is reduced and thus the
(d) during winter. The treatments (b) and (d) only if selection pressure for anthelmintic resistance decreased,
positive 'monitoring findings' (= detection of strongyle (b) pasture contamination with strongyle eggs and (c)
eggs in faecal samples from individual animals or pooled use of anthelmintics are reduced.
faecal samples from a maximum of 5 animals per group).
5-year-old and older horses: as yearlings and young • Measures. According to current recommendations
horses, but monitoring performed separately. only adult horses (>4 years) are included into this
programme. Regular egg counts are performed for the
When using macrocyclic lactones for treatments at whole group, but only those horses are treated having
the beginning of the grazing period and at housing, egg counts exceeding a predetermined threshold (e.g.
intermediate/winter treatments can possibly be >200 epg). According to a Swiss recommendation egg
dispensed due to the long-lasting suppression of egg counts should be performed in the first year every two
shedding by the drugs. The need for intermediate/ months (beginning in April/May), and later at least two
winter treatments is clarified by a coproscopic parasite times per grazing season. Furthermore, the efficacy of
monitoring. If positive, use BZ or pyrantel (if there is the treatments should be evaluated (by the FECRT)
no resistance) for the intermediate/winter treatment for each drug class every 1-2 years. The TST system
to reduce the selection pressure on MLs. Treat newly specifically targets the control of cyathostomins and
introduced animals in a separate horse stable and must be complemented by measures against other
integrate them at earliest after 3 days in the group. parasites (e.g. Parascaris, Anoplocephala, Gasterophilus,
Examine treatment success by faecal examination. and possibly Strongylus). Other aspects of the TST
system are discussed elsewhere (see above).
Detailed recommendations for a control concept
considering the various horse age and use groups Further measures against drug resistance of
with integrated parasite monitoring are provided small strongyles. Reduced usage and regular change
in the specialised literature (see references). Such of the anthelmintic chemical group are believed to limit
recommendations represent only a basic guideline and or delay the development of anthelmintic resistance.
should be applied (and modified if necessary) taking In case of confirmed BZ resistance only anthelmintics
into account the specific situation of the individual effective against BZ-resistant populations should be used.
farm (e.g. stocking rate, grazing behaviour, hygiene Suitable drugs are (depending on the type and degree
measures) as well as current environmental conditions of resistance): pyrantel, ivermectin and moxidectin.
(e.g. weather conditions).
 Part VII. Parasitoses of different animal species and organ systems, antiparasitic drugs and strategic control
19.3.2.4 Dictyocaulosis
Lungworm infections( ► p. 303), caused by Dictyocaulus
arnfieldi, occur usually only in horses which graze
together with donkeys. The parasite is well adapted to
donkeys which are more susceptible and can remain
shedders of eggs/larvae for long periods. In contrast,
patent infections usually only develop in young, 6-9
month-old horses. Infection occurs by ingestion of
infectious larvae (13) with fodder plants.
Control. Horses and donkeys should be kept on
separate pastures, and donkeys treated at the end of
the grazing season against Dictyocaulus infections
(ivermectin 0.2 mg/kg b.w. p.o. or moxidectin 0.4 mg/
kg b.w. p.o.). Repeat treatment before the grazing season
in spring when eggs or larvae are detected in the faeces.
19.3.2.5 Parascariosis
Parascaris equorum or P. univalens(horse roundworms)
are common parasite in foals( ► p. 330). The infection
occurs by oral uptake of eggs containing third stage
larvae.
Control. Regular cleaning and disinfection of stables
and removal of faeces from paddocks and pastures( ► p.
593). In problem herds metaphylactic treatment of foals
for the first time at the age of 6-8 weeks to eliminate
immature stages from the intestine. Subsequently, further
treatments depending on results of faecal examination at
intervals of about 12 weeks until the age of 6-12 months.
Older horses are treated at coproscopically confirmed
infection. When performing metaphylactic treatments
against strongyles no special measures against Parascaris
are usually required. In several countries (DE, NL, SE,
USA, etc.) Parascaris strains with AR to ML occur. If
such resistance is detected in problem herds, pyrantel
pamoate, piperazine citrate or BZ can be used.
19.3.2.6 Oxyuriosis
Infections with Oxyuris equi are frequent in horses( ► p.
343). Oviposition occurs in the perianal area, infections
happen by oral uptake of eggs, which contain infective
larvae.
Control. Hygiene: good stable hygiene, frequent
deaning, regular disinfection, avoid feeding offthe floor,
dean the anal area of the horses with water containing a
detergent at weekly intervals. Drug treatment of horses;
if necessary, repeat several times ( ► Table 19.10).
19.3.2.7 Infestation with ticks
In Central Europe, horses may get infested with different
species of ticks, most often with Ixodes ricinus ( ► p.
396) (various parts of the body), and regionally with
Dermacentor marginatus(attached preferably to the tip
of the tail), Dermacentor reticulatus, Haemaphysalis spp.
and other species( ► p. 396).
Control. The options for control are inadequate.
Treat(spray) tick infested horses with phoxim solution
(0.05%). According to a study in DE, horses grazing on
forest pastures that received such treatments at intervals
of 7 days were protected against tick infestation.
19.3.2.8 Control of flies and other Diptera
Horses are often greatly disturbed by flies (tabanids,
Musca spp., Haematobia spp., Stomoxys calcitrans, and
others ( ► p. 472), as well as biting midges ( ► p. 469)
and blackflies( ► p. 465). Insect bites in the auricles and
other areas of the head are most irritating. The options
for protecting the horses are limited.
Mechanical protection. Several devices for protecting
horses from insects are commercially available, including
covers('fly masks') or ear nets for the head, 'fly boots' for
the legs or blankets for larger body regions. Protection of
horses against biting midges(Culicoides spp.) is difficult.
However, contacts with these insects can be reduced by
stabling horses at night and the use of net protection in
housing systems.
Insecticides and repellents. For insect control in
horses there are many commercial products available
containing insecticides (pyrethrins, pyrethroids,
coumaphos, etc.) and/or repellents in various application
forms(sprays, spot-ons, roll-ons, etc.). Only a few can
be mentioned here: Wellcare• Emulsion (permethrin),
RepeJ-x• Lotion (cypermethrin, pyrethrins), Co­
Ral" (coumaphos), Centaur J• (icaridine). They may
be applied with a sponge to predilection sites (head,
neck, shoulder, brisket). The duration of action against
tabanids is up to 6 days, against flies up to 14 days,
though this is variable. Heavy rain(not sweating) washes
the emulsion off, thereby eliminating the effect. The
application (gel, spray) of the repellent icaridine (e.g.
EquiRepeU-) protects against flies and also ticks for a
few hours.
Insecticide-impregnated nets ('Power Fences'), that
are attached to paddock fences, can significantly
reduce fly and tabanid numbers in grazing horses as
shown in a pilot study in Brandenburg/DE (see also
Glossinidae, ► p. 481). However, such nets are currently
not commercially available.
 19. Parasitoses of different animal species and organ systems, antiparasitic drugs and strategic control

19.3.2.9 Gasterophilosis and 19.3.3 Export and import of horses

hypodermosis
The health status, including parasitic and 'exotic' (/)

The larvae of Gasterophilus species ( ► p. 491) are easily infections (dourine, surra, piroplasmosis, etc.), is an Q)
C
accessible for control measures during their stay in the important issue in the import and export of horses, and ·u
()
digestive tract of horses. Occasionally horses get infested is governed by EU regulations (e.g. Council Directive co
>
with warble flies (mainly Hypoderma diana) ( ► p. 2009/ l 56/EC) and the national veterinary authorities. -0
C
494) which may sometimes cause numerous warbles These should be consulted for details. co
(/)
in the skin. ()
:;::;
·v;
Control. To control Gasterophilus the horses are treated 19.4 Parasitoses of dogs and cats co
0..
in late autumn (November/early December) systemically :;::;
C
with a macrocyclic Iactone (moxidectin 0.4 mg/kg b.w. 19.4.1 Parasitoses of organ <!
p.o. or ivermectin 0.2 mg/kg b.w. p.o.). This treatment systems, antiparasitics and
is also effective against other gastro-intestinal parasites vaccines
like strongyles. Possible residual infestations or late
infestations with Gasterophilus spp. will be covered by For the control of major helminths and arthropods in
the usual spring treatment against strongyles, provided dogs and cats ( ► Table I 9.12), numerous anthelmintics,
ML are used ( ► Table 19.10). Warble fly infestations ectocides and insect growth regulators (IGR) are
are treated by manual removal of the larvae following available as mono- or combination products ( ► Tables
incision of the skin or by local treatment of the warbles 19.13 to 19.16). In contrast, some protozoa} infections
with organophosphates. Migrating warble fly larvae will can only be treated with drugs that are approved for
be killed by systemic treatment with ML in autumn other target species, including humans or must b e
(see above). obtained from other countries ( ► Table 19.13).
Combination products that contain 2-4 different agents

Table 19.12. Parasitoses (selection) of organ systems in dogs and cats 1.

Infestation with ticks ( ► p. 396) lxodes rlcinus, I. hexagonus, I. canisuga, Dermacentor reticulatus,
Rhlplcephalus sangulneus, etc.
Cheyletiellosls ( ► p. 430) Cheyletlella spp. Cheyletiella spp.
Demodlcosls (► p. 426) Oemodex spp. Demodex spp.
Trombiculosis ( ► . 431) Trombicula spp. Trombicula spp.
Ear mange ( ► p. 440) Otodectes cynotls 0. cynotls
Sarcoptic mange ( ► p. 442) Sarcoptes scablei var. canis
Notoedres mange(► p. 447) Notoedres cati
Chewing or b iting lice infestation Trlchodectes canis, Linognathus Felico/a subrostratus
(► p. 450) setosus
Wound myiasis ( ► p. 483) Larvae of various fly species like iri dogs
Flea infestation(► p. 500) Ctenocephalides fells, C. car-1is, C. felis, C. canis, rarely other flea
Q)
otmerr flea species species C
Subcutls, Dirofilariosis ( ► p. 357) Dirofilaria repens D. re�ens
·c:s
musculature Neosporosis ( ► p. 110) Neospora caninl!lm
Q)

Hepatozoonosis ( ► p. 81) Hepatozoon car:iis

co
Trichlnellosis ( ► p. 376) Tricf:Jinella spiralis, T. b,itovi, larval T. spiralis, T. britovi, larval C
·;:::
Respiratory Crenosomosis ( ► p. 318) Crenosoma vwlpis
organs Troglostrongylosis ( ► p. 318) Troglostrongylus spp. �
-�
Aelurostrongylosis ( ► p. 322) Aelurostrongy/us abstrusus >,
Oslerosis ( ► p. 325) Oslews osier/ Oslerus rostratus
Anglostrongylosis (► p. 320) Anglostrongy/us vasorum
·u;
Ca12illariosls ("" Q. 373) Cag_il/ada aeroQ.hlla C. e C. aerog_ ila co
co
 Part VII. Parasitoses of different animal species and organ systems, antiparasitic drugs and strategic control

Table 19.12. Continued.

� -· - - -· - . -- · , ..,...,- - .•. ,·
Organ Parasitosis2 Parasites
�ystem
'"'
lit . ' . .,.,._ .� - .,�-, - � .
Dog
��- 1·' - Cat
.
Lymphatic Leishmaniosis ( ► p. 72) Leishmania infantum Leishmania infantum
system Cytauxzoonosis ( ► p. 145) Cytauxzoon felis, Cytauxzoon sp.
Blood, blood Babesiosis ( ► p. 129) Babesia spp. Babesia spp.
vessels Cytauxzoonosis ( ► p. 145) Cytauxzoon fe/is, Cytauxzoon sp.
Dirofilariosis ( ► p. 357) 0irofi/aria immitis 0. immitis
Angiostrongylosis ( ► p. 320) Angiostrongylus vasorum
Oesophagus, Ollulanosis ( ► p. 302) 01/ulanus tricuspis
stomach Spirocercosis ( ► p. 349) Spirocerca /upi
Capillariosis ( ► p. 373) Capil/aria putorii
Small Giardiosis ( ► p. 47) Giardia duodena/is G. duodena/is
intestine Cystoisosporosis ( ► p. 100 Cystoisospora spp. Cystoisospora spp.
Sarcocystiosis ( ► p. 116)) Sarcocystis spp. Sarcocystis spp.
I,
IJ Hammondiosis ( ► p. 109) Hammond/a heydorni H. hammondi
,_• Neosporosis ( ► p. 110) Neospora caninum
1�
,_ Cryptosporidiosis ( ► p. 122) Cryptosporidium spp. Cryptosporidium spp.
,--
,.. Toxoplasmosis ( ► p. 101) Toxoplasma gondii
I:- Diphyllobothriosis( ► p. 208) 0iphyllobothrium spp. 0iphyllobothrium spp.
I•·

.
i,...J Mesocestoidosis( ► p. 213)
Dipylidiosis ( ► p. 222)
Mesocestoldes spp.
0ipylidium caninum
Mesocestoides spp.
0. caninum
-
·- Taeniosis ( ► p. 232) Taenia hydatigena, T. pisiformis, etc. Taenia taeniaeformis
j,
Echinococcosis ( ► p. 240) Echinococcus granulosus s.l., E. multilocularis
-
E. multilocu/aris
Strongyloidosis (► p. 259) Strongyloides stercoralis
Hookworm infection( ► p. 280) Ancy/ostoma caninum Ancylostoma tubaeforme
Uncinaria stenocepha/a U. stenocephala
Roundworm infection ( ► p. 333) Toxocara canis, Toxascaris leonina Toxocara cati, T. leonina
Large Tritrichomonosis ( ► p. 54) Tritrichomonas foetus
intestine Trichuriosls ( ► p. 368) Trichuris vu/pis
Uver Leishmanlosis ( ► p. 72) see skin see skin
Oplsthorchlosis ( ► p. 197) 0plsthorchis fellneus 0. telineus
Echinococcosis, alveolar ( ► p. 247) Echinococcus multllocularls, larval
Capillariosis ( ► p. 373) Cap/I/aria hepatics C. hepatica
Urinary Capillariosis ( ► p. 373) Capil/arla plica Capillaria spp.
bladder
Eye Thelaziosis ( ► p. 346) T he/azja callipaeda T. callipaeda
Onchocercosis( ► p. 366) 0nchocerca lupi
CNS Toxoplasmosis ( ► p. 101) Toxoplasma gondii T. gondii
Q)
C Neosporosis ( ► p. 110) Neospora caninum
·c3 1 This list is not exhaustive. The data refer predominantly to parasites occurring in Europe.
'6 2 In bold: parasitic diseases of particular interest.
Q)

ro
C
·.::
Q) have the advantage of a broad activity spectrum (e.g. combination products may lead to an 'over-therapy'
against nematodes, cestodes and arthropods). The use of certain parasitic infections or infestations. In some
_!; of such agents makes sense when the target parasites countries vaccines for the prevention of babesiosis
>,
0)
actually or probably occur with a certain frequency, (Pirodog-) or leishmaniosis (CaniLeish•) in dogs are
0 and epidemiological factors justify the use of these registered.
0
·u5 preparations. On the other hand the arbitrary use of
ro
ro
a..
 19. Parasitoses of different animal species and organ systems, antiparasitic drugs and strategic control
Table 19.13. Antiprotozoals (selection) for use in dogs and cats.
Indication Active substance
Babesiosis lmidocarb
Leishmaniosis Allopurinol
Miltefosine
N-methylglucamine
antimoniate
Hepatozoonosis lmidocarb
Giardiosis Fenbendazole
Cystoisosporosls (syn. Toltrazuril
lsosporosis)
Toxoplasmosis: acute, systemic Clindamycin
toxoplasmosis in dog and cat;
exception: cerebral form
Neosporosis3 : systemic Pyrimethamine +
infection in dog Sulfonamides
Clindamycin +
Sulfonamides
1 Registration of drugs (► p. 556); - not approved.
2 Notes on application and tolerability see labels or databases(► p. 576).
3 With the listed combination therapies, clinical recovery was achieved in some cases.
19.4.2 Strategic control of important
parasitoses of dogs and cats
In contrast to the situation in ruminants, pigs and horses,
relatively few systematic studies have been performed on
the strategic control of certain parasitic diseases of small
animals with respect to the epidemiological impact,
sustainability and cost-effectiveness of the recommended
measures. Exceptions are, for example, studies on the
control of Dirofilaria immitis and Echinoccus granulosus
s.l. in dogs or flea infestations of dogs and cats. This is
partly due to the fact that the dog and cat populations
are very heterogenous concerning their breed and
age structures, their spatial distribution as well as the
types of maintenance and nutrition. Therefore, some
of the recommendations for control, which are based
primarily on epidemiological considerations of experts,
on practical experiences and individual studies, are
still under discussion and require further evaluation.
In recent years the 'European Scientific Counsel
Companion Animal Parasites' (ESCCAP) has developed
guidelines for the control of protozoa, helminths, and
ectoparasites in dogs and cats (www.esccap.org).
19.4.2.1 Leishmaniosis in dogs
Leishmaniosis in dogs is common in southern parts
of Europe ( ► p. 72). The causative agent, Leishmania
infantum, is transmitted by Phlebotomus spp. (sandflies).
Prevention of sandfly bites plays a central role in
protecting dogs from the disease and in reducing
transmission.
-
Target apeclel DoH (P« kg b.w.) and appllcatlw i
approval 1
dogFA 5.0-6.0 mg/kg s.c., if needed repeat after 2 weeks
human dog: 20 mg/kg daily p.o.. 3 months to years C
0
dog 2 mg/kg p.o. over 4 weeks (.)
- ► p. 76 ·5,
Q)
- 5.0-6.0 mg/kg s.c. at intervals of 14 days
ti5
dog, cat 50 mg/kg daily over 3-5 days
dog, cat dog: 10 mg/kg dally at 4-5 days, p.o.
cat: 18 mg/kg p.o.
dog, cat dog: 12.5 mg/kg p.o. every 12 h for 2-4 weeks
cat: 12.5-25.0 mg/kg p.o. every 12 h for 2-4 weeks
human, dog pyrlmethamine: 1 mg/kg daily p.o. + sulfadiazine/
trlmethoprim 15 mg/kg 2>< daily p.o. for 4 weeks
human, dog 12.5 mg/kg 2x daily for 4-8 weeks+ sulfadiazine/
trlmethoprlm 15 mg/kg 2>< daily p.o. for 4-8 weeks
Prophylaxis. For dogs that are permanently or
temporarily (e.g. during holiday travel) residing in
endemic areas prophylaxis against sandfly bites is
recommended during the period of vector activity
(southern Europe: April to November). At the beginning
of this period or a week before entering an endemic area
dogs should be provided with an insecticide-impregnated
collar (e.g. Scalibor•, Seresto•) which gives maximum
protection (up to 90%) for approx. 6 months against
sandfly bites. Active components of such collars are
pyrethroids alone or combined with other substances.
An alternative for dogs is spot-on treatment (24 h prior
to entry) with permethrin (e.g. E xspot•) every 4 weeks
or with permethrin + imidacloprid (e.g. Advantix•)
every 3 weeks. These measures provide simultaneously a
protective effect against ticks and fleas ( ► Table 19.16)
and have the potential to reduce the incidence of dog
leishmaniosis in endemic areas if used in large-scale
programmes. If possible, dogs should be kept indoors
during the night, and access to breeding sites of sandflies
(basements, waste places, stables) should be prevented.
Vaccination. Recently, the EMA has authorised for
the EU a vaccine (CaniLeish�) that is based on purified
excretory-secretory Leishmania infantum antigens ( ► p.
569). lt should be noted that vaccination may complicate
the serological diagnosis, and experiences on the efficacy
of the vaccine are still limited.
Other measures. If dogs have been exposed to an
infection risk without protection they can be submitted
to serological examinations immediately after return
from an endemic area and 6-12 months later. Seropositive
animals should be monitored and treated as soon as
Parasitology in Veterinary Medicine

Table 19.14. Antiparasitic mono-products (selection) for use in dogs {D) and cats (C) (selection of commercial products ►Chapter 20, p. 615).

.,_°'"'"'
mglqb.w.ll
1llkeM

'
g. i
i
j
it,,

I
CD �

ig la
c"
a
S!
I9: 'i}
�
i
I:I
r..
II a
� �
� !iii 2 ::,-
C: 1§. �
i- i- i :I
[
C:
:I :I lb Ill Dog

Fenbendazole (BZ) DIC DIC: 50 x 3d ip.o. • • • • t) • t) >10 >3

Flubendazole (BZ} DIC 0/C: 22 x 2-3d lp.o. • • • • >7
Mebendazole (BZ) DIC DIC: 20-22 x 3-5 d
I
p.o. t) • • t) >20
Selamectin (ML) DIC DIC:6.0 spot-on • • • >10
Praziquantel (ISO) DIC DIC: 5.0 ,p.o. t) • • • • >20 >20
DIC: 5.7 s.c. t) • • • •
C:8.0 spot-on • • • •
Epsiprantel (ISO) DIC 0:5.5 p.o. • • • 90 36
C:2.75 p.o.
Nitroscanate (VO) D D: 50-100 p.o. • • t) • • >5
Pyrantel-base (PY) DIC 0:5.0 p.o. t) • >10
C:20.0
1 Chemical group: BZ = benzimidazoles; ISO = isoquinolines; ML = macrocyclic lactones; PY = pyrimidines; VO = various other active substances.
2 Registration of drugs see ► p. 556.
3 Selection of recommended doses; additional information see labels and databases(► p. 576).
4 Efficacy: • = good to very high; C> = partially effective or only in increased dose or with repeated application; - = insufficient effect; empty fields: no information or drug not recommended in this indication.
 fI f
• • • • •
I I I I
Febantel + Praziquantel + Pyrantel embonate D 15.0+5.0+5.0 p.o. () - - - -

Fenbendazole + Praziquantel DIC 50.0 + 5.0 x 2-3 d p.o. () • • • • • I • () • I -

Pyrantel embonate + Praziquantel C 20.0+5.0 p.o. () • • () • - I - I - - I
Pyrantel base + Epsiprantel D 5.0+5.5 p.o. • • • • - I - - I ' - - I
Pyrantel + Oxantel + Praziquantel D 5.0+20.0+5.0 p.o. () • • • I • I • - '
Milbemycin oxime + Praziquantel DIC D: 0.5+5.0 p.o. () • • ()J• • • I • I • • () •
Milbemycin oxime + Lufenuron D 0.5+10 p.o. tl/e • • • • • • •
• • • • • • • • •
I
Milbemycin oxime + Lufenuron + Praziquantel D 0.5+10.0+5.0 p.o. tll•

I
()

Moxidectin + lmidacloprid DIC D: 2.5+10.0 spot on • • • • • • () • •

C: 1.0+10.0
Eprinomectin + Praziquantel + Fipronil + C 0.5+10+10+12 spot on • • • • • • •
S-Methoprene
Emodepside (VO) + Praziquantel C 3.0+ 12.0 spot on • • • •
Emodepside (VO) + Praziquantel D 1.0+ 5.0 p.o. • • • • • ()

Emodepside (VO) + Toltrazuril (VO) D 0.45+9.0 p.o. • • •

1 ► Table 19.14.
2 Selection of recommended doses; additional information see labels or databases (► p. 576).
3 Efficacy: • = good to very high; tl = partially effective or in increased dose or with prolonged application; - = insufficient effect; empty fields: no information or not reco,r■rl8i,ded in this indication.

Parasitology in Veterinary Medicine Dogs and cats Strategic control

 Part VII. Parasitoses of different animal species and organ systems, antiparasitic drugs and strategic control

Table 19.16. Ectocides and insect growth regulators (selection) for use in dogs (D) or cats (C).

"
Indication, form of application, active Commercial Target Dose (mg/kg b.w.)3, E: duration of efficacy (w:
§.ubstance (generic name) and chemical products species weeks)
1 (examples) approval2
-�group
Infestation with hard ticks
Collar
Deltamethrin (P) Scalibor® D E: 5-6 months
Flumethrin (P)+ lmidacloprid (VO) Seresto® DIC E: 7-8 months
Spot-on
Fipronil (VO) Frontline® DIC D, C: 6.7 mg/kg, E: 2 (C) to 4 (D) w
Fipronil (VO) + Methoprene (IGR)+ Certifect® D 6.7 mg/kg+ 6 mg/kg + 8 mg/kg, E: 5 w
Amitraz (FORM)
lmidacloprid (VO)+ Permethrin (P) Advantix® D 10 mg/kg+ 50 mg/kg, E: 4 w
Metaflumizone (VO)+ Amitraz (FORM) ProMeris Duo ®
D 20 mg/kg+ 20 mg/kg, E: 4 w
Permethrin (P) Exspot® D 50 mg/kg, E: 4 w
Per os
Fluralaner (ISO) Bravecto® D 25-56 mg/kg, E: 12 w
Sarolaner (ISO) (per os) Simparica® D 2-4 mg/kg, E: 5 w
Demodicosis
Fluralaner (per os) Bravecto® D minimum 25 mg/kg b.w., repeat if necessary
Metaflumizone (VO)+ Amitraz (FORM) ProMeris Duo® D 20 mg/kg+ 20 mg/kg, 1x per month until clinical
(spot-on) cure
lmidacloprid (VO)+ Moxidectin (ML) Advocate® D 1 O mg/kg + 2.5 mg/kg, min. 4x in intervals of 4 w
(spot-on)
Cheyletiellosis or tromblculosis
Fipronil (VO) (spot-on) Frontline® DIC D, C: 6.7 mg/kg, repeat after 2 w
Selamectin (ML) (spot-on) Stronghold® DIC D, C: 6.0 mg/kg, repeat after 4 w
Sarcoptlc mange
Sarolaner (ISO) (per os) Simparica® D 2-4 mg/kg, repeat after 4 w
Selamectin (ML) (spot-on) Stronghold® D 6 mg/kg, repeat after 4 w
lmidacloprld (VO)+ Moxldectln (ML) Advocate® D 10 mg/kg+ 2.5 mg, repeat after 4 w
(spot-on)
Ear mange (Otodectes Infestation)
lmidacloprld (VO)+ Moxldectln (ML) Advocate® DIC D: 10 mg/kg+ 2.5 mg/kg, repeat after 4 w
(spot-on) C: 10 mg/kg+ 1.0 mg/kg, repeat after 4 w
Selamectln (ML) (spot-on) Stronghold® DIC D, C: 6 mg/kg, repeat after 4 w
Infestation with biting and chewing lice
Flpronil (VO) (spot-on) Frontline® DIC D, C: 6.7 mg/kg, repeat after 2 w
Selamectin (ML) (spot-on) Stronghold® DIC D, C: 6.0 mg/kg, repeat after 4 w
Flea lnfestatlon 4
Collar
Deltamethrin (P) Scaliboi4D D E: 4 months
Q)
DIC
·o
C Flumethrin (P)+ lmidacloprid (VO) Seresto® E: 7-8 months
=o
-
Spot-on
Q)
� Fipronil (VO)+ Methoprene (IGR) Frontline® DIC D: 6.7 mg/kg+ 6.0 mg/kg
�
co
Combo C: 5.0 mg/kg+ 6.0 mg/kg
C E: adult fleas 4-8 w, developmental stages 6-12 w
·;:::
Fipronil (VO)+ Eprinomectin (P) + Broadline® C min. dosages 10.0 mg/kg+ 0.5 mg/kg+ 12 mg/
Methoprene (IGR)+ Praziquantel (VO) kg+ 10 mg/kg
E: adult fleas and developmental stages longer
.£
>, than one month
CJ)
0 Fipronil (VO)+ Methoprene (IGR)+ Certifect® D 6.7 mg/kg+ 6.0 mg/kg+8 mg/kg, E: 5 w
0 Amitraz
·u5 lmidacloprid (VO) Bayvantage® DIC D, C: 10 mg/kg, E: 4 w
co Advantage ®
0...
 19. Parasitoses of different animal species and organ systems, antiparasitic drugs and strategic control

Table 19.16. Continued.

.,.
Indication, fonn of application, active
substance (generic name) and chemical
group1
Commerclal
pnxluctl
(uamPI•)
.,,..,,.
'111,get
approwaP
. ---,
•
. -• .� �.
(w:

<
Flea infestation (continued) ...
C
Spot-on (continued) "' 0
u
lmidacloprid (VO) + Moxidectin (ML) Advocatel!b DIC D: 10 mg/kg + 2.5 mg/kg, E: 4 w u
C: 10 mg/kg + 1.0 mg/kg, E: 4 w '6>
I
Q)
lmidacloprid (VO) + Permethrin (P) Advantixl!b D 10 mg/kg+ 50 mg/kg, E: 4 w
Metaflumizone (VO) ProMeris® C 40 mg/kg, DE: 4-6 w U)
Metaflumizone (VO)+ Amitraz (FORM) ProMeris Duo® D 20 mg/kg+ 20 mg/kg, E: up to 6 w
Permethrin (P) Exspot4'> D 50 mg/kg, E: 4 w
Pyriprol (VO) Prac-tic 4'> D 12.5 mg/kg, E: 4 w
�
Pyriproxyfen (IGR)5 Cyclio4'> DIC D: 2.0 mg/kg, E: 3 months
C: 1O mg/kg, E: 3 months
Selamectin (ML) (spot-on) Strongholdl!b DIC D, C: 6.0 mg/kg, E: 4 w
Spray
Pyriproxyfen (IGR)+ Permethrin (P) Duowin® D 94 mg/kg + 1.0 mg/kg
E: 4 w adult fleas, 8 w developmental stages -
Per os or subcutaneously
Spinosad (VO) (p.o.) Comfortis® DIC 45-70 mg/kg, E: 3-4 w
Fluralaner (VO) (p.o.) Bravecto® D 25-56 mg/kg, E: 12 w
Afoxolaner (VO) (p.o.) NexGard® D 2.7-6.9 mg/kg, E: 5 w
Lufenuron (IGR) 5 (p.o.) Program® DIC 10 mg/kg, E: 4 w
Lufenuron (IGR)5 (s.c.) Program® C 10 mg/kg, E: 6 months
Nitenpyram (VO) (p.o.)6 Capstar® DIC D, C: 1.0 mg/kg, as soon as fleas occur on animal
Sarolaner (ISO) (p.o.)6 Simparica® D 2-4 mg/kg, E: 5 w
Sand fly (Phlebotomus) infestation
Deltamethrin (P) (collar) Scalibor® D E: up to 6 months
lmidacloprid (IGR) + Permethrin (P) (spot- Advantix® 10 mg+ 50 mg/kg, E: 2-3 w
on)
Permethrin (P) (spot on) Exspot® D 50 mg/kg, E: 4 w
1 C = carbamates; FORM = formamidines; IGR = insect growth regulator; ISO = isoxazolines; ML = macrocyclic lactones; P =
pyrethroids; VO = various other active substances.
2 Registration of drugs (► p. 556).
3 Indicative dose; see also databases (► p. 576).
4 Numerous types of insecticide collars for flea control are commercially available.
5 Has no effect on adult fleas, but inhibits the development of fleas.
6 Immediate efficacy against adult fleas.

pathological blood parameters indicate the beginning
of the disease.
In non-endemic areas with confirmed presence of
competent vector sandflies(e.g. southern Switzerland,
southern Germany) it cannot be excluded that imported
dogs with untreated or treated leishmaniosis could
become infection sources for autochthonous vectors.
As a temporary preventive measure it is therefore
recommended to protect such dogs during the summer
months from sandfly attacks (see above).
19.4.2.2 Babesiosis in dogs
Autochthonous infections of dogs with Babesia species
are widely distributed in Europe, especially in southern
and eastern parts, but with recent expansions up to the
Baltic States. In Central Europe canine babesiosis is one
of the most frequently imported diseases(► p. 129). The
agents are transmitted by bites of several tick species,
including Rhipicephalus and Dermacentor species. Only
sporadic cases of babesiosis in cats have been observed
in Europe.
Control options include the following measures:
prophylaxis against ticks by applying a collar with
acaricidal effect to dogs(e.g. Scalibor e, Seresto•) and cats
(Serestro•). Alternatively acaricides can be applied to
the skin or orally(► Table 19.16). Even if only a partial
protection against ticks is achieved, these measures can
substantially reduce the risk of infection with Babesia
spp. Vaccination of dogs against babesiosis with a
 Part VII. Parasitoses of different animal species and organ systems, antiparasitic drugs and strategic control

subunit vaccine (Pirodog"') usually protects most of Control in dogs. Highly efficient cestocides
the animals from serious disease, but does not reliably (praziquantel, epsiprantel) are available for treatment
prevent infection. Chemoprophylaxis with imidocarb of infected animals(► Table 19.14 and 19.15). Repeated
(lx 6.0 mg/kg b.w., s.c. or 2x 4.0-6.0 mg/kg s.c. every treatments in intervals corresponding to the prepatent
14 days) protects dogs from disease for about 4 weeks periods of the Taenia species are indicated when an
(imidocarb is registered in FR). Prophylaxis against ticks infection risk persists. Routine treatment of all imported
and vaccination can be combined. dogs is recommended because these animals can be
carriers of tapeworms that are transmissible to domestic
19.4.2.3 Toxoplasmosis in cats livestock (e.g. of Taenia multiceps: dog--. sheep). For
prophylaxis dogs should be prevented from access to
Cats are the most important primary sources of infection slaughterhouse waste and viscera of game animals.
for other animals and humans because they can excrete If such material (liver, lung, musculature, etc.) is to
oocysts of Toxoplasma gondii in the faeces, which be used as dog food it has to be pre-cooked or frozen
sporulate under favourable conditions in a few days (-18 °C, 3 d).
in the environment and are infectious to humans and
other hosts( ► p. 101). Control in cats. Cats exposed to an infection risk
by hunting rodents may be treated with a cestocide at
Control. The following prophylactic measures can help regular intervals of about 8-12 weeks or when infections
reduce the infection risk for cats: feeding with canned or have been confirmed.
dry food or with meat or offal which has been cooked
or deep-frozen (3 days or longer at -18 °C); prevention 19.4.2.6 Echinococcosis in dogs and cats
of the cats from hunting small mammals(rodents, etc.)
and birds; daily cleaning and washing of litter boxes Echinococcus granulosus s.l. and E. multilocularis,
with hot water (use disposable gloves!). However, free­ which are endemic in Europe (and other regions), are
ranging cats can acquire the infection by ingestion of important zoonotic agents that require special attention
infected intermediate hosts or of sporulated oocysts ( ► p. 240). The main endemic areas of the E. granulosus
from the environment. s.l. (definitive host: dog) comprise countries in the
Mediterranean region as well as in south-eastern and
Due to concern about the alleged risk of infection for eastern Europe; in large parts of northern, central and
humans, cats are sometimes euthanised. However, western Europe E. granulosus s.l. occurs sporadically or
a coproscopy can determine whether or not a cat is is restricted to regional foci. In contrast, E. multilocularis
currently shedding oocysts and is thus a source of (definitive hosts: fox, raccoon dog, dog, rarely cat) is
infection. Furthermore, the detection of specific serum widespread in western, central and eastern Europe and
antibodies indicates that the likelihood of future oocyst occurs frequently in foxes and less often also in dogs
shedding is relatively low. Cats which excrete Toxoplasma hunting rodents. General options for echinococcosis
oocysts can be held in quarantine under strict hygienic control are described elsewhere ( ► p. 246, p. 251).
conditions until the oocyst shedding has stopped. The Here only measures directly related to dogs and cats
long-term use of toltrazuril in feed (daily 5 mg/kg b.w.) are mentioned.
may limit though not completely suppress the excretion
of oocysts. In practice this measure is only useful in E. granulosus: control and prevention. Dogs must
special cases. not be fed with raw organs(especially liver and lung) of
slaughter animals or wildlife in areas where E. granulosus
19.4.2.4 Dipylidiosis in dogs and cats s.l. is endemic. Cooking or freezing at -18 °C for at least
3 days kills the metacestodes which may be hidden in
Dipylidium cantnum is a fairly common cestode species the organs. Dogs imported from endemic areas (e.g.
in dogs and cats( ► p. 222). Transmission occurs orally from Mediterranean countries) may be E. granulosus s.l.
Q)
by ingestion of fleas containing Dipylidium cysticercoids. carriers. Therefore, it is recommended to treat imported
·u
C

i5 Control measures comprise the treatment of infected dogs with praziquantel. In some European countries,
.
�
Q)
animals with a cestocide ( ► Table 19.13 and 19.14) and such treatments are officially prescribed. In cases of
flea control (see below). a confirmed infection with E. granulosus s.l. specific
co treatment with praziquantel or epsiprantel should be
C
·;::
19.4.2.5 Taeniosis in dogs and cats performed under safety precautions.

C Dogs may become infected with one or several Taenia E. multilocularis: control and prevention. In
>,
CJ)
species (► p. 232) by ingesting offal of slaughter or dogs and cats which hunt and eat small mammals in
0 wild animals containing metacestodes. The only species endemic areas, the development of gravid intestinal
0

"in occurring in cats is Taenia (Hydatigera) taeniaeformis, stages of E. multilocularis can be prevented by treatment
co whose metacestodes develop in rodents. In differential with praziquantel at intervals of 4 weeks. As potential
co sources of infection for humans cats are less important
(l. diagnosis Echinococcus spp. must be considered (see
below).
 19. Parasitoses of different animal species and organ systems, antiparasitic drugs and strategic control
than dogs because they rarely harbour large numbers
of egg-producing stages of E. multilocularis.
19.4.2. 7 Toxocarosis in dogs and cats
Puppies and kittens are frequently infected with
Toxocara canis and Toxocara cati, respectively ( ► p.
333). They usually excrete large numbers of eggs, which
are infectious for humans and other hosts after third
stage larvae have developed inside the eggs. Although
older animals develop patent infections less frequently,
they may contribute to environmental contamination
with eggs. Regarding control measures it is especially
important to note that puppies can acquire the infection
by prenatal and lactogenic transmission of T. canis
larvae. In contrast, only lactogenic transmission occurs
in T. cati infections of cats.
Control of T. canis infection in dogs
Hygiene measures (cleaning, disinfection) in dog
maintenance and anthelmintic treatments of dogs
of various age groups represent the available control
options.
• Puppies. First treatment at the age of 2 weeks in
order to eliminate immature intestinal stages originating
from prenatal infection before the onset of egg shedding.
Further treatments at 2-week intervals up to 2 weeks
after weaning. Monodrugs highly effective and well
tolerated by puppies include fenbendazole, flubendazole,
mebendazole, and pyrantel ( ► Table 19.14; combination
preparations ► Table 19.15).
• Bitches. Treatment 2 weeks post-partum, since
patent infections may develop at this time originating
from somatic larvae or from T. canis stages ingested by
the bitch with faeces of puppies.
• Dogs older than 12 weeks. Selected anthelmintic
treatments should be performed when egg shedding
has been detected by coproscopic examinations. If
no coproscopy is conducted, experts recommend 2-4
treatments per year, depending on the infection risk to
which the dogs are exposed. When dogs are considered
as specific risk factors for zoonotic infections (e.g. close
contact with children or patients in convalescent homes)
more frequent treatments at intervals of 4 weeks may
be indicated. However, further studies are required for
evaluating the reliability and epidemiological effects of
these measures.
• Prevention of prenatal and lactogenic
infections. Prenatal and lactogenic infections of
puppies can be prevented or greatly reduced (>95%)
by anthelmintic treatment of pregnant bitches infected
with somatic T. canis stages. Effective and safe tolerable
treatment options (off-label use!) include: moxidectin
(2.5 mg/kg b.w. spot on) on the 50th day of pregnancy;
selamectin (6 mg/kg b.w. spot on) 40 and IO days ante­
partum as well as IO and 40 days post-partum. In cats
lactogenic infections can be prevented by treatment of
the queen with emodepside (3 mg/kg b.w. spot-on) a
few days ante-partum. e
0
(.)
Control of T. cati in cats (.)
·5,
<D
Because of the potential lactogenic infections kittens are
first treated at the age of 2-3 weeks, at weaning and 14
days post weaning. Subsequently, monthly treatments
are recommended until the age of 6 months ( ► Table
19.15 and 19.16). At the first treatment of kittens the
nursing queens shouJd also be treated, as intestinal
infections may establish arising from activated somatic
larvae. In cases of a low infection risk, treatments of
kittens can be reduced to each one at 8 and 12 weeks of
age. Treatments every 3 months are advised for adult
cats.
19.4.2.8 Toxascariosis in dogs and cats
Special control measures are not required as Toxascaris
leonina ( ► p. 332) is covered by the measures against
Toxocara.
19.4.2.9 Hookworm infections in dogs
In temperate climate zones of Central Europe Uncinaria
stenocephala is the most common hookworm species of
dogs ( ► p. 280), in warmer areas, however, Ancylostoma
caninum dominates. U. stenocephala infections are
predominantly acquired by oral uptake of infective
larvae. In A. caninum several infection routes are
possible (per os, percutaneously, lactogenic). Control
measures against T. canis (see above) are also effective
against hookworm infections.
19.4.2.10 Trichuriosis in dogs
In problem kennels young dogs should be treated with
an anthelmintic effective against Trichuris beginning at
the 1 oth week of life and repeatedly if required. In dog
breeds and animal shelters cleaning and disinfection are
particularly important for reducing the environmental
contamination with infective Trichuris eggs.
19.4.2.11 Dirofilariosis in dogs and cats
T he causative agent, Dirofilaria immitis (heartworm)
( ► p. 357), is transmitted by mosquitoes. In endemic
areas dogs and cats are exposed to an infection risk
during the mosquito season. Currently, the European
endemic area comprises ES, PT, southern FR, IT
(including Mediterranean islands, CY, TR, most of the
Balkan states and CZ and SK (the latter with sporadic
transmission).
 Part VII. Parasitoses of different animal species and organ systems, antiparasitic drugs and strategic control
Control. Dirofilariosis can be effectively prevented
by treating dogs and cats with macrocyclic lactones
(milbemycin oxime, moxidectin or selamectin; ► Tables
19.15 and 19.16) during the mosquito season (southern
Europe from May to November) at intervals of 4 weeks.
The first treatment must be performed at the latest
4 weeks after entering the endemic area, and the last
treatment up to 4 weeks after leaving the area. Depending
on the applied dosage macrocyclic lactones alone or in
combination with other agents also cover a wide range
of other parasites. In the USA resistance of D. immitis to
ML has recently been identified as an emerging problem.
19.4.2.12 Tick infestation in dogs and cats
In Central Europe, dogs and cats are often exposed to tick
attacks (Ixodes ricinus, Ixodes hexagonus, Dermacentor
reticulatus, etc.) from March/April until late autumn.
However, depending on the tick species and weather
conditions infestations may occur also during winter.
Control. Measures against existing infestation of dogs
and cats with ticks are described elsewhere( ► p 396).
Several prophylactic options exist both for dogs and cats.
• Dogs. During the tick season(also while travelling!)
application of a collar containing an acaricide effective
against ticks (protection up to about 5-8 months).
Alternatives: oral treatment(protection up to 3 months)
as well as spray or spot-on applications of acaricides
(protection up to 5 weeks)( ► Table 19.16).
• Cats. Application of acaricide collars as in dogs or
spot-on application of products containing e.g. fipronil,
eprinomectin or flumethrin (permethrin is toxic!).
19.4.2.13 Flea infestation
The most common flea species in dogs and cats
is Ctenocephalides felis (cat flea, ► p. 500). The
developmental stages of fleas (larvae, pupae) do not
live on the animal, but in the environment. Therefore,
fleas can only successfully be controlled by treatment
of the host animals and the environment.
Flea control on the animal
Q)
·o
C
=o • Application of insecticide collars. ► Table
�
Q)
19 .16. Protective �ffect of 4-8 months, especially suitable
as an individual protection against new infestations.
co
C Effect is not always complete since it can be impaired
·;::
Q) by various factors, such as moisture and dirt.
C • Application of insecticides as spray. ► Table
>,
0)
19.16. Especially suitable for immediate relief of the
0 animals from infestation with adult fleas. This can also
0
·u5 be achieved by oral administration of nitenpyram.
co
0..
• Oral administration of nitenpyram or other
ectocides. ► Table 19.16. T he effect on fleas begins
15-30 min after administration of nitenpyram and results
in the elimination of the flea population within 24 h.
Repeated treatment is indicated when fleas are found
again on the animal. Simultaneous treatment of the
environment is recommended (see below).
• Spot-on application of insecticides. Examples
are listed in ► Table 19.16.
• Application of insect growth regulators (IGR).
Lufenuron, an IGR, is given orally to dogs or cats once a
month from spring for at least 6 months or throughout
the year. The IGR taken up with the blood ingested by
the female flea gets into eggs, inhibits the formation
of chitin structures and thus blocks the development
of larvae and pupae. The adult fleas are not killed and
must be treated at the beginning of control action with
an insecticide on the animal. Lufenuron is also used in
combination with milbemycin oxime, thus fleas and
different groups of nematodes are covered ( ► Table
19.15). Another IGR, methoprene, is also used as active
ingredient in combination with insecticides for flea
control( ► Table 19.16).
Fleas in the environment
• Mechanical elimination. Thorough vacuum
cleaning of all locations that may serve as hiding places
for developmental stages of fleas can remove a significant
portion of the flea population and is an important
component of the control measures. Spraying the
environment with insecticides and IGR: resting places
of dogs and cats and the environment (underside of
carpets, floor cracks, pillows, upholstered furniture, etc.)
must be sprayed with insecticides and/or an insecticide/
IGR mixture. For this purpose special commercial
products are available.
• Insecticide resistance. In local flea populations
resistance to insecticides(usually low level) of different
drug classes(pyrethrins, pyrethroids, organophosphates,
carbamates) has been demonstrated. Therefore, annual
changing of insecticide drug class is recommended, but
there is little evidence that this procedure can actually
prevent or delay selection for resistance.
19.4.3 Parasitoses and companion
animal travel
Companion animals (dogs, cats, ferrets, rodents,
domestic rabbits, etc.) travelling with their owners
or animals to be exported or imported are subject to
veterinary regulations issued by the EU (Regulation
[EC] no. 998/2003) or other international or national
authorities. Based on EU regulation 998/2003 some
countries require the treatment of dogs and cats against
 19. Parasitoses of different animal species and organ systems, antiparasitic drugs and strategic control

peworms (Echinococcus) and ticks prior to entry (more
ormation ESCCAP, www.esccap.org).
om a parasitological perspective, the following
official measures are recommended:
Before travelling abroad with a dog, cat or other
pet animal, seek information on export and import
regulations and infection risks existing at the
destination and contact a veterinary practice at least
1 month before departure.
Perform recommended prophylaxis particularly
against vector-borne diseases (VBD), e. g .
protection against ticks and sandflies, vaccination or
chemoprophylaxis against babesiosis, chemoprophy­
laxis against Dirofilaria immitis when travelling to
certain Mediterranean or other endemic regions (for
more information about VBD, see www.esccap.org).
Never take stray dogs or cats to the home country
(risks: rabies, Echinococcus, other pathogens). An
official import of dogs or cats requires health and
vaccination certificates and - in some countries -
treatment of the animals against intestinal helminths
and ectoparasites.
19.5 Parasitoses of rabbits
Rabbits are raised in small stocks or in larger commercial
husbandries as production animals for meat and skin,
and also play a role as pet and laboratory animals. Some
parasitoses are listed in ► Table 19.17 together with
hints for control.
In production animals intestinal and liver coccidiosis,
the Encephalitozoon infection and Psoroptes ear mange
are the most important parasitic infections. The control
of coccidioses is based on hygiene measures and the
prophylactic use of approved anticoccidials ( ► p. 89).
In pet rabbits, the potential spectrum of parasites is
wider. Since only a few antiparasitics are approved for
use in rabbits, off-label use is unavoidable in some cases.

Table 19.17. Rabbits: parasitoses and antiparasitics(selection).

Parasite Active substance

(generic name and target
species registration) 1
.
o...... -...
for edible tlsaues
anc1-po,tod1
-
Protozoa
Eimeria spp. Toltrazuril(RA) therapy: 1 x 15 mg/kg b.w. p.o.: repeat after 5 days,
Intestinal and liver coccidiosis( ► p. W: 35 days
95) Robenidine(RA) prophylaxis: 50-66 ppm in feed, W: 5 days
Salinomycin-Na(RA) prophylaxis: 20-25 ppm in feed, W: 5 days
Encephalitozoon ( ► p. 157) Fenbendazole(RA) daily 20 mg/kg b.w., p.o. for 4 weeks applied
directly or in pellets, W: not HC
Helminths
Cittotaenia spp.( ► p. 215) Praziquantel(0) 1 x 10 mg/kg b.w. p.o., W: n.s.
Strongyloides ( ► p. 259) lvermectin(0) 0.2-0.4 mg/kg b.w. s.c., repeat after 7 days, W: n.s.
Graphidium and Trichostrongylus Fenbendazole(RA) 1 x 5-10 mg/kg b.w. p.o., repeat after 14 days,
(► p. 301) W: n.s.
Passalurus( ► p. 344) Fenbendazole(0) 25 ppm in feed for 5 days; repeat treatment if
necessary; hygiene measures are important! W: n.s.
Arthropods
Cheyletiella spp.( ► p. 430) Selamectin (DIC) 30 mg/animal, spot on at neck; treatment of all
Sarcoptes, Notoedres( ► p. 442) contact animals; decontamination of environment,
W: n.s.
lvermectin(0) 0.3 mg/kg b.w., s.c. 3x in intervals of 1 week,
treatment of all contact animals; decontamination of
environment, W: n.s.
Psoroptes(ear mange)( ► p. 435) Selamectin(D/C) as in Cheyletiel/a
lvermectin(0) 0.25 mg/kg b.w. in each ear, treatment of all contact
animals: decontamination of environment, W: n.s.
Haemodipsus, Spilopsyllus ( ► p. 500) lmidacloprid(RA) 10 mg/kg b.w. spot-on, repeat after 2 weeks,
W: not HC
1 Approved for rabbits(RA) or other(0) target species(D: dog, C: cat).
2 n.s. = not specified; not HC = not to be used for animals intended for human consumption.
Part VII. Parasitoses of different animal species and organ systems, antiparasitic drugs and strategic control

different cestode species whose development depends on

19.6 Parasitoses of poultry
19.6.1 Parasitoses of organ
systems, antiparasitics and
vaccines
In Europe and other regions manyparasite species are
known to occur in poultry( ► Table 19.18 and 19.19).
Of those only a few are common and of practical
significance in chickens kept indoors. Currently, most
important among the ectoparasites are the red mite
(Dermanyssus gallinae) and among the endoparasites
Eimeria species, the agents of coccidiosis. Infections
with various nematode species (Ascaridia galli,
Heterakis gallinarum and Capillaria spp.) are also a
frequent problem. Further species occur in free-range
chicken such as the gapeworm (Syngamus trachea) or
intermediate hosts. In turkeys histomonosis (blackhead
disease) is of greatest relevance in addition to helminth
infections as in chickens. Pigeons can become infected
during free flight with a wide range of parasites, but
relevant infections are relatively rare. In some cases
the soft tick Argas reflexus, which is associated with
pigeons, may also infest humans. Furthermore, in
pigeon stocks trichomonosis (agent Trichomonas
gallinae) and coccidiosis regularly occur. If geese and
ducks are kept close to open waters, infections with
numerous parasite species are possible. In these hosts
trematode, cestode and acanthocephalan species are
quite common, and are transmitted by intermediate
hosts. Anticoccidial drugs are listed in ► Table 5.2
► p. 89. Only a few anthelmintics are available for the
control of helminths in poultry ( ► Table 19.20). The
same applies to ectocides.

Table 19.18. Parasites (selection) of the organ systems of chickens, turkeys and pigeons.
� ,,..,, u�.:-: ,.. ·�"
Organ systems Parasites 1

Chickens il'urkeys Pigeons

Plumage, skin Argas reflexus A· Argas reflexus A·

Dermanyssus gal/inae A•
Ornithonyssus sylv/arum A•
Megninia spp. A·
Epidermoptes bilobatus A'
Knemidocoptes mutans A·
chewing lice A'
Ceratophyllus gall/nae A·
Subcutis Lamlnosloptes cyst/cola A'
Musculature Sarcocystls horvathl P'
Trachea, bronchi Syngamus trachea N'
AJr bags Cytodites nudus A'
Blood, blood vessels P/asmodium circumflexum P'
Plasmodium rellctum P'
Leucocytozoon spp. P'
Oesophagus, crop Trichomonas gallinae P'
Acualia sp. N'
Cap/Ilaria annulata N'
Oispharynx nasuta N'
Glandular stomach Oispharynx nasuta N'
Tetrameres fissispina N"
Gizzard Acuaria hamulosa N'
Streptocara sp. N'
Small intestine Eimeria spp. p·
Spironucleus me/eagridis P'
Echinostoma spp. TR'
Amoebotaenia cuneata c·
Choanotaenia infundibulum c·
Oavainea proglottina c·
Dermanyssus gallinae A·
Ornithonyssus sylviarum A·
Megninia spp. A•
Cytodites nudus A'
Knemidocoptes mutans A·
chewing lice A•
Ceratophyl/us gallinae A'
Laminosloptes cysticola A·
Syngamus trachea N'
Cytodltes nudus A'
Haemoproteus meleagridls P
Leucocytozoon spp. P'
Trichomonas gal/inae P'
Acuaria sp. N'
Cap/Ilaria annu/ata N'
Oispharynx nasuta N"
Dispharynx nasuta N"
Tetrameres fissispina N'
Acualia hamulosa N'
Streptocara sp. N'
Eimeria spp. P'
Spironucleus meleagridis p·
Parastrigea robusta TR'
Amoebotaenia cuneata c·
Choanotaenia infundibulum c·
Oavainea proglottina c·
Dermanyssus gallinae A'
Ornithocheyletia hallae A'
Megninia columbae A'
Falculifer rostratus A'
chewing lice A'
Ceratophyllus columbae A·
Cimex columbarius A·
Laminosioptes cysticola A·
Syngamus trachea N'
Cytodites nudus A'
Haemoproteus columbae P'
Leucocytozoon spp. P'
Trichomonas gallinae P'
Acuaria sp. N'
Capillaria sp. N'
Ornithostrongylus sp. N'
Ornithostrongylus sp. N'
Tetrameres fissispina N'
Eimeria spp. P'
Spironuc/eus co/umbae P'
Parastrigea robusta TA'
Sobo/evicanthus gracilis c·
Oavainea proglottina c·
 19. Parasitoses of different animal species and organ systems, antiparasitic drugs and strategic control
Table 19.18. Continued.
·-
�--.:;:
.,_..,_1
·.""
Organ systerM
Chlcbnl
Small intestine (continued)
Echinolepis carioca c·
Raillietina spp. c·
Ascaridia ga/li N'
Capillaria bursata N'
Cap/Ilaria caudinflata N'
Cap/Ilaria obsignsta N'
Strongyloides avium N
Trichostrongylus tenuis N'
Caeca, rectum Chilomastix gaflinarum p•
Histomonas meleagrldls p•
Eimeria spp. p•
Echinostoma revolutum TA'
Cap/Ilaria anatis N'
Heterakis ga/llnarum N'
Trichostrongylus tenuis N
Liver Histomonas meleagridis p•
Oviduct Prosthogonimus sp. TR'
Conjunctiva, Oxyspirura mansoni N
nictitating membrane
Various organs Toxoplasma gondil P'
1 In bold parasites of particular interest. • = species occurring in Europe; A = arthropods; C = cestodes; N = nematodes; P = protozoa;
TR = trematodes.
Table 19.19. Parasites (selection) of organ systems of geese and ducks.
Organ systems
Plumage, skin Dermanyssus gallinae A'
Leptosphyra velata A•
chewing lice A'
Musculature Sarcocystis spp. P
Trachea, bronchi Cyathostoma bronchialis N'
Blood, blood vessels Bilharziella polonica TA'
Trichobilharzia spp. TR'
Oesophagus, crop Cap/Ilaria contorts N'
Echinuria uncinata N*
Eustrongylides papillosus N'
Glandular stomach Echinuria uncinata N'
Eustrongylides papillosus N'
Hystrichis tricolor N*
Streptocara crassicauda N'
Tetrameres fissispina N'
Gizzard Amidostomum anseris N•
Echinuria uncinata N'
Epomidiostomum uncinatum N'
Streptocara crassicauda N*
.
� ..
•·
a-
:..:.
.,,___
1'l1!11,11""ill"'
"j -,
-��
Echinolepls carioca c· Killigrewia detafondl c·
Raillietina spp. c· Ralllietlna bonln/
Ascaridfa dissimi/1s N' Ascarldls columbse N'
Gap/Ilaria bursata N'
Gapflfaria caudinflata N' Gap/Ilaria caudlnflata N'
Cspillaris obsignats N Capillsrls obslgnata N'
Ornlthostrongytus sp. N' ..
Trichostrongyfus tenuls N' Trlchostrongylus tenuls N'
Chllomastix gatllnarum P'
Histomonss meleagrldls p•
Elmerls spp. P' Elmerla spp. P'
Echinostoma revolutum TR" Echlnostoma revolutum TR'
Cap/Ilaria anatis N' Gap/Ilaria anatls N'
Heterakis gallinarum N' .
Trichostrongylus tenuis N' Trichostrongytus tenuls N"
Histomonas meleagridis P'
Prosthogonimus sp. TA'
Oxyspirura mansoni N Oxyspirura mansoni N
Toxop/asma gondil P* Toxoplasma gondi/ p•
Leptosphyra velata A'
chewing lice A'
Sarcocystis spp. P
Cyathostoma bronchialis N'
Bilharziella polonica TR'
Trichobilharzia spp. TR'
Capillaria contorts N*
Echinuria uncinata N*
Eustrongylides papillosus N'
Echinuria uncinata N'
Eustrongylides papillosus N'
Hystrichis tricolor N'
Streptocara crassicauda N'
Tetrameres fissispina N'
Echlnuria uncinata N'
Epomidiostomum uncinatum N*
Streptocara crasslcauda N"
 Part VII. Parasitoses of different animal species and organ systems, antiparasitic drugs and strategic control

Table 19.19. Continued.

¾ - ~ - ... ' ..

te;111··
.. . ..,·
Geese Ducks
' 1. ,,, � ..,
Small intestine Eimeria anseris, etc. P* Tyzzeria, etc. P*
Apatemon gracilis TR* Apatemon gracilis TR*
Cotylurus cornutus TR* Cotylurus comutus TR'
Echinostoma revolutum TR* Echinostoma revolutum TR*
Echinoparyphium recurvatum TR' Echinoparyphium recurvatum TR*
Hypoderaeum conoideum TR* Hypoderaeum conoideum TR'
Parastrigea robusta TR* Parastrigea robusta TR*
Hymenolepididae C*: Hymenolepididae C*:
Dichoris stefanskii • Dichoris stefanskii •
Dicranotaenia coronula* Dicranotaenia coronula'
Drepanidotaenia /anceolata* Orepanidotaenia lanceolata •
Rmbriaria fascio/aris' Rmbriaria fasciolaris'
11
Microsomacanthus compressa • Microsomacanthus compressa •
Ii
Ii-.
1,-
Sobolevicanthus graci/is' Sobo/evicanthus gracilis'
Ascaridia gal/I N* Ascaridia gal/I W
11 Capillaria caudinflata N' Capillarla caudinflata N'
Contracaecum rudolphll N' Contracaecum rudoiphii N •
Ii
Porrocaecum crassum N' Porrocaecum crassum N'
Trichostrongy/us tenuis N" Trichostrongy/us tenuis N'
Polymorphus minutus AC' Po/ymorphus minutus AC*
Filicol/is anatis AC* Fillcoi/ls anatis AC*
Caeca, rectum Chilomastix gallinarum p• Chi/omastix gailinarum P'
Cotylurus comutus TR' Cotylurus cornutus TR'
Echinostoma revolutum TR' Echinostoma revolutum TR'
Capillaria anatis N* Capil/aria anatis N*
,_ Heterakis dispar N' Heterakis dispar N*
Trichostrongyfus tenuis N* Trichostrongyius tenuis N*
Uver Metorchis bills TR* Metorchis bi/is TR*
,Kidney Eimer/a truncata P'
OViduct Prosthogonimus soo. TR' Prosthogonimus spp. TR'
Conjunctiva, nictitating Phllophthatmus cupensls TR' Phllophthalmus cupensis TR'
membrane Oxysplrurs mansoni N
Various organs Toxoplasma gondil P' Toxoplasma gondll p•
1 In bold: parasites of particular interest. • = species occurring In Europe; A = arthropods; AC = Acanthocephala, C = cestodes; N =
nematodes; P = protozoa; TR = trematodes.

Q)
T5
C 19.6.2 Strategic control of important 19.6.2.2 Helminth infections
'5 parasitoses of poultry
�
(I)
Under the conditions of intensive farming in stables
c
ro
19.6.2.1 Coccidiosis (eimeriosis) of prophylaxis is of particular importance in the control of
C chickens helminthoses. Prophylactic measures are primarily aimed
·c at nematodes like Ascaridia galli, Heterakis gallinarum
(I)
The aim of control measures against chicken coccidiosis and Capillaria obsignata that have direct life cycles. These
_!; is to prevent loss of performance and disease outbreaks. measures should also ensure that stables do not provide
>,
O>
The control is based on hygiene measures, the use of favourable living conditions for potential intermediate
0 anticoccidials ( ► Table 5.2, p. 89) and vaccination ( ► p. hosts of helminths (e.g. flies). In free-range chickens
·u; 569) prophylaxis is more difficult because the animals are
ro exposed to parasites with direct or indirect life cycles, and
ro
a.. effective disinfection of the environment is not possible.
 19. Parasitoses of different animal species and organ systems, antiparasitic drugs and strategic control

Table 19.20. Anthelmintics approved for use in poultry.

ndazole (benzlmldazole)
Flubenol® 5% (CH). Medicated premixture
Indication for use: nematodes: Ascaridia galli, Heterakis gallinarum, Capillaria spp., Amidostomum anseris, Trichostrongylus
tenuis, Syngamus trachea; cestodes: Raillietina spp. C
Dosage1 and administration: total dose: 10 mg/kg b.w. (chicken, geese), 20 mg/kg b.w. (pheasants, partridges) applied in 0
(.)
divided doses in feed over 7 days (.)
Withdrawal periods: meat (chickens): 3 days (other poultry): 4 days, eggs: 0 '6>
CD
Contra-indication: pigeons and parrots should not be treated with flubendazole
Flubenvet® 1% (UK). Medicated premixture
Indication for use: as in flubenol
Dosage 1 and administration: 30 ppm flubendazole (chicken, geese), 20 ppm (turkeys) in feed over 7 days
Withdrawal periods: meat (chickens, turkeys, geese): 7 days, eggs: 0
bendazole (benzlmldazole)

SGlubenol® 100 mg/g (DE). Emulsion

Indication for use: Ascaridia galli, Heterakis gallinarum, Capil/arla spp.
Dosage1 and administration: 1.4 mg/kg b.w./day, In drinking water over 7 days
Wlthdrawal periods: meat (chickens): 4 days, eggs: 0
Panacur® Aqua Sol 200 mg/ml (DE, UK). Suspension
Indication for use: Ascaridia galli, Heterakis gallinarum
Dosage1 and administration: 1.0-1.4 mg/kg b.w./day, in drinking water over 5 days
Withdrawal periods: meat (chickens): 6 days, eggs: 0
le (lmldazothlazole)
Concurat®-L 10% (DE). Powder
Indication for use: Ascandia spp., Heterakis spp., Capillaria spp., Amidostomum anseris
Dosage1 and administration: 40 mg/kg b.w.; Ascaridia: 20 mg/kg b.w., applied once in feed or drinking water.
Withdrawal periods: meat (chickens, turkeys, pheasants, guinea fowls, geese, ducks): 14 days. Not to be used in animals ,
producing eggs for human consumption
1 Dosage refers to active ingredient.

Chicken in stables with intensive floor followed by regular repeats at intervals of 4 weeks (or 3
husbandry weeks in case of Syngamus infections of turkeys).

Control. Thorough cleaning and effective disinfection 19.6.2.3 Dermanyssus infestation

of the stables and barn equipment after each production
cycle; keep deep litter dry; measures against the
introduction of helminth eggs and other pathogens
(put on plastic overshoes and protective clothing before
entering the poultry house, disinfection trough), keep
pigeons, sparrows and other wild birds away from
stables. Check state of infection with helminths by faecal
examination or necropsies.
Use of anthelmintics. In broilers, which are kept in
stables under strict hygiene standards for only about 5
weeks, the application of anthelmintics is generally not
required. In young and laying hens and in breeding
stocks anthelmintic treatments may be indicated when
helminth infections reach a significant level. Only a few
anthelmintics approved for use in poultry are available
(► Table 19.20).
Free-range chicken and turkeys
Infestation with Dermanyssus gallinae ( ► p. 420) is
a major problem in chicken farming, particularly in
laying hens. Control measures are predominantly
directed against the mites in their lairs (treatment of
the environment).
Control. Empty stables and equipment should
be thoroughly cleaned (steam jet cleaners) and, if
necessary, sprayed or misted with suitable acaricides (e.g.
pyrethroids, carbamates, organophosphates, spinosad).
In some countries poultry houses are heated above
45 °C for several days between production cycles to
control mites, sometimes in combination with acaricide
application. Measures to prevent the introduction
of mites into poultry houses by people, wild birds,
rodents or through materials are important. A constant
temperature below 20 °C in populated houses can help
to delay the reproduction of the mites.

Control. Depending on the spectrum of helminth Stables with young and laying hens. Spraying of
species and the intensity of infection, anthelmintic acaricides is a key component to control Dermanyssus
treatments may be required. If indicated, breeding and in poultry houses. It must be ensured that all potential
stocks should be treated the first time at 5 weeks of age, hiding places of the mites ( cages, nests, perches,
 Part VII. Parasitoses of different animal species and organ systems, antiparasitic drugs and strategic control
cracks, feeders, drinkers, other equipment, etc.) and
other targeted surfaces are thoroughly sprayed. Before
treatment the poultry house and equipment must be
cleaned, and eggs removed from laying nests. Only a
few acaricides, specifically developed for controlling
Dermanyssus in poultry houses, are currently available,
including phoxim and spinosad.
• Phoxim, an organophosphate compound, is applied
at a concentration of 2,000 ppm 2x at an interval
of 7 days. It reduces the mite population almost
completely (>97%) for 6-7 weeks, but the efficacy
may vary depending on various factors. During
treatment the animals may remain in the stable, but
must not be sprayed. When the abundance of mites
is high, treatments are indicated but they should
be limited to a total of 4 applications per year. A
phoxim-containing product (ByeMite") for use in
chickens is authorised in the EU and available in
several countries(AT, DE, IT, NL, FR, UK, etc.). The
following withdrawal periods are prescribed(AT):
edible tissues: 25 days after the second treatment,
eggs: 12 h. Eggs laid on the day of treatment have
to be discarded.
• Spinosad(Elector•), a more recent natural product
isolated from soil bacteria (Saccharopolyspora
spinosa), is available as biocide (with organic
certification) in the EU and is applied as spray
like phoxim. According to the manufacturer's
information this product controls red mites for up
to 12 weeks. It can be applied in the presence of
layers, and the eggs produced while spraying can
be marketed because spinosad application does not
leave harmful residues.
• Other acaricides and resistance. In some countries
various pyrethroids are approved for use in poultry,
but others (e.g. carbamates, amitraz) are also used
without approval. When using any of the acaricides
the resistance problem has to be considered.
Resistance of D. gallinae to pyrethroids and
carbamates has been observed in various countries
(e.g. IT, FR, SE, UK).
Monitoring. Control measures should be based on
monitoring the mite populations by regular inspections
and the use of mite traps (see below).
Alternative methods. Mite traps that are placed in
different areas of the stable can reduce Dermanyssus
populations, but the effect is limited to their immediate
surroundings. Several types of traps are described. for
example cardboard strips(14xl6 cm or other formats)
that are impregnated with an acaricide and folded so that
they provide shelter for the mites. Such traps prevent
direct contact between chickens and the acaricide and
can reduce the mite population by >95%. However, size
as well as number and arrangement of traps is critical. In
addition to conventional acaricides, an active ingredient
(azadirachtin) isolated from the neem tree has also
proven effective. As mentioned above certain types of
traps are used for monitoring purposes.
Silica (Si02) (diatomaceous earth) and other inert
substances (e.g. kaolin) absorb lipids upon contact
with Dermanyssus mites or other arthropods leading to
dehydration and death. These substances are distributed
in poultry houses as dusts or suspensions and are
especially recommended for use on organic farms.
Although these substances are regarded as chemically
'inert' and non-hazardous, the manufactures strongly
recommend users to wear face masks with special filters
when applying and handling such materials in order to
prevent inhalation of particles and the development of
lung silicosis.
19.7 Parasitoses of the honey bee
The importance of beekeeping is often underestimated.
In the EU, the number of beekeepers was estimated at
620,000 (9% of them professional), and annual honey
production at about 200,000 tons in 2010. In addition,
bees play an important role in plant pollination.
Therefore, the protection of bees from pathogens,
pesticides and other harmful factors is a major challenge.
Of the various parasitoses of the honey bee (Apis
mellifera) four are listed by OIE as notifiable (►Table
19.21). Currently, varroosis is the major hazard for
European bee populations, but acarapiosis is also quite
important. Tropilaelaps mites have not yet been found
in Europe, but there is a risk of introduction. By the
end of 2014, the small hive beetle, Aethina tumida, was
introduced to southern Italy and represents a new risk
for honey bees in other parts of Europe.
Control and prevention of bee diseases are subject
to regulations issued by the OIE, the EU (e.g. Council
Directive 82/894/EEC) and national authorities as briefly
indicated in ► Table 19.21.
Selected other parasitoses. Malphigamoebosis
(amoebosis) an infection of the Malphigian tubes of
the bees with the protozoon Malpighamoeba mellificae
( ► p. 46 }; nosemosis, an intestinal infection, caused
by Nosema apis(Microsporidia) ( ► p. 159); braulosis,
caused by the fly Braula coeca, which can be a pest in
high abundances(► p. 474).
 19. Parasitoses of different animal species and organ systems, antiparasitic drugs and strategic control

Table 19.21. Important parasites and parasitoses of the honey bee (,Apis mellifera).

Vaffoa destructor Worldwide distribution. except Australia. common and important in Europe. Parasite of adult bees
(Varroosls) and brood that causes malformations and other signs in bees; vector of 'Deformed Wing Virus'.
(► p, 424) Control: notifiable to OIE and national authorities (most European countries): surveillance, reduction
of mite numbers by hygiene measures. use of approved acaricides. such as coumaphos, flumethrin,
organic acids (lactic acid. oxalic acid. formic). thymol.
Acarapis woodi Almost worldwide. except Australia and New Zealand. The mites and developmental stages inhabit
(Acarapiosis) the tracheae of adult bees ('tracheal mite') causing loss of haemolymph and other damage. Control:
(► p. 434) notifiable to OIE and national authorities (-40% of European countries); cleaning, disinfection,
colony management: in-hive fumigation with formic acid can reduce mite numbers.
Tropilaelaps spp. Several species, all found in Asia. Mites feed on bee larvae and pupae, spreading by direct contact
(Tropilaelaps infestation) from bee to bee or movement of brood. Control: notifiable to OIE and national authorities (all
(► p, 424) European countries): prevention of introduction to free areas.
Aethina tumida Distribution: Sub-Saharan Africa, Egypt USA, Canada, Australia. recently (2014) introduced to Italy.
(small hive beetle (SHB) Major problem In Introduced areas. Both adult and larval stages of the beetle feed on bee brood,
infestation) pollen and honey. Larval development In the hive. pupation in soil near the hive; adults fly long
(► p. 457) distances (up to 10 km) to seek new hives. Therefore. high risk of spreading! Control: notifiable to
OIE and across European countries; destruction of Infested apiaries; prohibition of imports of bees,
bumble bees, bee products and equipment from affected areas; In lhe environment trapping of
adult beetles and mechanical (ploughing) and chemical destrucllon of larvae in the surroundings of
hives. Exceptional circumstances may require the In-hive use of Insecticides (CheckMite+® strips,
containing 10% coumaphos, the only approved product for SHB control, e.g. In Canada).

c.=:======
:.i Selected references
Ruminants
Charlier J, Morgan ER, Rinaldi L, Van Dijk J, Demeler J,
Hoglund J, Hertzberg H, Van Ranst B, Hendrickx G,
Vercruysse J, Kenyon F (2014) Practices to optimize
gastrointestinal nematode control on sheep, goat and cattle
farms in Europe using targeted (selective) treatments. Vet
Rec 175: 250-255.
Jacober P, Ochs H, Torgerson PR, Schnyder M, Deplazes
P (2006) A method for sheep scab control by applying
selective treatment based on flock serology. Vet Parasltol
136: 373-378.
O'Shaughnessy J, Earley B, Mee JF, Doherty ML, Crosson
P, Barrett D, De Waal T (2015) Controlling nematodes in
dairy calves using targeted selective treatments. Vet Parasltol
209: 221-228.
Rehbein S, Knaus M, Visser M, Winter R, Yoon S, Anderson
A, Cramer L (2015) Activity of ivermectin long-acting
injectable (lvomec® Gold) in first-season grazing cattle
exposed to natural challenge conditions in Germany. Parasitol
Res 114: 47-54.
Rinaldi L, Biggeri A, Musella V, De Waal T, Hertzberg H,
Mavrot F, Torgerson PR, Selemetas N, Coll T, Bosco
A, Grisotto L, Cringoli G, Catelan D (2015) Sheep and
Fascia/a hepatica in Europe: the GLOWORM experience.
Geospat Health 9: 309-317.
Rinaldi L, Catalan D, Musella V, Cecconi L, Hertzberg H,
Torgerson PR, Mavrot F, De Waal T, Selemetas N, Coll
T, Bosco A, Biggeri A, Cringoli G (2015) Haemonchus
contortus: spatial risk distribution for infection in sheep in
Europe. Geospat Health 9: 325-331.
Semetas N, Phelan P, O'Kiely P, De Waal T (2015) The effects
of farm management practices on liver fluke prevalence and
the current internal parasite control measures employed on
Irish dairy farms. Vet Parasitol; 207: 228-240.
Soll MD, Kunkle BN, Royer GC, Yazwlnskl TA, Baggott DG,
Wehner TA, Yoon S, Cramer LG, Rehbein S (2013) An
eprinomectin extended-release injection formulation providing
nematode control in cattle for up to 150 days. Vet Parasitol
192: 313-320.
Townsend L (2013) Insect control for horses, horse barns
and stables. Lexington, KY, USA: University of Kentucky,
College of Agriculture. Available at: http:/www2.ca.uky.edu/
entomology/entfacts/ef513.asp.
Pig
Kreiner T, Worliczek HL, Tichy A, Joachim A (2011) Influence
of toltrazuril treatment on parasitological parameters and
health performance of piglets In the field - an Austrian
experience. Vet Parasitol 183: 14-20.
Boes J, Kanora A, Havn KT, Christiansen S, Vestergaard­
Nlelsen K, Jacobs J, Alban L (2010) Effect of Ascaris suum
infection on performance of fattening pigs. Vet Parasitol
172: 269-276.
Horse
American Association of Equine Practitioners (2013) AAEP
parasite control guidelines. Available at: http://www.aaep.
org/info/parasite-control-guidelines.
Hertzberg H, Schwarzwald CC, Grimm F, Frey CF, Gottstein
B, Gerber V (2014) Helminth control in the adult horse: the
need for a re-orientation [in German]. Schweiz Arch Tierheillk
156: 61-70.
Lincoln VJ, Page PC, Kopp C, Mathis A, Von Niederhausern
R, Burger D, Herholz C (2015) Protection of horses against
Culicoides biting midges in different housing systems in
Switzerland. Vet Parasitol 210: 206-214.
Nielsen MK, Vidyashankar AN, Olsen SN, Monrad J,
T hamsborg SM (2012) Strongylus vulgaris associated
with usage of selective therapy on Danish horse farms-is it
reemerging? Vet Parasitol 189: 260-266.
 Part VII. Parasitoses of different animal species and organ systems, antiparasitic drugs and strategic co ntrol
Nielsen MK, Pfister K, Von Samson-Himmelstjerna G (2014)
Selective therapy in equine parasite control- application and
limitations. Vet Parasitol 202: 95-103.
Rehbein S, Visser M, Winter R (2013) Prevalence, intensity and
seasonality of gastrointestinal parasites in abattoir horses in
Germany. Parasitol Res 112: 407-413.
Schneider S, Pfister K, Becher AM, Scheuerle MC (2014)
Strongyle infections and parasitic control strategies in German
horses- a risk assessment. BMC Vet Res 10: 262.
Dog and cat
Beugnet F, Halos L (ed.) (2015) Parasitoses and vector borne
diseases of cats. Lyon, France: Merial S.A.S., pp. 379. ISBN
978-2-9550805-0-4.
Coles TB, Dryden MW (2014) lnsecticide/acaricide resistance in
fleas and ticks infesting dogs and cats. Parasit Vectors 7: 8.
Day MJ (2011) One health: the importance of companion animal
vector-borne diseases. Parasit Vectors 4: 49.
European Scientific Counsel Companion Animal Parasites
(ESCCAP) (2010) Worm control in dogs and cats. Guideline
1, 2nd ed. Available at: www.esccap.org.
European Scientific Counsel Companion Animal Parasites
(ESCCAP) (2011) Control of intestinal protozoa in dogs and
cats. Guideline 6, 1st ed. Available at: www.esccap.org.
European Scientific Counsel Companion Animal Parasites
(ESCCAP) (2012a) Control of ectoparasites in dogs and cats.
Guideline 3, 2nd ed. Available at: www.esccap.org.
European Scientific Counsel Companion Animal Parasites
(ESCCAPJ (2012b) Control of vector-borne diseases on dogs
and cats. Guideline 5, 2nd ed. Available at: www.esccap.org.
Taenzler J, Llebenberg J, Roepke RK, Heckeroth AR (2015)
Prevention of transmission of Babes/a csnis by Derrnacentor
retlculstus ricks to doge treated orally with fluralaner chewable
tablets (Bravecto ™), Paraelt Vectors 8:305.
---
Rabbit
Harkness JE, Turner PV, VandeWoude S, Whele CL (2010)
Harkness and Wagner's Biology and Medicine of Rabbits
and Rodents, 5th ed. Ames, IA, USA: Wiley-Blackwell; ISBN:
978-0-8138-1531-2.
Frank R, Kuhn T, Mehlhorn H, Rueckert S, Pham D, Klimpet
S (2013) Parasites of wild rabbits (Oryctolagus cuniculus) from
an urban area in Germany, in relation to worldwide results.
Parasitol Res 112: 4255-4266.
Poultry
Blake DP, Tomley FM (2014) Securing poultry production from
the ever-present Eimeria challenge. Trends Parasitol 30:
12-19.
Meyer-Kuhling B, Pfister K, Muller-Lindloff J, Heine J (2007)
Field efficacy of phoxim 50% (ByeMite®l against the poultry
red mite Dermanyssus ga/linae in battery cages stocked with
laying hens. Vet Parasitol 147: 289-296.
Sparagano OA, George DR, Harrington OW, Giangaspero
A (2014) Significance and control of the poultry red mite,
Dermanyssus gallinae. Annu Rev Entomol 59: 447-466.
Swayne DE (ed.) (2013) Diseases of poultry, 13th ed. Ames,
IA, USA: John Wiley Blackwell; ISBN 978-0-470-95899-5.
Bees
Chauzat MP, Cauquil L, Roy L, Franco S, Hendrikx P,
Ribiere-Chabert M (2013) Demographics of the European
apicultural industry. PLoS One 8: 079018.
European Commission (2010) Communication from the
Commission to the European Parliament and the Council
on honeybee health. COM(2010) 714 final, Brussels. Belgium.
Available at: http://tinyurl.com/ojh4p97.
20. Trade names of antiparasitics and
vaccines
■

Alphabetical order of active ingredients, trade names antiparasitics and other veterinary drugs are available in
without further specification; data predominantly from some countries. The list is not exhaustive and presents
CH, DE, FR and UK (internet links ► p. 576). Apps of examples.

Antiparasitics (endo-, ecto- and endectoparasitics)

Cattle Sheep

• Monoproducts • Monoproducts
Albendazole: Albenil®, Albex®, Valbazen® Albendazol: Albenll®, Albex®, Valbazen®
Closantel: Flukiver® Closantel: Flukiver®
Cyfluthrin: Bayofly® Cypermethrin: Crovect®, Ectofly«'
Cypermethrin: Ektomin®, Flectron® Cyromazine: Vetrazin®
Deltamethrin: Deltanil®, Latroxin® Deltamethrin: Deltanll®, Latroxin®
Diclazuril: Vecoxan® Diazinone: Paracide®
Doramectin: Dectomax® Diclazuril: Vecoxan®
Eprinomectin: Eprinex® Dicyclanil: Clik®
Febantel: Rintal® Doramectin: Dectomax®
Fenbendazole: Panacur®, Panacur-SR® Bolus Febantel: Rintal®
Flumethrin: Bayticol® Fenbendazole: Panacur®, Zerofen®
Halofuginone: Halocur® lvermectin: Alfamectin®, Animec® , Bimectin®,
lmidocarb: Carbesia®, lmizol® lvomec®, Noromectin®, Virbamec®
lvermectin: Animec®, Bimectin®, lvomec®, Panomec®, Levamisole: Levamisol®, Ripercol®
Virbamec® Monepantel: Zolvix®
Levamisole: Chronomintic® Bolus, Levamsiol®, Moxldectin: Cydectin®
Levasole®, Levovermax®, Ripercol® Netobimin: Hapadex®
Moxidectin: Cydectin® Oxfendazole: Oxfenil®
Netobimin: Hapadex ® Oxyclozanide: Douvistome®, Zanil®
Oxfendazole: Bovex®, Oxfenil®· Systamex® Interval! Phoxim: Sebacil®
Bolus Praziquantel: Cestocur®
Oxyclozanide: Douvistome®, Zani!® Toltrazuril: Baycox®, Toltranil®, Tratol®
Phoxim: Sebacil® Triclabendazole: Fascinex®, Fasinex®
Toltrazuril: Baycox®, Toltranil®, Tratol®
Triclabendazole: Endofluke®, Fascinex®, Fasinex®, • Combination products
Tribex®, Triclaben® Abamectin + derquantel: Startect®
Levamisol + triclabendazole: Endex®
• Combination products Moxidectin + triclabendazole: Cydectin® Triclamox
Clorsulon + ivermectin: Bimectin® , lvomec® plus,
Virbamec®, Levatum® Goat
Closantel + ivermectin: Closamectin® Albendazole: Albex®, Valbazen®
Closantel + mebendazole: Flukiver® Combi Eprinomectin: Eprinex®, Eprivalan®
Triclabendazole + moxidectin: Cydectin® Triclamox Fenbendazole: Panacur®
Phoxim: Sebacil®
Triclabendazole: Fasinex®
Part VII. Parasitoses of different animal species and organ systems, antiparasitic drugs and strategic control

Pig Dog
Doramectin: Dectomax®
Febantel: Rintal® • Monoproducts
Fenbendazole: Coglazol®, Fenbenda®, Panacur®, Afoxolaner: NexGard®
Panacur® AquaSol Amitraz: Ectodex®
Flubendazole: Flubenol®, Flubendazol®, Solubenol® Deltamethrin: Scalibor®
lvermectin: Animec®, Bimectin ®, Diapec® S, Epsiprantel: Cestex®
Fermectin®, lvomec®, Noromectin®, Optimectin®, Fenbendazole: Panacur®
Virbamec® Fipronil: Effipro® , Eliminall® , Frontline®, Flevox®,
Levamisole: Belamsiol ®, Nilverm® nova Zeronil®
Phoxim: Sebacil® Flubendazole: Flubenol®
Toltrazuril: Baycox®, Cevazuril®, Dozuril®, Tolracol®, Fluralaner: Bravecto®
Tratol®, Toltarox®, Toltranil® lmidacloprid: Advantage®
lmidocarb: Carbesia®
Horse lndoxacarb: Activyl®
Lufenuron: Program®
• Monoproducts Mebendazole: Telmin® KH
Cypermethrin: Deosect® Metaftumizone: ProMeris®
Febantel: Rintal® Miltefosine: Milteforan®
Fenbendazole: Fenbendat®, Panacur® Nitenpyram: Capstar®
lcaridine: Centaura® Nitroscanate: Lopatol®
lmidocarb: Carbesia®, lmizol® Permethrin: Exspot®, Preventic® Permethrin
lvermectin: Animec®, Biomec®, lvomec-p®, Eraquell®, Praziquantel: Droncit®
Eqvalan®, Noromectin®, Optimectin®, Vectin® Propoxur: Bolfa®
Mebendazole: Telmin® Pyriprol: Prac-tic®
Moxidectin: Equest® Pyriproxyfen: Cyclio®
Oxibendazole: Equitac® Pyrantel: Banminth®
Pennethrin: Wellcare® emulsion Selamectin: Stronghold®
Phoxim: Sebacil® Soralaner: Simparica®
Praziquantel: Droncit®, Equitape® Spinosad: Comfortis®
Pyrantel: Banminth® , Equivermon® , Pyratape®, Toltrazuril: see Procox®
Strongid®, Verminal® P
• Combination products
• Combination products Emodepside + toltrazuril: Procox®
lvermectin + praziquantel: Equimax®, Eqvalan® Duo Emodepside + praziquantel: Profender®
Moxidectin + praziquantel: Equest® Pramox Febantel + praziquantel + pyrantel: Drontal® plus,
Permethrin + citronellol: Coopers Fly Repellent Plus® Cestem®, Endogard plus® , Veloxa®
Pennethrin + pyrethrins: Repel-X® lotion Fenbendazole + praziquantel: Caniquantel ®,
Optivermin®
Flpronil + (S)-methoprene: Frontline® Combo
Flpronll + (S)-methoprene + amitraz: Certifect®
Flpronll + permethrin: Effitix®
Flumethrln + propoxur: Kiltix®
lmidacloprid + flumethrin: Seresto®
lmldacloprid + moxidectin: Advocate®
lmidacloprid + permethrin: Advantix®
lndoxacarb + permethrin: Activyl® TickPlus for Dogs
Milbemycin + lufenuron: Program® Plus
Milbemycin + praziquantel: Milbemax®
Moxidectin + imidacloprid: Advocate®
Oxantel + pyrantel + praziquantel: Dolpac®
Permethrin + pyriproxyfen: Duowin®
Praziquantel + pyrantel: Drontal®
 20. Trade names of antiparasitics and vaccines

Cat Rabbit
Cyromazine: Rearguard®
• Monoproducts Fenbendazole: Lapizole®, Panacur®
Epsiprantel: Cestex® lmidacloprid: Advantage®
Fenbendazole: Panacur® lvermectin: Xeno
Fipronil: Effipro®, Eliminall®, Flevo x®, Frontlin e® Permethrin: Xenex®
Flubendazole: Flubenol® Toltrazuril: Baycox®
lmidacloprid: Advantage ®, Bayvantage®
lndoxacarb: Activyl ® Chicken
Lufenuron: Program ® Anticoccidials: ► Table 5.2, p. 89
Mebendazole: Telmin® KH Fenbendazole: Panacur® AquaSol
Metaflumizone: ProMeris® Flubendazole: Flubenol® , Flubenvet®, Flubendazol® ,
Nitenpyram: Capstar® Solubenol®
Propoxur: Bolfo® Levamisole: Concurat®
Praziquantel: Droncit® Phoxim: ByeMite®
Pyrantel: Banminth® Spionsad: Elector®
Pyriproxyfen: Cyclio ® Toltrazurll: Baycox® , Dazuril®, Tolcox®
Selamectin: Stronghold®
Spinosad: Comfortis® Pigeon
Amprolium: Chevi-kok®
• Combination products Carnidazole: Spartrix®
Emodepside + praziquantel: Profender® Clazuril: Appertex®
Eprinomectin + fipronil + methoprene + praziquantel: Dimetridazole: Alazol® , Chevi-col®
Broadline® lvermectin: Animec®
Fenbendazole + praziquantel: Caniquantel® , Zantel®
Fipronil + (S-) methoprene: Frontline® Combo Bees
lmidacloprid + flumethrin: Seresto® Coumafos: Perizin®
lmidacloprid + moxidectin: Advocate ® , Prinovox® Flumethrin: Bayvarol®
Milbemycin + praziquantel: Milbemax® Formic acid: Formivar®
Praziquantel + pyrantel: Drontal®, Prazitel® Oxalic acid: Oxuvar®
Thymol: Apiguard® , Thymovar®

Vaccines
Cattle Dog
Lungworm (Dictyocaulus viviparus): Bovilis® Dictol Babesiosis (Babesia canis): Pirodog®
Leishmaniosis (Leishmania infantum): Canileish®
Sheep
Toxoplasmosis (Toxop/asma gondil): Ovilis® Toxovax Chicken
Coccidiosis (Eimeriosis): Paracox®, Hipracox® ,
Livacox®

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 21. Glossary

Abbreviations and symbols: dim = diminutive; E = More terms are explained in various chapters of the
English; F = French; G = Greek; I = Italian; L = Latin; book.
pl. = plural; sgl. = singular; syn. = synonym. fL: see
keywords further up or down in the list.

A Anthelmintic (G: helmins: worm): substance used to kill

Aberrant host: host ! helminths (helminths !)
Abundance (L: abundantia: abundance): number of individuals Anthelmlntic resistance: drug resistance !
of a particular parasite species in the total host population, Antigen (G: anti: against; gennan: to create): molecule which
including parasite-free hosts; calculation: average parasite Is Immunologically recognised by a host (mostly high
prevalence x average infection intensity (prevalence !, molecular proteins, glycoproteins, also glycolipids)
intensity of infection !) • Hidden antigens of parasites: are not normally recognised
Acaricide (G: akari: mite; L: caedere: to smash): substance by the host's Immune system as they are hidden in the
used to kill Acari (mites and ticks) (Insecticide!, pesticide!) parasite, e.g. In Its Intestinal cells. If such antigens are used
Acarology (G: akari: mite or tick; logos: word, discourse): for the vaccination of hosts, antibodies are formed which
science dealing with Acari are ingested by blood-sucking parasites (e.g. nematodes,
Accidental host: host ! ticks) In which an antigen-antibody reaction takes place
Acephalic larva (G: a- without; kephale: head): Insect larva Inducing damage of the intestine
without head (maggot !) • Recombinant antigen: molecule produced by DNA
Acetabulum (L: acetabulum: small cup for vinegar): suction technology in a heterologous expression system (e.g.
cup of trematodes or cestodes bacteria, yeast) that triggers an immune response
Acyclic transmission: transmission ! r;
Antigen variation (antigen L: varietas: variety): capacity of
Adult (L: adultus: grown up): sexually mature stage of a parasite a pathogen to produce new variants of antigens
(imago !, larva !) Antiparasitic drugs (= antiparasitics): substances used to
Adulticide (L: adultus: grown up; caedere: to smash): substance control parasites (anticoccidium l, anthelmintic f, etc.):
used to kill adult parasite stages (larvicide !) • Drug application: application !
Agamogony (G: a-: without; gamos: marriage): asexual • Drug efficacy: term to describe the potency of a drug to kill
reproduction (gamogony !) parasites; usually defined as difference between parasite
Agent: disease-causing organism (pathogen !) burdens of Infected and treated versus infected and
Allopathy (G: a//os: different; pathos: suffering, disease): term untreated control animals, expressed in percentages, e.g.
used by homoeopathlsts (homoeopathy !) for classical efficacy of 98% means that the drug in the recommended
medicine (= science-based medicine) dose has the potential to eliminate almost all the parasite
Allopatry, allopatric (G: a//os-: different; L: patrla: fatherland): burden from an individual animal or a group of animals
occurrence of related species or subspecies in different • Drug resistance: capacity of a parasite population to
regions or biotopes (sympatry !) withstand a dose of an antiparasltlc drug (l) which would
Alloscutum (G: a//os: other; L: scutum: shield): dorsal extensible kill the majority of Individuals of a susceptible population
part of the tegument posterior to the scutum ! of female (resistance !)
and immature ticks • Residual (persistent) drug efficacy: drug efficacy against
Amastigote (G: a-: without; mastix: whip): stage of new infections, due to persisting efficacious drug levels
Trypanosomatidae without free flagellum (pro- !, epi- !, in the animal
Q)
C trypomastigote !) • Safety index: (L: indicare: to indicate): index for tolerability
·c3
'6 Anabiosis (G: an-: without; bios: life): temporary state of of antiparasitic drugs: ratio of the maximum tolerated
Q)
seemingly lifelessness, e.g. persistence of organisms in single dose (without causing adverse effects) to a single
adverse conditions (hypoblosis !) recommended therapeutic dose
co Aneurysma (G: aneurysma: dilation): localised dilation of an • Withdrawal (=withholding) period: interval between
C
·c arterial blood vessel due to innate or acquired changes application of an antiparasitic drug to animals and the
Q)
of the wall officially permitted use of food products originating from
-� Anorexia (G an-: without; orexis: eagerness, desire): complete treated animals (tissues, milk, eggs) for human consumption
>, loss of appetite and food uptake (inappetence !) Antiprotozoicum: substance used to kill protozoan parasites
0)
0 Antibody (G: anti: against): molecule which binds to a specific Apical complex (L: apex: tip; complexus: aggregate): complex
0
antigen (antigen !) of cell organelles at the anterior end (apex) of motile stages
'in
co Anticoccidium (G: anti: against): substance used to kill of Apicomplexa (sporozoites !, merozoites ! and other
co
a.. coccidia zoites !, kinete !)

Apicoplast (L: apex: tip; G: p/astos: formed, shaped): plastid­
like, non-photosynthetic organelle, surrounded by 3-4
membranes, with small genome (-35 kb), derived from
algae, present in most Apicomplexa (Eimeria, Toxoplasma,
Sarcocystis, Plasmodium); vital to the parasites, functions
not conclusively elucidated
Apod (G: apous: without foot): without extremities, e.g. fly
larvae (maggot!)
Apparent Infection (L: apparere: to appear, be visible): infection
with disease symptoms (unapparent infection !)
Application (L: app/icare: to apply) of drugs:
• Cutaneous (dermal) application (L: cutis: skin): to the skin
• Intramuscular application (L: Intra: into; musculus:
muscle): into musculature (i.m.)
• lntrarumlnal application (L: Intra: Into; rumlnare: chew
over again): into rumen
• Intravenous application (L: Intra: Into; vena: vessel): Into
a vein (i.v.)
• Oral (= peroral) application (L: per-: through; L: os:
mouth): through the mouth (p.o.)
• Pour-on application (E: to pour): application of a drug
solution evenly along the backllne from withers to tall head
• Spot-on application (E: spot): application of a drug
solution to a spot of the skin (neck or shoulder region)
• Subcutaneous application (L: sub: under; cutls: skin):
into subcutis (s.c.)
• Topic application (G: topos: spot, location): local
application to the body surface
Arachnology (G: arachne: spider; logos: word, discourse):
science dealing with Arachnids (mites, ticks, etc.)
Arista (L: arista: awn): appendage (typically filamentous) on
3rd antenna segment of Cyclorrhapha flies
Asexual reproduction: multiplication through binary or multiple
fissions without sexual stages (agamogony t, merogony!,
schizogony!)
Asymptomatic: infection without symptoms (= unapparent!)
Attractant (L: attrahere: to attract): chemical substance which
attracts animals
Autochthonous (G: autochthon: native, Indigenous): organisms
which are native in a habitat or country
Autocid technique (G: autos: self; L: caedere: to smash;
techne: handicraft): method for self-destruction of Insects
though sterilisation or introduction of a lethal mutant Into
the population (sterile insect technique !)
Autogeny (G: autos: self; gennan: to give birth): ability of
insects to lay mature eggs before having ingested blood
(or other food)
Autoinfection: spread of infection within the same host
(infection !)
Axenic (G: a- without; xenikos: foreign): in vitro cultivation
of an organism in absence of another organism or cells
Axostyl (G: axon: axis; stylos: support, pillar): rod-like or
filamentous, intracellular supporting structure consisting
of many microtubules, e.g. in Parabasala
B surface of a cell, an organ or organism, serving motility
Biocide (G: bios: life; L: caedere: to smash): general term for
substances which can be harmful for living beings (e.g.
chemicals in rivers)
21. Glossary
Biocoenosis (G: bios: life, koinonein: living together):
community which encloses all living organisms in a
habitat!
Biotic potential (G: bios: life; L: potentia: power, capacity):
capacity of organisms to reproduce to an extent that
enduring survival of the species is secured
Blotope (G: bios: live; topos: location): habitat of an organism
or a community of organisms within an ecosystem
(biocoenosis t, habitat !)
Bolus (pl. boli) (G: bolos: lump, clump): specific pharmaceutical
form of an anthelmintlc for intraruminal application (t) in
cattle or sheep
Bothrlum (pl. bothria) (G: bothros: trench, pit): dorsal or ventral
longltudlnal grooves or tubes in scolex of pseudophyllidean
cestodes
Bradyzolte (= cystozolte) (G: bradys: slowly; zoein: to live)
zolte (!) of Aplcomplexa, with slow multiplication through
endodyogeny W In cysts
Budding: asexual reproduction by forming an outgrowth from
a parent organism
Bursa copulatrlx (L: bursa: purse; copulare: to connect,
couple): characteristic copulatory organ of nematodes,
typically consisting of three lobes, supported by bursal rays
or papillae; similar structures also in other invertebrates
C
Capitulum (L: caput: head): basically fused mouthparts of
Meso- and Metastigmata, also known as gnathosoma !
(not homologous with head [caput) of insects)
Cephalothorax (G: kephale: head; thorax: chest): body part
of crustaceans und arachnids, formed through fusion of
head segments and a variable number of thorax segments
Cercarla (pl. cerarlae) (G: kerkos: tall): larval stage of digenetic
trematodes mostly with tail, produced by asexual
reproduction within a sporocyst!or redla !
Cercomer (G: kerkos: tall; meros: part): posterior, knob-like
attachment with hooks on a procercoid or cysticercoid
of cestodes
Cestoclde (G: kestos: tape; L: caedere: to smash): substance
used to kill cestodes, also known as cestodicide
Chelae (G: chele: claw): sharp, dented scissors on chelicerae !
Chellcerae (G: chele: claw; keras: horn): paired piercing
mouthparts of Chelicerata
Chemokines (G: kinein: to move): cytokines! with chemotactic
and immunomodulating activities
Chemoprophylaxis (L: pro-: for; G: phylax: custodian, guard):
prophylaxis against disease based on drug application
Chemotaxis (G: tassein: to put in order, to arrange): oriented
movement of a cell or an organism towards or away along
a gradient of a chemical stimulus (taxis !)
Chromidial bodies (G: chroma: colour; L: oideus: similar):
elongated structures in cysts of amoebae, composed
of helically structured ribonucleoproteins stainable with
basic dyes
Cilium (pl. ciliae) (L: cilium: eyelash): hair-like organelles on
or transport of particles, shorter and more numerous than
flagella but with the same basic structure (flagellum !)
Part VIII. Appendix
Cirrus (L: cirrus: ringlet): the male copulatory organ in
trematodes and cestodes
Clone (G: klon: twig, branch): genetically identical descendants
derived by asexual reproduction from a single cell or
individual
Coelom (G: koi/ia: hollow): body cavity of higher metazoans,
lined with mesodermal epithelium (pseudocoel!)
Coenurus (G: koinos: together; oura: tail): larval (metacestode)
stage of some taeniid cestode species (metacestode !)
Coevolution (L: cum: with; evo/vere: to unroll, develop): mutual
adaptation of two or several species in course of their
common evolution (evolution!)
Colonisation (L: co/onia: settlement): (a) presence of
apathogenic or pathogenic organisms on skin or mucosa
without penetration into tissues; (b) establishment of a new
population by founder individuals (e.g. by imported ticks
in a previously tick-free area) (infection O
Congenital (L: cum: with; genitus: be born): a condition present
at birth (prenatal !, transmission routes!)
Commensalism (L: cum: with; mensa: table): association
between organisms of different species where one benefits
without significantly harming the other (mutuallsm !,
parasitism!, symbiosis !)
Conoid (L: conus: cone; G: eidos: similar): organelle of the apical
complex (i) in Apicomplexa; absent in haemosporidians
and piroplasms (micronemes!, rhoptries!)
Contamination (L: contaminatus: blotted, dirty): presence
of microorganisms on objects, in the environment, or in
analytical samples (decontamination !, infection !)
Control: all measures which are used to prevent, reduce or
eradicate diseases, including parasitoses (e.g. chemical,
biological, immunological measures):
• Integrated control: (a) combination of several measures
in a control programme (e.g. drug application and
prophylaxis), (b) programmes for combined control of
several parasitoses
• Selective chemotherapy: antlparasitlc chemotherapy only
of the most Important parasite carriers and not of the whole
animal group, with the aim of reducing both the Infection
exposure and the risk of development of drug-resistance
In the parasite population (treatment !)
• Strategic control: control with efficacious and
environmental-friendly antlparasltic drugs (and other
measures) at defined, epidemiologically determined times,
in order to disturb parasite life cycles enduringly with a
minimum of chemical Interventions and to achieve maximal
benefit for the host animals
Copro-antigen (G: kopros: faeces, dung): antigens excreted
in faeces
Copro-DNA (G: kopros: faeces, dung): DNA excreted in faeces
Coproscopy (G: kopros: faeces, dung; skopein: to observe):
macroscopic and microscopic examination of faeces
Coracidium: (G: korax: crow): first ciliated larval stage of lower
cestodes (Pseudophyllidea)
Coxal glands (L: coxa: hip): excretory glands of arachnids;
in nymphs and adults of Argasidae: glands with external
openings between coxae I and II
Ctenidium (pl. ctenidia) (G: kteis: small comb): row of spines
on head and/or thorax of fleas
Cuticle (L: cuticu/a: membrane): acellular covering, secreted by
the epidermis in nematodes and arthropods (integument!)
Cysticercus (pl. cysticerci) (G: kystis: bladder; kerkos: tail):
larval (metacestode) stage of some Taenia species
(metacestode !)
Cystozoite (= bradyzoite j) (G: kystis: bladder; zoein: to live):
stage of some Apicomplexa (e.g. Sarcocystis, Toxoplasma)
formed by continuous endodyogeny ! in tissue cysts
(endozoite !; merozoites !)
Cytokines (G: kytos: cell; kinein: to move): proteins, secreted by
distinct cell types, which modulate behaviour and features
of other cells (chemokines j, lymphokines, etc.)
Cytostome (G: kytos: cell, container; stoma: mouth): particular
area of cell surface of protozoa for uptake of food particles
D
DALY (Disability Adjusted Life Year): parameter for measuring
disease burdens in human populations: estimated number
of years lived with a certain level of disability and number
of years of human life lost due to mortality !, related to
a certain period and population group, associated with a
specific infection or disease
Dauerstage (German: Dauer: endurance, permanence):
parasite stages (eggs, larvae, cysts, oocysts, etc.) which
can survive considerable periods in the environment and
withstand harsh conditions
Decontamination (L: contaminatus: blotted, dirty): removal
or reduction of a microbial (or radioactive or chemical)
contamination (contamination j, disinfection!)
Definitive host: host !
Density: (a) number of individuals of a particular parasite
species in a sample unit taken from a habitat related to
unit area, volume or weight (e.g. number of strongyle larvae
per kg dry grass); (b) number of individuals of a particular
parasite species in or on a host (= infection/infestation
intensity !)
Deutonymph (G: deuteros: second; G: nymphe: girl, bride):
second nymphal stage in some Acari; In many Acari
this stage Is lost or transformed Into a hypopus stage
(hypopus !, protonymph !, trltonymph !)
Developmental cycle: life cycle !
Dlapause (G: dla: through; L: pausa: pause, rest): genetically
based, obligatory or facultative resting stage of insects
and some other invertebrates with reduced metabolism
(hypobiosis!)
Dictyosomes (G: diktyon: net; soma: body): sets of a few
flattened membranes resembling a stack of plates in a
Golgi body
Dioecious (G: di-: two; oikos: house): females and males are
different individuals (hermaphrodite, monoecious [with
arrows downwards))
Disinfection (L: de: off; infectus: disturbed): specifically
targeted antimicrobial or antiparasitic measure with the
objective to reduce the number of specific pathogens
and to prevent an infection or disease (decontamination l,
sterilisation!)
Disinfestation (L: infestus: dangerous): clearing of rooms or
stored goods from animal pests (mostly arthropods)

Dormozoite (L: dormire: to sleep; G: kytos: cell): resting zoite l,
stage of Protozoa
Drug {medicine): natural or synthetic substance with
pharmacological activity used in treatment and prevention
of diseases
Drug resistance of parasites: antiparasitic drugs (t)
E multicellular organisms containing a membrane-bound
Ecdysis (G: ekdysis: getting out of): casting off the cuticle
during moulting in arthropods and nematodes
Ecology (G: oikos: house; logos: word, discourse): science
dealing with interrelationships between living organisms
and their habitat (biotic and ablotlc factors) (habitat l)
Ectoclde (G: ektos: outside; L: caedere: to smash): substance
used to kill ectoparasltes (endectoclde l)
Ectoparasite (G: ektos: outside; parasite 1): parasite of the
body surface of a host (endoparaslte !)
Egg count reduction test (ECR'D: test to measure the reduction
of egg counts per gram of faeces after defined Intervals
following chemotherapy (egg reappearance period U
Egg reappearance period (ERP): time between successful
chemotherapy of a host Infected with gastro-lntestinal
parasites and reappearance of egg shedding in faeces
Embryophore (G: embryon: seedling, fetus; pherein: to carry):
inner membrane enclosing the oncosphere l within the
shell of cestode eggs
Empodium (G: en-: in; pous: foot): structure on pretarsus of
arthropods
Endectocide (G: endon: internal; ektos: external; L: caedere:
to smash): substance used to kill endo- and ectoparasites
(ectocide t)
Endemic (= enzootic) stability (G: endemos: native): factors
influencing disease occurrence are relatively stable,
resulting in little fluctuation of disease incidence. Endemy l
Endemy (G: endemos: native): permanent occurrence of a
disease in a population (humans or animals) in a restricted
area (epidemy l, pandemy l)
Endodyogeny (G: endon: internal; dyos: two; gennan: to
generate): formation of two daughter cells surrounded
by their own membrane, while still In the mother cell
(endopolygeny l)
Endoparasite (G: endon: internal}: parasite living within a
host ! (ectoparasite t)
Endopolygeny (G: endon: internal; polys: many; gennan:
to generate): formation of many daughter cells, each
surrounded by its own membrane, while still in the mother
cell (endodyogeny t)
Endozoite (= tachyzoite) (G: endon: internal; zoein: to live):
zoite of Apicomplexa formed by endodyogeny t in a host
cell in a fast multiplication process t (endopolygeny t)
Entomology (G: entomon: insect): science dealing with insects
(arachnology t)
Epidemy (G: epi-: upon; demos: people): significantly increased
occurrence of an infectious or non-infectious disease in
a population of humans or animals within a given region
and time period (endemy t, pandemy !)
Epidemiology (G: epi-: upon; demos: people; logos: word,
discourse): science that studies the origin, distribution, and
time-dependent dynamics of infectious and non-infectious
21. Glossary
diseases and their biotic and abiotic determinants;
epizootology is a complementary term to epidemiology
but restricted to animal populations
E pimastigote (G: epi: upon; mastix: whip): stage of
Trypanosomatidae with klnetoplast and origin of flagellum
located near the nucleus (amastigote t, trypomastlgote !)
Eukaryote (G: eu: nice, good; karyon: nucleus): unicellular or
nucleus and further characteristic cellular structures
Euryxeny (G: eurys: broad; xenos: host): broad host spectrum
of a parasite species (hOst specificity l, oligoxeny l)
Evolutlon (L: evolvere: to develop): process of phylogenetic
development of organisms, change of genetic composition
of populations, eventually leading to new species
Exposition (L: ex: out; posltlo: position): an organism is
confronted (exposed) to Infectious agents or environmental
factors
Exaheathment: ecdysls t, sheath !
F
FAMACHA® (FAffa MAian CHArt), refers to Or. 'Faffa' Malan):
assessment of the degree of anaemia in sheep (goats)
by comparing the colour of the conjunctiva! mucous
membrane with a colour scale on a chart
Festoon (F: feston: garland): in some genera of hard ticks
rounded patterns or crenellations on the posterior body
margin; can be indistinct or absent in fully engorged
females
Flagellum (L: flagellum: whip): cell organelle, mostly serving
motility, consisting of a plasma membrane that encloses
a matrix and an axoneme; the latter is composed of 9x2
peripheral and 2 central microtubules (cilium t)
G
Gamete (G: gametes: husband): haploid sexual cell that unites
with another cell in sexual reproduction (gametogamy l)
Gametocyte (= gamont) (G: gametes: husband; kytos: cell):
cell giving rise to gametes t; macrogametocyte = female,
mlcrogametocyte = male
Gametogamy (G: gametes: husband; gamos: marriage): union
of two single-celled gametes to form the zygote (gamete t)
Gamogony (= Gametogony) (G: gamos: marriage; goneia:
procreation): sexual phase of development with formation
of particular cells (gametest), eventually leading to
fertilisation
Gamont: = gametocyte t
Gene (G: gignesthai: arise, originate): basic physical unit of
heredity; a linear sequence of nucleotides along a segment
of DNA that provides the coded instructions for synthesis
of RNA (genome !)
Generations, alternation (L: generatio: generation): alternation
between generations with sexual and asexual reproduction
or between sexual and parthenogenetic reproduction
(parthenogenesis l)
Genome (G: gignesthai: arise, originate): genetic material of an
organism, including both the genes t and the non-coding
sequences in DNA/RNA
Genotype (G: gignesthai: arise, originate; typos: type): genetic
make-up of a cell or an organism, usually with reference
 Part VIII. Appendix
to a particular characteristic under consideration, allowing
the discrimination of various genotypes (isolate ! , strain !)
Glycocalix (= surface coat) (G: glukos sweet; L: ka/yx: covering):
layer on the outer surface of eukaryotes (protozoa,
helminths), containing carbohydrate-rich compounds
(such as glycolipids, glycoproteins, and proteoglycans);
composition may change as the parasite encompasses
various developmental stages
Glycosomes (G: glukos: sweet; soma: body): small (~0.2-
0.3 µm) membrane-bound specific organelles, containing
glycolytic enzymes, in cytoplasm of trypanosome blood­
forms
Gnathosoma (G: gnathos: jaw; soma: body): anterior body
section bearing the mouthparts of Acari (mites, ticks)
(capitulum i)
Granzyme: (term composed of granula and enzyme): serine
proteases that are released by cytoplasmic granules within
cytotoxic T cells and natural killer (NK) cells
Guber naculum (L: gubernacu/um: rudder): part of the
copulation apparatus of male nematodes presumed to
function as guiding structure for the spicules !
H ones, which do not develop further or multiply (intermediate
Habitat (L: habitare: to dwell): environment (outside or within
a host) in which an organism occurs (biotope j)
Haematophagous parasites (G: haima: blood; phagein: to
eat): blood-feeding parasites
Helminth (pl. helminths) (G: helmins: worm): collective
term (without taxonomic status) for parasitic worm-like
metazoans of the phyla Platyhelmlntha, Nematozoa and
Acanthocephala
Helminthosls (G: helmlns: worm; nosos: disease): infection
caused by helminths f, Including apparent and unapparent
forms
Hemlmetabolous development (G: hemi: hal�: development
o f insects with Incomplete or partial metamorphosis
(without pupal stage) (holometabolous development!)
Hermaphrodite: (G: hermsphrodltos: name of the son of
Hermes and Aphrodite): Individual with reproductive organs
of both sexes (dloeclous t, monoeclous O
Heterogeny (G: heteros: different; gone/a: procreation): life
cycle of a parasite with alternating generations of bisexual
and parthenogenetlc reproduction (parthenogenesis i)
Heteroxeny (G: heteros: different; xenos: host): involvement of
different types of hosts in the life cycle of a parasite, e.g.
definitive and Intermediate hosts; di- and triheteroxenous
Q)
cycles with two or three obligatory hosts (monoxeny 1)
·u
C
'5 Holarctic (G: ho/os: total; arktos: north): biogeographic region
Q)
of the northern hemisphere with temperate or cold climate,
consisting of Nearctic l and Palaearctic l
co Holometabolous development (G: holos: whole; metabole:
·c:C change): development of insects with complete
metamorphosis including a pupal stage between larval
.£; and adult stage (hemimetabolous development l)
>­
CJ) Homeopathy (G: homoios: similar; pathos: suffering, disease):
0 method of treating disease by drugs, given in minute doses,
0
·u5 that would produce in a healthy person symptoms similar
to those of the disease; although widely used there is no
co
a..
science-based evidence for efficacy against parasitoses
(allopathy l)
Host (L: hospes: host): organism which provides adequate
living conditions for a parasite or another organism:
• Aberrant host (L: aberrare: deviate): host in which a
parasite cannot mature and survive for a longer period
• Accidental host (L: accidentia: casual event): untypical
host in which a parasite can settle, develop and persist,
but which does not play an epidemiological role
& Definitive host (syn. final host): host in which sexual stages
of a parasite develop
• Intermediate host (L: intermedius: between): host in which
a parasite passes through part of its life cycle, associated
with further development or differentiation with or without
asexual reproduction
• Main host: host in which a parasite species is most
frequently found (side host !)
• Naive host (L: nativus: innate, untouched): immunological
term: host which did not have previous contact with a
particular pathogen or antigen
• Paratenlc host (syn. transport h.) (G: parateinein: to retard):
host which harbours parasite stages, usually infectious
host l)
• Reservoir host: host harbouring pathogens for prolonged
periods, with the potential to serve as source of infection
• Side host: host in which a parasite is less frequently found
(main host i)
Host alternation: regular alternation of a parasite species
in its life cycle from one to another host (intermediate -­
definitive host), often associated with an alternation of
parasite generations (asexual - sexual)
Host specificity of parasites: restriction of a parasite
species to one or several host species, resulting in a
narrow (stenoxeny !) or wide host spectrum (euryxeny l),
respectively.
Hydatid (G: hydor, Gen. hydatos: water): metacestode stage
of Echlnococcus granulosus, fluid-filled bladder with
particular wall structure
Hydrogenosomes (G: hydor: water; gennan: to generate):
membrane-bound organelles In the cytoplasm, which
produce H2, CO2 and ATP; function as respiratory
organelles in the energy metabolism of anaerobic protozoa
(e.g. trichomonads)
Hyperinfectlon (G: hyper. above; L: inficere: to infect): massive,
often systemic Infection of a host with several overlapping
infections, often originating from autoinfectlons t, e.g.
infection with Strongyloides stercoralis
Hypobioeis (G: hypo: under; biosis: life): temporarily interrupted
(arrested) development of juvenile stages (3rd, 4th, 5th stage)
of parasitic nematodes in infected hosts (diapause t)
Hypopus (G: hypo: under; pous: foot): 'Dauerstage' t of
some mites (Acaridae, Glyciphagidae), which serves to
survive unfavourable living conditions, corresponds to
deutonymph t
Hysterosoma (G: hysteros: after; soma: body): posterior body
part without legs of Acari (ticks and mites s. s.) (idiosoma !,
proterosoma t, gnathosoma j)

ldiosoma (G: idios: peculiar, personal; soma: body): body of
Acari (mites and ticks) without gnathosoma t
Imago(L: imago: image): adult stage after metamorphosis t,
especially in insects
Immune evasion (L: immunis: free from; evadere: to escape):
capacity of a pathogen to escape the immune defence
of a host
Immunity(L: immunis: free from): actively or passively acquired
protection against pathogens or other antigens t (e.g.
toxins). In contrast to allergy, immune reactions usually
remain unapparent (resistance l):
• Active immunity (= adaptive or acquired immunity):
immunity acquired by a host after contact with pathogens
or other antigens t
• Concomitant immunity (non-sterile Immunity): immune
status, depending on continuous antigenic stimulation,
able to control superinfectlons !, but does not eliminate
existing Infections with parasites of the same species
• Passive Immunity: immunity based on application of
protective antibodies or immune cells from another host,
e.g. transmission of antibodies from mother to offspring
Immunisation: application of an antigen or a vaccine to a
host(vaccine !)
lmmunosuppression: impairment of immune defence
lmmunotolerance(or immune tolerance): an organism does
not react to a certain antigen, although the immune system
is functional
lnappetence (L: in: non; appetentia: demand, desire): reduced
appetite and food intake (anorexia t)
Incidence (L: incidere: to happen): number of new cases
of a disease in a population within a given period, e.g.
100 new cases per 1,000 or 100,000 population per year
(prevalence!, morbidity !)
Incubation period (L: /ncubare: to brood over): time between
infection and manifestation of disease symptoms
Infection (L: inficere: to infect): (a) act of establishment of a
pathogen on or in a host, associated with host reactions
(apparent or unapparent) and usually with proliferation
(multiplication) of the pathogen. 'Invasion', a term
previously used for infections with pathogens which do
not multiply (e.g. some helminths), is now regarded as
obsolete. 'Infection' relates to protozoa and helminths,
'infestation' to arthropods; (b) status of being infected
(infestation!, transmission !):
o Abortive infection(L: abortus: premature birth): shortened
course of infection that often leads to rapid improvement
or cure
• Latent infection (L: latere: hidden): infection that is
temporarily not detectable
• Neonatal infection (G: neos: young; L: natus: birth):
infection of the newborn
• Opportunistic infection (L: opportunitas: chance,
opportunity): infection which occurs only under a situation
that is favourable for a pathogen (e.g. impaired immunity
of the host)
• Perinatal infection (G: peri-: around; L: natus: birth):
infection around the due date of birth
21. Glossary
• Postnatal Infection (L: post: after; natus: birth): infection
after birth
• Prenatal Infection(L: prae: before; natus: birth): infection
before birth
• Primary infection (L: pr/mus: first): first infection of a naive
host (reinfection l, superinfection l)
• Recurrent Infection (L: recldere: fall back, relapse): re­
appearance of an unapparent infection due to activation
by lmmunosuppression, antigenic variation, etc.
• Re-Infection (L: re-: again): another Infection after a
previous infection with the same pathogen species has
been cleared
• Routes of Infection: see transmission !
• Secondary Infection (L: secundus: second): infection of
a host that is already Infected with a pathogen of another
species (or several species) (superinfection !)
• Superinfectlon (L: super: over): Infection of a host with a
particular pathogen species while it is still infected with a
pathogen of the same species (reinfection t, secondary
infection t)
• Unapparent Infection (= asymptomatic t): infection
without noticeable symptoms
Infestation (L: infestere: disturb, damage): establishment
of parasitic arthropods on or in a host with or without
subsequent multiplication (Infection t)
Insecticide(L: insectus: incised; caedere: to smash): substance
used to kill insects (acaricide t, pesticide !)
Isolate(L: insula: island; I: isolare: to isolate): subpopulation of
a pathogen with known origin (e.g. from a particular host
species or animal population) whose genomic or other
features are not characterised (strain !)
Integument (L: integumentum: covering): outer cover of
metazoan parasites, typically consisting of epidermal cells
with or without cuticle (cuticle t)
Intensity of Infection/Infestation: number of individuals of a
parasite species In or on a host (abundance t, density t,
prevalence !)
J
Juvenile hormone: hormone of arthropod larvae that controls
the way the larval stages differentiate at each moulting
Juvenile stage(L: iuventus: youth):(a) colloquial term used to
denote any stage of development prior to adulthood; (b)
often restricted to that stage immediately preceding the
sexually mature adult stage(= preadult stage);(c) immature
stage that resembles the adult in general morphology
Q)
except for gonadal development C
·u
'6
K Q)
Kinete (G: kinein: move): mostly club-shaped, motile stages
with apical complex which develop from zygotes during co
C
sporogony (in Adelaida, Haemosporida, Piroplasmida) ·;::
Kinetoplast(G: kinein: to move; plastos: formed): DNA structure
located within the large mitochondrion in kinetoplasta !, C
composed of a network of circular DNA molecules with >­
CT)
about 50 maxicircles (23-36 kb) and several thousand 0
0
minicircles(0.5-2.5 kb)(the former are coding for enzymes ·u5
of the respiratory chain and ribosomal RNA, the latter for co
co
guide RNAs) Q_
 Part VIII. Appendix
Kinetoplasta (Kinetoplast t): group of free-living or parasitic
protozoa containing a kinetoplast, such as Trypanosoma
and Leishmania
Kinin (G: kinein: to move): pharmacological highly active
oligopeptides, belonging to the tissue hormones which
are released by kallikrein from kininogens
L with reduced functions in protozoa, e.g. Entamoeba,
Larva (L: larva: mask): immature stage of an organism which
differs significantly from adult stage t, imago t
Larvicide: substance used to kill larval parasite stages
Lethality (L: feta/is: deadly, fatal): total number of disease­
associated cases of death within a given population of
diseased animals or humans in a defined time period
(mortality !)
Life cycle: (G: kyklos: circle): biological cycle of a parasite
species with a succession of several developmental stages
in one or more generations t, often associated with one
or more host changes (transmission cycles !)
M of 100,000 a year (mortality !)
Macrogamete: gamete t
Maggot: leg-less (apod t) and often head-less (acephalic t)
larva of Diptera, e.g. flies
Merogony (G: meros: part; goneia: procreation): form
of schizogony ! in Apicomplexa and Microsporida, in
which a mother cell (meront !) divides into daughter cells
(endodyogeny t, endopoiygeny t)
Meront = schizont (G: meros: part): multiple fission body
(merogony t) that forms merozoites ! or daughter
merozoites
Merozoite (G: meros: part; zoein: to live): usually uninucleated,
elongated, motile daughter cells with apical complex of
many Apicomplexa (merogony t)
Metacercarla (G: meta: after; kerl<os: tail): stage of Digenea
(frematoda) arising from cercarla, associated with loss
of tail during the infection process (e.g. schlstosomes) or
encystation (e.g. Fasc/o/a)
Metacestode (G: meta: after; kestos: tape): second larval stage
of taeniid cestodes which develops in an Intermediate host
and is infective at its mature stage to the definitive host
Metaphylaxls (syn.: mesophylaxls) (G: meta: after; phylax:
guard): prophylactic intervention (e.g. drug application)
at a time when hosts presumably are already infected
but adverse effects have not yet occurred (prophylaxis !)
Metamorphosis (G: meta: after; morphe: shape): (a) complete
(I)
C metamorphosis: transformation of insects (morphology,
·c3
'6 metabolism, lifestyle, etc.) encompassing larva, pupa
(I) and adult = holometabolous development f; (b) partial
metamorphosis (without pupal stage) = hemimetabolous
�
cu
C development t
·;:: Metazoa (G: meta: after; zoon: animal): multicellular organisms
(I)
= Animalia (protozoa !)
-� Microfilaria (G: mikros: small; L: filum: thread): uncoiled embryo
>, of filariae that either escapes the egg shell (unsheathed)
CJ)
0 or causes stretching of the shell into an elongated sheath
0
(sheathed)
·u5
cu Microgamete: gamete t
cu
CL
Micronemes (G: micros: small; nema: thread): numerous,
oblong, electron-dense organelles in the apex of zoites of
Apicomplexa involved in cell invasion (apical complex t)
Miracidium (G: meirakidion: young boy): first larval stage of
Digenea (Trematoda)
Mitosomes (G: mitos: thread; soma: body): membrane-bound
cell organelles without genes of mitochondrial origin, but
Giardia
Monoecious: (G: monos: alone, single; oikos: house): individual
with male and female reproductive organs (dioecious t)
Monophyletic taxon (G: monos: alone; phy/on: tribe):
taxon ! including all descendants of an ancestral species
(polyphyletic !, systematics !)
Monoxeny (G: monos: alone, single; xenos: host): a parasite
that infects/infests only one host species in its life cycle
(heteroxeny t)
Morbidity (L: morbidus: diseased): total number of disease
cases within a given population of animals or humans in
a defined time period, e.g. 10 individuals in a population
Mortality (L: mors: death): total number of disease-associated
cases of death within a given population of animals or
humans in a defined time period, e.g. 10 individuals in a
population of 100,000 a year (morbidity t)
Moulting (= molt) (L: mutare: to change): formation of a new
cuticle, followed by ecdysis t
Mutualism (L: mutuus: mutual): association of organisms of
different species to the benefit of both partners without
mutual dependence (commensalisms l, parasitism !,
symbiosis !)
N
Naive host: host t
Natural focus: biotope in which pathogens persist,
independently from humans or domestic animals, e.g. in
populations of vectors (ticks, etc.)
Nearctic (G: neos: new; arktos: north): blogeographic region
including North America from northern Mexico to Alaska
and Greenland (Holarctic f, Palaearctic !)
Nematozoa (syn. Nematoda) (G: nema: thread; zoon: animal):
phylum of Metazoa t
Neotroplc (G: neos: new; trop/kos: tropic): biogeographic
region, including Central and South America and the
Caribbean (Holarctlc j, Palearctic !, Nearctic j)
0
Occurrence (L: occurare: to occur): presence of a parasite or
another causative agent in certain hosts, in various habitats
or geographic regions:
• Autochthonous occurrence (G: autochthon: native):
native in a habitat, not introduced
• Endemic occurrence (endemy t): permanently occurring,
without time limit
• Imported occurrence (L: importare: to import): introduced
into a habitat
• Sporadic occurrence (G: sporadikos: scattered):
sporadically occurring without recognisable temporal and
spatial context of the cases

Off-label use: refers to the use of drugs outside the officially
approved indications, e.g. a drug approved for cattle
should be used for pigs; it can be allowed by the regulatory
authorities if other drugs are not available and the off-label
use does not pose a risk for human health (e.g. residues
in food of animal origin for human consumption)
Oligoxeny (G: o/igos: few; xenos: host): parasite species with
narrow host spectrum (euryxeny t, host specificity t)
Oncosphere (G: ogkos: hook; sphaira: ball): first larval stage
with three pairs of hooks in cestode eggs (= hexacanth
larva)
Ontogeny (G: ta onta: the being, individual; gennan: to
generate): development of an Individual organism from
fertilisation to the mature form (phylogeny !)
Oocyst (G: oion: egg; kystis: bladder): encysted zygote of
Apicomplexa (sporocyst !)
Ookinete (G: oion: egg; kineln: to move): motile, elongate
zygote t of Haemosporlda (sporoklnete !)
Organic farming (= organic agriculture): plant and animal
production based on ecological concepts using natural
sources and methods, rather than Inputs with potential
adverse effects (e.g. agrochemicals, pesticides, etc.).
Species-appropriate livestock husbandry is important.
Special regulations exist for parasite control in livestock
Ovijector (L: ovum: egg; iacere: to throw, to cast): muscular part
of the uterus of certain nematodes, serving the expulsion
of eggs
Ovovivipary (L: ovum: egg; vivus: living; parere: to give birth):
embryonated eggs, released by female parasites, larvae
develop after a short period (vivipary !)
p dealing with parasites and parasitic diseases of plants
Palaearctic (G: pa/aios: ancient; arktos: north): biogeographlc
region, including Europe, Iceland, North Africa (to southern
limit of the Sahara), Middle East, Russia, central Asia,
northern China, Japan and Korea (Holarctic t, Nearctlc t)
Pandemy (G: pan: all; demos: people): large-scale spread
of an infectious disease across countries or continents,
usually affecting a large number of people, limited In time
(endemy j, epidemy j)
Parasite (G: para: beside; sitos: food): organism that lives
in a more or less close association with an organism of
another species (the host), derives sustenance from It
and is pathogenic, although this potential is not always
expressed. In the medical field the term parasite is
traditionally restricted to parasitic eukaryotic organisms
belonging to the protozoa or metazoa (helminths,
arthropods, etc) (parasitism !, parasitoid !)
• Ectoparasite (G: ektos: outside, external): parasite of the
body surface of a host
• Endoparasite (G: endon: inside, internal): parasite living
within a host
• Facultative parasite (L: facu/tas: chance, opportunity):
organism with an occasional parasitic lifestyle; otherwise
free-living or commensalic (commensalism j)
0 Obligatory parasite (L: ob/igatus: obligatory): parasite
essentially depending on parasitism
• Opportunistic parasite (L: opportunus: suitable,
favourable): parasite which can make use of a favourable
21 . Glossary
opportunity (e.g. impaired immunity of a host) to infect
and harm a host
• Periodic parasite (G: periodos: recurrence): only particular
developmental stages are parasitic (e.g. mosquitoes: adult
females; permanent p. !)
• Permanent parasite (L: permanere: continue): all
developmental stages of a species are parasitic (e.g.
Sarcoptes mites) (periodic p. j)
• Phytoparasite (G: phyton: plant): parasite of plants
• Pseudoparaslte (G: pseudos: false): free-living organism
which Is found accidentally on or in a host
• Stationary parasite (L: stare: stand firm): the parasitic
developmental stages are present in or on a host
continuously
• Temporary parasite (L: tempus: time): the parasitic
developmental stages are present in or on a host for a
short time only
• Zooparaslte (G: zoon: animal, creature): parasite of animals
Parasltaemla (parasite t; G: haima: blood): presence of
parasites In blood, usually measured in percentage of
infected erythrocytes, leukocytes or number of parasites
per µI blood
Parasitism (parasite f): association between organisms of
different species in which one partner (parasite t) lives at
the expense of the other (host j). Parasites do not regularly
kill their hosts (compare parasitoid !) (commensalism t,
mutualism i, symbiosis !)
Parasitoid (parasite j; G: eides: like): parasite which kills
the host during its development (e.g. larvae of parasitic
Hymenoptera kill larvae of other insect species)
Parasitology (parasite f; G: logos; word, discourse): science
(phytoparasitology), animals (veterinary parasitology) and
humans (medical parasitology)
Parasltosis (parasite j; G: nosos: disease): an infection or
infestation, caused by parasites, regardless of whether it is
symptomatic (apparent j) or asymptomatic (unapparent !)
Paratenic host: host t
Paruterine organ (G: par: beside; L: uterus: uterus): in
Mesocestoidae capsule-like structure posterior to the
uterus to which eggs are passed; similar structures in
some other cestode groups
Pasture management: targeted use of pastures, taking into
account the demands of different animal species and
groups, stocking density, quantity and quality of pasture
forage, animal health care and profitability
Patency (L: patere: to open, lie open): time period after
prepatency !, during which parasite stages are detectable
in faeces, urine, body fluids, etc.
Pathogen (G: pathos: suffering, pain; L: generare: to procreate)
collective term for disease-causing organisms.
Pathogenesis (G: pathos: suffering, pain; genesis: procreation):
causes and development of pathological processes
Pathogenicity (G: pathos: suffering, pain; genesis: procreation):
capacity of a parasite species (or another pathogen) to
cause disease; within a species the degree of pathogenicity
may vary (virulence !)
 Part VIII. Appendix
Parthenogenesis (G: parthenos: virgin; genesis: procreation):
reproduction process with development of unfertilised
eggs into a new individual
Pellicle (L: pe//is: skin): in protozoans multi-layered cell cover
with underlying structures
Perforin (L: perforatus: perforated): cytolytic protein from
granules of cytotoxic (CD8+) T-cells
Peritreme (G: peri-: around; trema: hole): Sclerotised,
paired process associated with the stigma, especially in
mesostigmatid mites. Spiracle !, stigma !
Peroxisome (L: per: through; G: oxys: acid, soma: body):
. membrane-bound, small (~0.5-1.5 µm) cell organelles,
containing particular enzymes (such as katalases,
peroxidases)
Pesticide (L: pestis: plague; caedere: to cut down, smash):
chemical substances or biological agents for controlling
pests in the environment (herbicides, fungicides,
insecticides ; , molluscicides, etc.)
Phagocytosis (G: phagein: eat; kytos: cell, container): selective
ingestion of particles by a cell (plnocytosls !)
Phasmid (G: phasma: apparition): sensory organ, connected
with a gland, located behind the anus in Phasmldia, a
nematode group now called Secernentea
Pheromones (G: pherein: to carry; horman: to drive, to push):
ectohormones, secreted from glands to the environment
where they act as chemical signals (mostly species-specific)
for other individuals of the population; they play a role in
coordination of animal groups (e.g. aggregation hormones)
and in intersexual relationships (sexual hormones)
Phoresy (G: phoreus: carrier): transport of an organism by
temporary attachment to a host (e.g. mobile insect)
Phylogeny (G: phy/on: tribe; gennan: to create): evolution of
living organisms in general or of species, genera etc. in
course of earth history (ontogeny t)
Phylum (pl. phyla) (G: phy/on: tribe): main taxonomic category
In systematics l
Plnocytosls (G: plneln: to drink; kytos: cell): transport of
fluid into a cell by means of local lnvaglnation of the
cell membrane to form tiny vesicle around a droplet,
which is then taken Into the Interior of the cytoplasm
(phagocytosls t)
Polyphyletlc taxon (G: po/ys: many; phylon: tribe): group of
organisms of mixed evolutionary origin, not derived from
a common ancestor (monophyletic t)
Plasmodium (G: plasma: plasm): (a) multlnuclear cell, created
by repeated, mitotic divisions of nuclei without cell division
(])
C: (syncytlum l): (b) name of the protozoan genus Plasmodium
·c3
Plastld (G: p/astos: formed): membrane-bound cell organelles
of plants and algae, important for production and storage
of crucial substances; often containing pigments used in
�
co photosynthesis
C:
·c Polyxeny (G: po/ys: many; xenos: host): a parasite species
(])
which uses many different host species (euryxeny t,
-� oligoxeny t)
>, Population (L: populus: people): whole of individuals of a
0)
0 particular species within a defined habitat t of taeniid cestodes (metacestode j)
0
Postpatency (L: post: after; patency t): time period after
·u5
co patency in which the parasite infection still persists, but
co
a..
parasite stages are no longer detectable in diagnostic
samples (patency ; , prepatency l)
Predator (L: praedator. robber, plunderer): animal depending
on living animal prey
Predilection site (L: praedi/ectus: beloved): preferred location
of a parasite on or in a host, e.g. liver
Prenatal (L: prae: before; natus: birth): previous to birth
(transmission routes !)
Prepatency (= prepatent period) (L: prae: before; patency j):
time period between infection of a host by a parasite and
first release of products of reproduction (oocysts, eggs,
larvae, etc.) in faeces, urine, skin or body fluids (blood,
etc.) (patency j postpatency ; , incubation j)
Prevalence (L: praeva/ere: prevail): number of infected or
diseased individuals at a defined point or period of time,
related to the number of individuals examined (usually
expressed as a percentage (incidence i)
Prevention (L: praevenire: to precede, anticipate): measures
to maintain or Improve health (e.g. species-appropriate
husbandry, adequate stables, stable climate, diet, etc.), and
to prevent or reduce health risks (information, legislation,
screening, herd surveillance). There are overlaps between
the terms prevention and prophylaxis !
Proglottis (pl. proglottides) (G: pro: before; glotta: tongue):
segment of cestode stroblla !
Prokaryote (L: pro: before; G: karyon: nucleus): unicellular
organisms without a membrane-bound nucleus
(eukaryote j)
Promastigote (L: pro: before; G: mastix: whip): stage
of Trypanosomatidae with kinetoplast and origin of
the flagellum anterior to the nucleus (amastigotej,
epimastigote l, trypomastigote !)
Prophylaxis (L: pro: before; G: phylax: guard): protection of
humans or animals from infections or diseases through
measures of hygiene, chemoprophylaxls f, metaphylaxis f,
vaccination, etc. (prevention t)
Proterosoma (G: proteros: anterior; soma: body): first and
second body section (gnathosoma ; + propodosoma) of
Acar (mites and ticks) (hysterosoma f, ldlosoma i)
Protozoa (G: protos: the first, the earliest; zoon: animal,
creature): diverse group of mostly motile, unicellular
eukaryotlc microorganisms. Current classification assigns
the Protozoa to several 'supergroups' (Amoebozoa,
Excavata, and SAR [Stramenoplles, Alveolata, RhlzariaD
and considers the term 'Protozoa' as a collective name
without phylogenetic and taxonomic significance. However,
this term is still used for practical reasons
Protonephridla (G: protos: the first, the earliest; nephros:
kidney): excretory organs of platyhelminthes and other
invertebrates
Protonymph (G: protos: the first, the earliest; nymphe:
girt, bride): first (8-legged) nymph of mites (not of ticks)
(deutonymph f, tritonymph !)
Protoscolex (pl. -laces) (G: protos: the first, the earliest; sko/ex:
worm): juvenile scolex (!) formed in the metacestode stage
Pseudocoel (G: pseudes: false; koilia: hallow): body cavity
without lining with mesodermal epithelium (coelom f)
Pseudoparasite: parasite l

. Pulvillus (pl. pulvilli) (L: pulvil/us: little pillow): cushion-like
adhesive structure on pretarsus of some genera of mites
a are detected by a test in a population and described as
Quarantine (I: quaranta giorni: 40 days, first used in Venice
in the 14th century in defence against plague). Measure
to separate and restrict movement of animals or persons
who may possibly have been exposed to a communicable
disease
R fertile offspring. Since these criteria are difficult to verify
Aecidive (L: recidere: to relapse): recurrence of disease after
an asymptomatic period (recrudescence t)
Recrudescence(L: recrudescere: become worse): worsening
of a disease (recidive !)
Redia (Francesco Redi, Ital. physician, 1626-1698): larval
stage of dlgenetlc trematodes formed from germ balls in
sporocysts !
Re-infection: infection j
Repellent (L: repel/ere: drive back): chemical substance to
keep away parasites or other organisms, e.g. arthropods,
from animals (attractant t)
Residual drug efficacy: antiparasitic drugs t
Resistance (L: resistant/a: resistance): (a) natural resistance:
genetically determined, innate antigen-independent
defence mechanism of hosts against infections/
infestations, usually partial resistance(complete resistance
= unsusceptibiiity !); (b) resistance of organisms (parasite
eggs, larvae, etc.) against environmental factors(tenacity !);
(c) resistance of parasites or other agents against drugs
(drug resistance j)
Rhoptries (G: rophalon: club): club-shaped organelles,
constituents of the apical complex in zoites of Apicomplexa;
involved in cell invasion
Rostellum (L: roste//um: small beak): muscular organ of various
shapes, at scolex of cestodes, invaginable or not, often
bearing spines (scolex !)
s containing sporozoites
Safety index: (L: indicare: to indicate): Index for tolerability of
antiparasitic drugs: ratio of the maximum tolerated single
dose (which does not cause adverse effects) to a single
recommended therapeutic dose
Saprophage (G: sapros: rotten; phagein: to eat): organisms
living on decaying or rotting organic material
Schizogony (= merogony) G: schizein: to split; goneia:
procreation): process of multiple divisions in which a
protozoan mother cell (schizont) divides usually into many
daughter cells (merogony t, schizont !, sporogony !)
Schizont (= meront) (G: schizein: to split): protozoan cell
undergoing schizogony (= merogony) by asexual
reproduction involving multiple mitoses (schizogony i)
Scolex (G: sko/ex: worm): unsegmented, anterior part (head)
of a cestode, bearing holdfast organs (protoscolex t)
Scutum (L: scutum: shield): plate on the dorsal surface of hard
ticks (lxodidae), also called dorsal shield, covering about
1 /3 of the anterior surface of females, larvae and nymphs
and the entire surface of males (alloscutum t)
Secondary infection: infection t
21. Glossary
Sensillum (L: sensus: sense, feeling): sensory organ
Sensitivity (L: sens/bi/is: sensible): diagnostic sensitivity is
defined as the proportion of infected individuals that
'positive' (= proportion of correct diagnoses)(specificity !)
Sheath: cuticle not discarded after moulting, remaining on a
nematode larva (ecdysis j)
Species (L: species: species j): basic category (taxon !) of
systematics. Usually defined as a group of organisms
that can interbreed in natural populations and produce
in some groups of parasites (e.g. protozoa, helminths)
species characterisation is complementarily based on
genomic features
Specificity (L; spec/osus: plausible, presentable): diagnostic
specificity is defined as the proportion of uninfected
reference Individuals that test 'negative' in an assay (=
correct negative diagnoses), Sp. is high tf an assay detects
a high proportion of individuals Infected with a defined
parasite species and discriminates between uninfected
Individuals and those Infected with one or several other
parasite species (sensitivity f)
Splcula (sgl. -um) (L: splculum: sting, arrow): crescentric
or tube-like, protrudable and retractable structures of
nematode males, located in pouches of the cloacal region,
involved in sperm transfer during copulation
Spiracle: (L: spirare: to breath): external opening of the tracheal
system in insects
Sporadic: occurrence t
Spore (G: spora: seed): term for very different cyst-like
'Dauerstages' (t) of Protozoa, Microsporidia, Myxozoa,
Bacteria, etc.
Sporoblast (G: spora: seed; b/astos: germ): stage in
sporogony !
Sporogony (G: spora: seed; gonos: offspring): phase in life
cycle of Apicomplexa in which a zygote(= sporont) divides
first into sporoblastst and then into haploid sporozoites !
Sporocyst(G: spora: seed; kystls: bladder): (a) Coccidia: cyst,
!, located within an oocystt; (b)
Digenea (Trematoda): motile 'germinal sac', containing
germinal cells which produce daughter sporocysts or
rediae t
Sporokinete (G: spora: seed; kinein: to move): mostly ciub­
shaped, motile stages with apical complex t, formed in
a vector by protozoans of the genus Babesia and some
adeleidean coccidia during sporogony t Q)
Sporont (G: spora: seed): sporogony t C
Sporozoa (G: spora: seed; zoon: animal, creature): previous :Q
"D
Q)
name of the taxon Apicomplexa
Sporozoite (G: spora: seed; zoon: animal, creature): last,
infective stage of sporogony t, mostly uninuclear, cu
C
·;::
elongated cells with apical complex, infective for a new Q)
host (merozoite t)
Stenoxeny (G: stenos: narrow; xenos: host): narrow host C
spectrum(host specificity t) >.
0)
Sterile insect technique (SIT): method for self-destruction of 0
0
populations of an insect species through mass release of
·u5
cu
males of the same species which had been sterilised by
cu
y-rays or by other means(e.g. chemical treatment) CL
 Part VIII. Appendix
Sterilisation (L: steri/is: sterile): killing of all microorganisms
(pathogenic and apathogenic), including spores, on
objects, products, fluids, etc. (e.g. surgical instruments)
(disinfection t, decontamination t)
Stigma: (G: stigma: mark): external opening of the tracheal
system in ticks and mites, can be surrounded by a stigmata!
plate (spiracle t)
Strain: subpopulation of a pathogen species with defined
genomic or other features (e.g. drug resistant nematode
strains) (genotype t, isolate t)
Strategic control: control t
Strobila (pl. strobilae) (G: strobi/os: roundabout; refers to pine
cone-like stages of polyps multiplying by asexual division
transversely to the longitudinal axis): chain of proglottids t
in cestodes
Subtropics (G: tropikos: tropic): geographic region between
the tropics ! and the 38 ° parallel in both the northern and
southern hemisphere (tropics !)
Susceptibility (L: suscipere: to accept, receive): capability of
a host to provide suitable living conditions for a certain
parasite species (resistance !, unsusceptibllity !)
Superinfection: infection t
Symbiosis (G: sym- together; bios: life): persistent association
(often with physical attachment) between organisms of
different species where both partners (symbiont and host)
are physiologically complementary and entirely dependent
on each other (commensalism t, mutualism t, parasitism t)
Sympatry (G: sym-, syn-: together; L: patria: native country):
occurrence of two or more species In the same environment
(geographic region, habitat)
Symptomatic therapy: therapy !
Synanthropic (G: syn-: together; anthropos: man): associated
with humans (transmission cycles !)
Synbovine (G: syn-: together; L: bos: cattle): associated with
cattle
Syncytlum (G: syn-: together; kytos: cell, container):
multinuclear cell complex without Inner cell borders,
formed by fusion of several cells or lack of cell divisions
Syngamy (G: syn-: together; gamos: marriage): union of male
and female gametes following fertilisation to form a zygote
Systematics (G: systematlkos: classified, ordered): discipline
of biology which describes and discriminates various
organisms and assigns the identified, related groups
(taxa !) to a hierarchic system which should reflect
phylogenetic relationships
Q)
C T
·u Tachyzoite (= endozoite): zoite ! of Apicomplexa, undergoing
'6
Q)
quick asexual reproduction in a host cell (bradyzolte t)
c
cu
Tagma (pl. tagmata) (G: tagma: arrangement): group of
C segments forming functional body units in arthropods
·c
Q) (head, thorax, abdomen)
Taxis (G: taxis: arrangement): movement of a motile cell or
C organism directed to the source of a stimulus (= positive
>, taxis) or into opposite direction (= negative taxis), e.g.
0)
0 chemotaxis, phototaxis, thigmotaxis
0
Taxon (pl. taxa) (G: taxis: rank of order): a group of organisms
·u5
sufficiently distinct to merit being distinguished from other
cu
a..
groups and assigned to particular categories (e.g. species,
genus, family, etc.) (taxonomy !)
Taxonomy (G: taxis: rank of order; G: nomos: law): assignment
of organisms to a taxon t, based on distinct morphological,
biological, genomic or other features
Telamon (G: telamonios: strap): accessory copulatory organ
of the cloacal wall in some nematodes (strongyles)
Tenacity (L: tenacitas: to grasp, holding on a thing): resistance
of pathogen stages against environmental factors
(temperature, dryness, etc.)
T herapy (G: therapeia: cure): measures to cure or relieve
illnesses:
• Causal therapy (L: causa: cause): treatment directed
against the cause of the disease, i.e. agents of infection
• Palliative (= symptomatic) therapy (L: pal/ium: cover):
measures directed against disease symptoms
Toxin (G: toxikon: poison): term for any substance poisonous
to an organism. In the medical field often restricted to
substances produced by living organisms (e.g. bacteria,
fungi, animals, plants) with specific toxic and antigenic
properties (e.g. Botulinus toxin, snake, spider, bee toxins)
Translocatlon: epidemiological term for the dispersal of
nematode larvae on pasture
Transmission cycles: transmission cycles related to various
epidemiological situations:
• Domestic cycle (L: domus: house): domestic animals
involved as parasite hosts
• Intermediary cycle (L: intermedius: between): domestic
and wild animals involved as hosts
• Rural cycle (L: rus: country, farm): cycle in rural areas
e Silvatic cycle (L: si/va: wood, forest): cycle involving only
wild animal hosts
• Synanthropic cycle (G: syn-: together; anthropos: man):
cycle in the vicinity of humans, often influenced by
anthropogenic factors. Domestic and wild animals can
be Involved as hosts
• Urban cycle (L: urbs: city): cycle In urban areas
• WIidiife cycle: = sllvatlc cycle t
Transmission modes (Infection t)
• Acyclic transmission (= mechanical transmission):
transmission of a pathogen by a vector without biological
changes of the pathogen (cyclic transmission !)
• Cyclic transmission (= biological transmission):
transmission of a pathogen by a vector with biological
changes (differentiation, multiplication, reproduction) of
the pathogen in the vector (acyclic transmission j)
• Direct transmission: without involvement of an
intermediate or paratenic host (host t)
•
Indirect transmission: with involvement of an intermediate
or paratenlc host (host j)
Transmission routes: routes (selection) of pathogen
transmission to hosts:
• Airborne transmission: spread of pathogens by droplets
or dust through air
• Arthropod-borne transmission: pathogen transmission
by arthropods
• Alimentary transmission (L: alimentum: food): pathogen
transmission through ingestion of contaminated food

• Contact transmission (l. contigere: to touch): direct
transmission through contact between parasite carriers
and other hosts (e.g. Sarcoptes mites)
• Contaminative transmission (L: contaminatus: blotted,
dirty): transmission via excreta (e.g. faeces, urine) or
secretions of infected hosts or vectors
• Endogenous transmission (G: endon: inside): spread of
infection within the same host (autoinfection t)
• Faeco-oral transmission: transfer of pathogens from
faeces directly or through contaminated materials to the
mouth of a host
• Horizontal transmission: transmission between
individuals of the same generation (vertical transmission !).
• Iatrogenic transmission (G: latros: physician): transmission
by physicians or veterinarians, e.g. through contaminated
injection needles
• Inoculative transmission (L: lnoculare: to Implant):
transmission of infective stages to a host by bite of a vector
• Lactogenlc transmission (L: lac: milk): transmission via
milk (form of vertical transmission)
• Percutaneous transmission (L: cutis: skin): infection
through the skin
• Peroral (= oral) transmission (L: per. through; os: mouth):
infection through the mouth
Prenatal transmission (L: prae: before; natus: birth):
pathogen transmission before birth
• Transmammary transmission (L: mamma: udder):
infection via the mammary gland, corresponds to
lactogenic infection t
• Transovarial transmission (L: ovum: egg): transmission
of pathogens via eggs to the next generation
• Transplacental transmission (G: dia: through; L: placenta:
placenta, cake): transmission of pathogens through the
placenta barrier
• Transstadial transmission: transmission of pathogens
between subsequent stages of a vector (e.g. In ticks:
nymph -+ adult)
• Vertical transmission (L: vertex: peak, top): transfer of
pathogens from one host generation to the following
generation
Treatment:
• Targeted selective treatment (TSTI: only those animals
of a grazing group that are particularly vulnerable or
epidemiologically important are treated in a strategic
control programme
• Targeted treatment (TTI: strategic treatment of a whole
group of animals (t control, t TST)
Tritonymph (G: tritos: third; G: nymphe: girl, bride): third and
last nymphal stage in mites (not in ticks). Many parasitic
Acari have lost the second stage (deutonymph t); therefore
the first and third stages are called protonymph t and
tritonymph, respectively
Tropics (G: tropikos: tropic): geographic region surrounding
the equator between the 23 ° parallels of the northern and
southern hemisphere (subtropics j)
Trophe (G: trophe: food): nutritive fluid in cysts of Sarcocystis
Trophozoite (G: trophe: food; zoein: to live): active feeding
stage of Protozoa
21. Glossary
Trypomastlgote (G: trypanon: drill; mastix: whip): stage of
Trypanosomatidae with kinetoplast and origin of the
flagellum located posterior to the nucleus (amastigote t,
epimastigote j, promastigote t)
u
Unapparent (L: in-: not; apparere: appear, be visible): =
asymptomatic f
Unsusceptlbillty: property of a host species which does not
provide suitable living conditions for a particular parasite
species (resistance f. susceptibility t)
V
Vaccine (L: vaooa: cow): liquid that contains antigens t which
stimulate specific immune responses in vertebrate hosts
after parenteral or oral application
• Attenuated vaccine: containing live pathogens having
lost their virulence but retained their capability to induce
protective Immunity
• DNA vaccine: containing DNA sequences that code for
immunogenic proteins and are enclosed in appropriately
constructed plasmids
• Inactivated (= dead) vaccine: prepared from dead
pathogens
• Live vaccine: containing live pathogens
•· Recombinant vaccine: containing recombinant antigen(s)
(antigen t)
• Subunit vaccine: containing only specific antigens of an
infectious agent, either Isolated from the agent or produced
as recombinant antigen (antigen t)
Variant: strain t
Vector (L: vector. one that transports, carrier): arthropod or
other organism that transmits a pathogen from an infected
organism (or its wastes and surroundings) to uninfected
Individuals:
• Active vector: active transmission, for example by bite
of the vector
• Passive vector: transmission occurs in a passive manner,
e.g. by ingestion of a vector containing a pathogen by a
host
Vein of Insect wings: tubes with haemolymph or solid
structures supporting the wings of insects
Vivipary (L: vivus: living; parere: to give birth): females give
birth to living larvae (ovovivipary j)
Virulence (L: virulentus: full of poison): the relative ability of a
pathogen to cause disease, corresponding to degree of
pathogenicity t
w
Warble: swelling of skin caused by a larva of warble fly
(Hypoderma spp.)
Withdrawal (= withholding period): interval between
application of an antiparasitic drug to animals and the
officially permitted use of food products originating from
treated animals (tissues, milk, eggs) for human consumption
 Part VIII. Appendix

z
Zoite (G: zoein: to live): collective term for mostly mobile stages
of Apicomplexa and Ciliata (sporozoite j, merozoite i,
endozoite j, cystozoite t, trophozoite t, etc.)
Zoonosis (G: zoon: animal; nosos: disease): infectious
diseases the agents of which are transmissible under
natural conditions between vertebrate animals and humans
Zygote (G: zygotos: connected, conjunct): diploid cell, emerges
from fusion of two haploid gametes t

- Selected references c=====:.i:::::::i

Basinger Maggenti MA, Maggenti, A., Gardner SL (ed.)
(2005) Online dictionary of invertebrate zoology. Available
at: http://digitalcommons.unl.edu/onlinedictinvertzoology/2.
Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997)
Parasitology meets ecology on its own terms: Margolis et
al.: revisited. J Parasitol 83: 575-583.
Gordh G, Headrick D (2001) A dictionary of entomology.
Wallingford, UK: GABI Publishing; ISBN 0-85199-291-9.
Hiepe T, Lucius R, Gottstein B (eds.) (2006) Lehrbuch der
Allgemeinen Parasitologie. Stuttgart, Germany: Paray; ISBN
3-8304-4101-0.
Mack R (1988) Dictionary for veterinary science and biosciences.
Berlin, Germany: Paul Parey Scientific Publishers; ISBN 3-489
50516-6.
Mehlhorn H (ed.) (2008) Encyclopedia of parasitology 3rd ed.
Berlin, Germany: Springer. ISBN: 978-3-540-48997-9.
Sangster NC, Pope SE (2000) Quid slgnificat nomen? (What's
in a name?). Int J Parasitol 30: 231-238.
The American Heritage Medlcal Dictionary. Available at:
http://www.dictlonary.reference.com/medical.
Wehner R, Gehring W (2013) Zoologie. 25th ed. Stuttgart,
Germany: Thieme; ISBN 978-3-13-367•4 25·6
Wall R, Shearer D (2001) Veterinary ectoparasltes. 2nd ed.
Oxford, UK: Blackwell Science; ISBN 0·632·05618·5.
Werner FCL ( 1972) Wort elemente tatelnlsch-grlechlscher
FachausdrOcke In den blologlscllen Wlssanschalten. Leipzig,
Germany: Suhri<amp; ISBN 978-3-518-36564-9.

Q)
C
·u
'6
Q)

C
·c
Q)

C
>,
O>
0

·u;
22. Graphics and sources of pictures
Graphics that are marked with IPZ were designed by
J. Eckert and P. Deplazes and drawn by Salome Ehrat
(c/o IPZ), Marianne Mathys, Anne Seeger, Jeanne Peter
or Sandra Amrein (VetCom, Vetsuisse Faculty, Zurich,
Switzerland).
Sources of pictures
We are indebted to the following persons, institutions
or publishers who generously provided pictures and
the printing permission (some images were slightly
modified or relabelled):
Prof. Dr. A. Aeschlimann, Unlverslte de Neuchatel: see 'Nallonale
Akademie der Wlssenschaften'.
Dr. G. Buscher, Basel, Switzerland: Figures 5.27, 5.28.
Prof. Dr. H.C.E. Cortes, Laborat6rlo de Parasitologia, ICAAM,
Nucleo da Mitra. Universldade de �vora, Portugal: Figure
5.14.
Dr. J.-C. Delecolle and Prof. E. Gandolfi, lnstitut de Parasitologle
et de Pathologie Tropicale, Strasbourg, France: Figure 14.43.
Dr. J.P. Dubey, USDA, Animal Parasitic Diseases Laboratory,
Beltsville, MD 20705-2350, USA: Figure 5.11.
Eckert J, Braun R, Shirley MW, Coudert P (eds.). Guidelines on
Techniques in Coccidiosis Research, pp. 103-119. COST
89/820, 1995. European Commission. Directorate-General
XII: Science, Research and Development. Agriculture
Biotechnology. L-2920 Luxembourg, Luxembourg. ISBN
92-827-4970-3: Figure 16.9.
Greenberg B (ed.). Flies and disease, Vol. I, 1971 (Copyright
holder, Department of Biological Sciences, University of
Illinois, Chicago, IL, USA), with permission by Princeton
University Press, Princeton, NJ, USA: Figures 14.51, 14.56.
Prof. Dr. M. Hess, Klinische Abteilung fur Geflugelmedizin,
Veterinarmedizinische Universitat, Wien, Austria: Figure 3.1a.
Dr. G.W. Hutchinson, Elderslie, NSW, Australia: Figure 10.81.
IPB: lnstitut fur Parasitologie, Vetsuisse-Fakult/:it, Unlversit/:it
Bern, Bern, Switzerland (Prof. Dr. B. Gottstein): Figure 3.2.
IPG: lnstitut fur Parasitologie, Justus-Liebig Universiti:it, Giessen,
Germany (Prof. Dr. Anja Taubert): Figures 10.14b, 10.61,
10.71, 10.72, 10.77, 10.79, 14.30b.
IPH: lnstitut fur Parasitologie, Stiftung T ierarztliche Hochschule,
Hannover, Germany (Prof. Dr. T. Schnieder, Prof. Dr. C.
Strube): Figures 5.4, 5.6, 5.9b, 5.21e, f, 5.23b, 5.30, 7.4,
9.39, 9.44a, 9.45c, 9.46a, 10.59, 10.66, 14.8, 14.10c,
14.16a, 14.26b, 14.62a, 14.64a, 14.66.
IPZ: lnstitut fur Parasitologie, Vetsuisse-Fakultat, Universitat
Zurich, Zurich, Switzerland (Prof. Dr. P. Deplazes): all images
marked with IPZ.
ITPB: lnstitut fur Parasitologie und Tropenveterinarmedizin, Freie
Universitat Berlin, Berlin, Germany (Prof. Dr. Georg von
Samson-Himmelstjerna): Figures 5.21a-d, g, h.
ITPM: lnstitut fOr vergl. Tropenmedizin und Parasitologie,
Universitat Munchen, Munchen, Germany (Prof. Dr. K. Pfister):
Figure 10.14a.
Kuhn Fachverlag GmbH & Co. KG, 78054 Villingen-Schwenningen,
Germany (H.-U. Ziegler): from Hilbrich, P.: Krankheiten des
Geflugels unter besonderer Berucksichtigung der Haltung
und Futterung. 3. Aull. Hermann Kuhn GmbH & Co. KG,
Vllllngen-Schwenningen, 1978, and Mrs. Renate Kind
(Hllbrich), GroBburgwedel, Germany: Figures 5.7, 9.41b.
Prof. A. Latif, Parasites, vectors and vector-borne diseases,
Onderstepoort Veterinary Institute, Faculty of Veterinary
Science, University of Pretoria, Onderstepoort, South Africa:
Figures 4.Sb, 5.26.
Dr. G. Liebisch, Zecklab, Burgwedel, Germany: Figures 14.26c,
14.39, 14.46a, b, 14.47, 14.53a, b, 14.54b, 14.57.
Prof. Dr. H. Mehlhorn, lnstitut fur Zoomorphologie, Zellbiologie
und Parasitologie, Universiti:it Dusseldorf, Germany: Figures
1.1, 4.8, 5.23a, 5.25a, 9.32e, 14.40, 14.49c.
Nationale Akademie der Wissenschaften Leopoldina, Halle (Saale),
Germany (Dr. M. Kaasch): aus: A. Aeschlimann (1996):
Zecken als Vektoren unter besonderer Berucksichtigung
der Spirochaten. Nova Acta Leopoldina NF 71: Nr. 292,
11-25: Figures 14.3, 14.4.
Dr. T.J. Naucke, Parasitus Ex e. V., Niederkassel, Germany:
Figure 14.38b.
Novartis Firmenarchiv, Novartis AG, Basel, Switzerland: Figures
14.148-c.
Prof. Dr. J. Pohlenz; with permission by Friederike Pohlenz, Bern,
Switzerland: Figure 5.19.
Prof. Dr. A. Pospischil, lnstitut fur Veterinarpathologie, Vetsuisse­
Fakulti:it, Universit/:it Zurich, Zurich, Switzerland: Figure 7.3a.
Dr. N. Taira, Kyushu Research Station, National Institute of Animal
Health, Kagoshima, Japan: Figures 9.44c, 10.7.
Dr. K. Tomczuk, Zaklad Parazitologii i Chor6b lnwazyjnych, Wydz.
Med. Wet. Lublin, Polen: Figures 9.40a, b, 10.15.
Prof. Dr. P. Torgerson, Veterinar-Epidemiologie, Vetsuisse-Fakultat,
Universitat Zurich, Zurich, Switzerland: Figure 10.76.
Dr. U. Wree und E. Riedel, Beratungsring fur Schafhalter e. V.,
Blekendorf, Germany: Figures 14.24a, b.
 23. Index

agar plate method 532 - caninum 281, 282

A
Alaria 169 - ceylanicum 285
abamectin 558,561
- alata 200 - duodenale 285
abortion 55,11 0, 112, 113, 115, 117,
- americana 201 - tubaeforme 282
120,159
alariosis (zoonosis) 51O Ancylostomatidae 170,280
Acanthamoeba 46, 153
albendazole 560,561, 579, 585 ancylostomosis (zoonosis) 284, 512
- culbertsoni 153
alkylphosphocholines 562 - in carnivores 281
Acanthocephala 172
Allodermanyssus Angiostrongylldae 171, 320
Acanthocephalus 384
- sanguineus 422 angiostrongylosis (zoonosis) 512
Acanthocheilonema 171,353,362
allopurlnol 76, 562, 599 - in dogs and other canids 320
- reconditum 358, 362
alternation of generations 1 74, 259 Angiostrongylus 171, 320
acarapiosis 434,613
alveolar echinococcosis 225 - vasorum 320
Acarapis 393,434
Alveolata 44, 45, 79 Anguillicola 171, 346
- cerana 434
Amandibulata 393, 395 animal African trypanosomosis
- woodi 434
Amblphrya 45, 150 See: trypanosomosis, African
Acari 393
Amblycera (chewing lice) 394, 450 (animal)
- mites s.l. 395
Amblyomma 393, 415 Animalia 169, 393
Acaridae 393, 448
- americanum 397, 415 animal welfare legislation 566
acaridiosis in poultry 342
- cajennense 397, 415 Anisakidae 171, 339
Acarus 393
- hebraeum 397, 415 anisakldosis (zoonosis) 339, 512
- siro 448
- maculatum 415 Anisakis 171
acid
- pomposum 415 - physeteris 339
- formic 558
- variegatum 397, 415 - simplex 339
- lactic 558
amidines 558 anisogamy 79
- organic 558, 613
Amidostomatidae 170, 303 Anisus 188
- oxalic 558
amidostomosis 303 Anncaliia 46, 161
Acuaria 171
Amidostomum 170 Annelida 387
Acuariidae 171,347
- acutum 303 Anocentor 393
ADCC reactions 32
- anseris 303 Anopheles 394
Adeleida 45, 81
amlno-acetonltrlle derivatives 561 - clavlger 460
Adenophorea 172,258, 368
amltraz 558, 602,603 - macullpennls 460
adhesive tape method 525, 533
amoebae 151 - messeae 460
Aedes 394
amoebic dysentery 151 - plumbeus 460
- aegypti 462, 463
Amoebotaenla 170,220 Anoplocephala 170
- albopictus 460
Amoebozoa 44, 46,151 - glgantea 215
- cantans 460
amphlbla 47, 48, 51, 54, 69, 123, 125, - gorillas 215
- cinereus 460
153, 164, 188, 191 - magna 215,218
- communls 460
Amphistomida 169, 188 - manubriata 215
- genlculatus 460
Q)
T5
C amprolium 562 - perfollata 215,218
- japonlcus 460
anabiosis 258 Anoplocephalldae 170, 215
'5 - punctor 460
Q)
Analgidae 393, 448 Anoplura (sucking lice) 394, 453
- rossicus 460
anaplasmoses 409 antelopes 202
- stlctlcus 460
co
C Anaticola 394, 451 anthelmintics 559, 585
·c - vexans 460
Q) Anatoecus 394, 451 antibody dependent cellular cytotoxicity
aelurostrongytosis In cats 322
Anatrichosoma 172, 375 See: ADCC
C
Aelurostrongylus 171, 322
- buccalis 375 anticoccidials 89, 562
>, - abstrusus 322
0) - cutaneum 375 antigenic variation 65
0 Aethina tumida 457
0 anatrichosomosis antigen shedding 37
·wco afoxolaner 558, 603
- in monkeys 375 antimony compounds 562
African Horse Sickness virus 471
co
a.. Agamodistomum suis See: Alaria alata
Ancytostoma 170 antiparasitics 557, 576
 23. Index

- anthelmintics 559, 585 Armillifer 389 - bovis 131

» cattle (table) 579 armilliferosis (zoonosis) 514 - caballi 131,137
» dogs, cats (table) 600 arrested development 258 - canis 131,137
• poultry (table) 611 Arthropoda 392 - capreoli 131,137
» sheep, goats (table) 585 - classification 393 - conradae 131
- antiprotozoals 559 - general aspects 392 - divergens 131,135,137
» dogs, cats (table) 599 arthropods as vectors - felis 131
» (table) 562 - beetles 457 - gibsoni 131,138
- combination products, dogs, cats - Blattaria (cockroaches) 449 - jakimovi 137
(table) 601 - Ceratopogonidae 470 - major 131, 136
- ectocides 557 - Culicidae 462 - mlcroti 131
• cattle, sheep 583 - Drosophilidae 475 - motasl 131, 137
• dogs, cats (table) 602 - fleas 604 - ovis 131
» (table) 558 - flies 478 - rossi 131, 138
- honey bees 613 - Phlebotomlnae 464 - venatorum 131, 137
- horses (table) 592 - Slmullldae 469 - vogeli 131,138
- insect growth regulators 557,559 - Tabanidae 474 - vulpes 131,138
- in'traruminal boli, cattle 581 - ticks 403,409 Babeslldae 45,129
- mode of action 558,562 Ascarldla 171, 342 babesiosis (zoonosis) 129,411, 509
- nematocides (table) 561 - columbae 342 - In cattle 135
- off-label use 576 - disslmllls 342 - In dogs and other carnivores 137
- pigs (table) 589 - gall! 342 - In equids 137
- rabbits (table) 607 Ascaridida 171, 326 - in rodents 139
- repellents 557 ascarlds 326 - in sheep and goats 136
» (table) 559 ascariosis (zoonosis) 512 - in wild ruminants 137
- resistance See: drug resistance - in swine 327 Bacillus thuringiensis 468,567
- tolerability 557 Ascaris 171 Baermann technique 530
- trade names 615 - lumbricoides 327 Balamuthia 46, 153
- trematocides and cestocides (table) - suum 327 - mandrillis 153
560 Ascarops 171,347 Balantidiidae 45, 147
ants 191, 192, 193 Asiatica taeniosis 230 balantidiosis (zoonosis) 509
Aonchotheca 172 Asplculurls 171 - in pigs and other mammals 147
- bursata 372 - tetraptera 345 Balantldium 45
- caudinflata 372 Aspldobothrli See: Aspldogastrea - coli 147
- putoril 373 Aspldogastrea 169, 173 Barbervax 569
Apatemon 169 Astlgmata 393, 435 Baruscapillaria 172
- gracilis 201 Atractldae 171 - obsignata 372
Aphasmidia 172, 368 Atrlchopogon lutelcollls 469 baylisascariosis in carnivores 333
Apicomplexa 45, 79 Auchmeromya senegalensis 488 Baylisascaris 171
Apiosoma 45, 150 Austrobilharzla 169, 205 - procyonis 333
Apodemus 214 Austroconops 394, 469 beetles See: Coleoptera
Apophallus 169,197 Austropeplea 179 bendiocarb 558
- donicus 199 Austrosimulium 394,465 benzimidazoles 560,561
Aproctella 171, 366 autecology 16 benznidazole 71
Apteragia 170,300 avermectins 558,561 Bertiella 170
Arachnida 393,395 Avioserpens 171 - mucronata 215
Archaeopsylla 394 Avitellina 170 - studeri 215
- erinacei 501 - centripunctata 215 Besnoitia 45, 98,115
arecoline 245 - akodoni 115
Argas 393,416 - benetti 115
- persicus 397,418
B - besnoiti 115
Babesia 45,129
- reflexus 397, 416 - caprae 115
- annae 131, 138
Argasidae (soft ticks) 393, 397, 415 - darlingi 115
- bigemina 131,136
Argulus 449 - jellisoni 115
 Part VIII. Appendix

- neotomofelis 115 - trigonocephalum 285 Carios 393

- oryctofelisi 115 buparvaquone 145,562 - capensis 397
- tarandi 115 Buxtonella 45,149 carnidazole 562
- wallacei 115 - sulcata 149 carps 167
besnoitiosis 115 Caryophyllaeus 208
Bidentostomum 170,266 C Caryospora 45
Bilharziella 169 Caballonema 170,266 cathepsins 180
- polonica 202 Caenorhabditis 170 cat parasitoses of organ systems 597
Bilharziellinae 202 - elegans 19,23,259 cattle parasitoses of organ systems
bilharziosis 201 Calicophoron 169 576
bioactive fodder plants 567 - daubneyi 188 CD4+ T cells 32
biocoenoses 16, 23 - microbothrlum 188 Centramoebida 46, 153
bison 185 Calliphora Cephalobaena 389
Bithynia 197 - vlcina 484 Cephalobldae 170
biting midges See: Ceratopogonidae - vomitorla 484 Cephenemyia 394, 490
black fly plague 465 Calliphoridae (blow flies) 394,483 - auribarbis 490
blackhead disease 52 Callitroga americana 488 - stimulator 490
Blatta 394 Calodium 172 Ceratophyllidae 394, 501
- orientalis 449 - hepaticum 373 Ceratophyllus 394
Blattaria 384 Caloglyphus 393 - gallinae 501,503
Blattaria (cockroaches) 394,449 - berlesi 448 Ceratopogonidae (biting midges) 394,
Blattella 386,394 Camallanidae 171 469
- germanica 449 Camallanina 171, 346 Ceratozetldae 393
blow flies See: Calliphoridae Camallanus 171 cercaria 174, 178
blow fly strike 484 camelids 60, 61,64,65,66,67,100, cercarial dermatitis (zoonosis) 200, 205,
Bluetongue virus 471 109,123,176,184,192,194,195, 510
Bodonidae 45,78 202,241,390 Cercomeromorpha 169, 205
Boophilus 393,413 See Campanulotes 394,451 Cercomonas 56
also: Rhipicephalus Canileish 76,569 Cercopithifilaria 171
borrelioses 411 Capillaria 172 - bainae 362
bot flies See: Oestrinae - aerophlla 373 - grass! 362
Bothriocephalus 170,208 - anatis 372 Cestoda 170
Bovicola 394, 451 - annulata 372 - Cyclophyllida 212
Bovilis Dictol 569 - boehml 373 - life cycle 207
Brachiola 161 - bovls 373 - properties 206
Brachycera (flies) 394,4 72 - bursata 372 - Pseudophylllda 208
brain worm 191, 193 - caudlnflata 372 Chabertla 170
Braula 394 - columbae 372 - ovina 275
- caeca 426,474 - contorta 372 Chabertiidae 170, 275
Bronchostrongylus 318 - hepatica 373 Chabertiosls 275
Brugia 171,353 - in mammals 373 chagas disease See: trypanosomosis,
Bt toxins 567 - in poultry and other birds 371 American (human)
Q)
C Buetschliidae 45 - longipes 373 chamois 194, 215
·5 buffalo 66,67,71,91,100,118,135, - mustelorum 373 Chandlerella 171, 366
Q)
136,141, 143,176,184,185,188, - obsignata 372 Cheilospirura 171, 347
i::'
cu
192,194, 200,202,215,226,229, - plica 373 Chelicerata See: Amandibulata
C 233,234,241,356,390 - putorii 373 Chelopistes 394, 451
·;:::
Q) bugs 457 chemokines 26
- retusa 372
Bulinus 202,203 Capillariinae 172,371 Cheyletiella 393,430
C
bulk-tank milk samples 178 capillariosis (zoonosis) 371, 512 - blakei 430
>,
0) Bunostominae 170
0 Capreocaulus 171, 314 - parasitovorax 430
0 bunostomosis in ruminants 285 - yasguri 430
carbamates 558
·u5
Bunostomum 170, 285 carbanilides 562 cheyleliellosis 430
cu - phlebotomum 282,285
Cl. Cardiofilaria 171,366 Chilodonella 45, 149
 23. Index

- piscicola 150 Coenurus 225 - striatum 318

chilodonellosis 149 - cerebralis 233,234 Crenosomatidae 171,318
Chilomastix 45,51 - serialis 233 crenosomosis In dogs and other canids
- gallinarum 51 Coleoptera (beetles) 394, 457 318
- mesnili 51 Collyriclum 169 Crustacea 394,449
Chlamydodontida 45 colonisation 22 Cryptobla 45
Choanotaenia 170,220 Columbicola 394, 451 Cryptosporida 45,122
Chorioptes 393,436, 439 combined sedimentation-flotation Cryptosporidiidae 45
- bovis 436,439 technique 528 cryptosporldiosis (zoonosis) 122,509
- texanus 436,439 commensalism 16 Cryptosporidium 45, 122
Chorioptes mange 439 common housefly 477 - andersoni 123
- in cattle 440 complement system 27 - baileyi 123
- in horses 440 Contracaecum 171 - bovis 123
- in sheep 440 - osculatum 339 - canis 123
Chronomintic Bolus 581 control See also: parasltoses - clchlidls 123
Chrysomya - blologlcal 479, 566 - cunlculus 123,127
- albiceps 484 - In organic farms 572 - tayeri 123
- bezziana 484 - integrated 572 - fells 123
Chrysops 394,473 - legal and regulatory measures 566 - fragile 123
- caecutiens 473 - metaphylaxis 572 - galli 123
Ciliata 147 - physical measures 566 - hominis 123
Ciliophora 45,147 - prophylaxis 572 - meleagridis 123
Cimex 394 - scheduled (= strategic) 572 - molnari 123
- columbarius 457 - therapy 572 - muris 123
- lectularius 457 - use of antiparasitics 566 - parvum 123
Cimicidae 394 Cooperia 170 - pestis 123
Cittotaenia 170 - curticel 289 - saurophilum 123
- ctenoides 215 - oncophora 289 - scrofarum 123
- pectinata 215 - pectinata 289 - serpentis 123
clazuril 562 - punctata 289 - ubiquitum 123
climate change 41,508 - zurnabada 289 - varanii 1 23
clindamycin 114,599 coproculture 532 - viatorum 123
clonorchiosis (zoonosis) 510 Coquillettldla 394 - wrairi 123
Clonorchis 169 - rlchiardll 460 Ctenocephalides 394
- sinensis 197,198 Cordylobla 487 - canis 501
clorsulon 560 - anthropophaga 484, 487 - felis 501
closantel 560,561, 579,585,592 Coronocyclus 170,266 Cuclotogaster 394,451
Cnephia 394,465 Corridor disease 141 Culex 394
Cobboldia 491 Cosmocercoidea 171 - modestus 460
Coccidea 45,79 Cestia necatrix 78 - pipiens 460
coccidiosis See: eimeriosis, Cotylophoron 169,188 Culicidae 394,459
cystoisosporosis Cotylurus 169 - species 460
(I)
Coccivac 569 - cornutus 201 Culicoides 394, 469 C
'(3
Cochlicopa 194 coumaphos 558,613 - chiopterus 469 '6
(I)
Cochliomyia 488 CoxAbic 569 - dewulfi 469
- hominivorax 484,488 Coxiella burnetii 410 - obsoletus 469
Cochlosoma 45 coxiellosis 410 - pulicaris 469
cu
C
·;:::
- anatis 57 coyote 214,247 - scoticus 469
Cochlosomatidae 45 Crataerina 394 Culiseta 394
C
cockroaches See: Blattaria - pallida 500 - annulata 460
>.
coenurosis Craterostomum 170,266 - morsitans 460 O>
0
- cerebral 236, 237 Crenosoma 171,318 Cuterebra 394 0
- non-cerebral 236 - goblei 318 Cuterebrinae 394,498 ·u;
coenurosis (zoonosis) 511 - melesi 318 Cutifilaria 171 cu
CL
 Part VIII. Appendix

Cyathospirura 171 - nudus 448 - microfilariae detection 526

Cyathostoma 170 Cytoditidae 393, 448 - Microsporidia detection 533
Cyathostominae 170, 264, 266 cytokines 26 - parasite detection
cyathostominosis 273 cytotoxic lymphocytes 32 » in blood etc. 525
Cyathostomum 170, 266 » in environmental samples 536
cyclooctadepsipeptides 561 D » in faecal samples 526
Cyclophyllida 170 Dactylogyrida 169 » in gastrointestinal tract 533
Cyclospora 45 Dactylogyrus 169, 206 » in liver and lung 535
cyfluthrin 558, 583 DALY 508 » in organ systems 521
cyhalothrin 558 Dasytricha 45 » in skin 525
Cylicocyclus 170, 266 data bank 576 » in urine 533
Cylicodontophorus 170, 266 Davainea 170, 220 - post mortem parasite detection
Cylicostephanus 170, 266 Davaineldae 170 533
Cylindropharynx 170, 266 decoquinate 89, 562 - preservation of parasites 536
cypermethrin 558, 583 deltamethrln 558, 583, 602, 603 - safety precautions 521
cyromazine 559 Demodex 393, 426 - samples 521
cyst, hydatid 241 - canis 427 - Trichlnella detection 535
cystic echinococcus 225 Demodicidae 393, 426 diamldines 562
cysticercosis demodicosls 426 Diantennata See: Crustacea
- in cattle 224, 229 - In dogs 428 diclazuril 89, 562
- in humans 231 - In other hosts 429 Dicranotaenia 170
- in man 225 Dermacentor 393, 414 Dicrocoeliidae 169
- in pigs 230, 231 - marginatus 397, 403, 414 dicrocoeliosis (zoonosis) 51 0
- storms 229 - reticulatus 397, 403, 414 Dicrocoelium 169
cysticercosis (zoonosis) 511 Dermanyssidae 393, 420 - chinensis 191
Cysticercus 225 dermanyssosis in poultry 420 - dendriticum 191, 192, 194
- bovis 226 Dermanyssus 393 - hospes 192
- cellulosae 226, 231 - gallinae 420 Dictyocaulidae 170, 303
- fasciolaris 233 Dermatobia 394 dictyocaulosis 303, 305
- longicollis 233 - hominls 498 - in cattle 305
- ovis 233 Dermatophagoides 393 - in equids 310
- plsiformis 233 - pteronyssinus 448 - in small ruminants 310
- tarandi 233 Dermatophilus congolense 411 Dictyocaulus 170, 303
- tenuicollis 233 dermatoses - arnfieldi 305
- viscerotropicus 226, 230 - flea 514 - capreolus 305
Cystidicola 171 - mite 514 - eckertl 305
Cystocaulus 171 derquantel 561 - maria 305, 31 o
- ocreatus 314 diagnostic dewormlng 245 - vlvlparus 305
Cystoisospora 45, 97, 98 diagnostic metagenomlcs 520 dlcyclanil 559
- burrowsi 100 diagnostic parasite stages Dlentamoeba 45
- canis 100 - dog and cat 548 - fragilis 54
- felis 100 - equidae 544 diflubenzuron 559
Q)
- ohioensis 100 Digenea 169, 173
·o - rivolta 100
- pig 547
Dilepldidae 170
- poultry 551
Q)
� - suis 45, 97, 98, 123 - ruminants 538 diloxanide furoate 152
c cystoisosporosis - tick genera 552 dimetridazole 562
C - in carnivores 100 diagnostics diminazene aceturate 65, 562
·c
Q)
+-' - in pigs (coccidiosis) 98 - Cryptosporidia detection 533 dimpylate (= diazinon) 558
Cytauxzoon 45, 145 - detection of antibodies, antigens, Dioctophyma 172
C
- felis 145 DNA 526 - renale 383
0
- manul 145 - intravital parasite detection 521 Dioctophymatidae 172, 383
0 cytauxzoonosis 145,412 Diorchis 170
+-' - in vitro culture 526
·1n cythioate 558
CIJ - laboratories 521 Dipetalonema 171, 353, 362
a.. Cytodites 393 - laboratory procedures 520 - dracunculoides 358
 23. Index

Diphyllobothriidae 170 • counter-measures 565 - artoingi 93

diphyllobothriosis (zoonosis) 511 • diagnosis 563 - aubumensis 92
Oiphyllobothrium 170 • flies 479 - aythyae 90
- dendriticum 210 • in animal parasites (table) 564 - babatica 97
- erinaceieuropaei See: Spirometra • reversion 564 - bakuensis 94
erinaceieuropaei Ouddingtonia flagrans 567 - bovis 92
- latum 208 Duttonetla 61 - brasiliensis 92
- nihonkaiense 210 dysregulation of parasites 567 - brunetti 83
- pacificum 21 O - bukidnonensis 92
Diplodinium 45 - canadensis 92
Diplogonoporus 170 E - caprina 93
Diplomonadida 45, 47 East Coast fever 141 - caprovina 93
Diplopylidium 170 Echidnophaga 394 - carpelli 97
- nolleri 223 - gallinacea 501 - caviae 97
- sexcoronatum 223 echinococcosis (zoonosis) 511 - christenseni 93
- species 222 - alveolar 240,241,247 - coecicola 95
Diplostomidae 169,200 - cystic 239,241 - columbarum 90
Diplozoon 169 - polycystic 241 - crandallis 94
- paradoxum 206 - unicystic 241 - cylindrical 92
Oiptera 394, 458 Echinococcus 170,224,239 - danailovi 90
Oipylidiidae 170 - canadensis 241 - deblieckl 98
dipylidiosis (zoonosis) 511 - equinus 241 - dispersa 90
Dipytidium 170 - felidis 241 - ellipsoidalis 92
- caninum 222 - genotypes 241 - europaea 97
- sexcoronatum 222 - granulosus 239, 240, 241 - exigua 95
Dirofilaria 171,353, 357 - intermedius 241 - fafciformis 97
- immitis 358 - multilocularis 239,241,247 - faurei 94
- repens 358, 362 - oligarthrus 241 - flavescens 95
dirofilariosis 512 - ortleppi 241 - gallopavonis 90
Discocotyle 169,206 - shiquicus 241 - gilruthi 94
Discocotylidae 169 - vogeli 241 - granulosa 94
disinfectants 571 Echinocotyle 170 - gruis 98
disinfection 571 Echinolepis 170,221 - hirci 93
Dispharynx 171, 347 Echinoparyphlum 169 - innocua 90
DNA analyses 520 - recurvatum 187 - intestinalis 95,161
dog parasitoses of organ systems 597 Echinorhynchida 172 - intricata 94
donkey 176, 184, 191,194,215,268 Echinorhynchus 172,384 - irresidua 95
doramectin 558, 561, 579, 583,584, Echinostoma 169 - kotlani 90
585,589 - revolutum 187 - labbeana 90
Dourine 61,67 Echinostomatidae 169, 186 - leporis 97
Dracunculidae 171 echinostomatidosis in birds 186 - leuckarti 95
Dracunculus 171 Echinostomida 169,175 - magna 95
- medinensis 346 Echinuria 171,347 - marsica 94
egg and oocyst counting 529 ·c3
dragonflies 197 - maxima 83
Draschia 171,347,350 egg hatch test (EHT) 563 - media 95 Q)

- megastoma 350 ehrlichioses 41 0 - meleagrimitis 90 c

Drepanidotaenia 170,221 eicosanoids 27 - mitis 83
·;:::
Drosophila 394 Eimeria 45, 82 - mulardi 90 Q)

- melanogaster 475 - acervulina 83 - necatrix 83 �

Drosophilidae 394,474 - adenoides 90 - neodebliecki 98 .s
drug - ahsata 94 - nieschulzi 97
- efficacy 557 - alabamensis 92 - ninakohlyakimovae 93
- residues 41, 557 - alijevi 93 - nocens 90 "ii)

- resistance 41, 88, 557, 563 - anseri 90 - nyroca 90

 Part VIII. Appendix

- ovinoidalis 94 » Fasciola hepatica 184 epsiprantel 560, 600, 601

- pallida 94 - copra-antigen Equine Protozoa! Myeloencephalitis
- papillata 97 » Fasciola gigantica 185 (EMP) 120
- paNa 94 » Fasciola hepatica 184 equine theileriosis 141
- perforans 95 elk 71, 186, 194, 497 Ergasilus 449
- perminuta 98 emodepside 561,601 ethylbutylacetylaminoproprionate 559
- piriformis 95 Encephalitozoon 46, 161 Euamoebida 46
- porci 98 - cuniculi 157 Eubothrium 170,208
- praecox 83 encephalitozoonosis 157,510 Eucestoda 170
- reichenowi 98 - in other species 159 Eucoleus 172
- robertsoni 97 - in rabbits 157 - aerophilus 373
- scabra 98 encephalomyelitis 363 - annulatus 372
- separata 97 Endolimax 46 - boehmi 373
- spinosa 98 - nana 151 - contortus 372
- subepithelialis 97 Enopllda 172,368 Eufilaria 171,366
- subrotunda 90 Entamoeba 46 Euglenozoa 45, 59
- subspherica 92 - anatls 153 Eukaryota 18, 44
- suis 98 - apis 153 Eulaelaps 393, 424
- tenella 83 - bovls 153 Eullmdana 171, 366
- townsendi 97 - caviae 153 Euparyphium melis See: lsthmiophora
- truncata 90 - cobayae 153 melis
- vejdovskyi 95 - coli 151 Eurytrema 169
- vermiformis 97 - cuniculi 153 - pancreaticum 192
- weybridgensis 94 - dispar 151 - procyonis 192
- wyomingensis 92 - equi 153 Eustrongylides 172
- zuernii 92 - equibuccalis 153 Euvarroa 393,426
Eimeriida 45, 82 - gallinarum 153 Excavata 44,45
eimeriosis 79 - gingivalis 153 Explanatum 169, 188, 190
- in cattle 91 - histolytica 151 Eyach virus 409
- in chickens 82 - in domestic and pet animals 153 eyeworm disease 346
- in ducks 90 - invadens 153
- in equids 95 - moshkovskii 151
- in fishes 97 - muris 153 F
- in geese 90 - ovis 153 face flies See: Musca autumnalis
- in hares 97 - poleckl 153 faecal egg count reduction test (FECRT)
- in laboratory rodents 97 - suls 153 529,563
- in pigeons, pheasants, guinea fowls, Entamoebldae 46, 151 Falcullfer 393
quails 90 entamoebosls (zoonosls) 509 Falcullferldae 393,448
- in pigs 94 - In humans and animals 151 fallow deer 120, 141, 233, 276, 497
- in rabbits 95 Enteroblus 171, 345 FAMACHA system 298, 565
- in sheep, goats 93 - vermlcularis 345 Fannia 394,478
- in turkeys 90 Enterocytozoon 46,161 - canicularls (lesser house fly) 476,
- in wild or captive birds 97 Enteromonadida 45 478
Baeophora 171, 353 Enteromonas 45, 51 Fanniidae 394, 475
elaphostrongylosis In wild ruminants Entodiniomorphida 45 farm, organic 572
317 Entodinium 45 Fasciola 169
Elaphostrongylus 1 71,317 epidemiology 40 Fasciola gigantica 176,184
- alces 317 Epidermoptes 393 - ELISA, copro-antigen 185
- ceNi 317 Epidermoptidae 393, 448 - life cycle 184
- rangifer 317 Epistylis 45, 150 Fasciola hepatica 175, 176
electric traps 479 Epomidiostomum 170 - clinical signs 183
elephant 112 - uncinatum 303 - diagnosis 183
ELISA eprinomectin 558,561, 579,583, 584, - ELISA, bulk milk samples 184
- bulk milk samples 585,601, 602 - ELISA, copra-antigen 184
 23. Index

- epidemiology 178 - flesh 484 Gasterophitlnae 394,491

- immunology 182 - garbage 478 gasterophilosis in equids 491
- life cycle 175 - head 480 Gasterophilus 394
- pathogenesis, pathology 180 - horn 480,481 - haemorrhoidaflS 492
- pathophysiology 182 - horse 472 - inemlis 492
- therapy, control 184 - louse 498 - intestlnalis 492
- zoonolic importance 184 - nasal bot - nasalis 492
Fasciolidae 169, 175 • in sheep 489 - nigricofnis 492
Fasciololdes 169 • in wild ruminants 490 - pecorum 492
- magna 176, 185 - pasture 479 GastrocflScidae 169
fasciolopslosis (zoonosis) 51 O - stable and house 475 Gastrodiscoldes 169
Fasciolopsls 169 - strike 483 - hominis 188
fasciolosls (zoonosis) 175,510 - Tumbu 487 Gastrodiscus 169
febantel 561, 579,585,589,592 - warble 494 - aegyptiacus 188
Felicola 394,451 notation and sequential sieving 530 Gas1ro1aen1a 170
fenbendazole 560, 561,562,579,581, flotation techniques 526 - species 221
585,589,592,599,600,601,607, flubendazole 561,589, 600,611 Gastrothylacidae 169
611 flukes See Trematoda Gastrothylax 169, 188
fenoxycarb 559 flumethrin 558, 583,602,613 Gavac 569
fenthion 558 fluralaner 558,602, 603 genetics 19
fever food-producing animals 516 genomics 19
- African swine 409 - parasites in domestic rabbits and Giardia 45,47
- Colorado tick 409 poultry 517 - agilis 47
- Crimean-Congo haemorrhagic 409 - parasites in fish and fish products - ardeae 47
- Omsk haemorrhagic 409 517 - bovis 48
- Q 410 - parasites in ruminants, pig, horse - canis 48
- red water 136 516 - cati 48
- Texas 136 - parasites in wildlife (boar, ruminants, - duodenalis 47
Filariidae 171, 353 etc.) 517 - enterica 48
Filarioidea 171, 352 Forcipomyia 394, 469 - intestinalis 4 7
- selected genera (table) 353 Formica 193 - lamblia 47
filariosis (zoonosis) 413,512 - cunlcularia 194 - microti 47
Filaroides 171, 324 - fusca 194 - muris 47
- hirthi 324 - pratensis 194 - psittaci 47
- milksi 325 - rufibarbis 194 - simondi 48
- osleri 325 Fossaria 179 giardiosis (zoonosis) 47,509
filaroidosis in dogs 324 fox 75, 81,105,109,111,112,113, Gigantobilharzia 169,205
Filicollis 172, 384 118,120,138,156,157,159,186, Gigantocotyle explanatum
Fimbriaria 170 187,198,199,200,209,210,213, See: E.xplanatum
- fasciolaris 221 214,223,232,233,234,236,241, Gliricola 394, 451
fipronil 558,601,602 318,321,349,362,389,430,440 global trade 508
Fischoederius 169, 188 Francisella Globidium gilruthi 94
fish 48,51,54,71, 78,123, 125, 149, - tularensis 41O Globocephalus 170
150,153,160,161,164,188,191, free-living mites as pathogens 448 - longemucronatus 282
208,209,339,346,384,387 Glossina 394
flatworms See: Platyhelminthes - fusca 482
flea 500 G - morsitans 482
- species (table) 501 Galba 176,187 - palpalis 482
flea-bite allergy dermatitis 504 - truncatula 175,179,185,188 - species 61
flesh flies See: Sarcophagidae Galumna 393 Glossinidae (tsetse flies) 61, 394,481
flies 458 See also: Brachycera Galumnidae 393 glucantime 76
- blow 484 Gamasida See: Mesostlgmata Glugea 46
- bot 489 gamogony 127 - anomala 161
- face 479 garbage flies See: Ophyra aenescens glycocalyx 173,254
 Part VIII. Appendix

Glycyphagidae 393,448 - contortus 289 - gallinarum 341

Glycyphagus 393 Haemoproteidae 45 - isolonchae 341
- destructor 448 Haemoproteus 45, 128 Heterakoidea 171
- domesticus 448 - columbae 128 Heterobilharzia 169
Gnathostoma 171, 347 Haemosporida 45, 127 - americana 200, 202
Gnathostomatidae 171,347 Halarachnidae 393 heterogony 174
goat parasitoses of organ systems 576 Halicephalobus 170, 259, 263 Heterolobosea 45
Gongylonema 171, 347 Halocercus 171 Heterophyes 169
Gongylonematidae 171, 347 halofuginone 89, 126, 562 - heterophyes 199
Goniocotes 394 halogenated benzenesulfonamides 560 Heterophyidae 169, 197, 199
Goniodes 394, 451 Hammondia 45, 98, 109 Heteroptera (true bugs) 394,457
Grammocephalus 170 - hammondi 109 heteroxeny 174
Graphidium 170 - heydorni 109 Hexamita 45, 51
- strigosum 301 - pardalls 109 - meleagridis 50
grasshoppers 192 hammondlosls In carnivores 109 - pitheci 51
guanidines 562 hard ticks See: lxodidae Hexamitldae 45, 4 7
Gyalocephalus 170, 266 hare 75, 97, 105, 178, 191, 192,194, hexamitosls See: spironucleosis
Gyrodactylida 169 215,233,234,237,261 Hippobosca 394
Gyrodactylus 169, 206 Hartmannella 46 - equina 499
Gyropus 394,451 - cantabrigensis 153 - longipennis 499
Gyrostigma 394,491 Hartmannellidae 46 - variegata 499
hay 180,228 Hippoboscidae 394, 498
heartworm disease 358 Hipracox 89, 569
H hedgehog 187,318 Hirstionyssus 393,424
Habronema 171, 347, 350 Helicella 194 Hirudo
- majus 350 Heligmonellidae 170 - medicinalis 387
- microstoma 350 Heligmosomoides 170 - orientalis 387
- musca 350 - polygyrus 23 - verbana 387
Habronematidae 171,347,349 helminths 169 hirudotherapy 388
habronematidosis in equids 350 Hemiclepsis 78 Histomonas 45, 52
Haemaphysalis 393,407 - marginata 387 - meleagrldis 52,341
- concinna 397,407 Hepatlcola hepatica 373 histomonosls in poultry 52
- inermis 397,407 Hepatocystls 45, 128 Histrichls tricolor 383
- punctata 397, 403, 407 - kochl 128 Hoferellus cyprinl 165
Haematobia 394 - slmlae 128 Hohorstlella 394,451
- irritans 476,480 Hepatozoldae 45, 81 hologamy 79
- stimulans 476, 481 Hepatozoon 45, 81 honey bee parasltoses 612
Haematopinldae 394,454 - amerlcanum 81 hookworms 280
Haematoplnus 394 - canis 81 Hoplopleuridae 394, 454
- asini 454 - fells 81 horse
- eurysternus 454 - muris 82 - parasitoses of organ systems 590
- suis 454 hepatozoonosis 411 - strongyles 264
Q) Haematopota 394, 472 hepatozoonosis in dogs and cats 81 • clinical signs 273
·o
C
- pluvialis 472 Heptatoma 394 • diagnosis 273
'5
Q) Haematozoea 45,127 herd • epidemiology 268
Haementeria ghilianil 387 - prevalences 178 • genera 266
co Haemodipsus 394
C - surveillance 184 • life cycle 266
·;;::
- ventricosus 454 Herpetosoma 61, 71 • pathogenesis 271
Haemogamasus 393, 424 herring worm disease 339 » therapy 274
-� haemoglobinuria (babesial) in cattle 135 Heterakidae 171, 341 host 16
>,
CJ) Haemogregarina 45,82 Heterakiosis - categories 21
0
0 Haemogregarinidae 45 - in poultry 341 - properties 20
·enco haemonchosis in sheep 294 Heterakis 52, 171, 341
co Haemonchus 170 - dispar 341
0...
 23. Index

human African trypanosomosis - multifiliis 149 isoxazolines 558

See: trypanosomosis, African imidacloprid 558,601, 602, 603,607 lsthmiophora 169
(human) imidazothiazoles 561 - melis 186,187
human American trypanosomosis imidocarb 82,145,562, 599 ivermectin 558,561, 579,583, 584,
See: trypanosomosls, American lmmucox 90, 569 585,589,592,607
(human) immunity lxodes 393,405
Hyalomma 393,414 - adaptive 25 - canisuga 397,407
- aegyptlum 397,415 - antigenic variation 36 - hexagonus 397,403,406
- lusitanicum 397 - cellular reactions 27 - persulcatus 397
- marginatum 397, 403,415 - concomitant immunity 28, 31,204 - riclnus 397, 403, 405
Hybomitra 394,472 - effector mechanisms 30 - trianguliceps 397, 407
- species 472 - evasion strategies 37 lxodlda 396 See also: Metastigmata
Hydatigera taeniaeformis See: Taenla - humoraJ reactions 27 lxodldae (hard ticks) 393, 397, 399
taenlaeformis - hypersensitivity 39
Hydrotaea 394, 480 - Immune complexes 65
J
- species 476,480 - Immune evasion 36, 204
jackals 214
hydroxynaphthoquinones 562 - lmmunopathology 39
Joyeuxlella 1 70
hyena 241 - lmmunosuppression 37,65
- pasqualei 223
Hymenolepididae 170,221 - innate 25
- species 222
hymenolepiosis (zoonosis) 511 - parasite antigens 30
Hymenolepis 1 70 - partial immunity 31
Hymenostomalida 45 - self-cure reactions 33 K
Hyostrongylus 170 - sterile immunity 28,31 kangaroos 178
- rubidus 300 - to arthropods 35 Karyolysidae 45
hypobiosis 35, 38, 258,275,277, 289, - to helmlnths 32 Karyolysus 45, 82
291,293,300 - to protozoa 31 Khawia 208
- in cyathostomins 270 immunological kidney sphaerosporosis 167
- in Dictyocaulus 306 - memory 28 Killigrewia 170, 220
- trichostrongylids 291 - mimicry 36 - delafondl 215
Hypoderaeum 169 indoxacarb 558 Kinetoplasta 45, 59
- conoideum 187 infection 22 Klossiella 45
Hypoderma 394, 495 - opportunistic 40 - boae 82
- actaeon 497 - prenatal 229 - cobayae 82
- bovis 495, 496 - routes 22 - equi 82
- diana 497 Infestation 22 - muris 82
- lineatum 495, 496 lnovocox 569 Klossiellidae 45
- tarandi 497 lnsecta 394,449 Knemidocoptes 393
Hypoderminae 394,494 insect growth regulators 567 - gallinae 448
hypodermosis insecticide-treated traps 482 - mutans 448
- in cattle 495 integument 1 73 - pilae 448
- in wild ruminants 497 invasion 22 Kudoa 164
Hystrichis 172 in vitro cultivation 520 - thyrsites 165, 168
lodamoeba 46 Kyasanur forest disease 409
- butschlii 151
ionophore polyethers 562
ibex 194 lschnocera (chewing lice) 394, 450 L
icaridin 559 isometamidium 65 laboratory
lchthyobodo 45 lsospora See also: Cystoisospora - animal 48,156, 345
- necator 78 - bigemina 109 - rodents 50, 51, 97
ichthyobodosis 78 - in wild or captive birds 97 lactones See: macrocyclic lactones
lchthyophthiriidae 45,149 - serini 97 Laelaps 393, 424
ichthyophthiriosis (white spot disease) isothiocyanates 560,561 Laelaptidae 393, 424
149 lsotricha 45 Laminosioptes 393
lchthyophthirius 45 lsotrichidae 45 - cysticola 448
 Part VIII. Appendix

Laminosioptidae 393, 448 - serrata 389 - in humans 128

land snails 192 linguatulosis (zoonosis) 514 MALDI-TOF MS 520
larval Linognathidae 394, 454 Malpighamoeba 46
- development test (LD1) 563 Linognathus 394 Mammomonogamus 170, 278
- migration test (LM1) 563 - ovillus 454 - laryngeus 278
larva migrans - setosus 454 - nasicola 279
- cutanea 513 - stenopsis 454 Mandibulata 394, 449
- externa 263 - vituli 454 Mansonella 171, 353
- visceralis 513 lion 241 Mansonia 394
lasalocid 89, 562 Lipeurus 394,451 marine mammals See: wildlife
leeches 387 Liponyssoides 393, 422 marmot 194
Leishmania 45, 72 - sangulneus 422 Marshallagia 170
- adleri 72 Lipoptena 394 - marshalli 301
- aethiopica 72 - capreoll 500 mass spectrometry 520
- amazonensis 76 - cervl 499,500 McMaster technique 529
- braziliensis 72 liquid manure 228 meat
- infantum 72, 76 Llstrophorldae 393, 448 - Inspection 380, 535
- major 72 Llstrophorus 393 - safety 381
- mexicana 72,76 Lltomosoides 171 mebendazole 561, 585, 592, 600
- tropica 72 Lltostomatea 45, 14 7 Meclstocirrus 170
- venezuelensis 76 Llvacox 89, 569 Megatrypanum theileri
leishmaniosis (zoonosis) 509 Loa 171,353 See: Trypanosoma theileri
- in bovines 76 Lobosea 46 Megninia 393
- in cats 76 Loma 46 melarsomine 65, 67, 68
- in dogs 72 - salmonae 160 Melophagus 394, 499
- in equines 76 louping-ill 409 - ovinus 499
- in humans 72, 76 Lucilia 484 Menacanthus 394, 451
- in macropods 76 - caesar 484 Menopon 394, 451
Leishmune 569 - cuprina 484 Mesocestoides 170, 213
Leish-Tec 569 - illustris 484 - corti 213
Lemdaninae 171 - sericata 484 - lineatus 213
Lepidoglyphus 393 lufenuron 559, 601, 603 - litteratus 213
Leptoconops 394, 469 Lutzomyia 72, 394, 463 - perlatus 213
Leptomyxildae 46 Lymnaea 176 - vogae 213
Leptosphyra 393 - fuscus 179 Mesocestoidldae 170
Leptotrombidium 433 - truncatula See: Galba truncatula mesocestoidosls, larval 214
Lernaea 449 Lymnaeldae 202 Mesostlgmata 393, 420
lesser house fty See: Fannla canlcularls lymphatic filarloses 512 metabolism 257
Leucocytozoidae 45 lynx 202, 210, 233, 235 metacercaria 174, 178
Leucocytozoon 45,128 metacestodes 207,224
- simondi 128 M metaflumizone 558,602, 603
- smithl 128 Macdonaldius oschei 418 metagonimosis (zoonosis) 511
Q)
C levamisole 561,579, 581,585, 589, macracanthorhynchosis (zoonosis) 513 Metagonimus 169
·c::;
=-a
Q)
611 Macracanthorhynchus 172, 384 - yokogawal 197, 199
lice See: Phthiraptera macrocyclic lactones 558,561 Metamonada 45, 47
- chewing lice See: Amblycera, Macronyssidae 393, 422 Metastigmata 393, 396
co lschnocera Metastrongylidae 171, 312
·c
C
maduramicin 89, 562
Q)
+-' » species of birds 451 main infection 180 metastrongylidosis in pigs 312
» species of mammals 451 Metastrongyloldea 171
C
- period 180, 270, 290
- sucking lice See: Anoplura Metastrongylus 171, 312
>, Major Histocompatibility Complex 27
CJ) Ugula 170, 208 - apri 312
0 Malacobothrii See: Digenea
0 Umnatis nilotica 387 - pudendotectus 312
·enco
+-'

Unguatula
Malacosporea 164
- salmi 312
malaria (zoonosis) 127, 509
co - arctica 389 methoprene 602
0... - in animals 128
 23. Index

methylbenzoquate 562 Multiceps multiceps See: Taenia Nematodirus 170,302

Metorchis 169 multiceps - battus 289
- albidus See: Metorchis bilis Musca 394,4 77 - filicollis 289
- bilis 197, 198, 199 - autumnalis (face fly) 4 76,479 - helvetiahus 289
microhaematocrit technique 525 - domestica 476, 477 - spathiger 289
Micronema 263 - sorbens 476 Nematozoa See: Nematoda
Microsomacanthus 170 MuscaMorte 479 Neodactylogyrus 169
Microspora See: Microsporidia Muscidae 394,475 Neoechinorhynchida 172
Microsporidia 46, 155 muskrat 198 Neoechinorhynchus 172, 384
- in fish 160 mustelids 197,198,235 Neolipoptena 394
- in mammals 156 mutualism 16 neohicotinoids 558
- zoonotic 510 mycoplasmosis 411 Neorickettsia helminthoeca 197
microsporidiosis 155 myiasls (zoonosis) 483, 514 Neospora 45, 98
Microsporidium 161 - forms and agents (table) 485 - caninum 111
Microtetrameres 171 Myobia 393 - hughesl 114,121
Microtus 214 - muscull 433 neosporosis
Miescher tubes 117 Myoblldae 393, 433 - In cattle 110
milbemycin 558, 561 Myocoptes 393 - In dogs 110, 113
- oxime 558, 561, 601 - muscullnus 433 - In horses 114
miltefosine 76, 562, 599 Myocoptldae 393, 448 - In other ruminants 113
mink 198 Myodes 214 - In wild animals 113
miracidium 174 Myxidium Neostrongylus 171
mites, oribatid 215 - anatidum 164,165 - linearis 314
Mobilida 45, 150 - glardi 165 Neotrombicula 393
molecular biology 19 - lieberkuehni 165 netobimln 560, 561, 579, 585
Molineidae 170, 302 Myxobolus neurocysticercosis 231
Molineus 170 - cerebralis 165 Nippostrongylus 170
monensin 89,562 - cyprini 165 nitazoxanlde 562
monepantel 561,585 - encephallcus 165 nitenpyram 558,603
Moniezia 1 70 - neurobius 165 Nitidulidae 394
- benedeni 215 Myxosporea 164 nitrolmidazole 152, 562
- expansa 215 Myxozoa 164 nltroscanate 560,561, 600
moniliformiosis (zoonosis) 513 nitrothiazole salicylamides 562
Moniliformis 386 N-methylglucamine antimoniate 562,
monkey 107,118,123,128,147,151, N 599
152, 153,156, 159, 192, 202, 205, Naeglerla 153 Nosema 46,161
211,215,230,231,235,247,250, - fowleri 153 - apis 159
251,259,261,278,384 Nagana 61,62 - ceranae 159
Monocercomonadidae 45, 52, 54 Nairobi sheep disease 409 Nosematidae 46, 157
Monocercomonas 45, 56 Nannomonas 61 nosemosis in honey bees 159
- cuniculi 54 Nanophyetus 169 notifiable diseases 566
- ruminantium 54 - salmincola 197 Notoedres 393,447
Monodontella 170 narasin 89, 562 - cati 443,447
Monogenea 169,205 Necator 170 - mange 447
moose 120,185,233,241 See - americanus 285 - muris 443
also: elk neglected tropical diseases 508 - musculi 443
Morellia 394 Nematobibothrioides histoidii 173 nutria 178
Mosgovoyia 170 Nematocera (thread-horn flies) 394,
mosquitoes 459 458
moxidectin 558, 561,579,583,584, Nematoda 170, 254 0
- classification 258 Obeliscoides 170
585,592, 601,602
- features 254 - cuniculi 301
Muellerius 171
- life cycle 257 Ochlerotatus 394
- capillaris 314
nematodirosis in sheep 294 Octomitus 45,51
- tenuispiculatus 314
 Part VIII. Appendix

Oeciacus 394 - viverrini 197, 198 - equi 343

- hirundinis 457 organic farms 572
Oedemagena See: Hypoderma organophosphates 558
p
Oesophagodontus 170, 266 Orientobilharzia 169
palaeoparasitology 19
Oesophagostominae 170 - turkestania 200
Panacur SR Bolus 581
oesophagostomosis 276 - turkestanicum See: Schistosoma
Panstrongylus 69
Oesophagostomum 170, 276 turkestanicum
Parabasala 52
- bifurcum 278 Ornithobilharzia 169, 205
Parabronema 171
- columbianum 277 Ornithocheyletia 393
Paracox 89, 569
- dentatum 276, 277 Ornithodorinae 418
Parafasciolopsis 169
- quadrispinulatum 276, 277 Ornithodoros 393, 418
- fasciolaemorpha 176, 185
- radiatum 277 - coriaceus 418
Parafilaria 171, 353
- sikae 277 - erraticus 397
- bovicola 353
- venulosum 277 - hermsi 418
- multipapillosa 355
Oestrinae (bot flies) 394, 489 - lahorensis 397
parafilariosis
oestrosis in sheep and goats 489 - moubata 397, 418
- in bovines 353
Oestrus 394 - moubata porcinus 418
- in equines 355
- ovis 489 - parkeri 418
Paragonimidae 169, 197
Oligacanthorhynchida 172 - savignyi 397,418
paragonimosis (zoonosis) 197, 511
Oligohymenophorea 45, 147 - turicata 418
Paragonimus 169
ollulanosis in cats and other hosts 302 Ornithomyia 394
- kellicotti 197
Ollulanus 1 70, 302 ornithonyssosis in poultry 422
Parahistomonas 45
- skrjabini 302 Ornithonyssus 393, 422
Paramphistomidae 169
- suis 302 - bacoti 422
Paramphistomum 169
- tricuspis 302 - bursa 423
- cervi 188, 189
Omphiscola 179 - sylviarum 422
- daubneyi 188
Onchocerca 171, 353, 364 Ornithostrongylidae 170, 303
- ichikawai 188
- cervicalis 364 Ornithostrongylus 170
- microbothrium 188
- gibsoni 364 - quadriradiatus 303
Paranoplocephala 170
- gutturosa 364 oslerosis in canids 325
- mamillana 215,218
- lienalis 364 Oslerus 171
parascariosis in equines 330
- lupi 364 - osleri 325
Parascaris 171
- ochengi 364 - rostratus 325
- equorum 330, 331
- reticulata 364 Ostertagia 170
- univalens 331
- volvulus 364 - leptosplcularls 289, 300
paraslte(s)
Onchocercidae 171, 357 - lyrata 289
- adaptations 19
onchocercosis 364, 512 - ostertagl 289
- adverse effects 24
- in birds 366 ostertaglosls/cooperiosls In cattle 292
- antigens 30
- In bovids, equids 364 Otoblnae 419
- categories 19
- in carnivores 366 Otoblus 393
- definition 16
Oncomelanla 202, 203 - megnini 397, 419
- development (direct, indirect) 20
One Health concept 508 Otodectes 393, 436, 440
(]) - development In/on hosts 22
T5
C Ophlonyssus 393 - cynotis 436, 440
- ectoparasites 18
'6 - natricis 423 Otodectosis 440
(]) - endoparasites 18
� Ophryoscolecidae 45 Otostrongytus 171
- evolution 18
� Ophyra 394, 478 Ovilis Toxovax 569
(1j - genes and genomes 19
C - aenescens (garbage fly) 476, 478, oxadiazine 558
·c - genotypes and strains 1 7
(]) 479 oxfendazole 561, 579, 581, 585
- habitat selection 23
Ophyra aenescens (garbage fly) 567 oxibendazole 561, 592
.£ Opisthokonta 44, 46 oxyclozanide 560, 579, 585
- host-finding 20, 21
>,
0) - host relationships 16, 21
0 Opisthorchiida 169, 197 Oxyspirura 171, 347
0 - host specificity 20
opisthorchiosis (zoonosis) 197, 511 Oxyurida 171, 343
·v; - immune effects 25
Opisthorchis 169 oxyuriosis in equids 343
- important categories 18
- felineus 197, 198 Oxyuris 171
- important groups 17
 23. Index

- in fish/fish products 340 Pectobolhrii See: Monogenea Placentonema gigantissima 254

- in food 508, 515 PecflCl.ltdae 394 Plagiorchiida 169, 191, 197
- life cycles 20 Pediculus 394 Ptanorbarius 176, 185, 202, 203
- mechanisms of pathogenicity 25, Pelecitus 171, 366 Planorbidae 188,189
26 Pelodera 1 70, 259, 263 Planorbis 187, 188
- migrations in hosts 24 Pentastomida 389, 393 Ptasmoditdae 45, 127
- nomenclature 1 7 pentastomidosis Plasmodlum 45, 127
- origin of term 17 - nasopharyngeal 390 - brasilianum 128, 510
- pathogenicity 24 - visceral 390 - cynomo1gi 128, 510
- properties 19 Pentatrichomonas 45, 54 - eylesi 128,510
- reproduction rate 20 Percolozoa 45, 151 - falciparum 128
- systematics 17 Periplaneta 394 - gallinaceum 128
- taxonomic categories 18 - amerlcana 449 - inui 128, 510
- taxonomy 1 7 permethrin 558, 583, 602, 603 - iuxtanucleare 128
parasitic wasp 479 Petrovinema 1 70, 266 - knowlesi 128
parasitism 16 phagocylosis 27 - malariae 128
parasitoldism 16 Pharyngomyia 394,490 - ovale 128
parasitology - plcta 490 - praecox 128
- general aspects 16 Phasmidia 170 - schwetzi 128, 510
- in veterinary education 16 phenamidine isethionate 562 - simium 128, 510
parasitoses 566, 576 phenylpyrazoles 558 - vivax 128
- control 40 pheromones 567 - zoonotic agents 128
- definition 40 Philometra 171 Platycobboldia 491
- epidemiology 40 Philometridae 171 Platyhelminthes 169, 173
- nomenclature 40 Philometroides 171 Pleistophora 46, 161
- of organ systems and control 576 - cyprini 346 - hyphessobryconis 161
• cattle, sheep, goats 576 Phlebotominae 463 Pleistophoridae 46, 160
• chickens, turkeys, pigeons 608 Phlebotomus 72, 394, 463 Pneumonyssoides 393
• dogs and cats 597 - papatasi 464 - caninum 423
• geese and ducks 609 - sergenti 464 Pneumonyssus 393
• honey bees 612 Phocanema 171 - simicola 424
• horses 590 - declplens 339 polecat 198
• pigs 587 Phortica 394 Poiymorphida 172
• poultry 608 - varlegata 475 Polymorphus 172,384
Paraspirura 171 phoxim 558, 583, 589 Polyopisthocotylida 169
Parastrigea 169 Phthiraptera (lice) 394 Polyplax 394
- robusta 201 Phthirus 394 - serrata 454
Parelaphostrongylus 171 Physa 187 - spinulosa 454
- tenuis 317 Physaloptera 171, 347 ponazuril 562
paromomycin 152 Physalopteridae 171, 347 Porocephalus 389, 390
parvaquone 145,562 Physocephaius 171, 347 Porrocaecum 171
passalurosis in rabbits and hares 344 phytotherapy 567 - reticulatum 339
Passalurus 171, 344 pig parasitoses of organ systems 587 postpatency 40
- ambiguus 344 Piloboius 293, 305 Poteriostomum 170
pasture Pilogalumna 393 poultry parasitoses of organ systems
- contamination 291,306 pinworm 343 608
- management 300 - of equids 343 praziquantel 197, 560, 585, 592,600,
patency 40 - of lagomorphs 344 601,602, 607
pathogen associated molecular patterns - of primates 345 predacious fungi 567
(PAMPs) 25 piperazine 561 predation 16
pathogeniclty mechanisms 26 Pirodog 569 prepatency 40
pattern recognition receptors (PRRs) 26 Piroplasmida 129 pro-benzimidazoies 561
Pearsonema 172 Plscicola 78 Probstmayria 171
- plica 373 - geometra 387 Procyrnea 171
 Part VIII. Appendix

prokaryotes 18 - rabbit 439 reindeer 115, 120,133,137, 233,241,

proliferative kidney disease (PKO) 167 - sheep 438 497
propoxur 558 Psoroptidae 393, 435 repellents 559, 567
Prosimulium 394, 465 Psychodidae 394, 463 reproductive potential 225,236
- hirtipes 465 Pterygodermatites 171, 347 reptiles 48, 54, 69, 72, 82, 97, 115,
- tomosvaryi 465 Pulex 394 116, 118, 123, 125, 128,151,153,
Prosthenorchis 172,384 - irritans 501 164, 188, 191, 201, 211,212,213,
Prosthogonimidae 169,197 Pulicidae 394, 501 384,389,423
Prosthogonimus 169 Pycnomonas 61 residual effect 557,580,581
- cuneatus 197 Pycnotrichidae 45,149 resistance See also: drug resistance
Prostigmata 393,426 Pyemotes 393 - breeding 567
Protocalliphora 488 - tritici 434 - factor 563
protonephridia 173 - ventrlcosus 434 Retortamonadida 45
Protospirura 171 Pyemotidae 393,433 Retortamonas 45, 51
Protostrongylidae 171,313 pyrantel 561 Ahabditida 170, 258
- in ruminants and rabbits 314 - base 592,600,601 Ahabditidae 170
protostrongylidosis 313 - embonate 601 Rhabditis 170
Protostrongylus 171 pyrazinoisoquinollnes 560 rhinoceros 112
- brevispiculum 314 pyrazolopyrimidines 562 rhinoestrosis in equids 490
- commutatus 314 pyrethrins 558 Rhinoestrus 394,490
- oryctolagi 314 pyrethroids 558, 559 - purpureus 490
- pulmonalis 314 pyrimethamine 114, 599 Rhinonyssidae 393, 424
- rufescens 314 pyrimidinamines 559 Rhipicephalus 393, 408,413
- rupicaprae 314 pyrimidines 561 - annulatus 397
- tauricus 314 pyriprole 558 - bursa 397,408
Protozoa 45 pyriproxylen 559,603 - decoloratus 397
- classification (table) 45 Pyroglyphidae 393, 448 - microplus 397, 413
- general aspects 44 - other species 413
Przhevalskiana 394, 495, 497
Q - sanguineus 403,408
- infestation of goat 497 quinazolinones 562 - sanguineus s.l. 397
- silenus 497 quinolones 562 - turanicus 397, 408
Pseudaliidae 171 Rhizaria 44
Pseudalius 171 Rhodnius 69, 394,457
Pseudamphistomum 169 R rickettslosis 41 O
- truncatum 197,198 rabbit 178,191, 192,194,205, 215, Rictularildae 171,347
Pseudolynchia 394, 500 233,234,237,261 Aictularloidea 171
Pseudomyiasis 485 - parasltoses of organ systems 607 Ainadia 170, 300
pseudoparasites 19 raccoon 192, 197,202 robenidlne 89, 562, 607
Pseudophyllida 170 raccoon dog 100, 186, 198, 199, 200, Rodentolepls 1 70
Pseudosuccinea 179 213,214,223,233,235,236,247 Rodhainomyia 491
Pseudoterranova 171 Radfordia 393 roe deer 48,61, 71, 105, 109,112,
- decipiens 339 - ensifera 433 115, 133, 137,141,185,194,215,
Psorergates 393 Radix 176,202 233,277,497
- ovis 433 Aaillietia 393,424 ronidazole 50, 56,562
- simplex 433 - auris 424 roundworms 254
Psorergatidae 393 Raillietiella 389 - large intestinal 326
Psoroptes 393,435,436 Aaillietina 170,220
- cuniculi 436 rapid diagnostic test 520
- natalensis 436 red deer 105,112,115, 133, 141,185, s
215,233,276,277,317, 497 SAFC technique 530
- ovis 436
redia 174, 178 safety index 557,579
Psoroptes mange 435
Reduviidae 61, 69, 394 safety precautions 251
- cattle 438
refugia 563, 565 salicylanilides 560, 561
- goat 439
Aeighardia 389 salinomycin 89, 607
- horse 439
 23. Index

salmonids 167 Scheloribates 393 - ovis 345

SAR 44,45 Schistocephalus 170,208 skrjabinemosis in ruminants 345
Sarcocystidae 45, 98 Schistosoma 169, 200 sleeping sickness 61
sarcocystiosis - bovis 200,202 See: trypanosomosis, African
- acute and subacute 120 - curassoni 202 (human)
- chronic 120 - haematobium 200, 205 slurry 180
- in birds 121 - indicum 202 small hive beetle 457, 613
- in carnivores 120 - japonicum 200, 202 S-methoprene 559, 601
- in domestic ruminants 120 - mansoni 200, 205 smokescreen antigens 37
- in squids 120 - mattheei 202 Sobolevicanthus 170, 220
- in wild ruminants 1 20 - nasale 200, 202 Sodalis glossinidius 482
sarcocystiosis (zoonosis) 510 - spindale 200, 202 soft licks See: Argasidae
Sarcocystis 45,98,116 - turkestanicum 202 Solenopotes 394
- arieticanis 118 Schistosomatidae 169,200,201 - capillatus 454
- bertrami 118 schlstosomosis (zoonosls) 200,201, Soricimyxum
- capracanis 118 511 - fegati 165
- cruzi 118 Schizotrypanum 61 sparganosis (zoonosis) 211, 512
- fayeri 118 Schmallenberg virus 471 species, definition 17
- gigantea 118 seals 198 Sphaerospora 164
- hardangeri 120 seasonal dynamics 293 - dykovae 167
- hircicanis 118 Secernentea 170, 258 - molnari 165
- hirsuta 118 sedimentation technique 526 - renicoia 165
- hjorti 120 selamectin 558, 561,600, 602, 607 - tincae 165
- hominis 118 semduramicin 89 - truttae 165
- horvathi 118 semicarbazone 558 Spiculocaulus 171
- medusiformis 118 sequestration 36 - austriacus 314
- miescheriana 118 Sergentomyia 394,463 Spiculopteragia 170, 300
- moulei 118 Sessilida 45,150 Spilopsyllus 394
- neurona 118 Setaria 171, 353, 363 - cuniculi 501
- ovalis 120 - cervi 363 spinosad 558,603
- rangiferi 120 - digitata 363 Spirocerca 171,347, 349
- rommeli 118 - equi 363 - arctica 349
- suihominis 118 - marshalli 363 - lupi 349
- tarandi 120 - muitipapiiiosa 363 Spirocercidae 171,347,349
- tenella 118 Setariinae 171 spirocercosis in canids and felids 349
Sarconema 171, 366 sewage 228 spiroindoles 561
Sarcophaga 394 - sludge 230 Spirometra 170, 211
- carnaria 484 - works 228 - erinaceieuropaei 211
- haemorrhoidalis 484 sheep parasitoses of organ systems - mansonoides 211
Sarcophagidae (flesh flies) 394, 483 576 spironucleosis 51
Sarcoptes 393,442 silage 180,228 - in laboratory rodents 51
- forms 442 Silvius 394 - in turkeys 50
Q)
- mange 442 Simondsia 171,347 Spironucleus 45, 51 C
·c3
» in cats 445 Simuliidae 394,465 - barkhanus 51 '6
Q)
• in cattle 445 simuliotoxicosis 465, 467 - columbae 50
• in dogs 445 Simulium 394, 465 - meleagridis 50 c
co
» in other host species 445 - columbaschense 465 - muris 51 C
·;;::
• in pigs 445 - equinum 465 Spirura 171
» in sheep and goat 445 - erythrocephaium 465 Spiruridae 171,346,347
C
» in wild ruminants 445 - lineatum 465 Spirurina 171
>.
- scabiei 443 0)
- ornatum 465 - selected genera (table) 347 0
Sarcoptidae 393,442 - reptans 465 Splendidofilaria 171,366 0
·u5
Sarcoptiformes See: Astigmata Siphonaptera (fleas) 394, 500 sporocyst 174,178 co
sarolaner 603 Skrjabinema 171,345 Sporozoa 45,79
co
Cl..
 Part VIII. Appendix

stable flies See: Stomoxys calcitrans - edentatus 265, 266 - saginata-cysticercosis 226
Standardised Nomenclature of Parasitic - equinus 265,266 - serialis 233, 234
Diseases (SNOPAD) 40 - vulgaris 265,266 - solium 226,230
Stegomyia 394 suckers 173 » cysticercosis of pigs 230
Stenepteryx 394 Suifilaria 171 » taeniosis of humans 230
Stephanofilaria 1 71,353,356 sulfadiazine + trimethoprim 562 - species of carnivores 232
- assamensis 356 sulfadimidine 562 - species of man 224
- dedoesi 356 sulfaquinoxaline 562 - taeniaeformis 225,233,235
- species 356 - with pyrimethamine and others 562 Taeniidae 170,224
- stilesi 356 sulfonamides 88,114, 562,599 - metacestodes 225
stephanofilariosis in cattle and buffaloes summer bleeding 355 taeniosis
356 summer eczema of horses 469 - in humans (zoonosis) 512
Stephanurinae 170 summer lesions of cattle 356 taeniosis (zoonosis)
Stephanurus 170 Surra 61, 66 - in carnivores 232
- dentatus 280 swim bladder inflammation (S8I) 167 - in humans 224, 226,229, 230
sterile insect technique (SIT) 482,488, swimmer's itch 200, 205 tapeworms See: Cestoda
567 symbiosis 16 targeted selective treatments 581
sterilisation 571 synecology 16 targeted treatments 529
Sternostoma 393 Syngamidae 170,278 Tarsonemidae 393, 434
- tracheacolum 424 Syngaminoses 278 Teladorsagia 170
sticky flypaper 479 Syngamosis 279 - circumcincta 289
Stilesia 1 70 Syngamus 170 - trifurcata 289
- globipunctata 215 - laryngeus 278 tenacity
- hepatica 215 - nasicola 279 - Ascaris eggs 328
stomach bots 491 - trachea 279 - Cryptosporidium oocysts 125
stomach worms of equids 350 syngamy 124, 127, 132 - Cystoisospora oocysts 99
Stomoxys 394 Synhimantus 171 - Eimeria oocysts 86
- calcitrans (stable fly) 476, 478 Syphacia 171 - Giardia cysts 50
Stramenopiles 44 - muris 345 - Toxocara eggs 336
Streptocara 171 - obvelata 345 - Toxoplasma oocysts 104
Streptopharagus 171 Syringophilidae 393, 431 - Trichinella muscle larvae 379
Strigea 169 Syringophilus 393, 431 Terranova 171
Strigeatida 169, 200 - bipectinatus 431 Tetracapsuloides 164
Strobilocercus fasclolaris - columbae 431 - bryosalmonae 165, 167
See: Cysticercus fasclolaris Systamex Interval Bolus 581 tetracyclic macrolides 558
Strongylidae 170, 264 - forte 581 Tetrameres 171,347
Strongyloldea 170 tetrathyrldiosis 213
Strongyloides 1 70, 259 tetrathyrldlum 213
T
- avium 261 Tetratrlchomonas 45,57
Tabanidae 394, 472
- cebus 261 T h 1/Th2 dichotomy 28
Tabanus 394, 472
- felis 261 T hecamoeba 46
- bovinus 472
- fuelleborni 261 T hecamoebidae 46
(l) Taenia 170, 224
C - papillosus 259, 261 Theileria 45, 140
·c3 - asiatica 226,230
'6 - planiceps 259 - annae 131,138
(I) - crassiceps 233, 234
- ransomi See: Strongyloides suis - annulata 141
� - gaigeri 234
cro - ratti 259, 261
- hydatigena 232, 233
- buffeli 141

-
- stercoralis 259, 260, 261 - capreoli 141
·;:: - krabbei 233
(l) - suis 259, 261 - equi 141
- martis 233, 235
- tumefaciens 261 - lestoquardi 141
-� - westeri 259, 261
- multiceps 233, 234
- mutans 141
- ovis 233

-
Ol Strongyloididae 170 - orientalis 141
0 - pisiformis 233
0 strongyloidosis (zoonosis) 513 - ovis 141
·w
ro Strongylus 170, 265
- polyacantha 233, 235
- parva 141
ro - saginata 224, 226
0..
- asini 266 - sergenti 141
 23. Index

- taurotragi 141 toltrazuril 88, 93, 99, 562, 589,599, trichinellosis(zoonosis) 376,513
T heileriidae 45, 140 601, 607 Trichobilharzia 169
theilerioses 412 tongue worms 389 - frank! 202
theileriosis 140 toxascariosis in dogs and cats 332 - regentl 202
- benign African 14 1 Toxascaris 171,332 - szidatl 202
- benign bovine 141 - leonina 332 Trichodectes 394, 451
- benign (of sheep and goats) 141 Toxocara 171, 333 Trichodina 45, 150
- in cattle 144 - canis 333, 334 Trichodinella 45, 150
- in equines 144 - Cati 338 Trichomitus 45
- malignant (of sheep and goats) 141 - malayensis 338 Trichomonadida 45, 52
- oriental 141 - mystax 338 Trichomonas 45, 54
- tropical or Mediterranean 14 1 - vitulorum 338 - equlbuccalis 57
- Zimbabwe 141 Toxocarinae 171 - gallinae 56
Thelazia 171, 34 7 toxocarosis - vaginalis 57
- californensis 348 - In cattle and buffalos 338 trichomonosls, avian 56
- callipaeda 346 - In dogs and other canlds 333 Trlchorlbates 393
- gulosa 346 - In fellds 338 Trlchosomoldes 172
- lacrymalis 346 Toxoplasma 45, 98, 101 Trlchosomoldlnae 172, 375
- modesi 346 - gondli 101 Trlchostrongylidae 170, 287
- skrjabini 346 - in food products 108 trichostrongylidosis(zoonosis) 287, 513
Thelaziidae 171, 346, 347 toxoplasmosis(zoonosis) 101, 510 - In sheep and goats 294
thelaziosis (zoonosis) 346, 513 - in cats 106 - ostertagiosis/cooperiosis(cattle)
Thelohanellus 164 - in dogs 106 291
Thelohania 46 - in humans 107 trichostrongylids
therapy 556 - in other animals 107 - of domestic ruminants 287
- curative treatment 556 - in pigs 107 - of equines 300
- metaphylactic(= mesophylactic) - in sheep and goats 106 - of pigs 300
treatment 556 Trachipleistophora 46, 161 - of poultry 301
- prophylactic treatment 556 translocation of Infective larvae 292 - of rabbits and hares 301
- strategic(= planned) treatments travelling 508 - of wild ruminants 300
556 treatment See also: therapy Trichostrongyloidea 170
- targeted selective treatment (TST) - strategic 300 Trichostrongylus 170
556 - targeted selective 300 - axei 289, 300
- targeted treatment (TT) 556 Trematoda 169, 173 - capricola 289
Theromyzon tessulatum 387 Trepomonadea 45, 47 - colubriformis 289
thiamethoxam 558 Trlaenophorus 170, 208 - longispicularis 289
thiamine analogues 562 Trlatoma 69, 394, 45 7 - retortaeformis 301
Thominx anatis 372 triazlne derivatives 562 - tenuis 301, 303
thread-horn flies See: Nematocera TrichGuard 56 - vitrinus 289
thymol 613 Trlchinella 172, 376 Trlchuridae 172,368
Thysaniezia 170 - britovl 377 trichuriosis 368
- giardi 215 - encapsulated clade, in mammals Trichuris 172
Q)
Thysanosoma 1 70 377 - campanula 368
·u
C:

- actinioides 215 - murrelli 377 - felis 368 '6

Q)
Thysanosomatinae 170 - nativa 377 - globulosa 368
tick-borne - nelsoni 377 - ovis 368
co
- encephalitis(TSE) 409 - non-encapsulated clade, in - serrata 368 C:
·;:::
- infections(table) 403, 409 mammals, birds, reptiles 377 - skrjabini 368
TickGard 569 - papuae 377 - vulpis 368
C:
ticks - patagoniensis 377 triclabendazole 560, 579, 585, 592
>,
- hard ticks See: lxodidae - pseudospiralis 377 Trimenopon 394,451 CJ)
0
- soft ticks See: Argasidae - spiralis 377 trimethoprim 562 0
toll-like receptors (TLRs) 26 - zimbabwensis 377 Trinoton 394, 451 ·w
�
Trichinellidae 172, 376 Triodontophorus 170, 266 co
CL
Part VIII. Appendix

Tripartiella 45,150 Trypanosomatidae 45,59 - sagittatus 314

Tritrichomonas 45,54 trypanosomes Varroa 393,424
- enteris 57 - in birds and fish 71 - destructor 160, 424, 425
- equi 57 - Salivaria group 60 - jacobsoni 425
- foetus 52 - Stercoraria group 69 varroosis in bees 424,613
- foetus B (bovine strain) 55 trypanosomosis vegetable oils and derivatives 559
- foetus C (cat strain) 56 - African (animal) 61 Vestibuliferida 45, 14 7
- muris 52,57 - African (human) 61, 509 Viannia 72
- ruminantium 54 - American (human) 61,69, 71, 509 Vittaforma 46, 161
- suis 55 Trypanozoon 61
tritrichomonosis tsetse flies See: Glossinidae (tsetse
- bovine 55 flies) w
- feline 56 tularaemia 410 wapiti 241

Trixacarus 393,447 Tunga 394 wastewater 228, 230

- caviae 443,447 - penetrans 501,503 waterfowl 186,384, 609

troglostrongylosis in felids 318 tungaosis 514 Wenyonella 45, 90

Troglostrongylus 1 71,318 Tungidae 394, 501 whipworm 368

- brevior 318 Turbatrlx 170 whirling disease of salmonids 165

- subcrenatus 318 - acetl 254 white spot disease

- wilsoni 318 Tyroglyphus 393 See: lchthyophthiriosis

Troglotrema 169 Tyrophagus 393 Wigglesworthia glossinidia 482

- acutum 197
Troglotrematidae 169,197
Trombicula 393,431
- alfreddugesi 432
- autumnalis 432
- sarcina 432
Trombiculidae 393,431
Trombiculosis 431
Trombidiformes See: Prostigmata
Tropilaelaps 393,424,613
- clareae 424, 426
true bugs See: Heteroptera
Trypanoplasma 45
- borreli 78
Trypanosoma 45,60
- avium 71
- brucei brucei 61,62
- putrescentlae 448 wildlife
Tyzzeria 45,90 - carnivores 81 See also: raccoon
- parvula 90 dog, fox, wolf
- pellerdyi 90 - marine mammals 112,118, 121,
- perniciosa 90 339
- ruminants 61, 71,113,176,188,
u 189,202,500
wild pigs 105,108,147,212,226, 241,
Uncinaria 170
247,250,261,277,312,368,384
- stenocephala 281,282
withdrawal period 557,573,579,583,
uncinariosis 284
585,589,592
- in carnivores 281
Wohlfahrtia 394,487
urbanisation 508
- magniflca 484,487
Wolbachia pipientis 482
V wolf 200,214,233,235,236,247,389
vaccination 231,238, 245, 246,567 Wuchereria 171,353
vaccine 50,569

- brucei equiperdum 61,67 - babeslosls (dogs) 138,569

- coccldiosis (chicken) 89,569 X
- brucei evansi 61,66
- dictyocaulosis (cattle) 309,569, Xenopsylla 394
- brucel gambiense 61,66
582 - cheopis 501
- brucel rhodesiense 61, 66
- cervi 61 - echinococcosis (sheep, pig) 569

- congolense 61, 62 - giardiosis (dogs) 50,569

z
- cruzi 61,69 - haemonchosis {sheep) 569
Zabrina 194
- danilewskyi 71 - leishmaniosis (dogs) 76,569
zoonoses 40,508
- lewisi 61, 71 - theileriosis (cattle) 145,569
- arthropod-borne 508
- melophagium 61, 71 - tick infestation (cattle) 569
- definition, nomenclature 508
- nabiasi 71 - toxoplasmosis (sheep) 107,569
- fish-borne 508
- simiae 61,62 - tradenames 615
- food-borne 508
- Stercoraria group 61 - tritrichomonosis {cattle) 56
- significance 508
- suis 61 Vampirolepis 170
- soil-borne 508
- theileri 61,71 Varestrongylus 171
- water-borne 508
- vivax 61,62 - capreoli 314
zoonotic agents 509
 23. Index

- Acanthocephala 513
- Arthropoda 514
- Cestoda 511
- Microsporidia 51 O
- Nematoda 51 2
- Pentastomida 514
- Protozoa 509
- Trematoda 51 0

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