You are on page 1of 387


Life Sciences Department,
The Natural History Museum, London, UK

Reader in Parasite Epidemiology, Immunology and Infection Section,
Department of Infectious Disease Department of Biological Sciences,
Epidemiology Faculty of Medicine Sir Alexander Fleming Building, Imperial
(St Mary’s campus), Imperial College, College of Science, Technology and
London, London, UK Medicine, London, UK

Wellcome Trust Research Fellow and Johns Hopkins Malaria Research
Professor, London School of Hygiene and Institute & Department of Epidemiology,
Tropical Medicine, Faculty of Infectious Johns Hopkins Bloomberg School of Public
and Tropical, Diseases, London, UK Health, Baltimore, MD, USA

Department of Veterinary Science, Head, WHO Collaborating Centre for
The University of Melbourne, Parkville, the Molecular Epidemiology of Parasitic
Victoria, Australia Infections, Principal Investigator,
Environmental Biotechnology CRC
N. HALL (EBCRC), School of  Veterinary and
School of Biological Sciences, Biomedical Sciences, Murdoch University,
Biosciences Building, University of Murdoch, WA, Australia
Liverpool, Liverpool, UK
R. C. OLIVEIRA Professor, Director, National Institute of
Centro de Pesquisas Rene Rachou/ Parasitic Diseases, Chinese Center for
CPqRR - A FIOCRUZ em Minas Gerais, Disease Control and Prevention, Shanghai,
Rene Rachou Research Center/CPqRR - People’s Republic of China
The Oswaldo Cruz Foundation in the State
of Minas Gerais-Brazil, Brazil

Advances in

Edited By

Life Sciences Department,
The Natural History Museum,
Cromwell Road,
London, UK


Academic Press is an Imprint of Elsevier
Academic Press is an imprint of Elsevier
The Boulevard, Langford Lane, Kidlington, Oxford, OX5 1GB, UK
32 Jamestown Road, London NW1 7BY, UK
Radarweg 29, PO Box 211, 1000 AE Amsterdam, The Netherlands
225 Wyman Street, Waltham, MA 02451, USA
525 B Street, Suite 1800, San Diego, CA 92101-4495, USA

First edition 2013

Copyright © 2013 Elsevier Ltd. All rights reserved.

No part of this publication may be reproduced, stored in a retrieval system or

transmitted in any form or by any means electronic, mechanical, photocopying,
recording or otherwise without the prior written permission of the publisher.

Permissions may be sought directly from Elsevier’s Science & Technology Rights
­ epartment in Oxford, UK: phone (+44) (0) 1865 843830; fax (+44) (0) 1865 853333;
email: Alternatively you can submit your request online by
visiting the Elsevier web site at, and selecting
Obtaining permission to use Elsevier material.

No responsibility is assumed by the publisher for any injury and/or damage to persons
or property as a matter of products liability, negligence or otherwise, or from any use
or operation of any methods, products, instructions or ideas contained in the material
herein. Because of rapid advances in the medical sciences, in particular, independent
­verification of diagnoses and drug dosages should be made.

ISBN: 978-0-12-407706-5
ISSN: 0065-308X

For information on all Academic Press publications

visit out website at

Printed and bound in UK

13 14 15  1 2 3 4 5 6 7 8 9 10

Mohammed A. Alfellani
Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical
Medicine, London, UK; Department of Parasitology, Faculty of Medicine, Sebha
University, Sebha, Libya
Adel Al Jasari
Malaria Control Programme, Ministry of Public Health and Population, Yemen
Mohammad H. Al Zahrani
Ministry of Health, Kingdom of Saudi Arabia
Punam Amratia
Malaria Public Health Department, Kenya Medical Research Institute–Wellcome
Trust–University of Oxford Programme, GPO, Nairobi, Kenya
Hoda Atta
Malaria Control & Elimination, Division of Communicable Diseases Control, World
Health Organization Regional Office for the Eastern Mediterranean, Cairo, Egypt
Louisa J. Castrodale
Alaska Department of Health and Social Services, Division of Public Health, Section of
Epidemiology, Anchorage, AK, USA
C. Graham Clark
Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical
Medicine, London, UK
Simone J. C. de Rosemond
Department of Veterinary Microbiology, University of Saskatchewan, Saskatoon, SK S7N
5B4, Canada
Brent R. Dixon
Microbiology Research Division, Bureau of Microbial Hazards, Food Directorate, Health
Canada, Ottawa, ON, Canada, K1A 0K9
Stacey A. Elmore
Department of V
  eterinary Microbiology, University of Saskatchewan, Saskatoon, SK S7N
5B4, Canada
Mahmoud Fikri
Ministry of Health, United Arab Emirates
Karen M. Gesy
Department of V
  eterinary Microbiology, University of Saskatchewan, Saskatoon, SK S7N
5B4, Canada
Andrea L. Graham
Department of Ecology and Evolutionary Biology, Princeton University, Princeton, USA

viii Contributors

Eric P. Hoberg
United States National Parasite Collection, United States Department of Agriculture,
Agricultural Research Service, Beltsville, MD, USA
Emily J. Jenkins
Department of V
  eterinary Microbiology, University of Saskatchewan, Saskatoon, SK S7N
5B4, Canada
Julius Lukeš
Biology Centre, Institute of Parasitology, Czech Academy of Sciences, and Faculty of
Science, University of South Bohemia, České Budějovice, Czech Republic
Ziad A. Memish
Ministry of Health, Kingdom of Saudi Arabia
Clara W. Mundia
Malaria Public Health Department, Kenya Medical Research Institute–Wellcome
Trust–University of Oxford Programme, GPO, Nairobi, Kenya
Abdisalan M. Noor
Malaria Public Health Department, Kenya Medical Research Institute–Wellcome
Trust–University of Oxford Programme, GPO, Nairobi, Kenya; Center for Tropical
Medicine, Nuffield Department of Clinical Medicine, University of Oxford, Oxford, UK
Lydden Polley
Department of V
  eterinary Microbiology, University of Saskatchewan, Saskatoon, SK S7N
5B4, Canada
Janna M. Schurer
Department of V
  eterinary Microbiology, University of Saskatchewan, Saskatoon, SK S7N
5B4, Canada
Manon Simard
Nunavik Research Center, Makivik Corporation, Kuujjuaq, QC, Canada, J0M 1C0
Robert W. Snow
Malaria Public Health Department, Kenya Medical Research Institute–Wellcome
Trust–University of Oxford Programme, GPO, Nairobi, Kenya; Center for Tropical
Medicine, Nuffield Department of Clinical Medicine, University of Oxford, Oxford, UK
C. Rune Stensvold
Statens Serum Institut, Copenhagen S, Denmark
R. C. Andrew Thompson
School of V
  eterinary and Biomedical Sciences, Murdoch University, Murdoch, WA,
Mark van der Giezen
Biosciences, College of Life and Environmental Sciences, University of Exeter, Exeter, UK
Jiří Vávra
Biology Centre, Institute of Parasitology, Czech Academy of Sciences, and Faculty of
Science, University of South Bohemia, České Budějovice, Czech Republic; Faculty of
Science, Charles University in Prague, Prague, Czech Republic
Contributors ix

Mark E. Viney
School of Biological Sciences, University of Bristol, Woodland Road, UK
Ghasem Zamani
Malaria Control & Elimination, Division of Communicable Diseases Control, World
Health Organization Regional Office for the Eastern Mediterranean, Cairo, Egypt

Recent Developments in
Blastocystis Research
C. Graham Clark*,1, Mark van der Giezen†, Mohammed A. Alfellani*,§,
C. Rune Stensvold‡
*Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, UK
†Biosciences, College of Life and Environmental Sciences, University of Exeter, Exeter, UK
‡Statens Serum Institut, Copenhagen S, Denmark
§Department of Parasitology, Faculty of Medicine, Sebha University, Sebha, Libya
1Corresponding author: E-mail:

1. Introduction2
2. Background2
3. Subtypes5
3.1. Current Status 5
3.2. Intra-Subtype Diversity 8
4. Geographic Variation in Blastocystis Prevalence 10
5. Linking Blastocystis to Disease 11
5.1. Prevalence and Intensity of Infection 11
5.2. Links to Irritable Bowel Syndrome 12
5.3. Case Studies 18
5.4. The Way Forward? 19
6. Genome Studies 20
6.1. Blastocystis MLO Genomes 21
6.2. Blastocystis Nuclear Genome 21
7. Future Developments 25

Blastocystis is a common parasite of the human large intestine but has an uncertain
role in disease. In this review, we appraise the published evidence addressing this and
its weaknesses. Genetic diversity studies have led to the identification of numerous
subtypes (STs) within the genus Blastocystis and, recently, methods for studying varia-
tion within STs have been developed, with implications for our understanding of host
specificity. The geographic distribution of STs is summarised and the impact this may
have on investigations into the role of the organism in disease is discussed. Finally, we
describe the organelle and nuclear genome characteristics and look to future develop-
ments in the field.

Advances in Parasitology, Volume 82 © 2013 Elsevier Ltd.

ISSN 0065-308X, All rights reserved. 1
2 C. Graham Clark et al.

Organisms assigned to the genus Blastocystis are the most common
eukaryotes reported to colonise humans, yet remain an enigma on many
levels. Despite having been described more than 100 years ago (Alexeieff,
1911; Brumpt, 1912), the question of whether Blastocystis causes ­disease
or is a commensal of the human gut still has no definitive answer. Our
­understanding of its taxonomy has improved but our knowledge of its
genetic diversity, host specificity and geographic distribution remains very
incomplete. This review will critically evaluate the information that has
recently become available on the pathogenicity of this organism, summarise
our understanding of its prevalence, diversity and distribution, and give an
overview of the data emerging from genome projects.

After bouncing between many taxonomic ‘homes’ during most of the
twentieth century, Blastocystis finally came to rest among the stramenopiles
in 1996 (Silberman et al., 1996), a grouping that did not exist before 1989
(Patterson, 1989). Blastocystis is an atypical stramenopile as this group is
named for the straw-like tubular hairs on the flagella and sometimes the cell
body – Blastocystis has no flagella or tubular hairs. The link was made using
phylogenetic analysis of small subunit ribosomal RNA gene (SSU-rDNA)
sequences and has been confirmed using other gene sequences (Arisue et al.,
2002). Within the stramenopiles, Blastocystis is specifically related to the
Proteromonadidae and Slopalinida (Kostka et al., 2007), which are mostly
commensal flagellated or ciliated organisms found in reptiles and amphibia.
They include the genera Proteromonas, Opalina, Protoopalina, Karotomorpha,
and Cepedea.The absence of typical stramenopile morphology in Blastocystis
is clearly the result of secondary loss.
In fact, Blastocystis morphology is not well understood. A large number
of morphological cell types have been described (Zierdt, 1991) but, in the
opinion of the present authors, many are likely to be artefactual and due to
oxygen exposure rather than actually occurring in vivo (Stenzel et al., 1991;
Vdovenko, 2000). Nevertheless, it can be stated confidently that Blastocystis
is normally a spherical cell of ca. 5–10 µm in diameter that is multinucleated
and contains multiple mitochondrion-like organelles (MLOs), Golgi appa-
ratus and other typical eukaryotic cellular features.Transmission of infection
Recent Blastocystis Research 3

is via a small cyst stage that is difficult to detect in stool samples (Stenzel
and Boreham, 1991); when Blastocystis is observed by light microscopy, it is
primarily the vegetative form that is noted. Under the electron microscope,
the nucleus has a distinctive appearance, with a crescent of dark-staining
chromatin being seen on one side (Zierdt, 1991).
The secondary loss of morphology has been responsible for much of
the confusion surrounding the species names and host ranges, because all
small spheres look much alike. As a result, species names for Blastocystis were
until recently linked to the host in which they were found – the prime
example being Blastocystis hominis as the name applied to all Blastocystis seen
in humans. The advent of nucleic acid-based analyses in the mid-1990s
quickly revealed two things: 1. The SSU-rDNA from Blastocystis in humans
is genetically extremely diverse; 2. SSU-rDNA from Blastocystis in other
hosts can be indistinguishable from that in humans (Böhm-Gloning et al.,
1997; Clark, 1997). This meant that host origin was not a reliable indica-
tor of organism identity and that some other means of identifying types of
Blastocystis would be necessary.
Over the next 10 years, molecular analyses of Blastocystis became quite
popular and a number of groups in different parts of the world were work-
ing independently to understand the significance of genetic diversity in
Blastocystis. This had an unfortunate consequence, namely that each group
came up with its own nomenclature to denote the Blastocystis molecular
types that they detected. In addition, two distinct methods of analysis were
being employed: SSU-rDNA sequencing and polymerase chain reaction
(PCR) amplification of sequence-tagged sites (STS). The former has the
advantage of generating quantitative data and has the ability to detect new
molecular types as they are uncovered. The latter (Yoshikawa et al., 2004b)
has the advantage of better detection of mixed infections since a separate
PCR is performed to detect each major type, but has the limitation of
detecting only seven known types.
By 2006, the literature had become almost impenetrable for anyone not
intimately involved in Blastocystis typing, and even then it required an abil-
ity to cross-reference between nomenclatures to interpret newly published
data. Adding to the confusion, the identifiable variants were given different
names – genotype, clade, group, subgroup, subtype (ST), and ribodeme. As
a result, a consensus was developed and was published in 2007 (Stensvold
et al., 2007b).The consensus relied on multiple types of data being available
for some strains (e.g. ribodeme + sequence or STS + sequence) to allow
extrapolation of the nomenclature to other strains that shared the same
4 C. Graham Clark et al.

characteristics. Today, for the most part (but not always), new publications
follow the consensus nomenclature for ‘STs’ of Blastocystis. The ­proposed
replacement of all names for avian and mammalian species, including
­Blastocystis hominis, with the identifier ‘Blastocystis sp.’ followed by the ST
number is also widely employed. This consensus terminology will be fol-
lowed throughout this review.
It is perhaps appropriate here to propose a standard approach to subtyp-
ing.While we recognise that DNA sequencing will not be easily available to
everyone, the advantages greatly outweigh those of STS. The method used
to develop STS was sequencing of randomly amplified genome fragments
followed by the development of specific primers.These were then validated
by testing them against a panel of isolates of various STs. Now that much
more is known regarding diversity of Blastocystis, we feel that revalidation
would be appropriate. In our hands, the STS primers for ST4 amplify only
one of the two clades in this ST, at least in faecal DNA. As mentioned
above, only known STs can be detected and, as more have been named, the
specificity of STS has not been further explored nor the range of detect-
able STs expanded. STS is certainly of limited use if nonhuman samples are
of interest. STS typing is also more dependent on interpretation – size and
specificity of bands, for example – than is sequence analysis.
In contrast, SSU-rDNA sequencing is a pan-Blastocystis technique
and not limited to known STs. It has been shown that sequencing of the
­complete gene is not necessary for accurate ST classification, as long as a
diagnostic region is used that is known for all STs. Several regions of the
gene (Fig. 1.1) have been used by different authors for this purpose (Parkar
et al., 2010; Santín et al., 2011; Scicluna et al., 2006; Stensvold et al., 2006)
but in our hands the specificity of amplification and ease of sequencing of
the ‘barcode’ region (Scicluna et al., 2006) at the very 5′ end of the gene

Figure 1.1  Schematic representation of the Blastocystis SSU-rRNA gene. Examples

of the regions of the gene used for ST identification by various authors are indicated.
(Parkar et al., 2010; Santín et al., 2011; Scicluna et al., 2006; Stensvold et al., 2006)
Recent Blastocystis Research 5

make it the region of choice for subtyping.That is not to say it is universally

successful. It is likely that all of the primer pairs used occasionally produce
nonspecific amplicons, especially when screening DNA extracted directly
from faeces and when the sample is actually negative for Blastocystis.
The barcode region is by far the best represented in the databases, and
the correct ST can be identified by Basic Local Alignment Search Tool anal-
ysis in either GenBank or the new Blastocystis multilocus sequence typing
(MLST) database (; Jolley and Maiden, 2010;
Stensvold et al., 2012a). The latter has the added advantages of automati-
cally assigning allele types to the SSU-rDNA as well as using the consensus
ST nomenclature (unlike GenBank where the ST is included only if one
was part of the accession submission and no attempt to impose a standard
nomenclature is made). Because of the occasional problem of nonspecific
amplification, it is recommended that samples be screened first for positiv-
ity, where possible, using Real-Time PCR (Stensvold et al., 2012b) before
undertaking ST identification by sequencing.

3.1. Current Status
The use of numbers has the advantage of allowing new STs to be assigned
to novel sequences as they are discovered. However, this requires a consen-
sus, which does not as yet exist, on what the requirements are for designa-
tion of new STs.We suggest that new ST assignments be based on complete
or essentially complete SSU-rDNA sequences, not on just a small piece of
the gene like the barcode region, even though this may well be how their
novelty is first identified. In most cases, this should not be a burdensome
requirement, especially if cultures exist, but occasionally primary material
might be limited and inhibitors/nonspecific amplicons can interfere with
successful sequencing of some products.
An example of how necessary this approach can be exists in the case of
ST13. The ST was found in a Quokka (a marsupial) and named by Parkar
et al. (2010) in Australia, who showed it to cluster near ST5 in phylogenetic
trees.Their sequence consisted of the 3′ two-thirds of the SSU-rDNA, over
1000 bases (Fig. 1.1). Later, Petrášová et al. (2011) identified an infection
in a Colobus monkey in Tanzania as ST5 based on the sequence of the
5′ one-third of the gene – the barcode region defined by Scicluna et al.
(2006). The Colobus sequence was not identical to previously known ST5
sequences but that was the most closely related ST in the databases. In actual
6 C. Graham Clark et al.

fact, the Colobus sequence belonged to ST13. This only became appar-
ent when we compared the Colobus and Quokka sequences to a com-
plete ST13 sequence we had obtained independently (from a deer; Alfellani
et al., submitted). The overlap between the ‘barcode’ region and the Parkar
sequence is short and shows little variation among related STs. Hence the
link between the Petrášová et al. Colobus sequence and the available ST13
sequence was not obvious.
Nevertheless, agreement on how different a new sequence needs to
be before being considered a novel ST does not exist at present. In 2007,
only nine STs were known and all had been identified in humans. All
formed discrete clades in phylogenetic trees that were supported by maxi-
mum posterior probabilities in Bayesian analyses and very high bootstrap
values in maximum likelihood analyses.The minimum divergence between
sequences assigned to different STs was around 5%. As more hosts are sam-
pled and more sequence variants are discovered, two things are happening.
The amount of known diversity within existing STs is increasing and more
potentially new STs are being uncovered that differ by less than 5%. In our
opinion, when the divergence from known STs is less than this arbitrary
figure, care needs to be taken before assigning a new ST number unless sub-
stantial sampling has taken place. The reason for this is exemplified by ST3;
in this ST (and some others), the most divergent SSU-rDNA sequences
differ by almost 3%, yet the clade itself is strongly supported. If a single
new sequence is found that differs from others in a known clade by just
over 3%, one of two things can happen – 1. Additional sampling may ‘fill
in’ the gap between the new branch and the existing clade, indicating that
it is part of the same ST; or 2. Additional sampling will identify sequences
that are specifically related to the new variant and do not fall in-between,
in which case it can be considered a new ST. Initially, new variants will
often be represented by a single example and so the problem remains of
what to call them. In our opinion, a new sequence type that differs by 4%
or more can be considered a new ST with confidence. A sequence that
differs by less than 1.5% is most likely to fall within the range of variation
of an established ST. Those that fall between these cut-off values can be
tentatively assigned new ST numbers subject to confirmation by further
sampling; in a way this resembles the ‘Candidatus’ species names used for
bacteria although we would prefer not to use such a prefix for Blastocystis
STs! Ultimately, like species names, Blastocystis ST designations will be
accepted by those in the field or rejected as synonyms based on further data
(Boenigk et al., 2012).
Recent Blastocystis Research 7

One thing rarely mentioned is that the Blastocystis ST nomenclature

refers exclusively to organisms infecting birds and mammals, as these two
host groups share many of the same STs even though some host specific-
ity exists. Blastocystis is common in reptiles and amphibia, and has been
reported from other hosts, such as insects. The assumption exists that such
organisms are unlikely to overlap with the bird/mammal STs because of
the different body temperatures of the hosts. However, this need not always
be the case – one toad sequence reported belongs to ST5 (Yoshikawa et al.,
2004a). Nevertheless, most non-bird/non-mammal Blastocystis have their
own species names or at least do not cluster with bird/mammal STs. Should
interest lead to greater sampling of such hosts, perhaps a similar approach to
that outlined above will prove necessary to prevent the nomenclature from
becoming unwieldy.
When the consensus ST nomenclature was developed, nine STs were
recognised. Sampling from a wider range of hosts has led to five additional
STs being published; several additional unpublished STs are known to us.
We have no doubt that many more remain to be uncovered as more hosts
and more individuals within already-sampled hosts are studied. Therefore,
to discuss host specificity at this stage is certainly premature in that we
know the picture is incomplete. However, some general trends are starting
to emerge that are worth commenting on.
Of the nine definite STs detected in humans, only four are common –
ST1, ST2, ST3, and ST4.Together, these make up around 90% of all human
Blastocystis in surveys that involve subtyping (Alfellani et al., 2013). These
will be discussed further below.The other STs are only sporadically reported
in humans and may well prove to be the result of zoonotic transmission, as
they are mostly much more common in nonhuman hosts. ST5 is prevalent
in livestock, ST6 and ST7 occur frequently in birds, and ST8 is common in
some nonhuman primates (NHPs). Of the STs that are rare in humans, only
ST9 is yet to be reported from nonhuman sources.
Although ST5 is rare in humans, it is found commonly in captive apes,
although not in other NHPs (Stensvold et al., 2009a). Its highest frequency
seems to be in livestock, particularly cattle, pigs, sheep, and camels (­Stensvold
et al., 2009a). STs 6 and 7 have been detected primarily in ground-dwelling
birds, with only single ST7 samples from a goat and an NHP having been
found in nonhuman mammalian hosts (Alfellani et al., in press and submit-
ted). Other than in humans, ST8 appears to be restricted to arboreal NHPs
from Asia and South America—it has not been reported from ­African
NHPs (Alfellani et al., in press). The STs with numbers above 9 are, as far as
8 C. Graham Clark et al.

is known at present, confined to nonhuman hosts. Little experimental work

on host-specificity has been performed (Iguchi et al., 2007) and given that
diversity within STs may be linked to host range (see below), the results in
this respect must be seen as preliminary.

3.2. Intra-Subtype Diversity

As discussed above, analysis of SSU-rDNA sequences within certain STs
has revealed substantial genetic diversity (Scicluna et al., 2006; Yoshikawa
et al., 2009). Since SSU-rRNA genes are generally highly conserved within
species, this finding suggested that the study of variation within STs might
lead to further insights into host range and transmission patterns, as well
as potentially identifying surrogate markers for virulence. In particular, it
would help in determining the relevance of the subtyping system, which
could be too crude a classification tool. Investigations into genetic diversity
using non-SSU rRNA genes have therefore started. A MLST system has
been developed for ST3 and ST4 (Stensvold et al., 2012a). This is based on
the sequencing of 5–6 loci in the genome of the MLO (see below) chosen
for the presence of polymorphism. MLST systems for ST1 and ST2 are
currently in development, also based on markers in the MLO. MLST has
been used primarily in bacteria; its utility in eukaryotes is restricted by the
fact that most are diploid or have higher ploidy. The existence of heterozy-
gotes makes interpretation of the data much more difficult than in haploid
organisms. The organelle genome in Blastocystis is effectively haploid, but
this characteristic was only part of the reason for selecting the MLO as the
target for our MLST; very few nuclear gene sequences were available for
Blastocystis at the start of the project so options were limited!
Application of the MLST system to samples from humans and NHPs has
already led to some important observations.The phylogenetic tree obtained
from analysis of the SSU-rDNA sequence (the barcode region – Fig. 1.1;
Scicluna et al., 2006) is congruent with the one inferred from sequences of
loci in the MLO for both ST3 and ST4 (Stensvold et al., 2012a). Hence, the
MLST data have so far validated the use of the barcode region as a suitable
marker for inter- and intragenetic diversity.
The levels of intragenetic diversity in ST3 and ST4 differ dramatically.
MLST analyses of ST3 isolates showed a high discriminatory index com-
pared to the one obtained for ST4; in other words most strains can be
distinguished by MLST in ST3 while that is not the case for ST4. ST4
from humans shows a surprising degree of genetic homogeneity, with most
SSU-rDNA and MLO loci sequences being completely identical between
Recent Blastocystis Research 9

samples (Stensvold et al., 2012a). Conversely, many SNPs in MLO loci of

ST3 are shared by only a few strains or are unique. Importantly, the dif-
ferences between ST3 and ST4 are not attributable to the fact that ST4
samples were almost exclusively from humans, since the vast majority of the
ST3 alleles were detected within the human population. Due to the homo-
geneity of ST4, and perhaps also because of the fact that ST4 appears to be
absent or at least very rare in some parts of the world, we speculate that ST4
entered the human population relatively recently compared to ST3. ST4 is
common in Europe, but is rarely reported from Asian, Middle Eastern, and
South American populations; however, in many regions comparatively little
sampling has been undertaken.
ST3 is the most common ST in humans worldwide, and its occur-
rence is a frequent finding in analyses of ST distribution, irrespective of the
geographic origin of the population (Forsell et al., 2012; Malheiros et al.,
2011; Meloni et al., 2011; Nagel et al., 2012; Souppart et al., 2009, 2010;
Stensvold et al., 2009a, 2009b, 2011b).The high discriminatory index of the
ST3 MLST system makes it useful for surveillance of ST3 strains (reinfec-
tion or recrudescence; longevity of colonisation; patterns of transmission),
whereas that of ST4 would not be suitable for these purposes. Nevertheless,
two clades can be detected in ST4 SSU-rDNA and MLST analyses, one of
which consists mostly of nonhuman samples. Little is known about the host
range of ST4, but, in addition to humans, it has been found in rodents and
occasionally in NHPs (lemur (Santín et al., 2011; Stensvold et al., 2009d)
and woolly monkey (Stensvold et al., in preparation)).
Interestingly, MLST analysis of ST3 isolates from humans and NHPs
revealed that NHP ST3s are significantly more diverse than human ST3s,
most of which fell into one clade. Human ST3 samples are found only
rarely in the ‘NHP clades’ and are likely a result of zoonotic transmis-
sion, illustrated by the fact that one of the few such human isolates was
from an NHP keeper. In contrast, NHP samples were also detected in
the clade containing the vast majority of the human sequences. Together,
these results suggest that ST3 has largely co-evolved with humans, but
that either this co-evolution has been going on for a long time or ‘human
clade’ ST3 has entered the human population repeatedly from another
source. This is in contrast to ST4, where the same restriction of human
samples to one clade exists but little sequence diversity is detected, a
finding that implies a single and relatively recent origin in humans fol-
lowed by clonal expansion. ST3 has also been reported from a number of
nonprimate hosts and MLST analysis of such ST3s is needed to increase
10 C. Graham Clark et al.

our understanding of the currently observed cryptic host specificity and

thus the transmission and epidemiology of Blastocystis. Both clades of
ST4 have been detected in rodents but relatively little sampling has been
reported, so it is not yet clear whether these hosts are a significant reser-
voir for human colonisation.


The prevalence of Blastocystis is reported in many parasite sur-
veys performed across the world. Published infection rates fall anywhere
between 0.5 and 62%. A serious problem with such data is the often
highly selected nature of the population studied. Only rarely are the sur-
veys large enough or the population examined diverse enough to really
conclude that the infection rate reported is representative of the country/
cohort as a whole, yet that is often how the data are interpreted. A good
illustration of this is where more than one survey has been performed in
the same country. For example, two studies carried out in Malaysia found
prevalences of 15% (Suresh et al., 2001) and 52% (Noor Azian et al., 2007),
while two in Turkey reported 2% (Köksal et al., 2010) and 14% (Östan
et al., 2007). In Turkey, the studies were undertaken in different cities.
One surveyed school children (Östan et al., 2007), many of whom lived
in a shanty town, while the other surveyed adults. The diagnostic tech-
niques used, however, were basically the same. In Malaysia, the age range
of the populations was similar but one population lived in apartments in
the capital (Suresh et al., 2001) while the other (Noor Azian et al., 2007)
was in an aboriginal village settlement. In one of these Malaysian stud-
ies, a variety of techniques, including culture, were used for diagnosis of
infection, while the other involved microscopy only. In both countries,
the populations were demographically quite different in several ways and
whether either could be viewed as truly representative of the country as
a whole is debatable. The diagnostic technique used is potentially another
significant variable that can influence the reported prevalence (fresh stool
vs. fixed and concentrated; bright field vs. stained) as microscopy is gen-
erally thought to be less sensitive than culture, although the skill of the
microscopist is also a significant factor. In the future, it seems likely that
diagnostic PCR will become the tool of choice where it can be afforded,
which will make comparison of results with studies using only micros-
copy even more difficult.
Recent Blastocystis Research 11


5.1. Prevalence and Intensity of Infection
Like the simple population prevalence surveys, many comparisons of Blas-
tocystis prevalence in symptomatic and asymptomatic individuals have been
published. Approximately equal numbers of papers report significantly
higher prevalences of Blastocystis in symptomatic individuals and no sig-
nificant difference at all. Here, some of the same variables are notable con-
founding factors – how can studies be compared in which researchers have
variously used fixed material or fresh, direct or concentrated samples, iodine,
trichrome, or haematoxylin as the stain for microscopy? Furthermore, shed-
ding of Blastocystis may be cyclical (Vennila et al., 1999), yet it is unusual for
more than one stool sample to be examined. However, when the aim is to
explore links to disease, the main complication is again the selection of the
populations—in this case, the definitions of symptomatic and asymptomatic
and comparability of the symptomatic group and the asymptomatic con-
trols. Most, if not all, investigations have been cross-sectional, meaning that
carriers will have harboured Blastocystis for different periods of time, which
may affect whether they are experiencing symptoms, if acquired immunity
to Blastocystis plays a role in symptom resolution.
Since Blastocystis is a faecal-orally transmitted parasite, carriers will also
have been exposed to other intestinal organisms, some of which may be
pathogens, at the time of Blastocystis colonisation. Most association studies
do not exclude all other possible origins of the symptoms. Likewise, most
control populations are not case-matched and there is some suggestion that
‘asymptomatic’ individuals who volunteer for such studies do not represent
a random selection but may have a history of intestinal problems (Stensvold
et al., 2009b, 2011a). However, one of the most peculiar variables used is the
fact that some studies define colonisation with Blastocystis as having more
than 5 organisms per microscope field. The rationale for this is unexplained
– why would having 4 vs. 6 organisms per field be a significant difference?
The recent descriptions of Real-Time PCR diagnostic tools for Blastocys-
tis (Poirier et al., 2011; Stensvold et al., 2012b) will make detection of the
organisms easier as well as allowing exploration of any role for infection
intensity in symptomatology.
One might assume that animal models are an obvious way of poten-
tially establishing a link between Blastocystis and pathology. However, the
studies performed to date are, in our opinion, inconclusive. For example,
12 C. Graham Clark et al.

experimental infections of laboratory mice (Elwakil and Hewedi, 2010)

resulted in tissue invasion – something never reported in humans. Another
study showed increased oxidative stress in Blastocystis—infected rats
­(Chandramathi et al., 2010)—again something not linked to human coloni-
sation. Studies that provided evidence for induction of cytokines, contact-
mediated apoptosis, and barrier disruption all used axenic Blastocystis and
in vitro mammalian cell cultures, with no evidence provided that these
effects occur in vivo. One other issue is the use of appropriate controls – for
example, experimental infection of animals with Blastocystis from cultures
growing in the presence of bacteria need to have the appropriate controls –
namely, exposure to the accompanying bacterial flora alone – before it can
be concluded that Blastocystis is responsible for any effects seen (Hussein
et al., 2008). It has to be said that, to date, animal models are not showing
much promise in resolving the question of the pathogenic potential of

5.2. Links to Irritable Bowel Syndrome

One of the popular associations made in the literature is between Blasto-
cystis and Irritable Bowel Syndrome (IBS; Poirier et al., 2012). There are
two reasons for this. The most telling is that people diagnosed with IBS
appear in several studies to have a much higher infection rate with Blas-
tocystis – often twice as high or more (Giacometti et al., 1999; Jimenez-
Gonzalez et al., 2012;Yakoob et al., 2004, 2010). The second is that many
of the symptoms ascribed to Blastocystis infection are very similar to those
defining some types of IBS (diarrhoea, vomiting, abdominal cramps, and
bloating), suggesting either that Blastocystis colonisation may be a differen-
tial diagnosis or that Blastocystis is the causative agent in some cases of IBS.
Alternatively, it could mean that Blastocystis colonises the IBS gut more
efficiently than a healthy gut. As mentioned above, the presence of Blasto-
cystis means exposure to faecal organisms and so superficially at least the
data support a link between faecal exposure and IBS rather than a specific
link to Blastocystis.
A diagnosis of IBS should include the exclusion of other potential
causes of the symptoms, but it is not always possible to tell from publica-
tions whether this has been done and what pathogens have been excluded;
it is unlikely that every possible intestinal disease agent has been tested
for. IBS is also not a disease with a unique and specific diagnosis; it is a
syndrome having several different forms. Diagnosis is currently based on
the Rome III criteria: “Recurrent abdominal pain or discomfort at least
Recent Blastocystis Research 13

3 days per month in the last 3 months associated with 2 or more of the
• Improvement with defecation
• Onset associated with a change in frequency of stool
• Onset associated with a change in form (appearance) of stool
The ‘change in frequency’ covers diarrhoea (IBS-D) and constipation (IBS-
C) or alternation of the two (IBS-M), yet in several Blastocystis studies these
are not differentiated.
One illustration of the problem can be found in the study by Giacometti
et al. (1999) in Italy. The authors compared Blastocystis prevalence in IBS
patients (15/81) to that in patients with other gastrointestinal complaints
(23/307) and found it to be significantly different (p = 0.006). However,
when the IBS patients were followed up 6 months later, 53/72 returning
patients no longer met the criteria for a diagnosis of IBS. Since IBS is con-
sidered a chronic disease, this calls into question the original diagnosis as
such a high rate of ‘cure’ would not be expected.
In a study in Pakistan, Hussain et al. (1997) found that levels of anti-
body against Blastocystis were higher in patients with IBS than in controls
but, surprisingly, levels in IBS patients were the same whether the parasite
was detected concurrently or not. In Mexico and Thailand, three studies
failed to show a higher prevalence of Blastocystis in IBS patients (Ramirez-
Miranda et al., 2010; Surangsrirat et al., 2010; Tungtrongchitr et al., 2004).
One of the factors that make the interpretation of all these studies of
Blastocystis/IBS prevalence and association difficult is the existence of nine
STs in humans that, as judged by molecular criteria, could be considered
distinct species. More than 20 countries have been surveyed for the range
of STs present and this number is gradually increasing. Differences in the
STs present in a country could be responsible for the differing conclusions
from research investigating links between Blastocystis and disease. However,
only a small number of studies to date have compared distribution of STs in
symptomatic and asymptomatic individuals.
From the geographic ST surveys (Table 1.1), several interesting observa-
tions have emerged. The first is a technical one. Surveys that use the STS
method of subtyping detect ST6 and ST7 at a much higher frequency on
average than those using SSU-rDNA sequencing. It is difficult to interpret
this, however, as the STS method is most widely used in continental Asia
and there are no comparable sequencing studies in the same countries that
can be compared to STS. The exception to this disjunction is Egypt, where
two STS studies found many ST6 and ST7 (48/144) but sequencing did
Table 1.1  ST Geographic Distributions
ST distribution
Country of No. of Mixed Unknown
samples Technique samples ST1 ST2 ST3 ST4 ST5 ST6 ST7 ST8 ST9 ST ST Reference
Germany RFLP 166 35 1 110 12 – – – – – 8 – Böhm-­
et al., 1997
UK RFLP 29 2 1 22 4 – – – – – – – Clark, 1997
Japan STS 32 1 – 30 – – 1 – – – – – Yoshikawa
et al., 2000
Japan RFLP 64 11 13 30 7 – – – – – – 3 Kaneda
et al., 2001
Thailand RFLP 153 138 – 7 – – – 2 – – 6 Thathaisong
et al., 2003
Japan STS 50 4 – 26 2 – 11 5 – 2 – – Yoshikawa
et al., 2004b
Bangladesh STS 26 2 – 24 – – – – – – – – Yoshikawa
et al., 2004b
Pakistan STS 10 2 – 7 – – 1 – – – – – Yoshikawa
et al., 2004b
Germany STS 12 3 2 5 2 – – – – – – – Yoshikawa
et al., 2004b
Thailand STS 4 1 – 1 – – 1 – – – 1 – Yoshikawa
et al., 2004b
Philippines RFLP 12 10 – – – – – – – – – 2 Rivera and
Tan, 2005
Denmark Sequencing 29 1 6 15 7 – – – – – – – Stensvold
et al., 2006
UK Sequencing 49 2 8 20 16 – – 1 1 – 1 – Scicluna et al.,
China STS 35 13 – 14 – – – 2 – – 5 1 Yan et al.,
Denmark Sequencing 28 5 9 13 1 – – – – – – – Stensvold
et al., 2007a
China STS 192 47 9 116 1 – 1 – – – 10 8 Li et al., 2007
Egypt STS 44 8 – 24 – – 8 4 – – – – Hussein et al.,
Greece SSCP 45 9 6 27 1 – 1 1 – – – – Menounos
et al., 2008
Malaysia STS 20 9 1 10 – – – – – – – – Tan et al.,
Ireland Sequencing 14 1 6 4 3 – – – – – – – Scanlan and
Iran RFLP 45 20 4 16 – – – – – – – 5 Motazedian
et al., 2008
Turkey Sequencing 87 8 12 66 1 – – – – – – – Özyurt et al.,
Singapore RFLP 9 2 – 7 – – – – – – – – Wong et al.,
Turkey STS 92 17 20 51 – – – – – – 4 – Dogruman-Al
et al., 2008
Spain RFLP 51 1 2 – 48 – – – – – – – Domínguez-
et al., 2009
Table 1.1  ST Geographic Distributions—cont’d
ST distribution
Country of No. of Mixed Unknown
samples Technique samples ST1 ST2 ST3 ST4 ST5 ST6 ST7 ST8 ST9 ST ST Reference
France Sequencing 40 8 4 20 4 – – 1 – – 3 – Souppart et al.,
Nepal STS 20 4 4 12 – – – – – – – – Yoshikawa
et al., 2009
Malaysia STS 40 5 – 20 – – 11 2 – – – 2 Tan et al.,
Turkey STS 32 20 3 9 – – – – – – – – Eroglu et al.,
Denmark Sequencing 99 20 15 39 16 – 1 – 1 – 7 – Rene et al.,
Denmark Sequencing 116 21 22 21 20 – – 5 – 1 26 – Stensvold
et al., 2009b
Turkey STS 19 0 8 10 – – – – – – 1 – Dogruman-Al
et al., 2009a
Turkey STS 66 10 9 38 – – – – – – 9 – Dogruman-Al
et al., 2009b
Egypt Sequencing 20 3 4 12 – – – – – – 1 – Souppart et al.,
Pakistan STS 179 87 10 49 8 7 6 10 – – – 2 Yakoob et al.,
Turkey STS 25 9 6 10 – – – – – – – – Eroglu and
Koltas, 2010
France Sequencing 27 1 1 4 17 – 1 3 – – – – Poirier et al.,
Colombia Sequencing 12 4 3 4 – – – – – – 1 – Santín et al.,
Denmark Sequencing 25 1 4 1 19 – – – – – – – Stensvold
et al., 2011a
Denmark Sequencing 22 9 11 – – – – – – – 2 – Stensvold
et al., 2011b
Italy Sequencing 30 2 5 13 6 – – – – – 4 – Meloni et al.,
Brazil Sequencing 66 27 21 11 7 Malheiros
et al., 2011
Egypt STS 100 15 – 39 – – 23 13 – – 10 – Fouad et al.,
Sweden Sequencing 63 10 9 30 13 – – 1 – – – Forsell et al.,
Total 2299 608 239 987 208 7 66 50 2 3 106 23
Reports using different techniques and older terminologies have been translated into the consensus terminology of STs (Stensvold et al., 2007a).
RFLP = restriction fragment length polymorphism; SSCP = Single strand conformation polymorphism; Sequencing = partial or complete SSU-rRNA gene.
18 C. Graham Clark et al.

not (0/20). Nevertheless, it is possible that ST6 and ST7 are simply more
common in humans in Asia.
The second observation has to do with the distribution of ST4. This ST
is very common in Europe (often the second most common ST found after
ST3), but apparently absent in Egypt, Libya, Iran, Nepal, the Philippines,
Thailand, Malaysia, and Brazil, and rare in many other countries (see sum-
mary in (Alfellani et al., 2013). Again, there may be some link to the method
used (STS in Asia) but not in all countries, as sequencing was used in the
studies from Libya and Brazil, for example. One possible explanation would
be an inability of the STS method to amplify certain clades within STs (as
discussed earlier). However, if this is the case, more unidentified Blastocystis
isolates would be expected in STS analysis, and these are not commonly
reported. Thus, it appears that ST4 has a very uneven distribution across
the world, with the focus being in Europe – perhaps that is where this ST
entered into the human population in the recent past – while STs 6 and 7
are rare in humans outside of Asia. There is no immediately obvious reason
why humans in Europe might be more exposed to rodents and those in Asia
to birds, so zoonotic transmission seems an unlikely explanation. Perhaps
some dietary, cultural, or other demographic variables are responsible – at
present, it is not useful to speculate.
Three studies have investigated the possibility of a link between Blasto-
cystis STs and IBS. However, the results are very inconsistent. In Pakistan
(Yakoob et al., 2010) and Egypt (Fouad et al., 2011), significant differences
in ST distribution were found, with ST1 being much more common in IBS
patients than controls. A study in the UK found ST4 to be more common
and ST1 less so in patients from IBS clinics than in other diagnostic labora-
tory samples, but not reaching statistical significance (Alfellani et al., 2013).
Again, there was a difference in methodology (STS vs. sequencing) as well
as many other variables, not the least of which is geography and the pres-
ence of ST4, so the potential relationship needs further investigation. What
can be concluded is that no single ST is found in IBS patients. Perhaps this
is not surprising, given the variability in the combination of symptoms that
can lead to a diagnosis of IBS.

5.3. Case Studies

The other source of information on the link between ST and symptoms
has been individual case studies. In such reports, an individual with gastro-
intestinal symptoms, Blastocystis infection, and no other identifiable cause is
investigated and treated. Often the report correlates clearance of the parasite
Recent Blastocystis Research 19

with resolution of symptoms and, in the recent past, the ST of the organ-
ism present has often been determined. There are two problems with such
reports.The first is that the drugs used to ‘eliminate’ Blastocystis are many and
varied but have no known specificity for the parasite. It seems equally likely
that the treatment perturbs the intestinal flora, indirectly making it a poor
or unsuitable habitat for Blastocystis.The second problem is that all common
STs and certain others have been linked with symptoms, which seems an
unlikely situation (Dogruman-Al et al., 2008; Domínguez-Márquez et al.,
2009; Jones et al., 2009; Stensvold et al., 2008, 2011a; Vassalos et al., 2010;
Vogelberg et al., 2010). Treatment of Blastocystis colonisation is contentious
and no widely accepted drug regimen exists (Stensvold et al., 2010). It is
certainly not surprising that STs differ in their susceptibility to drugs, given
the large genetic differences that exist between them (Mirza et al., 2011),
and in vitro drug resistance has been generated successfully in the laboratory
(Dunn et al., 2012).

5.4. The Way Forward?

To summarise current data on the relationship between Blastocystis and
disease is not easy, since we feel that the definitive investigations are yet to
be carried out. Because of the valid argument that if disease is associated
with one ST, the signal may be masked when the overall prevalence in a
population is considered, we believe that it is necessary for subtyping to
be performed, sequencing should be used if possible in preference to the
indirect STS method, and DNA extracted directly from faeces should be
used in preference to cultures, in case cultivation selects in favour of cer-
tain STs. It is possible that Blastocystis is a pathogen but that this is unlinked
to the ST of the organism. Nevertheless, subtyping should be done if only
to rule this out as a variable. It is also important that studies be carried
out in more than one country, given the apparent geographic differences
in ST distribution. For example, ST4 is prevalent in Europe and has been
linked to symptoms in more than one investigation. If ST4 is the only ST
linked to disease, a study in a country where the ST has not been reported
or is rare will not reveal an association of Blastocystis with disease even if
one exists.
The appropriate study population is difficult to define. The presence of
4 common STs (in Europe at least) means that more individuals are needed
in order to have the same power to detect an association. Most crucial of all
are the faecal samples themselves. An advantage of using IBS patients is that
they have usually had an extensive microbiological workup to eliminate
20 C. Graham Clark et al.

other pathogens as a cause of their symptoms, which is a deficiency in many

other studies. However, it seems unlikely that if Blastocystis causes IBS, it is
responsible for both IBS-D and IBS-C. The question remains of how to
obtain a suitable control group for IBS patients.
In many cultures, people are very happy to provide blood samples but
reluctant to donate faecal specimens unless they are ill, which has impaired
the ability of controlled studies to be undertaken in many countries. Nev-
ertheless, research has been successfully undertaken where a large number
of individuals with gastrointestinal symptoms and a similarly large asymp-
tomatic population of individuals have been sampled for investigation of
intestinal pathogens (e.g.Tam et al., 2012). Unfortunately, Blastocystis has not
been included in those studies.
An alternative approach is to identify a smaller number of individuals
infected with Blastocystis but no other potential pathogen, and then match
these as closely as possible with asymptomatic controls. Recruitment of
individuals from web panels (for instance, the ‘YouGov’ panel in Denmark)
has previously been used successfully to obtain data on the prevalence of
gastrointestinal symptoms in the background population (Reimer and
Bytzer, 2009). Again, the presence of 4 common STs means that the sample
numbers needed might make this approach difficult. It is also possible that
symptoms resulting from Blastocystis infection are acute but resolve, and
we have no knowledge of how long Blastocystis colonisation may persist
for afterwards. Until appropriate studies are performed and a clear answer
obtained, the question of whether Blastocystis is a pathogen will continue to
be contentious.
Whatever the ultimate outcome, it must be emphasised that infection
with Blastocystis is a surrogate marker for exposure to faecal contamination,
and in an individual with symptoms and Blastocystis colonisation, an infec-
tious agent (whether it is Blastocystis or not) seems the most likely cause.

Other than investigations into Blastocystis diversity and the role of the
organism in disease, the most important recent advances have been those
involving genome studies. These consist of projects that have given rise to
the sequences of one nuclear genome and several mitochondrial genomes.
The latter represent a number of different STs and, as mentioned earlier,
these sequences have been the basis for development of MLST schemes for
the most common STs.
Recent Blastocystis Research 21

6.1. Blastocystis MLO Genomes

The presence of MLOs in Blastocystis was for many years an enigma as it was
unclear why a strictly anaerobic eukaryote needs an organelle traditionally
associated with aerobic metabolism. Nevertheless, it was shown quite early
on using DNA stains that these organelles contain DNA and this attracted
the attention of those interested in organelle evolution. The presence of
mitochondrion-derived organelles had been the subject of investigation for
some years but it became clear that the mitosomes of Entamoeba, micro-
sporidia, and Giardia and the hydrogenosome of Trichomonas are actually
quite different end products of reductive evolution from the mitochon-
drial endosymbiont, and none have retained any trace of a genome in the
organelle (van der Giezen, 2009). The possibility that the Blastocystis MLO
represents an intermediate step in the ‘degeneration’ of the mitochondrion
is intriguing.
Three MLO genomes were published almost simultaneously, represent-
ing by chance three different STs, one from each of the three main clades
of human Blastocystis: ST1, ST4 (Pérez-Brocal and Clark, 2008), and ST7
(Wawrzyniak et al., 2008). All three encode the same 27 proteins and 18
RNAs, and the gene order is identical. The 27.7–29.2 kb genomes were
found to contain several nad genes, encoding proteins of mitochondrial
Complex I, and ribosomal protein genes; none of the genes encoding cyto-
chromes and ATPase subunits found in other stramenopile genomes are
present. A reduced set of tRNA genes identified in the Blastocystis MLO
genome implies that tRNAs for some codons must be nuclear encoded and
imported from the cytoplasm.

6.2. Blastocystis Nuclear Genome

Of all stramenopile nuclear genomes sequenced to date, the one from Blas-
tocystis strain B (ST7) is the smallest. It is just under 19 Mb in size and
contains about 6000 genes, which is just over half the number in the stra-
menopile genome with the next lowest number of genes (see Table 1.2).
It is also relatively intron rich, but its introns are by far the smallest found
among stramenopiles as the median size is only 32 bp (Denoeud et al.,
2011). Although it is useful to make comparisons with other stramenopile
genomes, those genomes available are of relatively distant species, and none
are for human pathogens. Although the Phytopthora and Pythium genomes
can provide some useful reference material because of the pathogenic
nature of these organisms (in plants), it should not be forgotten that Blasto-
cystis is the only anaerobe among the sequenced stramenopiles, and hence
Table 1.2  Comparison of Several Features of Stramenopile Genomes
Average GC Average Introns/
Species Size (Mb) Chromosomes Genes gene length content Introns intron length gene Reference
Blastocystis sp. 18.8 15 6020 1299 – 18,560 32 bp 3.1 Denoeud et al., 2011
Ectocarpus 195.8 – 16,256 6859 54% 113,619 704 bp 6.98 Cock et al., 2010
Thalassiosira 34.3 24 11,242 992 47% 15,739 – 1.4 Armbrust et al.,
pseudonana 2004
Phytophthora 240.0 8–10 17,797 1523 51% – 125 bp – Haas et al., 2009
Phytophthora 95 – 19,027 1613 54% – 124 bp – Tyler et al., 2006
Phytophthora 65 – 15,743 1625 54% – 123 bp – Tyler et al., 2006
Phaeodactylum 27.4 33 10,402 – – 8169 – 0.79 Bowler et al., 2008
Pythium 42.8 – 15,290 – 52% 24,464 115 bp 1.6 Lévesque et al., 2010

C. Graham Clark et al.

Several more stramenopile genome projects are currently ongoing but not all information for inclusion in this table is readily available.
‘–’ = data not available.
Recent Blastocystis Research 23

the special features of its genome could have been driven by environmental
factors as well as being reflective of its evolutionary distance from the other
sequenced stramenopiles.
Nonetheless, it might be useful to look at the presence of potential
effector proteins encoded in the Blastocystis genome and other proteins
that might play a role in pathogenesis. Such analyses might provide useful
avenues for exploring the potential pathogenicity of this organism. Many
eukaryotic pathogens use effector proteins to remodel their host's cells/
tissues into more suitable niches for proliferation. If Blastocystis is truly a
pathogen, then one might expect it to use strategies similar to those of
other eukaryotic pathogens, perhaps in particular those used by Phytoph-
thora species. Effectors are molecules that either facilitate infection (viru-
lence factors or toxins) or that trigger host defence (avirulence factors
or elicitors) (Kamoun, 2006). In order to be able to affect the host, these
effectors need to be secreted by the pathogen, and analysis of the Blastocys-
tis genome using SignalP has suggested that 307 proteins contain secretion
signals (Denoeud et al., 2011). Whether these potentially secreted proteins
contain any additional host cell targeting signals, such as the Plasmodium
RxLxE/D/Q motif, or the Phytophthora infestans RxLR motif (Haldar
et al., 2006) still needs to be investigated. Among the proteins making up
the putative Blastocystis secretome are hydrolases, proteases, and protease
inhibitors. The latter are generally involved in protecting parasite proteins
from degradation.The Blastocystis genome encodes a cystatin A homologue,
a type-1 proteinase inhibitor and an endopeptidase inhibitor-like protein
(Denoeud et al., 2011). However, only one of these seems to encode a
putative secretion signal, using SignalP, and none contain the Kazal-like
domains that are often found in secreted protease inhibitors of eukaryotic
parasites (Haldar et al., 2006). The genome is predicted to encode several
hydrolases that might be involved in attacking host tissue (Denoeud et al.,
2011), although tissue invasion by Blastocystis has never been observed in
humans.The most likely possible effectors found in the Blastocystis genome
are cysteine proteases, considering that these genes are also present in large
numbers in the pathogenic protist Entamoeba histolytica (Bruchhaus et al.,
2003). Nonetheless, these predictions all need further elucidation in the
laboratory in order to determine whether they have any role in pathogen-
esis and disease and to prove that they are secreted. Two secreted proteases
have recently been characterised (Wawrzyniak et al., 2012). It is antici-
pated that more STs will have their genomes sequenced in the near future.
This will help to confirm that the oddities of the ST7 genome apply to
24 C. Graham Clark et al.

all Blastocystis and are not ST-specific, and so are relevant to the common
human-infective STs.
In common with other protistan genomes (Carlton et al., 2007; ­Loftus
et al., 2005), Blastocystis seems to contain a number of genes that may
have been acquired by lateral gene transfers. Two possible red algal genes
might hint at a lost chromalveolate plastid while others might be involved
in some aspects of anaerobic fermentation (Denoeud et al., 2011). The
anaerobic nature of Blastocystis combined with the presence of MLOs with
cristae that are capable of taking up active dyes such as Rhodamine 123
(Nasirudeen and Tan, 2004) has sparked an interest in the nature of these
organelles (Denoeud et al., 2011; Lantsman et al., 2008; Stechmann et al.,
2008). Unlike classic mitochondria, the Blastocystis organelles contain the
enzymatic capability to convert pyruvate into CO2 and H2 using enzymes
normally encountered in hydrogenosomes (van der Giezen, 2009).
Although hydrogen production has not been detected (Lantsman et al.,
2008), the enzyme hydrogenase does localise to the organelle (Stechmann
et al., 2008). Furthermore, the organelle contains the unusual acetate:
­succinate-CoA transferase shuttle, which allows for the production of ATP
via substrate-level phosphorylation. The absence of cytochromes had been
reported early on (Zierdt, 1986), so the lack of mitochondrial Complex
III and IV components in the genome came as no surprise. Many genes
encoding proteins that make up Complex I, possibly involved in proton
pumping, have been detected, as has a complete Complex II (Denoeud
et al., 2011; Stechmann et al., 2008). As no further downstream electron
transport chain components have been found, the question whether Com-
plex II functions as a succinate dehydrogenase, as in classical mitochondria,
or as a fumarate reductase, is still open. Because of the anaerobic nature
of Blastocystis, a fumarate reductase using rhodoquinone seems a plausi-
ble possibility. Currently, the terminal electron acceptor (Denoeud et al.,
2011) seems to be the alternative oxidase (Standley and van der Giezen,
2012) but the choice of molecular oxygen as a substrate seems odd for an
intestinal organism.
Overall, the complete genome of Blastocystis (Denoeud et al., 2011)
has confirmed many previous studies (Lantsman et al., 2008; Stechmann
et al., 2008; Zierdt, 1986; Zierdt et al., 1988) with respect to the bio-
chemical nature of the MLO but several questions still remain. Perhaps
the most significant one relates to the anaerobic status of this organism
(Zierdt, 1986), as its genome suggests that it most likely is not a strict
anaerobe after all.
Recent Blastocystis Research 25

It is probable that new genomes will become available in the
­immediate future, both from MLOs and from nuclei of different STs, and
hopefully also from non-bird/non-mammalian Blastocystis as well, so that
features common to Blastocystis can be distinguished from those that may be
lineage-specific adaptations. We fully expect that surveys of Blastocystis STs
from previously unsampled regions of the world will be forthcoming. The
current impression of ST distribution being geographically disjunct might
be affirmed by such studies, or they may result in ST prevalence numbers
being seen as part of a continuum from common to absent. Further sam-
pling of an increasing range of nonhuman hosts will also help confirm or
refute the current impression of partial host-specificity of certain STs and
The situation regarding the role of Blastocystis in disease is more ­difficult
to predict as the necessary investigations will be expensive and time-­
consuming to conduct in a way that will give unambiguous answers. They
will also have to be carried out in different parts of the world, given the
observed geographic variation in ST prevalence. Nevertheless, we feel that
these are the most important types of study to perform, because until the
uncertainty surrounding the role of Blastocystis in disease is settled, it seems
likely that it will continue to be dismissed by many clinicians as an organism
of no importance. In the meantime, screening by Real-Time PCR and bar-
code-sequencing of Blastocystis in human cohorts with varying symptoms
and different geographic origins will continue to provide useful prevalence,
ST, and parasite load data.

Alexeieff, A., 1911. Sur la nature des formations dites “Kystes de Trichomonas intestinalis”.
C. R. Soc. Biol. 71, 296–298.
Arisue, N., Hashimoto, T., Yoshikawa, H., Nakamura, Y., Nakamura, G., Nakamura, F., Yano,
T.-A., Hasegawa, M., 2002. Phylogenetic position of Blastocystis hominis and of stra-
menopiles inferred from multiple molecular sequence data. J. Eukaryot. Microbiol. 49,
Alfellani, M.A., Stensvold, C.R., Vidal-Lapiedra, A., Onuoha, E.S.U., Fagbenro-Beyioku,
A.F., Clark, C.G., 2013. Variable geographic distribution of Blastocystis subtypes and its
potential implications. Acta Trop. 126, 11–18.
Alfellani, M.A., Jacob, A.S., Ortíz Perea, N., Krecek, R.C., Taner-Mulla, D., Verweij, J.J.,
Levecke, B., Tannich, E., Clark, C.G., Stensvold, C.R. Diversity and distribution of
Blastocystis sp. subtypes in non-human primates. Parasitology (in press).
26 C. Graham Clark et al.

Armbrust, E.V., Berges, J.A., Bowler, C., Green, B.R., Martinez, D., Putnam, N.H., Zhou, S.,
Allen, A.E., Apt, K.E., Bechner, M., Brzezinski, M.A., Chaal, B.K., Chiovitti, A., Davis,
A.K., Demarest, M.S., Detter, J.C., Glavina, T., Goodstein, D., Hadi, M.Z., Hellsten, U.,
Hildebrand, M., Jenkins, B.D., Jurka, J., Kapitonov, V.V., Kröger, N., Lau, W.W.Y., Lane,
T.W., Larimer, F.W., Lippmeier, J.C., Lucas, S., Medina, M., Montsant, A., Obornik, M.,
Parker, M.S., Palenik, B., Pazour, G.J., Richardson, P.M., Rynearson, T.A., Saito, M.A.,
Schwartz, D.C., Thamatrakoln, K., Valentin, K., Vardi, A., Wilkerson, F.P., Rokhsar, D.S.,
2004.The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metab-
olism. Science 306, 79–86.
Boenigk, J., Ereshefsky, M., Hoef–Emden, K., Mallet, J., Bass, D., 2012. Concepts in protistol-
ogy: species definitions and boundaries. Eur. J. Protistol. 48, 96–102.
Böhm-Gloning, B., Knobloch, J., Walderich, B., 1997. Five subgroups of Blastocystis hominis
isolates from symptomatic and asymptomatic patients revealed by restriction site analysis
of PCR-amplified 16S-like rDNA. Trop. Med. Int. Health 2, 771–778.
Bowler, C.,Allen,A.E., Badger, J.H., Grimwood, J., Jabbari, K., Kuo,A., Maheswari, U., M ­ artens,
C., Maumus, F., Otillar, R.P., Rayko, E., Salamov, A.,Vandepoele, K., Beszteri, B., Gruber,
A., Heijde, M., Katinka, M., Mock, T., Valentin, K., Verret, F., Berges, J.A., Brownlee, C.,
Cadoret, J.-P., Chiovitti, A., Choi, C.J., Coesel, S., De Martino, A., Detter, J.C., Durkin,
C., Falciatore, A., Fournet, J., Haruta, M., Huysman, M.J.J., Jenkins, B.D., Jiroutova, K.,
Jorgensen, R.E., Joubert, Y., Kaplan, A., Kröger, N., Kroth, P.G., La Roche, J., Lindquist,
E., Lommer, M., Martin-Jézéquel, V., Lopez, P.J., Lucas, S., Mangogna, M., McGinnis,
K., Medlin, L.K., Montsant, A., Oudot-Le Secq, M.-P., Napoli, C., Obornik, M., Parker,
M.S., Petit, J.-L., Porcel, B.M., Poulsen, N., Robison, M., Rychlewski, L., Rynearson,T.A.,
Schmutz, J., Shapiro, H., Siaut, M., Stanley, M., Sussman, M.R.,Taylor, A.R.,Vardi, A., von
Dassow, P., Vyverman, W., Willis, A., Wyrwicz, L.S., Rokhsar, D.S., Weissenbach, J., Arm-
brust, E.V., Green, B.R.,Van de Peer,Y., Grigoriev, I.V., 2008. The Phaeodactylum genome
reveals the evolutionary history of diatom genomes. Nature 456, 239–244.
Bruchhaus, I., Loftus, B.J., Hall, N., Tannich, E., 2003. The intestinal protozoan parasite Ent-
amoeba histolytica contains 20 cysteine protease genes, of which only a small subset is
expressed during in vitro cultivation. Eukaryot. Cell 2, 501–509.
Brumpt, E., 1912. Blastocystis hominis n. sp. et formes voisines. Bull. Soc. Pathol. Exot. 5,
Carlton, J.M., Hirt, R.P., Silva, J.C., Delcher, A.L., Schatz, M., Zhao, Q., Wortman, J.R.,
Bidwell, S.L., Alsmark, U.C.M., Besteiro, S., Sicheritz–Ponten, T., Noel, C.J., Dacks, J.B.,
Foster, P.G., Simillion, C., Van de Peer, Y., Miranda–Saavedra, D., Barton, G.J., Westrop,
G.D., Müller, S., Dessi, D., Fiori, P.L., Ren, Q., Paulsen, I., Zhang, H., Bastida-Corcuera,
F.D., Simoes-Barbosa, A., Brown, M.T., Hayes, R.D., Mukherjee, M., Okumura, C.Y.,
Schneider, R., Smith, A.J.,Vanacova, S.,Villalvazo, M., Haas, B.J., Pertea, M., Feldblyum,
T.V., Utterback, T.R., Shu, C.-L., Osoegawa, K., de Jong, P.J., Hrdy, I., Horvathova, L.,
Zubacova, Z., Dolezal, P., Malik, S.-B., Logsdon Jr., J.M., Henze, K., Gupta, A., Wang,
C.C., Dunne, R.L., Upcroft, J.A., Upcroft, P., White, O., Salzberg, S.L., Tang, P., Chiu,
C.-H., Lee,Y.-S., Embley,T.M., Coombs, G.H., Mottram, J.C.,Tachezy, J., Fraser-Liggett,
C.M., Johnson, P.J., 2007. Draft genome sequence of the sexually transmitted pathogen
Trichomonas vaginalis. Science 315, 207–212.
Chandramathi, S., Suresh, K., Shuba, S., Mahmood, A., Kuppusamy, U.R., 2010. High levels
of oxidative stress in rats infected with Blastocystis hominis. Parasitology 137, 605–611.
Clark, C.G., 1997. Riboprinting: a tool for the study of genetic diversity in microorganisms.
J. Eukaryot. Microbiol. 44, 277–283.
Cock, J.M., Sterck, L., Rouzé, P., Scornet, D., Allen, A.E., Amoutzias, G., Anthouard, V.,
Artiguenave, F., Aury, J.-M., Badger, J.H., Beszteri, B., Billiau, K., Bonnet, E., Both-
well, J.H., Bowler, C., Boyen, C., Brownlee, C., Carrano, C.J., Charrier, B., Cho, G.Y.,
Coelho, S.M., Collén, J., Corre, E., Da Silva, C., Delage, L., Delaroque, N., Dittami,
Recent Blastocystis Research 27

S.M., Doulbeau, S., Elias, M., Farnham, G., Gachon, C.M.M., Gschloessl, B., Heesch,
S., Jabbari, K., Jubin, C., Kawai, H., Kimura, K., Kloareg, B., Küpper, F.C., Lang, D., Le
Bail, A., Leblanc, C., Lerouge, P., Lohr, M., Lopez, P.J., Martens, C., Maumus, F., Michel,
G., Miranda-Saavedra, D., Morales, J., Moreau, H., Motomura, T., Nagasato, C., Napoli,
C.A., Nelson, D.R., Nyvall-Collén, P., Peters, A.F., Pommier, C., Potin, P., Poulain, J.,
Quesneville, H., Read, B., Rensing, S.A., Ritter, A., Rousvoal, S., Samanta, M., Samson,
G., Schroeder, D.C., Ségurens, B., Strittmatter, M., Tonon, T., Tregear, J.W., Valentin, K.,
von Dassow, P., Yamagishi, T., Van de Peer, Y., Wincker, P., 2010. The Ectocarpus genome
and the independent evolution of multicellularity in brown algae. Nature 465, 617–621.
Denoeud, F., Roussel, M., Noel, B., Wawrzyniak, I., Da Silva, C., Diogon, M.,Viscogliosi, E.,
Brochier-Armanet, C., Couloux, A., Poulain, J., Ségurens, B., Anthouard, V., Texier, C.,
Blot, N., Poirier, P., Ng, G.C.,Tan, K.S.W., Artiguenave, F., Jaillon, O., Aury, J.-M., Delbac,
F., Wincker, P.,Vivares, C.P., El Alaoui, H., 2011. Genome sequence of the stramenopile
Blastocystis, a human anaerobic parasite. Genome Biol. 12, R29.
Dogruman-Al, F., Dagci, H., Yoshikawa, H., Kürt, O., Demirel, M., 2008. A possible link
between subtype 2 and asymptomatic infections of Blastocystis hominis. Parasitol. Res.
103, 685–689.
Dogruman-Al, F., Kustimur, S.,Yoshikawa, H.,Tuncer, C., Simsek, Z.,Tanyuksel, M., Araz, E.,
Boorom, K., 2009a. Blastocystis subtypes in irritable bowel syndrome and inflammatory
bowel disease in Ankara, Turkey. Mem. Inst. Oswaldo Cruz 104, 724–727.
Dogruman-Al, F.,Yoshikawa, H., Kustimur, S., Balaban, N., 2009b. PCR-based subtyping of
Blastocystis isolates from symptomatic and asymptomatic individuals in a major hospital
in Ankara, Turkey. Parasitol. Res. 106, 263–268.
Domínguez-Márquez, M.V., Guna, R., Muñoz, C., Gómez-Muñoz, M.T., Borrás, R., 2009.
High prevalence of subtype 4 among isolates of Blastocystis hominis from symptomatic
patients of a health district of Valencia (Spain). Parasitol. Res. 105, 949–955.
Dunn, L.A., Tan, K.S.W., Vanelle, P., Juspin, T., Crozet, M.D., Terme, T., Upcroft, P., Upcroft,
J.A., 2012. Development of metronidazole-resistant lines of Blastocystis sp. Parasitol. Res.
111, 441–450.
Elwakil, H.S., Hewedi, I.H., 2010. Pathogenic potential of Blastocystis hominis in laboratory
mice. Parasitol. Res. 107, 685–689.
Eroglu, F., Koltas, I.S., 2010. Evaluation of the transmission mode of B. hominis by using PCR
method. Parasitol. Res. 107, 841–845.
Eroglu, F., Genc, A., Elgun, G., Koltas, I.S., 2009. Identification of Blastocystis hominis isolates
from asymptomatic and symptomatic patients by PCR. Parasitol. Res. 105, 1589–1592.
Forsell, J., Granlund, M., Stensvold, C.R., Clark, C.G., Evengård, B., 2012. Subtype analysis of
Blastocystis isolates in Swedish patients. Eur. J. Clin. Microbiol. Infect. Dis. 31, 1689–1696.
Fouad, S.A., Basyoni, M.M.A., Fahmy, R.A., Kobaisi, M.H., 2011. The pathogenic role of
different Blastocystis hominis genotypes isolated from patients with irritable bowel syn-
drome. Arab J. Gastroenterol. 12, 194–200.
Giacometti, A., Cirioni, O., Fiorentini, A., Fortuna, M., Scalise, G., 1999. Irritable bowel
syndrome in patients with Blastocystis hominis infection. Eur. J. Clin. Microbiol. Infect.
Dis. 18, 436–439.
Haas, B.J., Kamoun, S., Zody, M.C., Jiang, R.H.Y., Handsaker, R.E., Cano, L.M., Grab-
herr, M., Kodira, C.D., Raffaele, S., Torto-Alalibo, T., Bozkurt, T.O., Ah-Fong, A.M.V.,
Alvarado, L., Anderson,V.L., Armstrong, M.R., Avrova, A., Baxter, L., Beynon, J., Boevink,
P.C., Bollmann, S.R., Bos, J.I.B., Bulone,V., Cai, G., Cakir, C., Carrington, J.C., Chawner,
M., Conti, L., Costanzo, S., Ewan, R., Fahlgren, N., Fischbach, M.A., Fugelstad, J., Gilroy,
E.M., Gnerre, S., Green, P.J., Grenville-Briggs, L.J., Griffith, J., Grünwald, N.J., Horn, K.,
Horner, N.R., Hu, C.-H., Huitema, E., Jeong, D.-H., Jones, A.M.E., Jones, J.D.G., Jones,
R.W., Karlsson, E.K., Kunjeti, S.G., Lamour, K., Liu, Z., Ma, L., MacLean, D., Chibucos,
M.C., McDonald, H., McWalters, J., Meijer, H.J.G., Morgan, W., Morris, P.F., Munro,
28 C. Graham Clark et al.

C.A., O'Neill, K., Ospina-Giraldo, M., Pinzón, A., Pritchard, L., Ramsahoye, B., Ren,
Q., Restrepo, S., Roy, S., Sadanandom, A., Savidor, A., Schornack, S., Schwartz, D.C.,
Schumann, U.D., Schwessinger, B., Seyer, L., Sharpe, T., Silvar, C., Song, J., Studholme,
D.J., Sykes, S., Thines, M., van de Vondervoort, P.J.I., Phuntumart, V., Wawra, S., Weide,
R.,Win, J.,Young, C., Zhou, S., Fry,W., Meyers, B.C., van West, P., Ristaino, J., Govers, F.,
Birch, P.R.J., Whisson, S.C., Judelson, H.S., Nusbaum, C., 2009. Genome sequence and
analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461, 393–398.
Haldar, K., Kamoun, S., Hiller, N.L., Bhattacharje, S., van Ooij, C., 2006. Common infection
strategies of pathogenic eukaryotes. Nat. Rev. Microbiol. 4, 922–931.
Hussain, R., Jaferi, W., Zuberi, S., Baqai, R., Abrar, N., Ahmed, A., Zaman, V., 1997. Sig-
nificantly increased IgG2 subclass antibody levels to Blastocystis hominis in patients with
irritable bowel syndrome. Am. J. Trop. Med. Hyg. 56, 301–306.
Hussein, E.M., Hussein, A.M., Eida, M.M., Atwa, M.M., 2008. Pathophysiological variability
of different genotypes of human Blastocystis hominis Egyptian isolates in experimentally
infected rats. Parasitol. Res. 102, 853–860.
Iguchi, A., Ebisu, A., Nagata, S., Saitou,Y.,Yoshikawa, H., Iwatani, S., Kimata, I., 2007. Infec-
tivity of different genotypes of human Blastocystis hominis isolates in chickens and rats.
Parasitol. Int. 56, 107–112.
Jiménez-González, D.E., Martínez-Flores,W.A., Reyes-Gordillo, J., Ramírez-Miranda, M.E.,
Arroyo-Escalante, S., Romero-Valdovinos, M., Stark, D., Souza-Saldivar, V., Martínez-
Hernández, F., Flisser, A., Olivo-Díaz, A., Maravilla, P., 2012. Blastocystis infection is asso-
ciated with irritable bowel syndrome in a Mexican patient population. Parasitol. Res.
110, 1269–1275.
Jolley, K.A., Maiden, M.C.J., 2010. BIGSdb: scalable analysis of bacterial genome variation at
the population level. BMC Bioinformatics 11, 595.
Jones, M.S., Whipps, C.M., Ganac, R.D., Hudson, N.R., Boorom, K., 2009. Association of
Blastocystis subtype 3 and 1 with patients from an Oregon community presenting with
chronic gastrointestinal illness. Parasitol. Res. 104, 341–345.
Kamoun, S., 2006. A catalogue of the effector secretome of plant pathogenic oomycetes.
Annu. Rev. Phytopathol. 44, 41–60.
Kaneda, Y., Horiki, N., Cheng, X.-J., Fujita, Y., Maruyama, M., Tachibana, H., 2001.
Ribodemes of Blastocystis hominis isolated in Japan. Am. J. Trop. Med. Hyg. 65, 393–396.
Köksal, F., Başlanti, I., Samasti, M., 2010. A retrospective evaluation of the prevalence of
intestinal parasites in Istanbul, Turkey. Turkiye Parazitol. Derg. 34, 166–172.
Kostka, M., Cepicka, I., Hampl,V., Flegr, J., 2007. Phylogenetic position of Karotomorpha and
paraphyly of Proteromonadidae. Mol. Phylogenet. Evol. 43, 1167–1170.
Lantsman, Y., Tan, K.S.W., Morada, M., Yarlett, N., 2008. Biochemical characterization of a
mitochondrial-like organelle from Blastocystis sp. subtype 7. Microbiology 154, 2757–2766.
Lévesque, C.A., Brouwer, H., Cano, L., Hamilton, J.P., Holt, C., Huitema, E., Raffaele, S.,
Robideau, G.P., Thines, M., Win, J., Zerillo, M.M., Beakes, G.W., Boore, J.L., Busam,
D., Dumas, B., Ferriera, S., Fuerstenberg, S.I., Gachon, C.M.M., Gaulin, E., Govers, F.,
Grenville-Briggs, L., Horner, N., Hostetler, J., Jiang, R.H.Y., Johnson, J., Krajaejun, T.,
Lin, H., Meijer, H.J.G., Moore, B., Morris, P., Phuntmart, V., Puiu, D., Shetty, J., Stajich,
J.E., Tripathy, S., Wawra, S., van West, P., Whitty, B.R., Coutinho, P.M., Henrissat, B.,
Martin, F.,Thomas, P.D.,Tyler, B.M., De Vries, R.P., Kamoun, S.,Yandell, M.,Tisserat, N.,
Buell, C.R., 2010. Genome sequence of the necrotrophic plant pathogen Pythium ulti-
mum reveals original pathogenicity mechanisms and effector repertoire. Genome Biol.
11, R73.
Li, L.H., Zhang, X.-P., Lv, S., Zhang, L., Yoshikawa, H., Wu, Z., Steinmann, P., Utzinger, J.,
Tong, X.-M., Chen, S.-H., Zhou, X.-N., 2007. Cross-sectional surveys and subtype
classification of human Blastocystis isolates from four epidemiological settings in China.
Parasitol. Res. 102, 83–90.
Recent Blastocystis Research 29

Loftus, B., Anderson, I., Davies, R., Alsmark, U.C.M., Samuelson, J., Amedeo, P., Roncaglia, P.,
Berriman, M., Hirt, R.P., Mann, B.J., Nozaki, T., Suh, B., Pop, M., Duchene, M., Ackers,
J., Tannich, E., Leippe, M., Hofer, M., Bruchhaus, I., Willhoeft, U., Bhattacharya, A.,
Chillingworth, T., Churcher, C., Hance, Z., Harris, B., Harris, D., Jagels, K., Moule, S.,
Mungall, K., Ormond, D., Squares, R., Whitehead, S., Quail, M.A., Rabbinowitsch, E.,
Norbertczak, H., Price, C.,Wang, Z., Guillén, N., Gilchrist, C., Stroup, S.E., Bhattacharya,
S., Lohia, A., Foster, P.G., Sicheritz-Ponten, T., Weber, C., Singh, U., Mukherjee, C.,
El-Sayed, N.M., Petri, W.A., Clark, C.G., Embley, T.M., Barrell, B., Fraser, C.M., Hall,
N., 2005. The genome of the protist parasite Entamoeba histolytica. Nature 433, 865–868.
Malheiros, A.F., Stensvold, C.R., Clark, C.G., Braga, G.B., Shaw, J.J., 2011. Molecular
characterization of Blastocystis obtained from members of the indigenous Tapirapé
ethnic group from the Brazilian Amazon region, Brazil. Am. J. Trop. Med. Hyg. 85,
Meloni, D., Sanciu, G., Poirier, P., El Alaoui, H., Chabé, M., Delhaes, L., Dei-Cas, E., Delbac,
F., Fiori, P.L., Di Cave, D., Viscogliosi, E., 2011. Molecular subtyping of Blastocystis sp.
isolates from symptomatic patients in Italy. Parasitol. Res. 109, 613–619.
Menounos, P.G., Spanakos, G., Tegos, N., Vassalos, C.M., Papadopoulou, C., Vakalis, N.C., 2008.
Direct detection of Blastocystis sp. in human faecal samples and subtype assignment using
single strand conformational polymorphism and sequencing. Mol. Cell. Probes 22, 24–29.
Mirza, H.,Teo, J.D.W., Upcroft, J.,Tan, K.S.W., 2011. A rapid, high-throughput viability assay
for Blastocystis spp. reveals metronidazole resistance and extensive subtype-dependent
variations in drug susceptibilities. Antimicrob. Agents Chemother. 55, 637–648.
Motazedian, H., Ghasemi, H., Sadjjadi, S.M., 2008. Genomic diversity of Blastocystis hominis
from patients in southern Iran. Ann. Trop. Med. Parasitol. 102, 85–88.
Nagel, R., Cuttell, L., Stensvold, C.R., Mills, P.C., Bielefeldt-Ohmann, H., Traub, R.J., 2012.
Blastocystis subtypes in symptomatic and asymptomatic family members and pets and
response to therapy. Intern. Med. J. 42, 1187–1195.
Nasirudeen, A.M.A., Tan, K.S.W., 2004. Isolation and characterization of the mitochon-
drion-like organelle from Blastocystis hominis. J. Microbiol. Methods 58, 101–109.
Noor Azian, M.Y., San, Y.M., Gan, C.C., Yusri, M.Y., Nurulsyamzawaty, Y., Zuhaizam, A.H.,
Maslawaty, M.N., Norparina, I.,Vythilingam, I., 2007. Prevalence of intestinal protozoa
in an aborigine community in Pahang, Malaysia. Trop. Biomed. 24, 55–62.
Östan, I., Kilimcioğlu, A.A., Girginkardeşler, N., Özyurt, B.C., Limoncu, M.E., Ok, U.Z.,
2007. Health inequities: lower socio-economic conditions and higher incidences of
intestinal parasites. BMC Public Health 7, 342.
Özyurt, M., Kurt, Ö., Mølbak, K., Nielsen, H.V., Haznedaroglu, T., Stensvold, C.R., 2008.
Molecular epidemiology of Blastocystis infections in Turkey. Parasitol. Int. 57, 300–306.
Parkar, U., Traub, R.J., Vitali, S., Elliot, A., Levecke, B., Robertson, I., Geurden, T., Steele, J.,
Drake, B., Thompson, R.C.A., 2010. Molecular characterization of Blastocystis isolates
from zoo animals and their animal-keepers.Vet. Parasitol. 169, 8–17.
Patterson, D.J., 1989. Stramenopiles: chromophytes from a protistan perspective. The Chro-
mophyte Algae: Problems and Perspectives, Clarendon Press, Oxford, pp. 357–379.
Pérez-Brocal, V., Clark, C.G., 2008. Analysis of two genomes from the mitochondrion-like
organelle of the intestinal parasite Blastocystis: complete sequences, gene content, and
genome organization. Mol. Biol. Evol. 25, 2475–2482.
Petrášová, J., Uzlíková, M., Kostka, M., Petrželková, K.J., Huffman, M.A., Modrý, D., 2011.
Diversity and host specificity of Blastocystis in syntopic primates on Rubondo Island,
Tanzania. Int. J. Parasitol. 41, 1113–1120.
Poirier, P.,Wawrzyniak, I., Albert, A., El Alaoui, H., Delbac, F., Livrelli,V., 2011. Development
and evaluation of a real-time PCR assay for detection and quantification of Blastocys-
tis parasites in human stool samples: prospective study of patients with hematological
malignancies. J. Clin. Microbiol. 49, 975–983.
30 C. Graham Clark et al.

Poirier, P., Wawrzyniak, I., Vivarès, C.P., Delbac, F., El Alaoui, H., 2012. New insights
into Blastocystis spp.: a potential link with irritable bowel syndrome. PLoS Pathog. 8,
Ramírez-Miranda, M.E., Hernández-Castellanos, R., López-Escamilla, E., Moncada, D.,
Rodríguez-Magallan, A., Pagaza-Melero, C., González-Angulo, A., Flisser, A., Kawa-
Karasik, S., Maravilla, P., 2010. Parasites in Mexican patients with irritable bowel syn-
drome: a case–control study. Parasit.Vectors 3, 96.
Reimer, C., Bytzer, P., 2009. A population-based survey to assess troublesome symptoms in
gastroesophageal reflux disease. Scand. J. Gastroenterol. 44, 394–400.
Rene, B.A., Stensvold, C.R., Badsberg, J.H., Nielsen, H.V., 2009. Subtype analysis of Blas-
tocystis isolates from Blastocystis cyst excreting patients. Am. J. Trop. Med. Hyg. 80,
Rivera, W.L., Tan, M.A.V., 2005. Molecular characterization of Blastocystis isolates in the
Philippines by riboprinting. Parasitol. Res. 96, 253–257.
Santín, M., Gómez-Muñoz, M.T., Solano-Aguilar, G., Fayer, R., 2011. Development of a
new PCR protocol to detect and subtype Blastocystis spp. from humans and animals.
Parasitol. Res. 109, 205–212.
Scanlan, P.D., Marchesi, J.R., 2008. Micro-eukaryotic diversity of the human distal gut
microbiota: qualitative assessment using culture-dependent and -independent analysis of
faeces. ISME J. 2, 1183–1193.
Scicluna, S.M., Tawari, B., Clark, C.G., 2006. DNA barcoding of Blastocystis. Protist 157,
Silberman, J.D., Sogin, M.L., Leipe, D.D., Clark, C.G., 1996. Human parasite finds taxonomic
home. Nature 380, 398.
Souppart, L., Sanciu, G., Cian, A., Wawrzyniak, I., Delbac, F., Capron, M., Dei-Cas, E., Boo-
rom, K., Delhaes, L.,Viscogliosi, E., 2009. Molecular epidemiology of human Blastocystis
isolates in France. Parasitol. Res. 105, 413–421.
Souppart, L., Moussa, H., Cian, A., Sanciu, G., Poirier, P., El Alaoui, H., Delbac, F., Boorom,
K., Delhaes, L., Dei-Cas, E.,Viscogliosi, E., 2010. Subtype analysis of Blastocystis isolates
from symptomatic patients in Egypt. Parasitol. Res. 106, 505–511.
Standley, D.M., van der Giezen, M., 2012. Modeling the alternative oxidase from the human
pathogen Blastocystis using automated hybrid structural template assembly. Res. Rep.
Biochem. 2, 1–8.
Stechmann, A., Hamblin, K., Pérez-Brocal, V., Gaston, D., Richmond, G.S., van der Giezen,
M., Clark, C.G., Roger, A.J., 2008. Organelles in Blastocystis that blur the distinction
between mitochondria and hydrogenosomes. Curr. Biol. 18, 580–585.
Stensvold, C.R., Brillowska-Dabrowska, A., Nielsen, H.V., Arendrup, M.C., 2006. Detection
of Blastocystis hominis in unpreserved stool specimens by using polymerase chain reac-
tion. J. Parasitol. 92, 1081–1087.
Stensvold, C.R., Arendrup, M.C., Jespersgaard, C., Mølbak, K., Nielsen, H.V., 2007a. Detect-
ing Blastocystis using parasitologic and DNA-based methods: a comparative study. Diagn.
Microbiol. Infect. Dis. 59, 303–307.
Stensvold, C.R., Suresh, G.K., Tan, K.S.W., Thompson, R.C.A., Traub, R.J., Viscogliosi, E.,
Yoshikawa, H., Clark, C.G., 2007b. Terminology for Blastocystis subtypes – a consensus.
Trends Parasitol. 23, 93–96.
Stensvold, C.R., Arendrup, M.C., Nielsen, H.V., Bada, A., Thorsen, S., 2008. Symptomatic
infection with Blastocystis sp. subtype 8 successfully treated with trimethoprim–sulfa-
methoxazole. Ann. Trop. Med. Parasitol. 102, 271–274.
Stensvold, C.R., Alfellani, M.A., Nørskov–Lauritsen, S., Prip, K., Victory, E.L., Maddox,
C., Nielsen, H.V., Clark, C.G., 2009a. Subtype distribution of Blastocystis isolates from
synanthropic and zoo animals and identification of a new subtype. Int. J. Parasitol. 39,
Recent Blastocystis Research 31

Stensvold, C.R., Lewis, H.C., Hammerum, A.M., Porsbo, L.J., Nielsen, S.S., Olsen, K.E.P.,
Arendrup, M.C., Nielsen, H.V., Mølbak, K., 2009b. Blastocystis: unravelling potential risk
factors and clinical significance of a common but neglected parasite. Epidemiol. Infect.
137, 1655–1663.
Stensvold, C.R., Smith, H.V., Nagel, R., Olsen, K.E.P., Traub, R.J., 2010. Eradication of
Blastocystis carriage with antimicrobials: reality or delusion? J. Clin. Gastroenterol. 44,
Stensvold, C.R., Christiansen, D.B., Olsen, K.E.P., Nielsen, H.V., 2011a. Blastocystis sp. sub-
type 4 is common in Danish Blastocystis-positive patients presenting with acute diarrhea.
Am. J. Trop. Med. Hyg. 84, 883–885.
Stensvold, C.R., Nielsen, S.D., Badsberg, J.-H., Engberg, J., Friis-Møller, N., Nielsen, S.S.,
Nielsen, H.V., Friis-Møller, A., 2011b. The prevalence and clinical significance of intes-
tinal parasites in HIV-infected patients in Denmark. Scand. J. Infect. Dis. 43, 129–135.
Stensvold, C.R., Alfellani, M., Clark, C.G., 2012a. Levels of genetic diversity vary dramati-
cally between Blastocystis subtypes. Infect. Genet. Evol. 12, 263–273.
Stensvold, C.R., Ahmed, U.N., Andersen, L.O., Nielsen, H.V., 2012b. Development and
evaluation of a genus-specific, probe-based, internal process controlled real-time PCR
assay for sensitive and specific detection of Blastocystis. J. Clin. Microbiol. 50, 1847–1851.
Stenzel, D.J., Boreham, P.F.L., 1991. A cyst-like stage of Blastocystis hominis. Int. J. Parasitol.
21, 613–615.
Stenzel, D.J., Boreham, P.F.L., McDougall, R., 1991. Ultrastructure of Blastocystis hominis in
human stool samples. Int. J. Parasitol. 21, 807–812.
Surangsrirat, S., Thamrongwittawatpong, L., Piyaniran, W., Naaglor, T., Khoprasert, C., Taa-
masri, P., Mungthin, M., Leelayoova, S., 2010. Assessment of the association between
Blastocystis infection and irritable bowel syndrome. J. Med. Assoc. Thai. 93 (Suppl. 6),
Suresh, K., Salim, H.R., Jamaiah, I., Anuar, A.K., 2001. Blastocystis hominis in high-rise flat
dwellers in Kuala Lumpur, Malaysia. Trans. R. Soc. Trop. Med. Hyg. 95, 377–378.
Tam, C.C., O'Brien, S.J., Tompkins, D.S., Bolton, F.J., Berry, L., Dodds, J., Choudhury, D.,
Halstead, F., Iturriza-Gómara, M., Mather, K., Rait, G., Ridge, A., Rodrigues, L.C.,Wain,
J., Wood, B., Gray, J.J.the IID2 Study Executive Committee, 2012. Changes in causes of
acute gastroenteritis in the United Kingdom over 15 years: microbiologic findings from
2 prospective, population-based studies of infectious intestinal disease. Clin. Infect. Dis.
54, 1275–1286.
Tan, T.C., Suresh, K.G., Smith, H.V., 2008. Phenotypic and genotypic characterisation of
Blastocystis hominis isolates implicates subtype 3 as a subtype with pathogenic potential.
Parasitol. Res. 104, 85–93.
Tan,T.C., Ong, S.C., Suresh, K.G., 2009. Genetic variability of Blastocystis sp. isolates obtained
from cancer and HIV/AIDS patients. Parasitol. Res. 105, 1283–1286.
Thathaisong, U., Worapong, J., Mungthin, M., Tan-Ariya, P.,Viputtigul, K., Sudatis, A., Noo-
nai, A., Leelayoova, S., 2003. Blastocystis isolates from a pig and a horse are closely related
to Blastocystis hominis. J. Clin. Microbiol. 41, 967–975.
Tungtrongchitr, A., Manatsathit, S., Kositchaiwat, C., Ongrotchanakun, J., Munkong, N.,
Chinabutr, P., Leelakusolvong, S., Chaicumpa, W., 2004. Blastocystis hominis infection
in irritable bowel syndrome patients. Southeast Asian J. Trop. Med. Public Health 35,
Tyler, B.M., Tripathi, S., Zhang, X., Dehal, P., Jiang, R., Aerts, A., Arredondo, F.D.,
Baxter, L., Bensasson, D., Beynon, J., Chapman, J., Damasceno, C.M.B., Dorrance, A.E.,
Dou, D., Dickerman, A.W., Dubchak, I., Garbelotto, M., Gijzen, M., Gordon, S.G., Gov-
ers, F., Grunwald, N.J., Huang, W., Ivors, K., Jones, R.W., Kamoun, S., Krampis, K.,
Lamour, K., Lee, M.-K., McDonald, W.H., Medina, M., Meijer, H.J.G., Nordberg, E.K.,
Maclean, D.J., Ospina-Giraldo, M.D., Morris, P., Phuntumart, V., Putnam, N., Rash, S.,
32 C. Graham Clark et al.

Rose, J.K.C., Sakihama,Y., Salamov, A., Savidor, A., Scheuring, C.F., Smith, B.M., Sobral,
B.W.S., Terry, A., Torto-Alalibo, T.A., Win, J., Xu, Z., Zhang, H., Grigoriev, I., Rokhsar,
D., Boore, J.L., 2006. Phytophthora genome sequences uncover evolutionary origins and
mechanisms of pathogenesis. Science 313, 1261–1266.
van der Giezen, M., 2009. Hydrogenosomes and mitosomes: conservation and evolution of
functions. J. Eukaryot. Microbiol. 56, 221–231.
Vassalos, C.M., Spanakos, G.,Vassalou, E., Papadopoulou, C.,Vakalis, N., 2010. Differences in
clinical significance and morphologic features of Blastocystis sp. subtype 3. Am. J. Clin.
Pathol. 133, 251–258.
Vdovenko, A.A., 2000. Blastocystis hominis: origin and significance of vacuolar and granular
forms. Parasitol. Res. 86, 8–10.
Vennila, G.D., Suresh Kumar, G., Khairul Anuar, A., Rajah, S., Saminathan, R., Sivanandan,
S., Ramakrishnan, K., 1999. Irregular shedding of Blastocystis hominis. Parasitol. Res. 85,
Vogelberg, C., Stensvold, C.R., Monecke, S., Ditzen, A., Stopsack, K., Heinrich-Gräfe, U.,
Pöhlmann, C., 2010. Blastocystis sp. subtype 2 detection during recurrence of gastroin-
testinal and urticarial symptoms. Parasitol. Int. 59, 469–471.
Wawrzyniak, I., Roussel, M., Diogon, M., Couloux, A., Texier, C., Tan, K.S.W.,Vivarès, C.P.,
Delbac, F., Wincker, P., El Alaoui, H., 2008. Complete circular DNA in the mitochon-
dria-like organelles of Blastocystis hominis. Int. J. Parasitol. 38, 1377–1382.
Wawrzyniak, I., Texier, C., Poirier, P., Viscogliosi, E., Tan, K.S.W., Delbac, F., El Alaoui, H.,
2012. Characterization of two cysteine proteases secreted by Blastocystis ST7, a human
intestinal parasite. Parasitol. Int. 61, 437–442.
Wong, K.H.S., Ng, G.C., Lin, R.T.P., Yoshikawa, H., Taylor, M.B., Tan, K.S.W., 2008. Pre-
dominance of subtype 3 among Blastocystis isolates from a major hospital in Singapore.
Parasitol. Res. 102, 663–670.
Yakoob, J., Jafri,W., Jafri, N., Khan, R., Islam, M., Beg, M.A., Zaman,V., 2004. Irritable bowel
syndrome: in search of an etiology: role of Blastocystis hominis. Am. J. Trop. Med. Hyg.
70, 383–385.
Yakoob, J., Jafri, W., Beg, M.A., Abbas, Z., Naz, S., Islam, M., Khan, R., 2010. Irritable bowel
syndrome: is it associated with genotypes of Blastocystis hominis. Parasitol. Res. 106,
Yan, Y., Su, S., Lai, R., Liao, H., Ye, J., Li, X., Luo, X., Chen, G., 2006. Genetic variability of
Blastocystis hominis isolates in China. Parasitol. Res. 99, 597–601.
Yoshikawa, H., Abe, N., Iwasawa, M., Kitano, S., Nagano, I., Wu, Z., Takahashi, Y., 2000.
Genomic analysis of Blastocystis hominis strains isolated from two long-term health care
facilities. J. Clin. Microbiol. 38, 1324–1330.
Yoshikawa, H., Morimoto, K., Wu, Z., Singh, M., Hashimoto, T., 2004a. Problems in specia-
tion in the genus Blastocystis. Trends Parasitol. 20, 251–255.
Yoshikawa, H., Wu, Z., Kimata, I., Iseki, M., Ali, I.K.M., Hossain, M.B., Zaman, V., Haque,
R., Takahashi,Y., 2004b. Polymerase chain reaction-based genotype classification among
human Blastocystis hominis populations isolated from different countries. Parasitol. Res.
92, 22–29.
Yoshikawa, H., Wu, Z., Pandey, K., Pandey, B.D., Sherchand, J.B., Yanagi, T., Kanbara, H.,
2009. Molecular characterization of Blastocystis isolates from children and rhesus mon-
keys in Kathmandu, Nepal.Vet. Parasitol. 160, 295–300.
Zierdt, C.H., Donnolley, C.T., Muller, J., Constantopoulos, G., 1988. Biochemical and ultra-
structural study of Blastocystis hominis. J. Clin. Microbiol. 26, 965–970.
Zierdt, C.H., 1986. Cytochrome-free mitochondria of an anaerobic protozoan – Blastocystis
hominis. J. Protozool. 33, 67–69.
Zierdt, C.H., 1991. Blastocystis hominis – past and future. Clin. Microbiol. Rev. 4, 61–79.

Tradition and Transition: Parasitic

Zoonoses of People and Animals
in Alaska, Northern Canada, and
Emily J. Jenkins*,1, Louisa J. Castrodale†, Simone J. C. de Rosemond*,
Brent R. Dixon‡, Stacey A. Elmore*, Karen M. Gesy*, Eric P. Hoberg§,
Lydden Polley*, Janna M. Schurer*, Manon Simard**, R. C. Andrew
*Department of V   eterinary Microbiology, University of Saskatchewan, Saskatoon, SK S7N 5B4, Canada
†Alaska Department of Health and Social Services, Division of Public Health, Section of Epidemiology,

Anchorage, AK, USA

‡Microbiology Research Division, Bureau of Microbial Hazards, Food Directorate, Health Canada, Ottawa,

ON, Canada, K1A 0K9

§United States National Parasite Collection, United States Department of Agriculture, Agricultural Research

Service, Beltsville, MD, USA

¶School of V
  eterinary and Biomedical Sciences, Murdoch University, Murdoch, WA, Australia
**Nunavik Research Center, Makivik Corporation, Kuujjuaq, QC, Canada, J0M 1C0
1Corresponding author: E-mail:

1. Introduction36
2. Methods41
3. Giardia spp. 42
3.1. Species and Strains Present in the North 43
3.2. Geographic Distribution in the North 43
3.3. Transmission, Prevalence, and Animal Health Impact in the North 43
3.4. Transmission, Prevalence, and Public Health Impact in the North 51
3.5. Future Impact of Climate and Landscape Change 56
4. Cryptosporidium spp. 56
4.1. Species and Strains Present in the North 56
4.2. Geographic Distribution in the North 57
4.3. Transmission, Prevalence, and Animal Health Impact in the North 58
4.4. Transmission, Prevalence, and Public Health Impact in the North 62
4.5. Future Impact of Climate and Landscape Change 64

Our chapter is dedicated to Robert and Virginia Rausch, in every sense true pioneers of
arctic parasitology and public health. We honour the memory of Robert Rausch, at his
passing on 6 October 2012, for his insights and friendship spanning 70 years at the frontiers
of northern science.

Advances in Parasitology, Volume 82 © 2013 Elsevier Ltd.

ISSN 0065-308X, All rights reserved. 33
34 Emily J. Jenkins et al.

5. Toxoplasma gondii65
5.1. Species and Strains Present in the North 66
5.2. Geographic Distribution in the North 66
5.3. Transmission, Prevalence, and Animal Health Impact in the North 71
5.4. Transmission, Prevalence, and Public Health Impact in the North 73
5.4.1. Transmission 73
5.4.2. Prevalence 73
5.4.3. Risk Factors 73
5.4.4. Impact and Control 74
5.5. Future Impact of Climate and Landscape Change 75
5.5.1. Oocyst Transmission 75
5.5.2. Frequency and Severity of Waterborne Outbreaks 76
5.5.3. Abundance of and Access to Harvested Wildlife 76
6. Trichinella spp. 77
6.1. Species and Strains Present in the North 78
6.2. Geographic Distribution in the North 79
6.3. Transmission, Prevalence, and Animal Health Impact in the North 80
6.3.1. Transmission 80
6.3.2. Prevalence 82
6.3.3. Impact and Control in Animals 89
6.4. Transmission, Prevalence, and Public Health Impact in the North 89
6.4.1. Transmission and Risk Factors 89
6.4.2. Prevalence 93
6.4.3. Alaska 94
6.4.4. Canada 95
6.4.5. Greenland 97
6.4.6. Impact and Control in People 98
6.5. Future Impact of Climate and Landscape Change 100
7. Toxocara spp. 102
7.1. Species Present in the North 103
7.2. Geographic Distribution in the North 104
7.3. Transmission, Prevalence, and Animal Health Impact in the North 105
7.4. Transmission, Prevalence, and Public Health Impact in the North 107
7.5. Future Impact of Climate and Landscape Change 109
8. Anisakid Nematodes 111
8.1. Geographic Distribution in the North 112
8.2. Species and Strains Present in the North 112
8.3. Transmission, Prevalence, and Animal Health Impact in the North 117
8.4. Transmission, Prevalence, and Public Health Impact in the North 119
8.5. Future Impact of Climate and Landscape Change 120
9. Diphyllobothriid Cestodes 121
9.1. Species Present in the North 128
9.2. Geographic Distribution in the North 129
9.3. Transmission, Prevalence, and Animal Health Impact in the North 131
9.3.1. Prevalence in Terrestrial Piscivores 131
9.3.2. Prevalence in Marine Piscivores 135
Arctic Zoonoses 35

9.4. Transmission, Prevalence, and Public Health Impact in the North 135
9.5. Diagnosis and Control 140
9.6. Future Impact of Climate and Landscape Change 141
10. Echinococcus granulosus/canadensis (Cystic Hydatid) 144
10.1. Species and Strains Present in the North 144
10.2. Geographic Distribution in the North 146
10.3. Transmission, Prevalence, and Animal Health Impact in the North 147
10.4. Transmission, Prevalence, and Public Health Impact in the North 150
10.5. Future Impact of Climate and Landscape Change 155
11. Echinococcus multilocularis (Alveolar Hydatid) 157
11.1. Species and Strains Present in the North 158
11.2. Geographic Distribution in the North 159
11.3. Transmission, Prevalence, and Animal Health Impact in the North 160
11.4. Transmission, Prevalence, and Public Health Impact in the North 164
11.5. Future Impact of Climate and Landscape Change 166
12. Conclusions169
12.1. Zoonotic Parasites in the Traditional North 169
12.2. Risk Assessment for Zoonotic Parasites in the North 170
12.3. Risk Mitigation 172
12.4. Zoonotic Parasites in a North in Transition 173
12.5. F uture Needs for Research and Surveillance of Zoonotic Parasites
in the North 175

Zoonotic parasites are important causes of endemic and emerging human disease in
northern North America and Greenland (the North), where prevalence of some para-
sites is higher than in the general North American population. The North today is in
transition, facing increased resource extraction, globalisation of trade and travel, and
rapid and accelerating environmental change. This comprehensive review addresses
the diversity, distribution, ecology, epidemiology, and significance of nine zoonotic
parasites in animal and human populations in the North. Based on a qualitative risk
assessment with criteria heavily weighted for human health, these zoonotic parasites
are ranked, in the order of decreasing importance, as follows: Echinococcus multilocu-
laris, Toxoplasma gondii, Trichinella and Giardia, Echinococcus granulosus/canadensis and
Cryptosporidium, Toxocara, anisakid nematodes, and diphyllobothriid cestodes. Recent
and future trends in the importance of these parasites for human health in the North
are explored. For example, the incidence of human exposure to endemic helminth
zoonoses (e.g. Diphyllobothrium, Trichinella, and Echinococcus) appears to be declining,
while water-borne protozoans such as Giardia, Cryptosporidium, and Toxoplasma may
be emerging causes of human disease in a warming North. Parasites that undergo
temperature-dependent development in the environment (such as Toxoplasma,
ascarid and anisakid nematodes, and diphyllobothriid cestodes) will likely undergo
36 Emily J. Jenkins et al.

a­ ccelerated development in endemic areas and temperate-adapted strains/species

will move north, resulting in faunal shifts. Food-borne pathogens (e.g. Trichinella,
Toxoplasma, anisakid nematodes, and diphyllobothriid cestodes) may be increasingly
important as animal products are exported from the North and tourists, workers, and
domestic animals enter the North. Finally, key needs are identified to better assess and
mitigate risks associated with zoonotic parasites, including enhanced surveillance in
animals and people, detection methods, and delivery and evaluation of veterinary and
public health services.

Worldwide, there is increasing recognition that zoonoses (especially
those with wildlife reservoirs) are an important source of emerging dis-
eases of people (Daszak et al., 2000; Kruse et al., 2004). Zoonoses are also
ongoing contributors to health inequities; for example, 7 of 27 infectious
diseases contributing significantly to the global Disability Adjusted Life
Years burden were zoonotic, and 5 of these were parasitic (Robinson et al.,
2003). Within the circumpolar north, there is increasing interest in priori-
tising zoonotic diseases (including parasites) in terms of the current public
health impact and predicting the effects of climate and landscape change
on the ecology of these pathogens and their animal and human hosts in
these ­vulnerable regions.
For purposes of this review, northern North America (‘the North’) was
functionally defined as Alaska, Greenland, and northern Canada. In Canada,
the North is functionally defined by the southern limit of the distribution
of discontinuous permafrost (Fig. 2.1). This definition of North best reflects
physical, cultural, and public health considerations and is more expansive
than a strict definition of North as the Arctic (north of 60° of latitude). In
total, the human population of the North (using this definition) is approxi-
mately 2.5 million people in 8.5 million square kilometres. The population
of Alaska is currently approximately 720,000 people, which represents <1%
of the U.S. population. Of the total population of Alaska, 17% self-identify
as indigenous (including Eskimo/Inuit, Aleut, Alaskan Athabaskan, Tlingit,
Haida, and Tsimshian) (
popover.pdf  ). In Greenland, the total population is approximately 56,000
people, 85% of which are Inuit (Kalaallit), descended from the Thule migra-
tion from Alaska and Canada in 800 A.C. (
about%20greenland/facts%20on%20greenland.aspx). In Canada, the func-
tional definition of the North corresponds well with health indicator peer
groups E, F, and H as determined by Statistics Canada based on demographic
Arctic Zoonoses 37

Figure 2.1  Functional definition of the North, including Greenland. Northern is con-
sidered north of the line demarcating the southern limit of discontinuous permafrost
(as low as 53°N in some regions). Abbreviations used in this figure and throughout the
review are as follows: Alaska (AK), United States of America (USA); provinces of ­Canada
including British Columbia (BC), Alberta (AB), Saskatchewan (SK), Manitoba (MB), Ontario
(ON), Quebec (QC) and Newfoundland Labrador (NL); territories of Canada including the
Yukon Territory (YT), Northwest Territories (NT), and Nunavut (NU).

parameters and socioeconomic characteristics. These peer groups include

the northern regions of the western provinces (British Columbia, Alberta,
Saskatchewan, and Manitoba), the northern territories (Yukon, Northwest
Territories, and Nunavut), northern Ontario, northern Quebec (Nunavik
and the James Bay region), and Labrador. Collectively, the population in
these peer groups is about 1.9 million people, representing 5.5% of the
entire Canadian population, and is characterised by a high proportion of
Indigenous people (First Nations, Metis, and Inuit) (http://www.statcan. In Canada, Inuit
living in Nunavut, Nunavik (in northern Quebec), and Nunatsiavut (in
Labrador) represent 84–90% of the total population in these regions, and
55% of the population in the Inuvialuit region of the Northwest Territories.
Based on 2006 census data, First Nations (primarily Cree, and Dene in
38 Emily J. Jenkins et al.

northwestern Canada) represent 76–97% of the population in northern

Quebec ( James Bay), Saskatchewan, and Manitoba (http://www12.statcan.
ca/census-recensement/2006/as-sa/97-558/index-eng.cfm). It is impor-
tant to note that northern residents are a diverse population, and generalisa-
tions about cultural and dietary preferences rarely apply from community
to community, let alone across all of North America.
Northern peoples have had a long and continuous association with zoo-
notic parasites, even prior to initial expansion into North America near the
end of the Pleistocene (20–30,000 years ago). Subsequent parasite expo-
sures were influenced by locally available food resources in aquatic and
terrestrial environments (Hoberg et al., 2012). In current times, residents of
northern and Indigenous communities in North America may be at higher
risk of exposure to parasitic zoonoses than the general population. His-
torically, prevalence of some zoonoses in northern residents has been dispa-
rately higher than the North American average, suggesting increased risk of
exposure resulting from a complex interaction of cultural, socioeconomic,
and bioclimatic variables (Curtis et al., 1988; Fortuine, 1961; Gyorkos et al.,
2003; Hotez, 2010). For example, cases of human cystic hydatid disease and
Giardia have the highest per capita rates in northern Canadians (Gilbert
et al., 2010; Public Health Agency of Canada, 2007). The seroprevalence of
toxoplasmosis is as high as 60% in Nunavik Inuit, as compared to the overall
North American estimate of 20% and a global prevalence of 30% ( Jones
et al., 2001; Messier et al., 2009; Tenter et al., 2000).
Risk factors for transmission of zoonotic parasites in northern popula-
tions include limited availability of veterinary and medical services, pres-
ence of large free-roaming dog populations, and consumption of locally
harvested fish and wildlife (Brook et al., 2010; Hotez, 2010; Salb et al.,
2008). Inuit and other northern residents often hunt and butcher their own
animals in the field or outside their home. Preferred species for harvest vary
among communities; barren-ground caribou (Rangifer tarandus groenlandi-
cus), marine mammals, and anadromous fish (e.g. char – Salvelinus alpinus,
salmon – Onchorhynchus spp.) are mainstays of harvested wildlife among
the Inuit, while in the sub-Arctic, moose (Alces alces), woodland caribou
(R. t. caribou), and freshwater fish (e.g. grayling – Thymallus spp., w ­ hitefish –
Coregonus spp.) dominate. Bears (Ursus spp.) and birds (e.g. sea ducks –
Somateria spp., geese – Chen spp., ptarmigan – Lagopus spp.) are s­ometimes
­harvested, and furbearers (e.g. lynx – Lynx canadensis,  fox – Vulpes spp., wolves –
Canis lupus, wolverine – Gulo gulo) are still trapped, albeit in much fewer
numbers than in the heyday of the fur trade (Mackey, 1988). Organs, meat,
Arctic Zoonoses 39

and fat are consumed fresh, thawed, frozen, partially cooked, fermented,
dried, and cured as sausages. Some of these preparations can be a poten-
tial risk for human health, linked to cases of trichinellosis, toxoplasmosis,
diphyllobothriosis, and cystic hydatid disease (indirectly through dogs with
access to carcasses of ungulates). Northern residents are also increasingly
connected to the global food chain and in contact with transient work-
forces and tourists, leading to adoption of dietary preferences from around
the world that may not translate safely to local methods of food preparation
(e.g. consuming raw pork or chicken) and to harvested foods (e.g. ceviche
made with locally caught fish).
Northern residents are also at greater risk of water-borne infections.
Water is generally brought to individual houses by truck. Although water
quality is monitored and water is chlorine treated, chlorine does not kill
protozoan parasites such as Giardia and Cryptosporidium, and water treatment
infrastructure is often not optimal, with boil-water advisories issued to
communities during spring run-off and heavy rainfalls. Chlorinated water
is also unacceptable to some community members who continue to collect
water from traditional sources (such as surface or rain water). Sewage is col-
lected by truck from house tanks and held in an open pit away from com-
munities. In some communities, wildlife are attracted to the sewage pits and
have been observed drinking from them. In addition, during heavy rainfalls
or ice thaws, sewage may overflow into surrounding groundwater. These
infrastructure limitations may contribute to increased risk of transmission
of parasitic zoonoses among people and wildlife in the Canadian North.
While risk factors for zoonoses in the North include traditional cultural
practices of hunting, fishing and trapping, this must be weighed against the
value of these activities and their palpable benefits for maintaining food secu-
rity in remote and Indigenous communities (Chan et al., 2006; Lambden
et al., 2007; Mackey, 1988; Ross et al., 1989). Indeed, zoonotic risks can
be substantially reduced through a combination of protective traditional
knowledge and modern food handling practices, as well as trends toward
increased use of store-bought foods – truly a culture in transition.
Northern residents (Indigenous and others) may be at increased risk of
exposure, and of developing disease, if zoonotic pathogens move north as a
result of the rapidly changing Arctic climate. Dr. R. L. Rausch, the found-
ing father of Arctic parasitology and to whom this review is dedicated, was
prescient to draw attention to the commonalities of parasite transmission
in northern and tropical regions, including relatively intact sylvatic cycles,
introduction of pathogens with disastrous consequences, and socioeconomic
40 Emily J. Jenkins et al.

and ecological drivers of disease (Rausch, 1974). Indeed, he laid the founda-
tions for anticipating that rapid and accelerating climate change might, in
the course of a few decades, bring parasites historically restricted to temper-
ate and tropical regions to the very threshold of the Arctic, where residents
are largely naïve to these pathogens.
Forecasting the effects of ongoing climate and landscape change on
transmission and impact of zoonotic parasites in the North is challenging
because of the current lack of synthesised information about the diversity
and distributions of parasites in these regions – a significant motivation for
the current review. There is a wealth of information in older studies based
on recovery of adult helminths from harvested animals; however, this review
addresses an urgent need to update the current knowledge in light of new
advances in molecular and immunological methods for detection and char-
acterisation of helminth and protozoan parasites. From the animal health
perspective, our knowledge of the distribution and abundance of parasites
in animals in the North is often based on a few, dated studies in dogs and
wildlife, and almost nothing is known about the impacts of parasitism on
northern wildlife, especially at the population level. From a public health
perspective, very few parasites in people are under surveillance (such as
mandatory physician or laboratory reporting), and therefore cases are likely
significantly underreported.
In addition, there is currently incomplete understanding of the local
ecological drivers of transmission, as well as uncertainty in the magnitude of
effects of climate change on temperature, precipitation, and habitat. How-
ever, there no longer appears to be much controversy over the direction of
climate change in the North, which is already moving into a warmer, wet-
ter future, with increased frequency and severity of extreme weather events
such as heavy rainfalls and storms. In marine systems, ocean temperatures
are warming and record losses of sea ice are already observed (ACIA, 2005;
Delecluse, 2008; Furgal and Prowse, 2008). Therefore, there is an urgent
need to establish baselines for parasites of public and animal health sig-
nificance against a future of climate, landscape, and cultural change in the
North (Hoberg et al., 2012; Kutz et al., 2012).
This review considers the past, present, and future ecology of endopara-
sitic zoonoses in animals, people, and the environment in the North Ameri­
can Arctic – a ‘One-Health’ approach. The following zoonotic parasites
are considered of ongoing and emerging importance in the North: pro-
tozoans (Giardia, Cryptosporidium, and Toxoplasma), nematodes (Trichinella,
Toxocara, and the zoonotic anisakids), and cestodes (diphyllobothriids and
Arctic Zoonoses 41

Echinococcus) (Curtis et al., 1988; Fortuine, 1961; Gyorkos et al., 2003; Hotez,
2010; Lantis, 1981; Rausch, 1972, 1974). For each parasite, we briefly review
the biology, genetic diversity, host and geographic range, epidemiology and
significance in both animals and people, and the potential impacts of envi-
ronmental change on these vulnerable host–parasite systems in a North
poised between tradition and transition.

The published literature was reviewed for each parasite as
­comprehensively as possible. Published studies (prevalence studies and case
reports) for each parasite in animals and people in northern North America
are summarised in tables. For maps, coordinates for the geographic loca-
tions in the tables were obtained from the original publication. When this
was not possible, we obtained coordinates for place names stated in the
publications from GeoNames (, Canadian
Geonames (­
geographical-name/search/5877), or Google Earth© (
com/earth/index.html). All maps were created in ArcGIS© version 10. For
studies where a pinpoint location was not available (i.e. reports covered a
broad study area, or where communities were anonymised to protect pri-
vacy), the centrum of the region was used. For some published data, it was
simply not possible to find localising information. Therefore, all the points
on the maps are derived from the corresponding tables, but not all data in
the tables are represented in the maps.
In addition to the published literature, we drew on notifiable disease
data for parasites (e.g. trichinellosis, giardiasis, and cryptosporidiosis) under
passive surveillance in people through physician and laboratory ­reporting.
Human cases summarised from passive surveillance data collected by public
health authorities in Alaska and Canada were not mapped as the local-
ising information was seldom available. These data were obtained from
published sources, including the Canada Communicable Disease Report
(, National Notifiable
Diseases Online (
eng.php), the Centers for Disease Control and Prevention Morbidity and
Mortality Weekly Report (, and bulletins
from the State of Alaska Health and Social Services (
Some of the Alaskan data were accessed through AK STARS, the State's
reporting system for infectious diseases. Population data to calculate rates
42 Emily J. Jenkins et al.

per 100,000 × 2 people were obtained from the U.S. and Canadian census
data available online. Cases (for those diseases with low incidence) and rates
per 100,000 × 2 people were graphed for each disease in order to demon-
strate changes over multiyear periods with a relatively consistent detection
effort. Laboratory methods no doubt changed over the reporting period
(many decades in some cases); presumably this would bias toward increased
detection as time progressed. Finally, some of the cases graphed may be
duplicates of those reported in the tables.

The flagellate protozoan Giardia is one of the most common enteric
parasites of people and domestic animals, and is increasingly recognised
in a diverse range of wildlife species (Appelbee et al., 2005; Thompson
et al., 2008, 2010). In the life cycle of Giardia, hosts become infected when
cysts voided in faeces are ingested, which may be through direct host-to-
host contact or via contaminated materials, water, food or arthropods (as
mechanical vectors). Following ingestion, cysts break down in the duo-
denum, where the trophozoites are released and subsequently proliferate
asexually on the brush border villous epithelium of the mucosal surface
(Thompson et al., 2008). Cysts released through the faeces are immediately
infectious and remain infectious for months in water and cool, damp areas
(Thompson et al., 2008).
An important aspect of the epidemiology of Giardia is understand-
ing the host range of different species and strains/genotypes, how they
are maintained in nature, and the potential for cross-transmission. This is
particularly important in determining zoonotic potential, as Giardia can
be maintained in a variety of transmission cycles that can operate inde-
pendently (Hunter and Thompson, 2005). A large number of species and
genotypes are now recognised that differ principally in their host range.
Some species and genotypes appear to be restricted to particular species or
types of hosts whereas others (the zoonotic assemblages) have broad host
ranges including people. Giardia (previously known as Giardia lamblia and/
or Giardia intestinalis) has been subdivided into seven Assemblages (A–H)
or genotypes, now more appropriately designated with host-specific spe-
cies names (Ballweber et al., 2010; Feng and Xiao, 2011; Lasek-Nesselquist
et al., 2010; Thompson and Monis, 2012; Thompson et al., 2008). Thus,
zoonotic assemblage A is now known as Giardia duodenalis, and zoonotic
assemblage B as Giardia enterica.
Arctic Zoonoses 43

3.1. Species and Strains Present in the North

Although few surveys have been undertaken in the North American Arc-
tic on the genetic diversity and zoonotic significance of Giardia, zoonotic
genotypes appear to be the only ones detected to date. Zoonotic genotypes
A and B (G. duodenalis and G. enterica) have been reported in muskoxen in
the western Canadian Arctic (Kutz et al., 2008), and G. duodenalis in dogs
in the Northwest Territories, northern Alberta, and northern Saskatchewan
(Himsworth et al., 2010b; Salb et al., 2008; Schurer et al., 2012). In the
marine system, seals in the eastern Canadian Arctic were infected with G.
enterica (Dixon et al., 2008). Further south, G. duodenalis has been reported
in seals in the Gulf of St. Lawrence (Appelbee et al., 2010). One human
isolate from a person in Alaska has been characterised as assemblage B (G.
enterica), and is one of the first entire genomes of Giardia to have been char-
acterised (Franzen et al., 2009).The presence of zoonotic assemblages A and
B, which are the only two genotypes reported in people, and the absence
of any animal host-specific genotypes, suggests that zoonotic transmission
commonly occurs among people, dogs, and terrestrial and marine wildlife
in the North American Arctic.

3.2. Geographic Distribution in the North

Giardiasis is widespread in northern North America and Greenland
(Fig. 2.2), and indeed a northern cline in prevalence has been noted (­Murphy,
1981). Cysts in faeces have been detected in people across northern North
America at latitudes up to 69°N, and in animals as far north as 72°N (Tables
2.1 and 2.2). Giardia cysts have been found in drinking water and sewage
effluent in the Yukon Territory (Roach et al., 1993) and in f­aecal samples
from wildlife (Hueffer et al., 2011; Hughes-Hanks et al., 2005; Johnson
et al., 2010; Kutz et al., 2008; Olson et al., 1997; Roach et al., 1993) and
domestic animals (Bryan et al., 2011; Himsworth et al., 2010b) in various
locations in ­northern ­Canada, Alaska, and Greenland (Fig. 2.2).

3.3. Transmission, Prevalence, and Animal Health Impact

in the North
Giardia cysts have been found in a number of domestic and wild animals in
the North. Domestic dogs in northern communities have been shown to
have unusually high prevalence of Giardia in faecal samples, with over half
the dogs infected with zoonotic strains of Giardia in one Saskatchewan com-
munity (Himsworth et al., 2010b), although prevalence was lower in other
communities in northern SK (Schurer et al., 2012).Thus, a domestic animal
44 Emily J. Jenkins et al.

Figure 2.2 Published reports of Giardia in animals and people in northern North

­America and Greenland. (Data from Tables 2.1 and 2.2).

reservoir of human infection exists which will be an important consider-

ation in control.
In the Yukon Territory, Canada, Giardia cysts were present in 14% of bea-
ver samples and 25% of muskrat samples, as well as other terrestrial herbi-
vore and carnivore species (Roach et al., 1993). Giardia infection in beavers
(Castor canadensis) in North America has been linked to human outbreaks
of Giardia infection for many years (Bemrick and Erlandsen, 1988; Davies
and Hibler, 1979; Parkinson and Butler, 2005; Thompson et al., 1990). This
was because of an association between cases of Giardia in campers who
had drunk freshwater from streams in which infected beavers were found
(Thompson et al., 2009). Subsequent studies have shown that beavers were
unlikely to have been the original source, which was probably a contamina-
tion event of human origin. However, the association was the prime reason
for the World Health Organisation's recognition of the zoonotic potential
of Giardia. Subsequent studies have also demonstrated that beavers are sus-
ceptible to infection with zoonotic genotypes of Giardia with no evidence,
to date, of a beaver adapted strain of Giardia (Thompson, 2011; Thompson
et al., 2009).
Table 2.1  Prevalence [% (n)] of Giardia in Animals in Alaska, Northern Canada, and Greenland

Arctic Zoonoses
Host Location [% (n)] Method References
Order Artiodactyla
Boreal Caribou (Rangifer tarandus caribou) Southwestern NT; Trout Lake 2 (149) SG-IFA Johnson et al. (2010)
Dall's Sheep (Ovis dalli dalli) Southwestern YT 40 (5) SFI Roach et al. (1993)
Muskoxen Sachs Harbour, Banks Island, 21 (72)*,† SG-IFA Kutz et al. (2008)
(Ovibos moschatus) NT
Order Carnivora
Dog (Canis familiaris) Villages, Kuskokwim River, AK <1 (234) MIF Fournelle et al. (1958)
Camps, Kuskokwim River, AK 3.6 (55) MIF Fournelle et al. (1958)
Hartley Bay, BC 40 (10) IFA Bryan et al. (2011)
Fort Resolution, NT 8 (48)* SF Salb et al. (2008)
Fort Chipewyan, AB 2 (48)* SF Salb et al. (2008)
Northeastern SK 61 (155)* SG-IFA Himsworth et al. (2010b)
Mamawetan Churchill River 21 (123)* SG-IFA Schurer et al. (2012)
region, SK
Coyote (Canis latrans) Southwestern YT 67 (3) SFI Roach et al. (1993)
Grizzly Bear (Ursus arctos) Southwestern YT 100 (3) SFI Roach et al. (1993)
Wolf (Canis lupus) Southwestern YT 33 (3) SFI Roach et al. (1993)
Order Cetacea
Bowhead Whale (Balaena mysticetus) Barrow and Kaktovik, AK 33 (39) IFA Hughes-Hanks et al. (2005)
North Atlantic Right Whale Bay of Fundy, Canada/Cape 71 (49) IFA Hughes-Hanks et al. (2005)
(Eubalaena glacialis) Cod, USA

Table 2.1  Prevalence [% (n)] of Giardia in Animals in Alaska, Northern Canada, and Greenland—cont’d

Host Location [% (n)] Method References
Order Pinnipedia
Ringed Seal (Phoca hispida) Barrow, AK 65 (31) IFA Hughes-Hanks et al. (2005)
Holman, NT 20 (15) SG-IFA Olson et al. (1997)
Nunavik, QC 80 (55)† SG-IFA- Dixon et al. (2008)
Harp Seal (Phoca groenlandica) Magdalen Islands, Canada 50 (30) SG-IFA Measures and Olson (1999)
Gulf of St. Lawrence, Canada 42 (38)* SG-IFA Appelbee et al. (2010)
Grey/Harbour Seal (Halichoerus Gulf of St. Lawrence/St. 23 (22) SG-IFA Measures and Olson (1999)
grypus/Phoca vitulina) Lawrence Estuary, Canada
Glacier Bay National Park, AK 6 (33) IFA Hueffer et al. (2011)
Bearded Seal (Erignathus barbatus) Nunavik, QC 75 (4) SG-IFA- Dixon et al. (2008)
Hooded Seal (Cystophora cristata) Gulf of St. Lawrence, Canada 80 (10)* SG-IFA Appelbee et al. (2010)
Order Rodentia
Beaver (Castor canadensis) Southwestern YT 14 (14) SFI Roach et al. (1993)
Muskrat (Ondatra zibethicus) Southwestern YT 25 (12) SFI Roach et al. (1993)
Phylum Mollusca

Emily J. Jenkins et al.

Blue Mussel (Mytilus edulis) Nunavik, QC 18 (11) IFA Lévesque et al. (2010)
Within a host species, reports move west to east. Abbreviations for states, provinces, and territories as in Fig. 2.1.
SG-IFA – Sucrose gradient/immunofluorescent assay on faeces, SFI – Sucrose flotation, centrifugation, and iodine staining on faeces, MIF – Merthiolate iodine
formalin faecal staining and concentration, IFA – Immunofluorescent assay on faeces, SF – Sucrose flotation and centrifugation on faeces, SG-IFA-FC – Sucrose
gradient, immunofluorescent assay, and flow cytometry on intestinal contents, IFA – Immunofluorescent assay on pooled tissue.
*Giardia duodenalis (Assemblage A).
†Giardia enterica (Assemblage B).
Table 2.2  Prevalence [% (n)] of Giardia in People in Alaska, Northern Canada, and Greenland Based on Published Literature

Arctic Zoonoses
Location Sampling Dates Prevalence [% (n)] Method References
Alaska, USA
Bethel 1949 1 (100) ZCF Hitchcock (1950)
Kotzebue 1950 1 (100) ZCF Hitchcock (1951)
Kuskokwim River 1955–1956 2.3 (1261; in villages) 3.8 MIF Fournelle et al. (1958)
(419; in fishing camps)
Kuskokwim River 1956–1957 6.3 (174) MIF Fournelle et al. (1959)
Alaska, statewide 1969–1979 3.3 (10,618) (∼66% from FFE Murphy (1981)
­northern AK)
Juneau 1982 54 (24); plus 2 siblings NR Alaska Epi. Bull. (1982)*
Ketchikan 1984 123 ill, 48 lab-confirmed NR Alaska Epi. Bull. (1984)†
Statewide 1984–1985 198 cases NR Jenkerson and Middaugh (1987)
Anchorage 1986 17 (35) IFA Alaska Epi. Bull. (1986)‡
Anchorage 1986 8 (24) IFA Jenkerson and Middaugh (1987)
Kodiak 1989 6 cases IFA Alaska Epi. Bull. (1990)**
Hunting Lodge; NR 1990 18 cases NR Herwaldt et al. (1992)
Juneau Falls, Kenai Peninsula 1991 13 (17) NR Alaska Epi. Bull. (1991)§
Not stated 1995 10 cases NR Centers for Disease Control¶
Fort Chipewyan, AB 1945 14 (140) FS Saunders (1949)
Southampton Island, NU 1947 3 (31) FE Brown et al. (1948)
Igloolik, NU 1949 2 (97); Ages 1–4 years old FE Brown et al. (1950)
Fort Chimo (Kuujjuaq), QC 1959 11 (46) Ages 0–9 years old FES Laird and Meerovitch (1961)


Table 2.2  Prevalence [% (n)] of Giardia in People in Alaska, Northern Canada, and Greenland Based on Published Literature—cont’d
Location Sampling Dates Prevalence [% (n)] Method References

Hall Beach, NU 1970–1971 29 (105) FES Freeman and Jamieson (1976)

Igloolik, NU 1970–1971 12 (247) FES Freeman and Jamieson (1976)
12 communities; Sioux ­ 1974–1975 8.6 (536); Highest in ages 1–10 FES Watson et al. (1979)
Lookout, ON years old
Arctic Bay, NU 1976 17 (153) NR Eaton (1976)
8 communities; James Bay, 1982 5.8 (382); Highest in ages 1–9 FES Brassard et al. (1985)
QC years old
Egedesminde and outposts 1957 7 (663); Highest in ages 0–4 FES Babbott et al. (1961)
(21%) and 5–14 (10%) years
Abbreviations for states, provinces, and territories as in Fig. 2.1.
ZCF – Zinc sulphate centrifugal flotation and iodine smear on faeces, MIF – Merthiolate iodine formalin staining and concentration on faeces, FFE – Faecal
formal-ether, NR – Not recorded, IFA – Immunofluorescent assay on faeces, FS – Faecal smear, FE – Faecal examination, FES – Formalin–ether sedimentation on

Emily J. Jenkins et al.


Arctic Zoonoses 49

In other northern terrestrial wildlife, Giardia cysts have been found

in faecal samples collected from boreal caribou (R. t. caribou) in northern
Alberta, northern British Columbia, and southern Northwest Territories
( Johnson et al., 2010). Giardia cysts have also been found in faecal samples of
Canada geese (Branta canadensis) residing in Maryland, USA (Graczyk et al.,
1998).This indicates that Giardia may be present in winter-feeding grounds
of migratory birds, which, when nesting in the Arctic in the summer, may
serve as a potential source of infection for both wildlife and people (Grac-
zyk et al., 2008).
People may be a source of infection for animals in some areas of north-
ern Canada. Muskoxen (Ovibos moschatus) are indigenous to remote regions
of the arctic tundra of Canada and Greenland. Giardia was first found in
muskoxen in the Canadian Arctic in 1994, on Banks Island, and subse-
quently proved to have a prevalence of 21% (Kutz et al., 2008, 2009b).
Genotyping has demonstrated that the muskoxen harbour zoonotic strains
of Giardia (assemblages A and B) (Kutz et al., 2008, 2009b). This has raised
many interesting questions regarding the origin and epidemiology of this
parasite in people and wildlife in this Arctic ecosystem. In particular, did
people introduce Giardia and contaminate the ecosystem shared with mus-
koxen? Is it now maintained in a sylvatic cycle involving muskoxen and
possibly cervids, and thus a wildlife reservoir of human infection has now
been established? The impact of infection on muskoxen is not understood,
either in terms of muskoxen being a naïve host for Giardia, and the con-
sequences of coinfection with other enteric parasites (Kutz et al., 2008,
2009b). It is known that Giardia occurs in the human population of Banks
Island but there have been no molecular epidemiological surveys that could
link human infections of Giardia with those in muskoxen (Hotez, 2010;
Kutz et al., 2009b).
A number of recent studies have reported G. duodenalis in marine wild-
life, particularly marine mammals and bivalve molluscs. In the marine
environment, Giardia cysts have been reported in seawater in a number of
studies, with the most likely source of contamination being sewage efflu-
ent and surface run-off (Appelbee et al., 2005; Robertson, 2007). However,
given the high prevalence of infection in some regions and the absence
of agricultural run-off, marine mammals themselves may contribute sub-
stantially to the contamination of the Arctic marine environment. Due to
migration patterns, some Arctic seals and whales may also become exposed
to Giardia in sub-Arctic and temperate marine environments, where human
sewage and agricultural run-off are more common.
50 Emily J. Jenkins et al.

The majority of prevalence studies on Arctic marine wildlife have been

done on seals. Moving from west to east, a relatively high prevalence of Giar-
dia spp. (64.5%) was found in faeces of 31 ringed seals (Phoca hispida) (but
not bearded seals – Erignathus barbatus) from Alaska (Hughes-Hanks et al.,
2005), but only 6% of 33 harbour seals (Phoca vitulina) from Glacier Bay
National Park, AK were infected (Hueffer et al., 2011). Olson et al. (1997)
reported the presence of Giardia sp. cysts in 20% of ringed seals in Holman,
NT in the western Canadian Arctic; however, Giardia was not detected in
faecal samples collected from ringed seals from Shingle Point, YT. In the
Gulf of St. Lawrence, Canada, G. duodenalis was identified in 42% of adult
harp seals (Phoca groenlandica, syn. Pagophilus groenlandicus) and 80% of adult
hooded seals (Cystophora cristata) (Appelbee et al., 2010). In Nunavik, QC,
G. duodenalis was found in the gastrointestinal tract (GIT) of 80% of ringed
seals and 75% bearded seals, which were collected for food by five different
northern communities: Kangiqsujuaq, Quanqtaq, Kangiqsualujjuaq, Kuujj-
uaq, and Inukjuak (Dixon et al., 2008). Giardia sp. cysts were also reported
in the faeces of harp seals (50%), grey seals (23%), and a harbour seal from
the east coast of Canada (Measures and Olson, 1999).
Other than seals, only a few other northern marine mammals have been
reported as hosts for G. duodenalis. Giardia has been found in 33.3% of
bowhead whales (Balaena mysticetus) residing off the coast of Alaska, USA
(Hughes-Hanks et al., 2005). Giardia was not detected in beluga whales
(Delphinapterus leucas) in Alaska or in the western Canadian Arctic (Hughes-
Hanks et al., 2005; Olson et al., 1997). Similarly, on the east coast of C
­ anada,
beluga whales and a northern bottle-nosed whale were all negative for
Giardia sp. cysts (Measures and Olson, 1999). However, further south, a
very high prevalence (71.4%) of Giardia spp. was found in North Atlantic
right whales from the Bay of Fundy, Canada, and Cape Cod, Massachusetts
­(Hughes-Hanks et al., 2005).
Giardia has been reported worldwide in a variety of bivalve molluscs
(Fayer et al., 2004; Robertson, 2007). Viable Giardia cysts have also been
identified in seawater (Robertson, 2007) and, as filter feeders, shellfish can
filter large volumes of seawater, thereby concentrating the cysts in their
tissues. There is very little information available, however, concerning
the prevalence of Giardia in shellfish harvested in the Arctic. Giardia was
reported in 18% of pooled samples of blue mussels collected in Nunavik,
Quebec (Lévesque et al., 2010). The inclusion of shellfish in the diet of
some seals, such as bearded seals, suggests this may be a potential source of
infection in these animals.
Arctic Zoonoses 51

The impact of giardiasis on northern animal populations, especially

wildlife, is unknown. Giardiasis can be clinically significant in people, young
livestock, and young companion animals. In young livestock, Giardia infec-
tions may adversely impact production (Olson et al., 2004;Thompson et al.,

3.4. Transmission, Prevalence, and Public Health

Impact in the North
Cases of Giardia in people are attributed to one of the two zoonotic geno-
types/species (A or B/G. duodenalis and G. enterica); however, there is a great
need for molecular epidemiological investigations to determine whether
the source of infection for human cases and outbreaks is other people or
animals (Porter et al., 2011). Giardia is most common in situations that
support a high frequency of transmission, usually as a result of environ-
mental contamination. Poor hygiene and inadequate sanitation are crucial
factors in enhancing transmission of Giardia, exacerbated through contact
with animal reservoirs (Thompson, 2011). Although the incidence of giar-
diasis in people in the Arctic is not known, as with other parts of the world,
­disadvantaged Indigenous communities will be at greatest risk (Hotez, 2010;
Kutz et al., 2009b).
Giardia is often transmitted through water and there is a clear associa-
tion between contamination of drinking water and Giardia-infected animals
and people residing within a watershed.The source of contamination is not
always zoonotic strains of animal origin; indeed, genotyping procedures have
often incriminated human effluent as the source of Giardia contamination
of watersheds (Hunter and Thompson, 2005). In Canada, Giardia has been
reported to be one of the leading causes of waterborne infections in people
and was responsible for 47% of all waterborne disease outbreaks that occurred
from 1974 to 2001 (Schuster et al., 2005). Furthermore, Wallis et al., 1996
analysed water samples collected from 72 municipalities across Canada and
found that 73% of the raw sewage samples, 21% of the raw water samples,
and 18% of the treated water samples contained Giardia cysts. In the Yukon,
water from 32% of 22 pristine sites and 17% of 42 sites in Whitehorse (an
urban region) were positive for Giardia cysts (Roach et al., 1993). According
to Hunter and Thompson (2005), zoonotic transmission of Giardia between
animals and people as a result of direct contact is considered rare; however,
increasing recognition of zoonotic genotypes in dogs closely associated with
human populations in northern Canada and elsewhere (Himsworth et al.,
2010b; Salb et al., 2008; Schurer et al., 2012; Thompson, 2011) suggests
52 Emily J. Jenkins et al.

some mechanism of transmission, be it direct contact or through shared

contaminated environments, food, or water.
In the North, food-borne routes may be an important type of zoonotic
transmission of Giardia, especially for residents who consume raw shellfish,
meat, and organs from harvested wildlife (Dixon et al., 2008; Hotez, 2010).
There is potential for transmission through the consumption of raw meat
or shellfish that have been contaminated with Giardia cysts of human or
animal origin. A number of marine mammal species represent important
food sources for the Inuit in Nunavik, Quebec (Ross et al., 1989), and
elsewhere. It has been suggested that the consumption of marine mam-
mals such as ringed seals, harp seals, and beluga may pose health risks due
to zoonotic parasites, and that hunters, biologists, and veterinarians could
also be at risk (Measures and Olson, 1999; Olson et al., 1997). The recent
reports of zoonotic genotypes and species of Giardia in seals support these
conclusions. For example, dried ringed-seal intestine is consumed widely in
Nunavik and it is feasible, therefore, that this practice could contribute to
the sporadic occurrence of giardiasis reported among the Inuit in the region
(Hodgins, 1997). Contamination of seal meat with intestinal contents is also
possible during the butchering process, and consumption of contaminated
raw or aged seal meat is, therefore, another potential transmission route for
Giardia in the North.
There is little evidence in the literature regarding outbreaks of giardiasis
in northern communities, which suggests that asymptomatic infections are
the norm, and/or that detection is suboptimal. Giardia is a common cause
of diarrhoeal disease, and chronic infections among disadvantaged groups
contribute to poor growth and other nutritional disorders, particularly in
children (Thompson and Monis, 2011). Giardia may be a relatively com-
mon cause of diarrhoeic illness in northern communities, where physicians
presumptively treat with metronidazole (Roach et al., 1993). It is difficult to
assess trends over time given the variety of laboratory techniques employed
to detect Giardia. In Igloolik, NU, prevalence increased from 2% in 1949
to 12% in 1970–71, but this may reflect a more sensitive method of detec-
tion. In Alaska, the number of Giardia isolations from samples submitted by
physicians to the state public health laboratories increased over a 10-year
period between 1969 and 1979 (Murphy, 1981). In Alaska, seasonal peaks in
human infection were noted in fall (September–October), and the majority
of clinical cases were people who had consumed or used untreated surface
water while travelling within Alaska in the preceding two months (Murphy,
1981). In several studies, prevalence was highest in children less than 10
Arctic Zoonoses 53

years of age (Table 2.2), and in people in contact with young children and/
or children in daycare centres (Jenkerson and Middaugh, 1990).
In Canada, giardiasis is a nationally notifiable communicable disease, and
laboratory surveillance data are available from 1989 to 2008. Overall, cases
per 100,000 people are declining Canada-wide. However, residents of the
three northern territories of Canada still have a higher per capita rate of
giardiasis than the Canadian average (Fig. 2.3). In theYukon, per capita infec-
tion was on average 3.4 (1.5–6) times higher than the Canada-wide average,
while results were more variable for the Northwest Territories (mean 1.4
times higher, range 0.3–2.2) and Nunavut (mean 2.3, 0.5–5.5). Only nine
years of data were available for Nunavut, Canada's newest northern terri-
tory; prior to 2000, data from this region were included in the NT. Over
a five year period (2002–2006), the mean annual number of isolations of
enteric protozoa per 100,000 population was 35 for NU and 39 for the YT,
more than double the Canada-wide average of 17 (Public Health Agency of

Figure 2.3  Passive surveillance for Giardia in people in the Yukon Territory (YT), North-
west Territory (NT), Nunavut (NU), and Canada-wide, 1989–2008. [Data from the Notifi­
able Diseases Online Database of the Public Health Agency of Canada (http://dsol-smed. and the Canadian Notifiable Disease
Surveillance System National Report: 2005–2008].
54 Emily J. Jenkins et al.

Canada, 2007). Of all reported enteric protozoal isolates in Canada in this

time period, 73% were Giardia, 13% were Cryptosporidium, 12% were Ent-
amoeba, and 3% were Cyclospora. Given a population of 30,000 in the Yukon
in 2006, and 29,000 in Nunavut, there would have been approximately nine
cases of giardiasis detected per year in YT and seven cases per year in NU
(number of cases of enteric protozoans × 0.73). Using underdiagnosis and
reporting multipliers of 46.3 and 1.3 from the U.S. national data (Scallan
et al., 2011), this suggests a total of 542 cases of giardiasis per year in YT, and
421 cases per year in NU. The underdiagnosis modifier may even be higher
in the North, where both social and physical barriers can limit access to
health care for residents, and clinicians may opt to treat presumptively given
decreased access to diagnostic laboratories.
In Alaska, giardiasis is also a nationally notifiable communicable disease,
and laboratory surveillance data are available from 1992 to 2010 (Fig. 2.4).

Figure 2.4  Passive surveillance for Giardia in people in Alaska (AK) and nationally for the
United States of America, 1992–2010. (Data from the U.S. Centers for Disease Control Mor­
bidity and Mortality Weekly Report Surveillance Summaries,
water/statistics/surveillance/health_data.html#giardia. Rates calculated for 1992–1997
using population estimates from
Arctic Zoonoses 55

Since 1994, cases of giardiasis per 100,000 people have consistently been
higher in Alaska (mean 1.9 times greater, range 1.3–2.8) than nationally in
the USA. Between 2009 and 2010, the average annual incidence in Alaska
(15.9 and 13.7 cases/100,000 population) was almost double the U.S. aver-
age (7.3 and 7.8 cases/100,000 people) over this two-year time period
(Yoder et al., 2010b). Giardia incidence therefore shows a northern cline
on the North American continent, although this is not apparent within
Alaska itself when regions are compared (Fig. 2.5). Giardia is the most com-
mon cause of enteric illness in Alaska (Porter et al., 2011), and is the most
­significant enteric protozoan in the entire North American Arctic.
A variety of drugs are available to treat infections with Giardia in humans.
However, it has been shown that therapeutic intervention is unlikely to
have any long-term benefits in endemic, community situations where the
frequency of reinfection is high because of environmental contamination
and poor hygiene conditions. For example, a sustained, community-based
control programme that used a regular 5-day treatment regimen of 400 mg
albendazole, an effective antigiardial treatment, over 6.5 years in an isolated
community effectively controlled coinfections with hookworm (Ancylos-
toma duodenalis) but had no sustained effect on the prevalence of Giardia
(Reynoldson et al., 1998; Thompson et al., 2001). Although Giardia was

Figure 2.5  Cases of giardiasis in people in Alaska by region, 1986–2010, as reported

to the State Health Department. 5 year rates calculated with the mid-year population
estimate. (Map from (For colour
version of this figure, the reader is referred to the online version of this book.)
56 Emily J. Jenkins et al.

well suppressed by multiple doses of albendazole, regular six-monthly single

doses of albendazole did not suppress the parasite in the long term. Rein-
fection rates with Giardia by the faecal-oral route are rapid in such environ-
ments in which cyst survival is possible, negating any transient benefits of
chemotherapy without concurrent behavioural changes (Thompson, 2011;
Thompson et al., 2001). Mass treatment must be combined with appropri-
ate education programmes designed to prevent re-infection (­Savioli et al.,
2006; Thompson et al., 2001).

3.5. Future Impact of Climate and Landscape Change

Giardia is currently well-established in harsh northern climates, where
cooler, wetter conditions favour survival and transmission of cysts. It is pos-
sible that warming temperatures will decrease environmental survival of
Giardia cysts. However, this will likely be offset by increased transmission
through changes in regional hydrology.
Among the abiotic ecosystem components, water is the most important
in terms of the impact of climate change (Polley and Thompson, 2009).
Climate-induced rises in temperature will affect Arctic regions earlier and
more severely than elsewhere given the diversity of water sources and this
will clearly enhance opportunities for waterborne transmission of Giardia
(Davidson et al., 2011). Climate change has long been predicted to increase
the public health impacts of Giardia in the Arctic as a result of flooding
events caused by heavy rain, snowfall, and melting, leading to outbreaks of
waterborne infections (Parkinson and Butler, 2005).
Increased precipitation and frequency of severe weather events could
overwhelm existing water treatment infrastructure, with a corresponding
increase in the frequency and severity of waterborne outbreaks. Giardia is
the most common cause of drinking water outbreaks in North America,
likely as a result of the resistance of the cysts to chlorine treatment. Water
treatment infrastructure in northern communities that does not involve fil-
tration or ozonation should be considered vulnerable under current and
future environmental conditions.

4.1. Species and Strains Present in the North
Cryptosporidium is a protozoan parasite, associated with enteric disease in
people and animals worldwide. The life cycle of Cryptosporidium includes
asexual phases of proliferation on the mucosal surface, as well as epicellular
Arctic Zoonoses 57

proliferation and a sexual phase of reproduction. Infective oocysts are released

in the faeces and are capable of prolonged survival in the environment
(Hunter and Thompson, 2005). Re-infection is achieved when the oocysts
are ingested; it is also possible for hosts to become superinfected when
­thin-walled cysts rupture inside the intestinal tract.
There are at least 19 different species and over 40 genotypes of Cryp-
tosporidium (Elwin et al., 2012; Fayer, 2010; Xiao and Fayer, 2008), many
of which are host-specific. For example, dogs are often infected with
C. canis and cats with C. felis; however, despite widespread contact between
people and pets, there appears to be limited transmission of these Cryp-
tosporidium species to immunocompetent people (Xiao and Fayer, 2008).
The zoonotic species Cryptosporidium parvum is the most widely distrib-
uted, has the broadest host range, and is the species most commonly asso-
ciated with human and livestock infections (Thompson and Smith, 2011;
Xiao et al., 2004). According to Thompson and Smith (2011), livestock
are the main reservoirs of zoonotic Cryptosporidium and may transmit this
parasite to people via contaminated water or through direct contact. The
absence of significant livestock populations may in part account for the
apparently low prevalence of Cryptosporidium in arctic wildlife and peo-
ple. However, many parasite studies in Arctic hosts have historically been
based on faecal surveys using flotation techniques optimised for eggs of
helminth parasites, and may be less sensitive for detecting the small oocysts
of C
­ ryptosporidium.
As a result, very little is known about the species or genotypes of Cryp-
tosporidium present in the North. A distinct genotype related to Cryptospo-
ridium muris, Cryptosporidium andersoni, and Cryptosporidium serpentis has been
described in barren-ground caribou in the North Slope region of Alaska
(Siefker et al., 2002). Santín et al., (2005) identified Cryptosporidium isolates
from ringed seals in Nunavik, Quebec as C. muris, as well as two novel seal
genotypes. Cryptosporidium oocysts recovered from blue mussels in Nunavik,
Quebec, were morphologically similar to those of C. muris (Lévesque et al.,
2010). The presence of C. muris is of concern with respect to public health
as this species has been reported in immunocompetent people in a number
of countries around the world (Xiao and Feng, 2008).

4.2. Geographic Distribution in the North

Cryptosporidiosis seems to be relatively uncommon in the North and has
not to our knowledge been reported in animals or people in Greenland,
although there have been few studies using methods that would detect this
58 Emily J. Jenkins et al.

parasite. In North America, Cryptosporidium oocysts have been detected in

marine animals as far north as 71°N, and in shellfish, water, and faeces of
terrestrial animals as far north as 61°N (Table 2.3; Fig. 2.6). Whether this
represents a true northern distributional limit is questionable in light of the
limited opportunities for detection. That said, several studies using sensitive
detection methods have found Giardia but not Cryptosporidium in terrestrial
and marine Arctic animals (Tables 2.1 and 2.3).
Cryptosporidium oocysts have been found in faecal samples or intesti-
nal contents collected from terrestrial wildlife (Johnson et al., 2010; Roach
et al., 1993) and domestic dogs in sub-Arctic regions of western Canada
(Bryan et al., 2011; Himsworth et al., 2010b; Schurer et al., 2012), and
in marine mammals and shellfish from Arctic waters (Dixon et al., 2008;
Hughes-Hanks, 2005; Lévesque et al., 2010). Cryptosporidium oocysts have
also been found in 5% of 42 water samples from Whitehorse and 14% of
11 raw water samples collected elsewhere in the Yukon Territory (Roach
et al., 1993).

4.3. Transmission, Prevalence, and Animal Health Impact

in the North
Although Cryptosporidium has been found in multiple species in north-
ern Canada, the prevalence of this protozoan in terrestrial animals was
relatively low or, in some areas, the parasite was not detected at all (in
comparable studies looking at the prevalence of Giardia). Prevalence in
terrestrial ungulates was less than 2% in boreal caribou (R. tarandus cari-
bou) in sub-Arctic Canada and 6% in barren-ground caribou (R. tarandus
groenlandicus) in northwestern Alaska; oocysts were not detected in moose
(A. alces) samples from Alaska nor from muskox (O. moschatus) on Banks
Island, Canada ( Johnson et al., 2010; Kutz et al., 2008; Siefker et al., 2002).
Prevalence in domestic dogs in the sub-Arctic was low, generally 2–3%
(Bryan et al., 2011; Himsworth et al., 2010b; Schurer et al., 2012). In
the Yukon Territory, Roach et al., (1993) did not find Cryptosporidium in
beaver (C. canadensis), muskrat (Ondatra zibethicus), coyote (Canis latrans),
Dall's sheep (Ovis dalli dalli), grizzly bear (Ursus arctos), and wolf (C. lupus)
scat. It is possible that Cryptosporidium may not have been detected in early
studies because of difficulties in detecting small oocysts on routine faecal
flotation. However, even using highly sensitive faecal recovery techniques
(sucrose gradient and immunofluorescent antibody specific to Crypto-
sporidium), Kutz et al. (2008) did not find Cryptosporidium in muskoxen
­during the summer of 2004.
Table 2.3  Prevalence [% (n)] of Cryptosporidium in Animals in Alaska and Northern Canada

Arctic Zoonoses
Host Location Prevalence [% (n)] Method References
Order Artiodactyla
Barren-ground Caribou (Rangifer Teshekpuk Lake and Western 6 (49)* IFA Siefker et al. (2002)
tarandus groenlandicus) Arctic herds, North Slope
Borough, AK
Boreal Caribou (Rangifer tarandus Trout Lake, Southwestern 1.3 (149) SG – IFA Johnson et al. (2010)
caribou) NT
Order Carnivora
Dog (Canis lupus familiaris) Bella Bella and Klemtu, BC 3 (35) IFA Bryan et al. (2011)
9 (11)
Mamawetan Churchill River 2 (43) SG – IFA Schurer et al. (2012)
and Keewatin Yatthe, SK 2 (66)
2 (57)
Northeastern SK 3 (155) SG – IFA Himsworth et al.
Order Cetacea
Bowhead Whale (Balaena Barrow and Kaktovik, AK 5.1 (39) IFA Hughes-Hanks et al.
mysticetus) (2005)
North Atlantic Right Whale Bay of Fundy, NB; Cape 24.5 (49) IFA Hughes-Hanks et al.
(Eubalaena glacialis) Cod, MA (2005)

Table 2.3  Prevalence [% (n)] of Cryptosporidium in Animals in Alaska and Northern Canada—cont’d
Host Location Prevalence [% (n)] Method References
Order Pinnipedia
Ringed Seal (Phoca hispida) Barrow, AK 22.6 (31) IFA Hughes-Hanks et al.
Nunavik, QC 9 (55)† SG – IFA Dixon et al. (2008)
(intestinal Santin et al. (2005)
Phylum Mollusca
Blue Mussel (Mytilus edulis) Nunavik, QC 72.7 (11) Pooled IFA (tissue) Lévesque et al. (2010)
Within a host species, reports move west to east. Abbreviations for states, provinces, and territories as in Fig. 2.1.
IFA – Immunofluorescent assay on faeces unless otherwise indicated, SG – IFA – Sucrose gradient and immunofluorescent assay on faeces unless otherwise
*Caribou-specific genotype.
†Observed C. muris and two novel genotypes.

Emily J. Jenkins et al.

Arctic Zoonoses 61

Figure 2.6  Published reports of Cryptosporidium in animals in the North. (Data from
Table 2.3. No human cases have been reported in the published literature).

In marine mammals, Cryptosporidium spp. have been found in faeces of

ringed seals, but not bearded seals, from Alaska (23%) and Nunavik (9%)
(Dixon et al., 2008; Hughes-Hanks et al., 2005). On examination of the
intestinal contents of ringed seals in the western Arctic region of Canada
by immunofluorescence microscopy, Cryptosporidium spp. oocysts were not
observed (Olson et al., 1997). Likewise, Cryptosporidium spp. oocysts were
not observed in harp or hooded seals from the Gulf of St. Lawrence, Canada
(Appelbee et al., 2010). Cryptosporidium spp. were detected in 5.1% of bow-
head whales from northern Alaska and 24.5% of North Atlantic right whales
from the Bay of Fundy, Canada, and Cape Cod, Massachusetts (Hughes-
Hanks et al., 2005). Cryptosporidium was not detected in beluga whales (D.
leucas) in Alaska or in the western Canadian Arctic (Hughes-Hanks et al.,
2005; Olson et al., 1997).
Viable Cryptosporidium oocysts have been identified in seawater, with
the most likely source of contamination being sewage effluent and surface
run-off (Appelbee et al., 2005; Robertson, 2007). Migratory Arctic seals
may become exposed to Cryptosporidium in sub-Arctic marine environ-
ments contaminated with human sewage as well as agricultural run-off.
62 Emily J. Jenkins et al.

Experimentally, captive harp seal pups became infected with C. parvum

through indirect transmission from the ingestion of seawater contaminated
with faeces from experimentally infected seal pups housed in the same tank
(Appelbee, 2006). Seals may also become infected through consumption of
filter-feeding invertebrates, as Cryptosporidium has been reported worldwide
in a variety of bivalve molluscs (Fayer et al., 2004; Robertson, 2007). Cryp-
tosporidium was present in 73% of pooled samples of blue mussels collected
in Nunavik, Quebec (Lévesque et al., 2010).
The impact of cryptosporidiosis on northern animal populations, espe-
cially wildlife, is unknown. Cryptosporidiosis can be clinically significant in
young livestock and people, especially if immunocompromised. Apart from
disease, other factors may act as stressors adversely affecting the immune
system of wildlife and thus rendering them more susceptible to novel infec-
tions and their clinical consequences. For example, a heavy infection with
Cryptosporidium hominis in a dugong (Dugong dugong) off the east coast of
Australia is thought to have contributed to the animal's death (Morgan
et al., 2001), probably because it was immunocompromised as a result of
another infection or exposure to contaminants from human sewage in the
sea-grass beds grazed by the dugong.

4.4. Transmission, Prevalence, and Public Health

Impact in the North
People may be infected with a number of species of Cryptosporidium;
C. parvum (zoonotic) and C. hominis (human-specific) are the two species
most likely to infect people (Appelbee et al., 2005; Graczyk et al., 2008;
Thompson et al., 2008). Cryptosporidium is most often transmitted among
people by means of direct person-to-person transmission (i.e. the faecal-oral
route), or indirectly through oocyst-contaminated drinking water or recre-
ational water. Food-borne transmission also occurs but is much less com-
mon. In the Arctic, the presence of Cryptosporidium in blue mussels and in the
intestinal tract of seals and whales, all of which are food sources for northern
residents, should be considered when evaluating the risk to human health.
Since 2000, cryptosporidiosis has been a nationally notifiable commu-
nicable disease in Canada, and therefore laboratory surveillance data are
available (Fig. 2.7). Based on the limited data available, residents of the three
northern territories in Canada may have slightly higher per capita rates of
infection with Cryptosporidium than the Canadian average; the pattern is
consistent with sporadic outbreak years interspersed with multiple years
with few or no reported cases. In Alaska, Cryptosporidium-mean annual
Arctic Zoonoses 63

Figure 2.7  Passive surveillance for Cryptosporidium in people in the Yukon Territory
(YT), Northwest Territory (NT), Nunavut (NU), and Canada-wide, 2000–2008. [Data from
the Notifiable Diseases Online Database of the Public Health Agency of Canada (http:// and the Canadian Notifiable
Disease Surveillance System National Report: 2005–2008].

incidence (1.1 and 0.8 cases/100,000 population) was almost three times
less than the U.S. average (2.5 and 2.9 cases/100,000 population) over a
two-year time period (2009–2010) (Yoder et al., 2010a), and was consis-
tently lower than the U.S. national rate over a 10-year period (Fig. 2.8).
Therefore, the evidence suggests that cryptosporidiosis is not currently a
significant public health concern under current conditions in the Arctic.
Furthermore, the lack of livestock and low level of infection in both marine
and terrestrial wildlife indicate that zoonotic transmission of Cryptosporidium
may not be common in northern regions. However, access to health care is
limited for some northern residents, and this along with challenges in col-
lecting and testing faecal specimens may result in a general ­underdiagnosis
of ­cryptosporidiosis in the North.
There is no effective therapy for cryptosporidiosis in humans or compan-
ion animals and maintaining fluid intake is thus essential until the development
of immunity results in clearance in immunologically competent individuals
64 Emily J. Jenkins et al.

Figure 2.8  Passive surveillance for Cryptosporidium in people in Alaska and nation-
ally for the United States of America, 1999–2010. (Data from the U.S. Centers for Disease
Control summaries of the Morbidity and Mortality Weekly Report Surveillance Summaries,

(Thompson et al., 2008). Although Cryptosporidium infections are usually of

short duration and self-limiting in individuals with an intact immune system,
the lack of effective anticryptosporidial drugs means the very young, elderly,
and immunocompromised may be at risk of severe disease as a result of Cryp-
tosporidium infection. An increase in the proportion of northern residents that
are immunocompromised, as observed in some regions of northern Canada
(Irvine et al., 2011), could lead to an emergence of this disease in the future.

4.5. Future Impact of Climate and Landscape Change

Given the similarity of transmission between Giardia and Cryptosporidium,
the mechanisms of climate change are likely to be similar for the two para-
sites. However, it should be noted that Cryptosporidium does not appear to
be as well established at northern latitudes as Giardia, and may therefore
have more to gain from a warming, wetter world. In particular, enhanced
Arctic Zoonoses 65

opportunities for northern agriculture might well lead to introduction of

highly suitable domestic livestock reservoirs for zoonotic species of Cryp-
tosporidium. From a climate change perspective, it would be interesting to
revisit earlier study sites to determine if Cryptosporidium is now present in
the environment, animals, and people in the North. If Cryptosporidium is cur-
rently excluded from northern regions due to environmental ­susceptibility
of the oocysts, climate change may relax these barriers.
Migratory birds, caribou, and marine mammals could serve as a mecha-
nism of introduction into newly susceptible regions. The role of Arctic-
nesting geese in transporting pathogens, including Cryptosporidium spp.,
from sub-Arctic areas should be considered. Canada geese (B. canadensis) are
carriers of C. parvum and C. hominis (Graczyk et al., 1998, 2008; Zhou et al.,
2004), inhabit freshwater and marine habitats, and migrate throughout
northern Canada for summer feeding grounds. Finally, if Cryptosporidium
is present at northern latitudes, increased precipitation and frequency of
severe weather events could overwhelm existing water treatment infrastruc-
ture, with a corresponding increase in the frequency and severity of water-
borne outbreaks. Along with Giardia, Cryptosporidium is one of the most
common causes of waterborne disease outbreaks in Canada, likely as a result
of the resistance of the oocysts to chlorine treatment.

Toxoplasma gondii is a protozoan parasite in the phylum Apicomplexa.
Three infective stages of T. gondii exist: tachyzoites, bradyzoites (within
tissue cysts), and oocysts. Tachyzoites and bradyzoites result from asexual
reproduction and can be produced in both intermediate and definitive
hosts, while oocysts are the result of sexual reproduction and are produced
in the definitive host (Dubey, 2009). The only known definitive hosts of
T. gondii are felids, but numerous intermediate host (IH) species have been
described (Frenkel et al., 1970). The primary mechanism for horizon-
tal transmission of T. gondii begins when an IH ingests sporulated oocysts
from contaminated food, water, or the environment (Fig. 2.9). A secondary
mechanism for horizontal transmission occurs via carnivory or cannibalism.
Once introduced into a food web, T. gondii can be maintained when one IH
ingests tissue cysts from another; this transmission cycle is only perpetuated
by asexual reproduction. Vertical transmission occurs transplacentally. If an
IH is infected while pregnant, the tachyzoites in the bloodstream will cross
the placenta, leading to congenital toxoplasmosis (Dubey, 2009).
66 Emily J. Jenkins et al.

Figure 2.9  Life cycle of Toxoplasma gondii in the North. Transmission by oocysts occurs
in boreal and sub-Arctic regions where free-ranging definitive hosts (felids) are present.
Migratory IH (such as Arctic nesting geese, barren-ground caribou, and marine mam-
mals) can become infected through consumption of oocysts when they seasonally
migrate into terrestrial or marine sub-Arctic environments contaminated with oocysts.
Carnivores in arctic regions become infected through consumption of tissue cysts in
migratory IH. In all mammalian IH, including felids and people, vertical transmission is
likely to occur in females infected during pregnancy.

5.1. Species and Strains Present in the North

Toxoplasma gondii is the only species in this genus to date. There are three
clonal lineages within T. gondii that dominate isolates from domestic ani-
mals and people worldwide. Recent characterisation of isolates from North
American wildlife has identified a fourth clonal type (Type 12) that domi-
nates in wildlife in North America, as well as clonal Type II and atypical
genotypes (9, 11) from Alaska. Unspecified atypical genotypes were also
reported from Kuujjuaq, Nunavik (Dubey et al., 2010, 2011). Otherwise,
little is known about the genotypes of T. gondii present in wildlife, pets, and
people in the North.

5.2. Geographic Distribution in the North

Almost all reports of toxoplasmosis in animals and people are based on
serology, as the organism is rarely detected (Elmore et al., 2012). Antibodies
to T. gondii have been reported in animals (Table 2.4) and people (Table 2.5)
Table 2.4  Prevalence [% (n)] of Exposure to Toxoplasma gondii in Animals in Alaska, Northern Canada, and Greenland

Arctic Zoonoses
Host Location [% (n)] Method References
Order Anseriformes
Geese Nunavik, QC 4.2 (24) NR Leclair and Doidge (2001)
Order Artiodactyla
Dall’s Sheep (Ovis dalli) Interior Alaska 6.9 (319) MAT Zarnke et al. (2000)
Muskoxen Holman, NT 5 (42) MAT Kutz et al. (2000)
(Ovibos moschatus) Kugluktuk, NU 40 (10)
Cambridge Bay, NU 5 (151)
Victoria Island, NU 2 (49) MAT Wu et al. (2010)
Jameson Land, Greenland 3 (129) Dye test Clausen and Hjort (1986)
Caribou/Reindeer Seward Peninsula, Interior, Southcentral AK 6.6 (241) MAT Zarnke et al. (2000)
(Rangifer tarandus) AK and YT <1 (452) MAT Stieve et al. (2010)
Fort Smith, NT 2.9 (104) IHAT Johnson et al. (2010)
NT and NU 29.1 (147) MAT Kutz et al. (2001)
Leaf River, QC <1 (535) NR Leclair and Doidge (2001)
George River, QC/NL 1.2 (82) NR Leclair and Doidge (2001)
Moose (Alces alces) Suscetna R., Alaskan and Kenai Peninsulas 23 (110) IHAT Kocan et al. (1986)
North Slope, Interior, Southcentral AK 1.3 (240) MAT Zarnke et al. (2000)
Bison (Bison bison) Interior AK 1 (241) MAT Zarnke et al. (2000)


Table 2.4  Prevalence [% (n)] of Exposure to Toxoplasma gondii in Animals in Alaska, Northern Canada, and Greenland—cont’d

Host Location [% (n)] Method References
Order Carnivora
Arctic Fox AK (NR) 59.3 (27) DAT Dubey et al. (2011)
(Vulpes lagopus)
Black Bear (Ursus Interior Fairbanks and Tanana Flats, AK 15 (40) LAT Chomel et al. (1995)
americanus) Interior, Southcentral, Southeastern AK 43.4 (143) MAT Zarnke et al. (2000)
Alexander Lake, AK 14 (7) MAT Dubey et al. (2010)
Kuujjuaq, QC NR Bioassay Dubey et al. (2008)
Dog (Canis lupus familiaris) Fort Resolution, NT 62.5 (56) DAT Salb et al. (2008)
Fort Chipewyan, AB 46 (52) DAT Salb et al. (2008)
Keewatin-Yatthé, SK 21 (47) DAT, IFA Schurer et al. (2013)
Grizzly Bear (Ursus arctos) AK (multiple sites) 18 (480) LAT Chomel et al. (1995)
AK (multiple sites) 25 (892) MAT Zarnke et al. (1997)
AK (NR) 66.7 (3) MAT Dubey et al. (2011)
Lynx (Lynx canadensis) Interior AK (multiple sites) 15.3 (255) MAT Zarnke et al. (2001)
Polar Bear (Ursus Eastern Greenland 11.1 (108) MAT Oksanen et al. (2009)
maritimus) North Slope, AK; Beaufort and Chukchi Seas 6 (350) LAT Rah et al. (2005)
Southern Beaufort Sea, AK 13.2 (136) LAT Kirk et al. (2010)
Red Fox (Vulpes vulpes) AK (NR) 12.5 (8) MAT Stieve et al. (2010)
AK (NR) 33.3 (9) MAT Dubey et al. (2011)

Emily J. Jenkins et al.

Wolf (Canis lupus) AK Interior and Seward Peninsula 17.8 (320) MAT Stieve et al. (2010)
North Slope, Interior and Southcentral, AK 8.8 (125) MAT Zarnke et al. (2000)
Wolverine (Gulo gulo) Kugluktuk, NU 41.5 (41) MAT Reichard et al. (2008a)
Arctic Zoonoses
Order Galliformes
Ptarmigan Nunavik, QC 2.5 (79) NR Leclair and Doidge (2001)
Order Pinnipedia
Pacific Walrus (Odobenus Southeastern AK to Bering Strait 5.6 (53) MAT Dubey et al. (2003)
Harbour Seal (Phoca Southeastern AK to Bering Strait 16.4 (311) MAT Dubey et al. (2003)
vitulina) NT/NU (multiple sites) 22.2 (9) DAT Simon et al. (2011)
Ringed Seal (Phoca hispida) Tuktoyaktuk, NT 5.9 (17) DAT Simon et al. (2011)
Sachs Harbour, NT 7.1 (28) DAT Simon et al. (2011)
Ulukhaktok, NT 5.8 (171) DAT Simon et al. (2011)
Arviat NU 15.6 (289) DAT Simon et al. (2011)
Chesterfield Inlet, NU 2.4 (41) DAT Simon et al. (2011)
Hall Beach, NU 23.1 (13) DAT Simon et al. (2011)
Sanikiluaq, NU 7.9 (229) DAT Simon et al. (2011)
Bearded Seal (Erignathus NT/NU (multiple sites) 10 (20) DAT Simon et al. (2011)
Seal Nunavik, QC 14 (28) NR Leclair and Doidge (2001)
Reports move from west to east within a host species. Abbreviations for states, provinces, and territories as in Fig. 2.1.
NR – not recorded, MAT – Modified agglutination test, IHAT – Indirect haemagglutination test, DAT – Direct agglutination test, LAT – Latex agglutination test,
IFA – Indirect fluorescent antibody test.

Table 2.5  Seroprevalence [% (n)] of Toxoplasma gondii in People in Alaska and Northern Canada
Location Sampling Dates [% (n)] Method Reference
Alaska, USA
West, Southeast, Interior 1970–1971 28 (1188) IFA Peterson et al. (1974)
16 (1188) IH Peterson et al. (1974)
Inuvialuit Settlement Region, NT 2007–2008 6 (281) ELISA Egeland et al. (2010a)
Keewatin Yatthé Region, SK 2011 14 (201) ELISA Schurer et al. (2013)
Nunavik, QC (Multiple sites) 1980s 6 (759) IH Tanner et al. (1987)
Nunavik, QC (Kuujjuaq and Salluit) 1983–1986 65 (264) ELISA/IH Curtis et al. (1988)
Nunavik, QC (Kuujjuaq) 1987 50 (22) IFA McDonald et al. (1990)
Nunavik, QC (Multiple sites) 2004 60 (917) ELISA Messier et al. (2009)
James Bay, QC (Multiple sites) 1980s 3 (436) IH Tanner et al. (1987)
James Bay, QC (Mistissini) 2005 10 (50) ELISA Lévesque et al. (2007)
James Bay, QC (Eastmain and Wemindji) 2007 5 (250) ELISA Campagna et al. (2011)
James Bay, QC (Chisasibi and Waskaganish) 2008 9 (266) ELISA Sampasa-Kanyinga et al. (2012)
Nunatsiavut, NL (multiple sites) 2007–2008 8 (275) ELISA Egeland et al. (2010b)

Emily J. Jenkins et al.

Abbreviations for states, provinces, and territories as in Fig. 2.1.
IFA – Indirect fluorescent antibody, IH – Indirect haemagglutination, ELISA – Enzyme-linked immunosorbent assay.
Arctic Zoonoses 71

Figure 2.10  Published reports of toxoplasmosis in animals and people in Alaska, north-
ern Canada, and Greenland, based on immunological methods of detection. (Data from
Tables 2.4 and 2.5).

throughout northern Canada and Alaska, and have also been reported in
wildlife (muskoxen and polar bears) in eastern Greenland (Fig. 2.10). Anti-
bodies have been detected in wildlife as far north as 71°N, and in people
at 67°N.

5.3. Transmission, Prevalence, and Animal Health Impact

in the North
In the North, antibodies to T. gondii have been detected in almost all terres-
trial and marine mammals examined, including herbivores and carnivores,
as well as some avian species (Table 2.4).The life cycle of T. gondii is unclear
in Arctic regions. In boreal and sub-Arctic regions of Alaska and northern
Canada, lynx may serve as definitive hosts. Lynx are reported as far North as
68°N in the western Arctic (Reichard et al., 2008a), and 57°N in the east-
ern Canadian Arctic (M. Simard, unpubl. obs). In Alaska, 15% of lynx were
seropositive (Zarnke et al., 2001), while in southern Quebec, 44% of lynx
were reported to carry Toxoplasma antibodies (Labelle et al., 2001); how-
ever, efforts to detect oocysts in faeces of lynx have not yet been successful,
72 Emily J. Jenkins et al.

possibly due to the short period of time that oocysts are shed (2–3 weeks in
domestic cats), and the difficulty in detecting the small oocysts on routine
faecal examination.
Above the tree line in Arctic regions, lynx are not present and domestic
felids are uncommon and rarely free-ranging (Miller et al., 2008). There-
fore, oocyst transmission is likely restricted to boreal regions in terrestrial
ecosystems in the North (Fig. 2.9). Terrestrial Arctic herbivores that sea-
sonally migrate into boreal regions (such as barren-ground caribou) and
consume oocysts could go on to infect carnivores upon their return to the
Arctic. Similarly, arctic nesting geese might introduce the parasite from sub-
Arctic and temperate areas into the Arctic, with subsequent transmission
to carnivores (Prestrud et al., 2007). Terrestrial carnivores and scavengers
(such as Arctic fox, grizzly bears, black bears, dogs, and wolverines) in the
North appear to have a higher seroprevalence (generally 10–60%) than her-
bivores (generally <10%) (Table 2.4), likely as a result of bioaccumulation
through repeated ingestion of infected prey and/or biomagnification up the
food chain. Carnivores in coastal regions would also have access to fish and
­carcasses of marine mammals.
In marine systems, oocysts could be disseminated from sub-Arctic and
temperate regions through ocean currents. Oocysts can survive in 4°C in
seawater for 2 years and still be infective (Lindsay and Dubey, 2009). Filter-
feeding invertebrates and fish may filter and concentrate the oocysts from
the marine environment, and remain infective for at least 8 h (Lindsay et al.,
2004, 2005; Massie et al., 2010).There is serological evidence that pinnipeds
are exposed to T. gondii in the North American Arctic (Dubey et al., 2003;
Simon et al., 2011). Most recently, antibodies have been detected in Ant-
arctic pinnipeds, suggesting that toxoplasmosis is well established in marine
ecosystems worldwide (Rengifo-Herrera et al., 2012).
Toxoplasma gondii may be a concern for the wildlife population health, as
the parasite causes abortion and congenital disease in many animal species,
including captive reindeer (Dubey et al., 2002). Toxoplasmosis has contrib-
uted to mortality in arctic foxes elsewhere in the Arctic (Sorensen et al.,
2005).Toxoplasmosis in some wildlife species, such as caribou, may additively
influence population declines, triggered by other anthropogenic and envi-
ronmental pressures (Kutz et al., 2000; Vors and Boyce, 2009). ­Barren-ground
caribou in the mainland arctic (Bluenose, Bathurst, and Beverly herds, which
migrate into the boreal region) are experiencing declines across Canada, and
have a relatively high seroprevalence (37% of 117) for antibodies to T. gondii
(Kutz et al., 2001), especially for a herbivore (Table 2.4).
Arctic Zoonoses 73

5.4. Transmission, Prevalence, and Public Health Impact

in the North
5.4.1. Transmission
People, like all IH for T. gondii, become infected through consumption of
oocysts in contaminated food and water, through consumption of tissue
cysts in undercooked fresh meat, and through congenital transmission (Fig.
2.9). The relative significance of these routes of infection in the North is
not known. Oocyst transmission is possible wherever domestic cats and
lynx are present, largely in sub-Arctic and boreal regions. Although cats are
present in Alaskan Eskimo communities (Peterson et al., 1974), domestic
cats and lynx are relatively rare in Canadian Inuit populations in Quebec
(Messier et al., 2009). Therefore, oocyst transmission is unlikely in Arctic
populations, unless ocean currents and watersheds bring oocysts up from
sub-Arctic locations. Food-borne transmission in Inuit populations in the
North is likely the most significant route of infection with T. gondii, given
the important contribution of wildlife to the diet and dietary preferences
for raw, fermented, or dried meat. Congenital human transmission has been
documented in the Canadian North (McDonald et al., 1990).

5.4.2. Prevalence
In recent studies, Inuit populations in Nunavik have high seroprevalence
(50–65%) for T. gondii (Table 2.5). Seroprevalences were higher in inhabitants
from southern and Hudson Bay communities than northern and Ungava
Bay communities (Messier et al., 2009). This overall prevalence is 3 times
the North American average (23%), and almost double the global average
(33%) ( Jones et al., 2001; Tenter et al., 2000). In one Nunavik community,
seroprevalence was higher (87%) in the Inuit population than in the sympat-
ric Cree population (10%), which was linked to preferences for raw meat in
the Inuit population (Messier et al., 2009). In Alaska, however, prevalences
between Eskimo (28%) communities on the west coast and on St. Lawrence
Island, and Indian communities in interior and southeastern Alaska (30%),
were not substantially different (Peterson et al., 1974). Other First Nations
and Inuit people living in northern Canada have a relatively low seropreva-
lence (5–14% in Table 2.5), which may reflect dietary preferences for cooked
meat and consumption of terrestrial (versus marine) wildlife.

5.4.3. Risk Factors

Seroprevalence of T. gondii increased with age in an Alaskan study (­Peterson
et al., 1974), and in Canadian Inuit populations in the Inuvialuit (NT) and
74 Emily J. Jenkins et al.

Nunatsiavut regions, seroprevalence was higher in people greater than or

equal to 40 years-old, as compared to those less than 40 years-old (Egeland
et al., 2010a, 2010b). Risk factors for seropositivity for T. gondii in a recent
study in Nunavik Inuit (QC) were water consumption, frequent cleaning
of water reservoirs, and consumption of seal meat and birds (Messier et al.,
2009); seropositive seals, geese, and ptarmigan have been detected in Nun-
avik and Nunavut (Leclair and Doidge, 2001; Simon et al., 2011). An epide-
miological study of two Cree communities in the James Bay region (QC)
showed that seropositivity in this community (which was very low) was
associated with being male, hunting, and dog ownership (Campagna et al.,
2011). In Alaska, food surveys demonstrated that all community members
consumed wild cervids, and about half consumed wild birds, raw eggs of
wild birds, and marine mammals, but links to serostatus of ­individuals were
not explored (Feldman, 1974; Peterson et al., 1974).
A food survey administered in the Inuvialuit region found that the food
items most commonly eaten in the year prior to the survey were caribou
meat (average 67 g/day) and Arctic char (average 116 g/day). Other items
consumed were berries, Canada goose, trout, whitefish, beluga oil and cari-
bou (heart, ribs, and marrow) (Egeland et al., 2010a). Similarly in Nunatsia-
vut, caribou meat (average 67.3 g/day), caribou heart (average 58.5 g/day),
and Arctic char (average 52.5 g/day) were the most common items eaten,
whereas consumption of berries, rock ptarmigan, Canada goose, partridge,
and caribou (ribs and marrow) also contributed to the diet to a lesser extent
(Egeland et al., 2010b).
Further investigation is needed into the significance of food-borne
routes of transmission of T. gondii in the North, especially the relative con-
tribution of migratory caribou, marine mammals, birds, and other wildlife.
Determining risk factors at the regional level is a key to implementing cul-
turally appropriate and effective local prevention measures, which recognise
the importance of wildlife for food security of northern residents.

5.4.4. Impact and Control

Toxoplasmosis has been described as the most important parasitic infection in
the North American Arctic, in terms of public health impact (Hotez, 2010).
Infection with T. gondii has potential to cause human disease, ranging from
asymptomatic infections and mild influenza-like illness to severe ocular and
neurological lesions, especially in congenitally infected children.The high sero-
prevalence in the general population of Nunavik Inuit in Canada led to close
monitoring of pregnant women by the regional public health department.
Arctic Zoonoses 75

A survey of 496 women between 1982 and 1987 showed that 4 women in
Nunavik seroconverted during pregnancy. Seroconversion was associated
with skinning animals for fur and frequent consumption of meat. Seropositive
women had eaten between 4 and 8 times more dried seal meat, seal liver, and
raw caribou meat than seronegative women (McDonald et al., 1990). From
this study, it was determined that congenital transmission led to toxoplasmosis
in at least two children. In response, a prevention programme was established in
1996 that requires every pregnant woman in Nunavik to be tested for T. gondii.
Serologic diagnosis is complicated by lifelong persistence of IgG antibod-
ies and the potential for prolonged persistence of IgM antibodies (­Montoya
and Rosso, 2005). Additionally, the false positive rate of IgM detection can
be high, depending on the type of laboratory test performed (Montoya and
Rosso, 2005). In response to these challenges, highly specialised tests have
been developed to track different antibody levels over time and it is recom-
mended that IgM-positive results are confirmed by a Toxoplasma ­reference
laboratory (Montoya and Rosso, 2005).
Control of human T. gondii infections in the North is possible by minimis-
ing dietary exposure and potential exposure when handling carcasses, espe-
cially during pregnancy. Most recommendations for the control of T. gondii
include wearing gloves while handling carcasses, washing hands and kitchen
knives frequently when preparing meat, and washing fruits and vegetables
before consumption (Kapperud et al., 1996). Additionally, cleaning litterboxes
daily, and disposing of litter in a place where it is unlikely to enter the water-
shed can minimise the risk of infection from domestic cats. Toxoplasmosis
treatment varies by country, but a combination of pyrimethamine, sulfadia-
zine, and folinic acid is commonly prescribed (Hotop et al., 2012; Kaye, 2011).
Due to potential renal side effects from sulfadiazine therapy, the search for
additional treatments is an active field of research (Alvarez et al., 2007).

5.5. Future Impact of Climate and Landscape Change

5.5.1. Oocyst Transmission
There is currently no evidence that oocyst transmission is a significant
route of infection in the terrestrial North American Arctic, where felids
are not well established. However, as the climate gets warmer, the habi-
tat range of lynx and their prey species are predicted to move north-
ward with the tree line, facilitating local oocyst transmission. Conditions
may also become more permissive for oocyst survival and development.
Sporulated oocysts of T. gondii can survive short periods of cold and
dehydration, and be infectious for at least 18 months in moist conditions
76 Emily J. Jenkins et al.

(Frenkel et al., 1975; Hutchison et al., 1969). An increase in humidity will

therefore enhance survival of oocysts, while increased soil temperatures will
increase the rate of sporulation of oocysts (Dubey et al., 1970; Lindsay et al.,
2002). This increased development rate may trade off with decreased sur-
vival of unsporulated oocysts, which experience higher mortality under
warmer conditions (Dubey, 2009). If, however, climate change leads to
increased winter temperatures, sporulated oocysts may have better survival,
as they are susceptible to freezing (Frenkel and Dubey, 1973).

5.5.2. Frequency and Severity of Waterborne Outbreaks

While oocyst transmission may not be significant under current conditions
in terrestrial Arctic ecosystems, oocysts survive in water for long periods,
especially in marine systems. Melting of ice and permafrost or landslides,
especially along riverbanks, may help transport oocysts to bays and estuaries,
where mollusks or other invertebrates can concentrate them, and in turn
infect their predators ( Jensen et al., 2010). Increased rainfall and weather
extremes will favour the transport and concentration of these oocysts in
water systems used by animals and people; indeed, one of the world's largest
outbreaks of waterborne toxoplasmosis occurred in western Canada as a
result of heavy rainfall washing cougar and cat faeces into a drinking reser-
voir (Berkes and Jolly, 2001; Bowie et al., 1997). Water treatment infrastruc-
ture in northern communities that does not involve filtration should be
considered vulnerable under current and future environmental conditions.

5.5.3. Abundance of and Access to Harvested Wildlife

Climate change may alter the habitat available for marine mammals of the
Arctic, which may experience loss of ice flows to rest, breed and feed, as
well as an increase in weather extremes. Both conditions may result in more
animal mortalities (Burek et al., 2008), hence increasing transmission of the
parasite to scavengers such as polar bears and arctic foxes, or to invertebrates
and marine benthic feeders such as walrus and bearded seals. Loss of near-
shore ice platforms may make it more difficult for hunters to harvest marine
mammals. If resident hunters (human and wildlife) are forced to switch to
more terrestrial diets, they may be exposed to different infection intensities
or strains of T. gondii. In addition, new wildlife IH species moving into Arc-
tic latitudes from sub-Arctic and temperate systems may bring new strains
of T. gondii (Gaydos et al., 2007; Goldstein et al., 2011; Hanni et al., 2003).
There is as yet little evidence for existing effects of climate change on
the transmission of T. gondii. Recent increase in the prevalence of exposure
Arctic Zoonoses 77

to T. gondii in polar bears on Svalbard, Norway, was thought to be due to

warmer waters in the North Atlantic current, with a corresponding increase
in filter-feeding invertebrates and survival of oocysts in marine waters.
Other potential changes in infection pressure for T. gondii on Svalbard
include an increase of migratory birds as well as increased tourism through
cruise ships and other human traffic ( Jensen et al., 2010). In the Canadian
Arctic, increased interest in resource exploration in Nunavik and Nunavut
has already led to an influx of mining boats and barges, raising concerns
about contamination of Arctic waters, and disruption of the migration pat-
terns of marine mammals.

Nematodes of the genus Trichinella are parasites of carnivores and
omnivores in all terrestrial systems and some marine environments globally,
and represent the causative agents of trichinellosis among people (Pozio
et al., 2009). Species of Trichinella are unique among nematodes in having
a “self-contained” (autohexeroxenous) life cycle, where a single vertebrate
serves as both DH and IH, harbouring adults and all of the larval stages
of the parasite (Fig. 2.11). Transmission is thus dependent on predation or

Figure 2.11  Life cycle of Trichinella species in northern North America L1 = first-stage
larvae encysted in tissue of host.
78 Emily J. Jenkins et al.

scavenging, and typically different species of Trichinella circulate among dif-

ferent assemblages of domestic or free-ranging animal hosts (Pozio, 2005).
Adult Trichinella are miniscule (1.0–4.0 mm in length) and live in the
small intestine of their hosts, where females produce first-stage larvae that
enter the lymphatic system and travel to a variety of sites in the body. Among
species of Trichinella circulating amongst placental mammals, larval parasites
become encapsulated, whereas those species circulating in avian and other
hosts remain free in the muscle tissue, representing life history patterns that are
phylogenetically determined (Zarlenga et al., 2006). Only encapsulated forms
are known to occur in the North. In the skeletal muscle, the larvae enter the
muscle cells as intracellular parasites and become surrounded by a collag-
enous capsule. Infection of a new host occurs by predation or by the inges-
tion of carrion containing infective larvae. In the intestine of the definitive
host, larvae emerge from the capsules, undergo 4 molts, and develop to adult
males and females in approximately 3 days (Doyle and Beuchat, 2007; Mit-
reva and Jasmer, 2006). Gravid females produce larvae for 3–4 weeks or more
until expelled by the host's immune system (Capo, 1996; Dupouy-Camet
et al., 2002). First-stage larvae in the musculature are infective by three to four
weeks postinfection (Murrell et al., 2000) and can remain infective for years.

6.1. Species and Strains Present in the North

Species of Trichinella include 8 named taxa among 12 distinct genotypes (9
recognised encapsulated and 3 unencapsulated species), all with potential
for human infection (Pozio et al., 2009; Zarlenga et al., 2006). During most
of the past century, all Trichinella infections were referred to a single species,
Trichinella spiralis, thought to circulate widely among domestic omnivores,
particularly swine and rats, and a range of wild carnivores, rodents and other
mammals. Concepts for broader diversity within the genus were initially
developed based on observations about parasite biology and patterns of
circulation (Britov and Boev, 1972). These ideas were later corroborated by
biochemical and molecular based methods and phylogenetic analyses that
define each of the currently recognised lineages (Pozio et al., 2009; Zarlenga
et al., 1999, 2006). Consequently, it is now recognised that species of Trichi-
nella vary among different regions, and reflect a complex evolutionary and
ecological history (Hoberg et al., 2012; Pozio et al., 2009).
Northern latitudes were important in the evolution of the Trichi-
nella assemblage following initial origins of encapsulated forms in Eurasia
(Hoberg et al., 2012). Diversification in North America (and South America)
resulted from independent episodes of geographic expansion and isolation
Arctic Zoonoses 79

with carnivore hosts starting in the late Miocene, nearly 10 million years
ago (Pozio et al., 2009; Zarlenga et al., 2006). Events culminating with cli-
mate cooling and isolation at high latitudes during the middle Pleistocene
(400–500,000 years ago) led to the origins of Trichinella nativa (T-2) and T-6,
which remain the primary source of human infections in northern North
America today (Hoberg et al., 2012; Pozio et al., 2009; Zarlenga et al., 2006).
Among the 4 species of Trichinella in North America (encapsulated-
T. nativa,T-6, T. murrelli; unencapsulated-T. pseudospiralis), only T-6 and T. nativa
are known to occur at high latitudes, and only these species have first-stage
larvae able to tolerate freezing conditions (Dick and Pozio, 2001). Trichinella
nativa is recognised as the primary zoonotic species present in the circumpolar
north, whereas Trichinella T-6 is restricted to the North (Gajadhar and Forbes,
2010; Larter et al., 2011; Reichard et al., 2008b). In northern Canada and parts
of Alaska,T-6 and T. nativa may occur in sympatry, circulating among an assem-
blage of sylvatic hosts including ursids, canids, mustelids, rodents, and marine
mammals (Gajadhar and Forbes, 2010; La Rosa et al., 2003; Larter et al., 2011;
Pozio et al., 2009; Reichard et al., 2008b). In some regions, hybridisation of
T-6 and T. nativa has been observed (La Rosa et al., 2003), and Nunavut and
the Northwest Territories in Canada may represent a contact zone between
these putative sister-species where populations have come into secondary sym-
patry since the termination of the Pleistocene (Dunams-Morel et al., 2012).

6.2. Geographic Distribution in the North

Wildlife and human cases of trichinellosis have been reported in Alaska,
northern Canada, and Greenland (Fig. 2.12). In Canada, there are no pub-
lished reports on trichinellosis in people in northern British Columbia,
Alberta, Manitoba, or Ontario, although Trichinella has been described in
wildlife in all provinces and territories in Canada. Reported human cases of
trichinellosis generally co-occur with reports of the parasite in free-ranging
mammals in the North (Fig. 2.12). Actual geographic limits for northern
species of Trichinella have yet to be clearly defined due to the lack of con-
temporary surveys, and the fact that most prior records refer to T. spiralis
(Rausch et al., 1956). In northern North America trichinellosis has been
reported as far north as 78° N in people, and 77° N in animals.
In North America, the predicted range for T. nativa is primarily north of
48° N, associated largely with the tundra to sub-Arctic eco-zones and the
4 °C isotherm (Masuoka et al., 2009). In contrast, T-6 is distributed from
the Arctic Circle to temperate regions south of 48° latitude and occurs in
zones of sympatry with T. nativa throughout northern Canada and Alaska
80 Emily J. Jenkins et al.

Figure 2.12  Published reports of trichinellosis in animals and people in Alaska, north-
ern Canada, and Greenland. (Data from Tables 2.6–2.9).

(Dunams-Morel et al., 2012; Gajadhar and Forbes, 2010; La Rosa et al.,

2003; Larter et al., 2011; Masuoka et al., 2009; Pozio et al., 2009; Reichard
et al., 2008b). In northern ecosystems, the distributions of these two encap-
sulated species are strongly tied to episodic climate change and exchange
of mammals and parasites between Eurasia and North America during the
middle to late Pleistocene (Hoberg et al., 2012; Pozio et al., 2009; Zarlenga
et al., 2006). Current distributions are to a great extent influenced by host
mobility and dispersal; consider the wide-ranging polar bear (Ursus mariti-
mus) and arctic fox (Vulpes lagopus) as primary hosts for T. nativa across the
Holarctic, and the occurrence of T-6 in large carnivores including bears
(U. arctos and U. americanus) and wolverine (G. gulo).

6.3. Transmission, Prevalence, and Animal Health Impact

in the North
6.3.1. Transmission
Factors influencing the transmission of Trichinella at high latitudes include
foraging behaviour and distribution of host species, the structure and function
Arctic Zoonoses 81

of food chains, and freeze resistance of larvae in tissues of dead mammalian

hosts. Species such as polar bears, brown bears, arctic fox, wolves, and wol-
verine are highly mobile, disperse rapidly over great distances, and share a
broad-based and diverse array of prey species. As opportunistic scavengers,
apex predators, and prey for larger carnivores, wolverines may be particu-
larly important for transmission of Trichinella (Reichard et al., 2008b; Slough,
2003). In terrestrial systems, other small mustelids (ermine and marten) and
arvicoline rodents may also play a role in transmission (Manning, 1960;
Rausch et al., 1956). In the North, dogs are often fed on or scavenge meat
from harvested carnivores, especially bears and walrus that might be infected
with Trichinella. The role of infected dogs in the transmission of the para-
site in the North is not known. Other domestic animal hosts for Trichinella
(e.g. pigs and horses) are largely absent from northern North America.
In marine systems, transmission of Trichinella among marine mammals
has remained somewhat enigmatic. A marine cycle involving polar bears
and their primary prey, ringed (P. hispida), bearded (E. barbatus) or harp
seals (P. groenlandica) has not been demonstrated, and there are no records
of natural Trichinella infections among these phocids from Canada (Forbes,
2000). Trichinella has been found, however, in bearded seals, ringed seals, and
an unidentified seal from other sectors of the Arctic (e.g. Russia, Alaska, and
Greenland) (Forbes, 2000), but minimal levels of infection suggest that these
pinnipeds are peripheral to the primary pathways for transmission in marine
systems (Taylor et al., 1985). In the near-shore and pelagic environments
associated with pack ice, polar bear and walrus (Odobenus rosmarus) are the
most important hosts for Trichinella (Manning, 1960; Taylor et al., 1985).
Walruses are mostly benthic (sea floor) feeders, although some animals
actively prey on other pinnipeds (Fay, 1960; Manning, 1960). Diets for wal-
rus are dominated by marine mollusks and other benthic invertebrates,
although they will opportunistically consume seals and marine birds such as
black guillemots (Cepphus grylle), thick billed murres (Uria lomvia), common
eider (Somateria mollisima) and arctic fulmars (Fulmarus glacialis) (Fay, 1960;
Fay et al., 1990; Gjertz, 1990; Lowry and Fay, 1984; Mallory et al., 2004;
Rausch, 1968). It is increasingly recognised that walruses become infected
through consumption of freeze-resistant first-stage larvae of T. nativa (or T-6)
in carrion (Fig. 2.11). For example, in Greenland, walruses may consume the
carcasses of hunted polar bears discarded in the ocean (Kapel, 1997).
Although considered secondary pathways of transmission, Britov (1962)
and Fay (1968) showed experimentally that the amphipod crustaceans
Gammarus spp., Anonyx nugax, A. laticoxa, and A. affinis that are prey for
82 Emily J. Jenkins et al.

some phocids can harbour viable first-stage larvae of Trichinella if fed with
infected meat. Additionally, fishes can acquire the larvae following inges-
tion of bird droppings or insects that have fed on infected carrion (Hule-
back, 1980; Kozlov, 1971); such larvae can remain viable in fish for at least
28 h (Hulebak, 1980). First-stage larvae of T. spiralis remained infective after
passing through the intestinal tract of experimentally infected ferrets, polar
bears, red foxes, rats, and swine (Smith, 1985; Zimmerman et al., 1959).
There may be extensive overlap between terrestrial and marine cycles of
transmission of T. nativa due to natural interactions, such as those observed
among brown bears and polar bears feeding on bowhead whale carcasses in
Kaktovik, Alaska (Burek et al., 2008), as well as the highly mobile nature of
arctic wildlife species, such as polar bears and arctic fox. In addition, human
practices, such as leaving carcasses of polar bears out for scavenging, feed-
ing polar bear meat to sled dogs, and disposal of dog carcasses on the ice or
at sea, may also serve to link terrestrial and marine cycles of transmission
(Kapel, 1997).

6.3.2. Prevalence
In the North, multiple surveys for Trichinella spp. in wildlife have been pub-
lished, beginning in 1933 (Masuoka et al., 2009; Polley at al., 2000) (Tables
2.6–2.8). Among northern wildlife, wolverines, polar bears, and brown
bears have the highest prevalence of Trichinella spp., whereas black bears (U.
americanus), Atlantic walrus (Odobenus rosmarus), and martens (Martes ameri-
cana) were reported to have the highest intensity of first-stage larvae in their
muscles (means of 117, 99, and 94 larvae per gram, respectively) (Gajadhar
and Forbes, 2010). The prevalence of Trichinella in walrus is generally lower
than in polar bears but exceeds that observed among phocid seals (Tables
2.6–2.8); intensity of infection in walrus may be relatively high, with a
maximum of 1193 larvae per gram of muscle tissue documented (Gajadhar
and Forbes, 2010).
Surveys of wildlife in northern Canada have not found Trichinella spp. in
Arctic hares (Lepus arcticus), beluga (D. leucas), bearded seal (E. barbatus), harp
seal (P. groenlandica), and ringed seal (P. hispida) (see reviews by Appleyard
and Gajadhar, 2000; Forbes, 2000; Gajadhar and Forbes, 2010). In sub-Arctic
and temperate regions of North America, T. nativa has also been recovered
from black bear and cougars (Puma concolor) (Gajadhar and Forbes, 2010),
while Trichinella T-6 has been found in brown bear, cougar, and wolverines
(Gajadhar and Forbes, 2010; La Rosa et al., 2003; Reichard et al., 2008b;
Zimmerman et al., 1959).
Table 2.6  Prevalence [% (n)] of Trichinella spp. in Animals in Alaska
Host Location(s) Prevalence [% (n)] Method References
Order Carnivora

Arctic Zoonoses
Arctic Fox (Vulpes lagopus) Adak Island 1 case MD Rausch et al. (1956)
Arctic Coast 10 (117) MD
St Lawrence Island 3 (94) MD
Black Bear (Ursus americanus) NR 24 (21) MD Rausch et al. (1956)
NR 28 (40) SE Chomel et al. (1998)
Coyote (Canis latrans) Southern AK 13 (8) MD Rausch et al. (1956)
Dog (Canis familaris) Adak Island 6 (16) MD Schiller (1952)
Adak Island 7 (13) MD Rausch et al. (1956)
Barrow 93 (41) MD
St Lawrence Island 85 (47) MD
NR 36 (64) MD
Ermine (Mustela erminea) Brooks Range 43 (40) MD Rausch et al. (1956)
Copper River 9 (11) MD Rausch et al. (1956)
Grizzly Bear (Ursus arctos) NR 50 (20) MD Rausch et al. (1956)
Multiple sites 49 (878) SE Zarnke et al. (1999)
NR 100 (1) TR Pozio (2000)
Least Weasel (Mustela nivalis) Brooks Range 2 cases MD Rausch et al. (1956)
Lynx (Lynx canadensis) Brooks Range, Copper River 24 (17) MD Rausch et al. (1956)
Multiple 19 (1065) MD Zarnke et al. (1999)
Polar Bear (Ursus maritimus) NR 53 (17) MD Rausch et al. (1956)
NR 47 (478) SE Chomel et al. (1998)
Beaufort Sea, Chukchi Sea 56 (500) SE Rah et al. (2005)
Red Fox (Vulpes vulpes) Multiple 41 (76) MD Rausch et al. (1956)
Wolf (Canis lupus) Fairbanks 37 (148) MD Zarnke et al. (1999)
Brooks Range 33 (154) MD Rausch et al. (1956)
Wolverine (Gulo gulo) NR 50 (38) MD Rausch et al. (1956)

Table 2.6  Prevalence [% (n)] of Trichinella spp. in Animals in Alaska—cont’d

Host Location(s) Prevalence [% (n)] Method References
Order Cetacea
Beluga Whale (Delphinapterus leucas) Wainwright 2 (49) MD Rausch et al. (1956)
Order Lagomorpha
Snowshoe Hare (Lepus americanus) Brooks Range 5 (40) MD Rausch et al. (1956)
Order Pinnipedia
Seals (Various) Arctic Coast, St Lawrence Island <1 (310) MD Rausch et al. (1956)
Walrus (Odobenus rosmarus) NR 53 cases NR Fay (1960)
Order Rodentia
Beaver (Castor canadensis) Kalgin Island 3 (29) MD Rausch et al. (1956)
Brown Lemming (Lemmus Brooks Range 5 (18) MD Rausch et al. (1956)
Brown Rat (Rattus norvegicus) Adak Island, 12 (224) MD Schiller (1952)
Multiple sites 11 (261) MD Rausch et al. (1956)
Ground Squirrel (Citellus undulatus) St Lawrence Island <1 (129) MD Rausch et al. (1956)
Muskrat (Ondatra zibethicus) Copper River <1 (113) MD Rausch et al. (1956)
Narrow-skulled Vole (Microtus gregalis) Brooks Range 2 (57) MD Rausch et al. (1956)
Red-backed Vole Kenai ­Peninsula 4 (49) MD Rausch et al. (1956)
(Myodes/Clethrionomys rutilus)

Emily J. Jenkins et al.

Red Squirrel (Tamiascurus hudsonicus) Brooks Range, Copper River 4 (94) MD Rausch et al. (1956)
Note that a case is equivalent to a single infected animal.
MD – Muscle digest, NR – Not recorded, SE – Serology, TR – Trichinoscopy.
Table 2.7  Prevalence [% (n)] of Trichinella spp. in Animals in Northern Canada
Host Location(s) Prevalence [% (n)] Method References
Order Carnivora

Arctic Zoonoses
Arctic Fox (Vulpes lagopus) NT 3 (1566) MD Smith and Snowden (1988)
NT 1 case NR Parnell (1934)
NU 4 cases BA Chadee and Dick (1982)
YT, NU 11 (28) MD Gajadhar and Forbes (2010)
Black Bear (Ursus americanus) Dehcho, NT 6 (120)*,† MD Larter et al. (2011)
Wollaston, SK 1 case NR Emson et al. (1972)
Black Lake, SK 1 case MD, TR Schellenberg et al. (2003)
QC 1 (107) MD Frechette and Rau (1977)
NL 1 case MD Butler and Khan (1992)
BC, NT, SK, QC 7 (193)*,† MD Gajadhar and Forbes (2010)
Dog (Canis familiaris) Devon Island, NU 1 case TR Kuitunen-Ekbaum (1950)
Cape Hopes Advance QC 2 cases TR Kuitunen-Ekbaum (1950)
Grizzly Bear (Ursus arctos) YT 71 (24) MD Choquette et al. (1969)
Dehcho, NT 73 (11)*,† MD Larter et al. (2011)
BC, NU 29 (68) MD Gajadhar and Forbes (2010)
Lynx (Lynx canadensis) AB 1 case MD Smith and Snowden (1988)
BC, NU 7 (107)* MD Gajadhar and Forbes (2010)
Marten (Martes americana) Stony Lake, MB 1 case NR Chadee and Dick (1982)
Southern Indian Lake, MB 1 (70) TR Poole et al. (1983)
BC, NU 3 (101) MD Gajadhar and Forbes (2010)
Polar Bear (Ursus maritimus) South Beaufort Sea,YT 100 (9) SE Rah et al. (2005)
NT 1 case NR Parnell (1934)
Cornwallis Island, NU 67 (3) NR Kuitunen-Ekbaum (1950)
Southampton Island, NU 67 (3) TR Brown et al. (1949)
Churchill, MB 1 case MD, BA Dick and Belosovic (1978)
NL 59 (278) TR Thorshaug and Rosted (1956)
NU, QC 66 (85)* MD Gajadhar and Forbes (2010)

Table 2.7  Prevalence [% (n)] of Trichinella spp. in Animals in Northern Canada—cont’d

Host Location(s) Prevalence [% (n)] Method References

Red Fox (Vulpes vulpes) NT 11 (19) MD Smith and Snowden (1988)

AB 6 (18) MD Smith and Snowden (1988)
Skunk (Mephitis mephitis) AB 6 (124) MD Gajadhar and Forbes (2010)
Wolf (Canis lupus) YT 47 (153) MD Choquette et al. (1973)
NT 13 (8) MD Smith and Snowden (1988)
NT 47 (153) MD Choquette et al. (1973)
Dehcho, NT 52 (27) MD Larter et al. (2011)
Fort McMurray, AB 1 case MD Dies (1980)
Fort McMurray, AB 1 case NR Smith (1985)
AB 33 (3) MD Smith and Snowden (1988)
QC 50 (2) MD Smith and Snowden (1988)
Nain, NL 1 case BA Smith (1985)
NL 4 (48) MD Smith and Snowden (1988)
YT, BC, NU 43 (28)* MD Gajadhar and Forbes (2010)
Wolverine (Gulo gulo) Snow Lake, MB 1 case NR Dick (1983)
YT, BC, NT 77 (111)*,† MD Gajadhar and Forbes (2010)
Order Pinnipedia
Walrus (Odobenus rosmarus) Southampton Island, NU 4 (394) NR Kuitunen-Ekbaum (1954)
Nunavik, QC 12 (52) NR Richardson et al. (2005)
NL 10 (74) TR Thorshaug and Rosted (1956)

Emily J. Jenkins et al.

NU, QC 41 (32)* MD Gajadhar and Forbes (2010)
Note that a case is equivalent to a single infected animal. Abbreviations for provinces and territories as in Fig. 2.1.
MD – Muscle Digest, NR – Not Recorded, BA – Bioassay, TR – Trichinoscopy, SE – Serology.
Table 2.8  Prevalence [% (n)] of Trichinella in Animals in Greenland

Arctic Zoonoses
Host Location(s) Prevalence [% (n)] Method References
Order Carnivora
Arctic Fox (Vulpes lagopus) NR 6 (266) MD Kapel et al. (1995)
NR 2 (1591) NR Forbes (2000); Roth and Madsen
West Greenland 3 (101) MD, TR Rausch et al. (1956); Roth
Dog (Canis familiaris) NR 62 (945) NR Forbes (2000); Roth and Madsen
NR 70 (66) MD, TR Rausch et al. (1956); Roth
NR 67 (227) NR Rausch et al. (1956); Roth
West Greenland 76 (54) NR Rausch et al. (1956); Thorborg
et al. (1948)
Polar Bear (Ursus maritimus) NR 24 (247) NR Forbes (2000); Roth and Madsen
NR 28 (112) NR Rausch et al. (1956); Roth
Scoresby Sund 32 (38) MD Born and Henriksen (1990)
West Greenland 32 (19) MD, TR Rausch et al. (1956); Roth
Wolf (Canis lupus) NR 50 (4) NR Forbes (2000); Roth and Madsen

Table 2.8  Prevalence [% (n)] of Trichinella in Animals in Greenland—cont’d
Host Location(s) Prevalence [% (n)] Method References
Order Pinnipedia
Bearded Seal (Erignathus NR <1 (245) NR Forbes (2000); Madsen (1961)
barbatus) NR <1 (234) NR Forbes (2000); Roth and Madsen
West Greenland 4 (28) MD, TR Rausch et al. (1956); Roth
Ringed Seal (Phoca hispida) NR <1 (1775) NR Forbes (2000); Madsen (1961)
Seal (Not specified) NR <1 (2318) NR Forbes (2000); Roth and Madsen
NR <1 (1657) NR Forbes (2000); Madsen (1961)
Walrus (Odobenus rosmarus) NR 1 (489) NR Forbes (2000); Madsen (1961)
NR 1 (481) NR Forbes (2000); Roth and Madsen
Barents Sea, 15 (47) TR Thorshaug and Rosted (1956)
Greenland Sea
Thule (Qaanaaq) 4 (24) TR Thing et al. (1976)

Emily J. Jenkins et al.

Thule (Qaanaaq) 2 (126) TR Born et al. (1982)
Note that a case is equivalent to a single infected animal.
NR – Not Recorded, MD – Muscle Digest, TR – Trichinoscopy.
Arctic Zoonoses 89

6.3.3. Impact and Control in Animals

The clinical significance of Trichinella infection in animals, especially
wildlife, is not well known. In Trichinella-naïve grey seals, experimental
infections of 5000 to 50,000 larvae resulted in increased sleep, decreased
activity, and decreased food consumption. Seventeen days after infection,
the seals stopped feeding (Kapel et al., 2003). In temperate regions, Trichi-
nella infections (likely T. spiralis) can be clinically significant in domestic
dogs and cats, and it seems likely that in the North, T. nativa and T-6 can
have similar effects on these hosts, although published reports of infection
or disease are few (Desrochers and Curtis, 1987; Fay, 1960). Prevention of
trichinellosis in domestic dogs and cats relies on thorough cooking (not
freezing) of raw meat prior to feeding and preventing access to human
garbage and infected wildlife. Control in sylvatic populations is not logis-
tically feasible.

6.4. Transmission, Prevalence, and Public Health Impact

in the North
6.4.1. Transmission and Risk Factors
Sporadic cases and outbreaks of human trichinellosis at high latitudes of
North America remain a public health concern. In the North American
Arctic, people are currently exposed to trichinellosis through preparation
and consumption of raw, undercooked, dried, frozen, or fermented meat
from wildlife hosts. Consumption of meat of walrus and bears (polar, grizzly,
and black) has caused most of the trichinellosis outbreaks in people across
high latitudes of North America (Table 2.9). Caribou, whale, and seal have
also been reported to be implicated in some human outbreaks; however,
trichinellosis is rare in these species and epidemiological studies including
source attribution are not always performed. The size of these animals (bull
walrus up to 1200 kg, polar and brown bears up to 550 kg, and black bears
up to 270 kg) means that a single carcass can provide meat, and potential
exposure to infection, for a large number of people. A few decades ago,
Inuit in northern Quebec reported consumption of raw pork products, a
potential source of T. spiralis (Ross et al., 1989). However, trichinellosis has
been largely eradicated from the Canadian domestic swine herd (Gajadhar
et al., 1997) such that all autochthonous cases of trichinellosis in northern
Canada are likely of sylvatic origin.
Culturally, patterns and sources of human infection with trichinellosis
are directly influenced by food preferences and preparation. Some culi-
nary practices appear to have emanated from early recognition of disease
Table 2.9  Prevalence [% (n)] and Potential Source(s) of Infection with Trichinella spp. in People in Alaska, Northern Canada, and Greenland

Location Prevalence [% (n)] Method Source(s) References
Alaska, USA
Anchorage 5 cases CS, SE Black Bear Clark et al. (1972)
Barrow 29 cases CS, SE Walrus Margolis et al. (1979)
Barrow 4 cases CS Walrus Margolis et al. (1979)
Bethel 14 cases CS, SE, EP Black Bear Maynard and Pauls (1962)
Goodnews Bay 4 cases CS, SE, EP Brown Bear Maynard and Pauls (1962)
AK (NR) 1 case CS, MB Black Bear Wilson (1967)
Aklavik, NT 15 (87) SE NR Eaton and Meerovitch (1982)
Back River, NT 15 (48) ST NR Davies and Cameron (1961)
Bathurst, NT 28 (58) ST NR Davies and Cameron (1961)
Cape Parry, NT 9 (22) ST NR Davies and Cameron (1961)
Fort McPherson, NT 29 (28) SE NR Eaton and Meerovitch (1982)
Fort Providence, NT 27 cases NR Black Bear Eaton and Meerovitch (1982)
Holman Island, NT 29 (42) ST NR Davies and Cameron (1961)
Inuvialuit Region, NT <1 (267) SE NR Egeland et al. (2010a)
Inuvik, NT 22 (27) SE NR Eaton and Meerovitch (1982)
22 (250) SE NR Gyorkos and Faubert (1980)
Sachs Harbour, NT 2 (101) SE NR Eaton and Meerovitch (1982)
Spence Bay, NT 49 (47) ST NR Davies and Cameron (1961)

Emily J. Jenkins et al.

21 (19) ST NR Davies and Cameron (1961)
2 cases CS, MB, ST Polar Bear Davies and Cameron (1961)
Tuktoyaktuk, NT 29 (51) SE NR Eaton and Meerovitch (1982)
Black Lake, Stony Rapids, SK 50 cases SE Black Bear Schellenberg et al. (2003)
Black Lake, Stony Rapids, SK 40 (78) SE NR Schellenberg et al. (2003)
Keewatin Yatthé Region, SK 16 (201) SE NR Schurer et al. (2013)
Wollaston Lake, SK 7 cases CS, MB Black Bear Emson et al. (1972)
Arctic Bay, NU 17 (102) SE NR Eaton and Meerovitch (1982)
Cambridge Bay (Iqaluktuuttiaq), 29 (108) ST NR Davies and Cameron (1961)

Arctic Zoonoses
NU 28 (39) ST NR Davies and Cameron (1961)
5 cases CS, SE Grizzly Bear Houzé et al. (2009)
Cape Dorset, NU 95 (20) ST NR Davies and Cameron (1961)
33 (9) ST NR Davies and Cameron (1961)
95 (20) ST NR Eaton and Meerovitch (1982)
Coral Bay, NU 1 case CS Polar Bear MacLean et al. (1989)
Coppermine (Kugluktuk), NU 15 (130) ST NR Davies and Cameron (1961)
Eskimo Point (Arviat), NU 1 case CS Whale, Caribou MacLean et al. (1989)
Igloolik, NU 30 (100) ST NR Brown et al. (1949)
28 (101) SE NR Brown et al. (1949)
King William Land, NU 35 (58) ST NR Davies and Cameron (1961)
18 (11) ST NR Davies and Cameron (1961)
Kitikmeot, NU 1 case NR NR Heinzig (1996)
Pangnirtung, NU 12 cases CS, MB Polar Bear Emmott and Eaton (1977)
Pelly Bay, NU 4 (28) ST NR Davies and Cameron (1961)
Pond Inlet, NU 24 cases CS, MB, SE Seal, Whale MacLean et al. (1989)
Repulse Bay, NU 16 cases NR NR ProMED, 2003
Southampton Island, NU 47 (195) ST NR Brown et al. (1949)
40 (98) SE NR Brown et al. (1949)
51 (NR) ST NR Brown (1949)
40 (265) SE NR Eaton and Meerovitch (1982)
Eastmain, QC 1 (111) SE NR Campagna et al. (2011)
George River, QC 17 cases CS Black Bear Gaulin et al. (2006)
Ivujivik, QC 47 cases CS, MB Walrus MacLean et al. (1989)
13 cases CS, MB Walrus, Seal MacLean et al. (1989)
Northern QC (NR) 3 (436) SE NR Tanner et al. (1987)
9 (759) SE NR Tanner et al. (1987)
Nouveau QC (NR) 5 cases SE NR Laurence et al. (1983)

Table 2.9  Prevalence [% (n)] and Potential Source(s) of Infection with Trichinella spp. in People in Alaska, Northern Canada, and

Location Prevalence [% (n)] Method Source(s) References

Nunavik, QC (NR) 8 (36) SE Walrus Proulx et al. (2002)

<1 (917) SE NR Messier et al. (2012)
Salluit, QC 32 cases CS, SE Walrus MacLean et al. (1989)
13 cases CS Walrus MacLean et al. (1989)
62 (68) CS Walrus MacLean et al. (1992)
Wemindji, QC 1 (140) SE NR Campagna et al. (2011)
NL, NR 2 cases CS, MB Seal, Bear Coffey and Wigglesworth (1956)
22 (112) SE NR Hockin and Meerovitch (1982)
Nunatsiavut Region, NL 1 (275) SE NR Egeland et al. (2010b)
Ammasalik (Tasiilaq) 3 (998) SE NR Møller et al. (2010)
Attu 6 cases CS, SE Bear, Walrus Møller et al. (2005)
Avssakatuk 30 cases CS, SE, ST NR Thorborg et al. (1948)
Christianshaab (Qasigiannguit) 12 cases CS, SE, ST NR Thorborg et al. (1948)
Claushavn 1 case CS, SE, ST NR Thorborg et al. (1948)
Egesdesminde 30 cases CS, SE, ST NR Thorborg et al. (1948)
NR 1 (1012) SE NR Møller et al. (2007)
2 cases CS, SE Polar Bear Nozais et al. (1996)
Holsteinsborg (Sisimiut) 15 cases CS, SE, ST NR Thorborg et al. (1948)
Jakobshavn Kutdligssat (Ilulissat) 32 cases CS, SE, ST Walrus Thorborg et al. (1948)

Emily J. Jenkins et al.

131 cases CS, SE, ST Walrus Thorborg et al. (1948)
Sukkertoppen 2 cases CS, SE, ST NR Thorborg et al. (1948)
Kekertak and Ikorfat 37 cases CS, SE, ST NR Thorborg et al. (1948)
Thule 1 case NR Walrus Thing et al. (1976)
Umanarssuk and Sarkak 5 cases CS, SE, ST NR Thorborg et al. (1948)
Note that a case is equivalent to a single infected person. Abbreviations for states, provinces and territories as in Fig. 2.1.
CS – Clinical signs, SE – Serology, EP – Epidemiology, NR – Not recorded, MB – Muscle biopsy,
ST – Skin test, T-2 – Trichinella nativa.
Arctic Zoonoses 93

associated with the consumption of undercooked or improperly prepared

meat (Connell, 1949; Rausch, 1951). In northern Quebec, Canada,
local customs protective against infection with trichinellosis included
thorough cooking of polar bear and arctic fox prior to consumption
(Ross et al., 1989). Likewise among the Nunamiut people in the Brooks
Range of Alaska, bear was usually only eaten after thorough cooking
(Rausch, 1951).
Hunting practices, together with traditional methods of food prepa-
ration, remain central to pathways for human exposure and possibly dis-
semination of Trichinella. For example, in the Canadian North, walrus
are harvested as a communal effort by Inuit using boats. Traditionally,
hunts have focused on a limited number of localities where these gre-
garious animals gather on pack ice to feed or rest on beaches. Numerous
walrus taken during a harvest are killed and butchered immediately and
cut into large pieces, either adjacent to or on the boats, or on nearby
beaches; some of this meat will be eaten on-site by the hunters. Pieces of
the carcasses that cannot be used are usually abandoned on the beaches
or floating on the ocean, although some will sink to the ocean floor
(M. Simard, personal observations); as carrion these are available to a
variety of scavengers. Once the walrus meat is brought into the commu-
nities, most is immediately frozen until eaten by people, but some is also
fed fresh to dogs. Walrus meat is often eaten frozen, raw, dried (nikku) or
fermented (resulting in a product called igunaq). Experimentally, first-
stage larvae of T. nativa and T-6 can survive such processing (including
freezing) and remain viable for a minimum of 5 months (Forbes et al.,

6.4.2. Prevalence
Historically, trichinellosis was first reported in people in 1835 (Wood,
1835), and in residents of the Arctic in 1914 (Stefansson, 1914). Fur-
ther recognition of cases from different circumpolar countries occurred
between 1934 and 1948 through the joint efforts of Stefansson and col-
leagues from Europe and North America (Connell, 1949). Records varied
from population epidemics in Inuit and Eskimo residents, to European
explorers who ate raw polar bears during their expeditions. In Canada,
the first documented records were from Southampton Island, Nunavut,
where Malcolm Brown from Queen's University discovered in 1948 that
51% of the population responded positively to a skin test for trichinellosis
94 Emily J. Jenkins et al.

(Connell, 1949). A few years later, Robert Rausch explored the ecology of
Trichinella in marine and terrestrial mammals of Barrow, Alaska (Brandly
and Rausch, 1950). In Greenland, an outbreak of trichinellosis in 1947
led to recognition that the parasite was well-established (Thorborg et al.,
1948), consistent with a longer historical presence of T. nativa extend-
ing into the Pleistocene. Species of Trichinella would have been potential
pathogens for the earliest people entering North America across Beringia
(Hoberg et al., 2012).

6.4.3. Alaska
Although there are many published reports of surveys of Alaskan wildlife
for Trichinella (Table 2.6), there are few describing cases in people. Likely
the first outbreak reported was in 1944, affected indigenous Alaskans
from Yakataga, and was associated with the consumption of insufficiently
cooked meat from a local bear (Maynard and Pauls, 1962). A fatal case,
again linked to bear meat, occurred in Selawik in 1946 (Maynard and
Pauls, 1962), and Rausch et al. (1956) described several outbreaks in
the early 1950s affecting both Indigenous and non-Indigenous residents.
Subsequently, outbreaks linked to meat from black bear, brown bear,
and walrus have been described (Table 2.9). The predominant species of
Trichinella in Alaskan wildlife is believed to be T. nativa (T-2), although
T-6 and T-2/T-6 hybrids have been detected in Alaskan wolves (La Rosa
et al., 2003).
Pooled national surveillance data for 1987–1990, 1991–1996, and
1997–2001 demonstrate that Alaska has been among the four or five
states that together experienced many of the cases of trichinellosis in
the United States. Annually between 1975 and 2007, the proportion of
the U.S. cases that occurred in Alaska ranged from 4% to 70% (Bailey
and Schantz, 1990). Historically Alaska has experienced a relatively high
incidence rate of this nationally rare disease (total 5 to 65 cases annually
in the United States, 1991–2010), likely because of the harvesting and
consumption of potentially infected bear and walrus (Adams et al., 2012;
Hall-Baker et al., 2010, 2011; Kennedy et al., 2009; Moorhead et al.,
1999; Roy et al., 2003). Recently, however, the rate has declined, perhaps
in part because of a reduction in the incidence of multicase outbreaks.
In Alaska, trichinellosis has been notifiable to the state public health
authorities since 1968, and surveillance displays an outbreak pattern of
disease with a decline in the size of outbreaks since 2000 (Fig. 2.13).
Arctic Zoonoses 95

Figure 2.13  Cases of human trichinellosis reported to the state public health authori-
ties in Alaska, 1968–2010.

No cases of trichinellosis were reported from the state in 12 of the 20

years from 1991 to 2010, and 1992 was the last year in which there were
10 or more cases in a year (Bailey and Schantz, 1990; McAuley at al., 1991;
Moorhead et al., 1999; Roy et al., 2003). In addition, risk groups appear
to be changing, with recent outbreaks reported in non-Indigenous
(versus Indigenous) residents (

6.4.4. Canada
In Canada, trichinellosis was nationally notifiable to public health authori-
ties from 1929 until 2000. Surveillance in the Northwest Territories
(including the region now known as Nunavut) revealed an outbreak pat-
tern of disease with some of the largest outbreaks reported just before the
disease was de-listed in 2000 (Fig. 2.14). Approximately three quarters of all
reported human cases of trichinellosis in Canada between 1971 and 2000
occurred in the Northwest Territories (including the region now known
as Nunavut) and Nunavik, QC (Appleyard and Gajadhar, 2000). Only 3
96 Emily J. Jenkins et al.

Figure 2.14  Cases of human trichinellosis in the northwest territories (including the
eastern portion now known as Nunavut) between 1961 and 1999, as reported to
national public health authorities in Canada. In 1999, 37 cases were from Nunavut, with
the other 4 from the northwest territories. The disease was de-listed for surveillance in

human cases have ever been reported in the Yukon Territory, one in each
of 1961, 1979, and 1980 (Statistics Canada Annual Report on Notifiable
Diseases 1961; Canada Diseases Weekly Report 1980; Canada Communi-
cable Disease Report 1994). After 2000, trichinellosis remained notifiable
to public health authorities in the Northwest Territories. Since this time, no
cases have been reported in the NT, coinciding with the establishment of
Nunavut from the eastern portions of what was previously considered the
Northwest Territories (
newsletters/epinorth.asp). Canada-wide, from 2001 to 2005, the risk of
hospitalisations (most serious cases) due to trichinellosis was still 2 times
higher for residents of Nunavut and Nunavik (incidence = 42/million/
year) than for those of the rest of Canada (incidence = 0.09/million/year)
(Gilbert et al., 2010).
Despite sporadic cases and outbreaks, recent surveys in Canadian Inuit
in communities from Nunatsiavut, Nunavik (QC), and the Inuvialuit (NT)
Arctic Zoonoses 97

settlement regions report low seroprevalences (less than 1%) (­Egeland et al.,
2010a, 2010b; Messier et al., 2012). Seroprevalence results from recent stud-
ies in Cree communities in Northern Quebec are also low, between 0 and
1% (Campagna et al., 2011; Lévesque et al., 2007; Sampasa-Kanyinga et al.,
2012). However, in a Dene population from northern Saskatchewan in the
sub-Arctic region of Canada, trichinellosis seroprevalence was high (16%),
(Schurer et al., 2013), suggesting that transmission is ongoing (Table 2.9).

6.4.5. Greenland
The first reported outbreak of what was believed to be trichinellosis in
people in Greenland occurred in 1933 near Nugssuak, and the likely
source of infection was walrus. A second outbreak in 1944 in Holsteins-
borg, with walrus the probable source, included 63 cases, and 20 deaths.
Subsequently, in 1947, there were outbreaks in several communities total-
ling 295 cases and 33 deaths (Thorborg et al., 1948) (Table 2.9). Between
1949 and 1959, more than 100 additional cases were reported (Møller
et al., 2005), but none between 1959 and 1971 (Møller et al., 2010).
This may in part reflect a lack of detection; in communities with out-
breaks, some people were likely infected without clinical signs and in
the absence of an outbreak, individual clinical cases might not have been
recognised. Since 1971, only 9 cases have been reported in the published
literature (Table 2.9).
Currently in Greenland, as elsewhere, diagnosis of trichinellosis in
people is most often based on a patient's history, especially risk factors
for infection, clinical signs (including haematology and blood chemistry),
and serology using an enzyme-linked immunosorbent assay (ELISA),
sometimes supplemented by a Western blot (Møller et al., 2005). In
recent studies, the incidence of trichinellosis in Greenland has decreased
and seroprevalence has been low (1–3%) (Møller et al., 2005, 2007,
2010). This likely reflects societal shifts from traditional foods and food
preparation techniques to a more western diet, coupled with greater
awareness of the disease (Pars et al., 2001). Also, since 1966, inspection
of all polar bear and walrus meat has been mandatory in Greenland, but
this is not always enforced or performed by trained personnel (Møller
et al., 2010).
To date, T. nativa (T-2) is the only species found in Greenland (La Rosa
and Pozio, 1990), and consumption of raw or undercooked meat from
polar bears and walrus remains the major source of human infection.
A recent survey of 1012 children aged 8–14 years from several
98 Emily J. Jenkins et al.

communities in Greenland demonstrated a seroprevalence of 1.1% for

Trichinella (Møller et al., 2007). In a second multicommunity survey
of 998 people aged 10 years or older, seroprevalence increased with
age, from 1.4% in people aged 40 years or younger to 12.3% in peo-
ple aged 60 years or older. Overall, significant risk factors for infec-
tion were ‘occupation as hunter or fisherman’ and ‘intake of polar bear
meat’ (Møller et al., 2010). While almost all reported cases have been in
Greenland residents, in 1994, two visitors from France acquired clini-
cally apparent infections from polar bear meat they consumed while in
Greenland (Nozais et al., 1996).
Assuming that the prevalence of Trichinella in a wide range of Greenland
wildlife observed in early surveys has been maintained (Table 2.8), con-
sumption of meat from free-ranging animals, especially polar bears and wal-
rus, will remain a risk for people in Greenland. This risk could be to some
extent mitigated by increased education, and by standardised preconsump-
tion testing of high-risk species, as practised for walrus in some northern
communities in Canada (Proulx et al., 2002). Hunting and the consumption
of wildlife in Greenland, however, are likely to remain an important part of
the cultural fabric of the Kalaallit, as they are for many northern residents.
Opportunities to continue these traditions, with minimal risk of disease,
should be protected.

6.4.6. Impact and Control in People

Healthcare personnel in the North must maintain an index of suspicion
of clinical trichinellosis, which can present as a vague myalgia, in order
to pursue a detailed food history and to order appropriate laboratory
testing. Symptoms associated with infection with T. nativa have been
decribed as primary and secondary trichinosis, caused by differences in
humoral responses (MacLean et al., 1992). The primary syndrome asso-
ciated with larvae in the muscle is characterised by oedema, fever, rash,
and myalgia. The secondary syndrome, mostly reported in previously
infected individuals with acquired immunity, is associated with persistent
diarrhoea, and few of the syndromes observed in primary trichinosis.
These differences are thought to be linked with timing and intensity
of IgG and IgM antibody response. Trichinellosis is suspected when a
patient shows one or more clinical signs coupled with high eosinophil
counts and an epidemiological investigation implicating consumption
of potentially infected meat as a risk factor (Proulx et al., 2002). Blood
Arctic Zoonoses 99

can be sent to a hospital laboratory to confirm the diagnosis with an

ELISA (MacLean et al., 1992; Serhir et al., 2001). When the suspected
meat source is still available for testing, the double separatory funnel and
digestion technique can be used to confirm the presence of the parasite
(Proulx et al., 2002). Once the potential source of infection has been
established, and there is a risk that other people in the community may
be infected, a health advisory is broadcast, warning of the risks, sources
of infection, and prevention measures (cooking or discarding the meat).
Treatments sometimes tried are anthelmintic drugs (i.e. mebendazole or
albendazole), and steroids (i.e. prednisone) for serious cases, depending on
the clinical signs (Kennedy et al., 2009; Møller et al., 2005; Proulx et al.,
2002; Schellenberg et al., 2003).
In recent years in some regions of northern Canada, there is increased
awareness of and local diagnostic capacity for trichinellosis. In Nunavik,
Quebec, a programme was initiated in 1992 to use a double separa-
tory funnel and digestion technique to test walrus tongues for Trichi-
nella infection prior to consumption, and to have the results available
to hunters within 24 h (Leclair et al., 2003). The Nunavik Trichinellosis
Prevention Program (NTPP) is based at the Nunavik Research Center
in Kuujjuaq. If a walrus is found to be infected, it is recommended that
the carcass is destroyed or the meat is eaten only after it is well cooked.
It is also recommended that meat from an uncooked infected carcass is
not to be fed to dogs.
An interesting consequence of the NTPP is that hunters in Nunavik
sometimes avoid the area from which an infected walrus has been har-
vested, perhaps for several years, and hunt further from their community.
This unfortunately decreases the yearly harvest since it costs more to pay
for fuel to reach more distant hunting areas. Another consequence of the
NTPP is that hunters harvest younger animals, which are better tasting
and less likely to be heavily infected with Trichinella. As a consequence
of the NTPP, there have been no cases of trichinellosis due to walrus
harvested in Nunavik since 2000, although one person from Nunavik
was infected from untested walrus meat eaten at a community feast in
Nunavut (Larrat et al., 2012). A testing programme has been in place
in Nunavut since 2003. The Northwest Territories has been using the
same techniques to monitor T. nativa and T-6 in terrestrial carnivores.
Despite the development and expansion of programmes for diagnosis of
100 Emily J. Jenkins et al.

Trichinella, it takes time for people to learn and adjust to the screening
programme (Larrat et al., 2012).
Trichinellosis may be declining in people in many areas of the
circumpolar North, in part due to control programmes such as that
implemented in Nunavik, as well as shifts in diet to store-bought foods
and changes in storage and preparation methods for meat from wild-
life. However, while people younger than 40 years of age eat more
store-bought food, many northern residents (86% of people from Inu-
vialuit, NT, and 25% from Nunatsiavut in Northern Labrador) still
prefer to eat ‘country foods’ (Egeland et al., 2010a, 2010b). In Nun-
avik, people still consume 8.7 meals/week of country food (Blanchet
and Rochette, 2008). Active hunters are present in 57%, 25%, and 45%
of the households studied in Inuvialuit, Nunatsiavut, and Nunavik,
respectively (Blanchet and Rochette, 2008; Egeland et al., 2010a,
2010b). Harvesting capacities have diminished over time due to lack
of money for transportation, gas and supplies, scarcity of animals, bad
weather, and lack of time. Fortunately, those that continue to hunt
still share their food, an important cultural activity and a source of
high quality nutrition in communities facing chronic food inse-
curity (lack of available, affordable, culturally acceptable, safe and
high-quality food). For example, 26–50% of women in northern Canada
could not afford to buy food at the store (Lambden et al., 2006).
Finally, successful public health messages emphasise the importance of
traditional foods that provide physical and social well-being, cultural
identity, economic value, and food security (Blanchet and Rochette,
2008; Egeland et al., 2010a, 2010b). Tools such as the Canadian food
guide now include country foods for Inuit and First Nations peoples
article&id=215&Itemid=138&lang=en). Finally, recognition of new
risk groups (visitors and new northern residents) has led to develop-
ment of targeted public health information, such as that provided to
the out-of-state bear hunters in Alaska (

6.5. Future Impact of Climate and Landscape Change

There is no current evidence that prevalence or intensity of Trichinella has
responded to climate or environmental change; however, there has been
limited surveillance and adequate comparative baselines are generally
Arctic Zoonoses 101

not available. Accelerated warming is likely to have the most important

effects on the ecology of Trichinella through changes in the behaviour,
diet, and distribution of mammalian hosts. Warming will lead to modified
migration routes for terrestrial and marine mammals through responses
to changing patterns of snow cover, extent of sea ice and other envi-
ronmental variables. For example, in the Hudson Bay area of Canada,
changes in the mean timing of ice freeze-up and break-up of 0.8–1.6
weeks have already been observed (Hochleim et al., 2010). These changes
in turn will influence the availability, quality, and species composition of
forage species in terrestrial and marine systems. For example, polar bears,
walrus, and ringed seals rely on ice platforms, and disruption of sea ice
can alter the location, extent and duration of these formations leading to
interference with resting, feeding, and breeding for these marine mam-
mals. Extreme events associated with climate change could also cause
hypothermia, drowning, or stranding from exhaustion among wildlife
(Burek et al., 2008).
New migration routes associated with habitat availability for mam-
mals may further influence shifts in foraging behaviour and diet, through
alterations in species composition, density, and distribution of pelagic
fishes and invertebrates as primary prey (Rausch et al., 2007). Among
pagophilic (ice-associated) marine mammals, such shifts in nearshore
food webs are predicted to directly influence the structure and diversity
of parasite faunas (Rausch et al., 2007). For example, over the past decade,
the edge of the permanent and annual pack ice has moved further off-
shore and considerably beyond the 100 m contour that defines the limit
of diving depth for Pacific walrus. As a consequence, walrus are now
occupying habitats beyond the typical foraging range, and diets are shift-
ing from mollusks and benthic invertebrates to other marine mammals
and carrion.
Concurrently, there are increasing opportunities for overlap among
marine and terrestrial cycles of transmission of trichinellosis. Increasing
numbers of polar bears from the Beaufort Sea, northern Alaska, and the
Chuckchi Sea are remaining on the land in summer and early fall. This is
leading to more encounters with brown bears because both are scavenging
bowhead whales that strand at that time of year (Burek et al., 2008). Similarly,
an increase in carcasses on islands and ice packs can also increase interac-
tions among marine mammals (walruses, seals) and bears (polar and brown).
This new abundance of carrion and prey has the potential to increase Trichi-
nella transmission among walrus, polar bears, and seals, and to modify the
102 Emily J. Jenkins et al.

distribution of species of Trichinella, and influence the potential for human

infection (Rausch et al., 2007).
First-stage larvae of Arctic-adapted species (T. nativa and T-6) in car-
casses are uniquely adapted to survive freezing conditions (Dick and Pozio,
2001). The degree of tolerance depends on several factors that might be
affected by climate change, including absolute temperature, number of
freeze-thaw cycles, host species, and duration of infection (Davidson et al.,
2008; Gottstein et al., 2009; Kapel et al., 1999, 2003). Shifting isotherms
may determine new contact zones for T. nativa and T-6 relative to T. mur-
relli, which is typically distributed at temperate-boreal latitudes. Addition-
ally, species now distributed in the southern region of North America,
including T. spiralis and T. murelli, may also be introduced into higher lati-
tudes as environments become increasingly permissive for agriculture and
new zones of contact are established for species of Trichinella circulating in
sylvatic and domestic cycles.
Finally, changes in human behaviour may alter the risks of transmission
of Trichinella in a warming North. Indigenous residents of the North may
be at decreasing risk of exposure due to increased awareness, capacity for
local detection, and changing food preferences and preparation techniques.
However, enhanced access to the North American Arctic (i.e. through
increased number of ice-free days in the Northwest Passage) may increase
the numbers of visitors, many of whom lack protective traditional knowl-
edge and therefore may be at increased risk of trichinellosis. For exam-
ple, recent emergence of cruise boat tourism in the Canadian North has
included many passengers who want to sample regional foods. In addition,
foreign hunters who come to the North to experience living in the tundra
and hunting their own food may be at risk of infection (Ancelle et al., 2005;
Gaulin et al., 2006; Houzé et al., 2009; Nozais et al., 1996).

Ascarid nematodes are members of the Order Ascaridida, of
which the Family Toxocaridae are the focus of this review. Life cycles
of these ascarids are often direct. Adult nematodes inhabit the GIT of
the vertebrate host. Unembryonated eggs are passed in faeces of the DH
and larvae develop in the eggs at rates dependent on abiotic conditions.
New definitive hosts become infected upon ingestion of eggs containing
second-stage larvae. For Toxocara spp., larvae undergo complex migration
routes depending on age and immune status of the host, and transplacental
Arctic Zoonoses 103

Figure 2.15  Life cycle of the canine roundworm, Toxocara canis. The infective stages for
people are second-stage larvae (L2) in eggs or in tissues of PHs (L1 – first-stage larvae).

and/or transmammary infection may occur within definitive hosts. The

life cycle of Toxocara may also involve vertebrate paratenic hosts (PHs)
with second-stage larvae encysting in tissue and infecting DHs upon
ingestion (Fig. 2.15). For Toxascaris leonina, the life cycle may be direct
or indirect, with second-stage larvae developing to third-stage larvae in
the tissue of an IH, and definitive hosts become infected through con-
sumption of the IH.Vertical transmission is not thought to occur for this

7.1. Species Present in the North

Toxocara canis and Toxocara cati, zoonotic nematodes responsible for ocular
and visceral larval migrans in people, are present in sub-Arctic regions of
northern Canada and Alaska (Fig. 2.16). Their presence is not well docu-
mented in Arctic regions of North America, and neither species has been
reported in Greenland. Other ascarid nematodes reported in carnivores in
the North include Toxascaris leonina and Baylisascaris spp. other than B. pro-
cyonis; however, the zoonotic potential of these parasites is considered low
(Choquette et al., 1969, 1973; Eaton and Secord, 1979; Gau et al., 1999;
Rausch and Fay, 2011). Toxascaris leonina has been identified as a potential
cause of eosinophilia in people in Alaska (Rausch and Fay, 2011).
104 Emily J. Jenkins et al.

Figure 2.16  Published reports of adults or eggs of Toxocara canis in dogs in the North
(data from Table 2.10) and seropositive people (data from Table 2.11). No clinical cases
of larval migrans have been reported in the North.

7.2. Geographic Distribution in the North

Toxocara eggs have limited survival in cold climates and are not regularly
reported in wild or domestic carnivores in Arctic regions of North ­America
(Fig. 2.16,Table 2.10). In Canada, the northernmost reports of T. canis origi-
nated from dogs (Canis lupus familiaris) in Cape Wolstenholme, QC and
Fort Rae, NT (both 63° latitude), while the northernmost report of T. cati
originated from lynx in northern Alberta (54° latitude) (Cameron et al.,
1940; Unruh et al., 1973; van Zyll de Jong, 1966). In Alaska, Toxocara spp.
have been reported in lynx (L. canadensis; presumably T. cati), as well as
dogs and wolves (C. lupus; presumably T. canis) (Dau, 1981). Laboratory
evidence indicates that T. cati eggs survive in colder conditions than T. canis
(O’Lorcain, 1995), suggesting that T. cati may have a more northern distri-
bution; however, case reports are sparse from the northern distribution of
either parasite. Eggs/adults of T. leonina have been reported as far north as
73° latitude, suggesting that efforts based on faecal surveillance could have
detected eggs of T. canis, which are morphologically distinct from those of
Toxascaris and Baylisascaris (Choquette et al., 1973).
Arctic Zoonoses 105

Table 2.10  Prevalence [% (n)] of Toxocara canis in Dogs (Canis lupus familaris) in Alaska
and Northern Canada
Location Latitude [% (n)] Methods References
Alaska, USA
NR NR <1 (414) N Rausch and Fay (2011)
Adak 51°N 31 (16) N Schiller (1952)
Fort Rae, NT 63°N <1 (1000) F Unruh et al. (1973)
Fort Resolution, NT 61°N 7 (70) F Salb et al. (2008)
Fort Chipewyan, AB 59°N 3 (59) F Salb et al. (2008)
13 locations, SK 50–57°N 30 (3370) F Allen and Mills (1971)
Loon Lake, La 54–55°N 48 (160) F Unruh et al. (1973)
Ronge, SK
1 location, SK ∼53°N 17 (155) F Himsworth et al.
3 locations, SK 55–59°N 11 (167) F Schurer et al. (2012)
Moosonee, ON 51°N NR N Cameron et al. (1940)
Wolstenholme, QC 63°N NR N Cameron et al. (1940)
Abbreviations for states, provinces and territories as in Fig. 2.1.
NR – Not recorded, N – necropsy, F – faecal flotation or sedimentation.

7.3. Transmission, Prevalence, and Animal Health Impact

in the North
Toxocara canis transmits predominantly among canids (dogs, wolves, coy-
otes, and foxes), through a variety of routes, including transplacental,
transmammary and faecal-oral; however, small mammals also play a lim-
ited role as PHs (Fig. 2.15). In the last century, dogs and wild canids at
latitudes greater than or equal to 58°N in the North were not commonly
infected with T. canis. In dogs, the parasite was not detected in 272 fae-
cal samples from dogs in northern Alberta, nor in 80 faecal samples or
14 intestinal tracts from dogs in Kuujjuaq, QC (Desrochers and Curtis,
1987; Unruh et al., 1973). In wild canids, postmortem examination of
173 wolves (C. lupus) from 60 to 80° latitude in the Yukon, Northwest
Territories, and Ellesmere Island, Nunavut, Canada failed to identify
T. canis, as did necropsy of 50 Arctic fox (V. lagopus) from Banks Island,
NT (73°N) (Choquette et al., 1973; Eaton and Secord, 1979). A recent
study in two communities at 59 and 61°N in western Canada found the
prevalence of T. canis in dogs to be 3 and 7%, respectively (Table 2.10)
(Salb et al., 2008), suggesting that this parasite may be more successful at
Arctic latitudes in recent times.
106 Emily J. Jenkins et al.

Prevalence of T. canis was higher in dogs at latitudes less than 58°N (as
opposed to north of this latitude) in Alaska and Canada, ranging from 30
to 48% in the last century, with lower prevalence (11–17%) in two recent
studies in western Canada (Table 2.10) (Allen and Mills, 1971; Himsworth
et al., 2010b; Schiller, 1952; Schurer et al., 2012; Unruh et al., 1973). This
may reflect changes in dog demographics (more pets as compared to sled
dogs) and better dog management practices. In wild canids from temper-
ate regions of Canada, T. canis has been reported in wolves from Manitoba
(1/601; 0.2%) and Alberta (2/98; 2%); coyotes (C. latrans) from Newfound-
land (13/69; 19%) and Alberta (1/75; 1%); and red fox (Vulpes vulpes) from
New Brunswick and Nova Scotia (43/61; 71%) (Baron, 1970; Holmes and
Podesta, 1968; Smith, 1978; Stronen et al., 2011).
Horizontal and vertical transmissions of T. cati occur among felids, as well
as via predator–prey interactions between felid DHs and rodent PHs.While
transplacental infection is the primary route of transmission for canids, felids
are most commonly infected by transmammary routes, and secondarily by
ingestion of encysted larvae and embryonated eggs (Overgaauw and van
Knapen, 2008). In northern Alberta, the prevalence of T. cati was 3.5% in
133 lynx examined by necropsy, as opposed to 22% in 274 lynx trapped in
various boreal regions of northern Ontario (Smith et al., 1986; van Zyll de
Jong, 1966). The prevalence of this parasite in other felid species, including
domestic cats, is currently unknown in the North.
Toxocara spp. do not generally cause severe adverse reactions in defini-
tive hosts, and it is unlikely that the health of northern canids and felids is
significantly compromised. However, high-infection intensities in transpla-
centally infected puppies can result in a pot-bellied appearance, failure to
thrive, and, although rare, intestinal blockage and/or death. Juveniles are
more likely to be infected than adults and are more likely to exhibit clini-
cal symptoms (Roddie et al., 2008; Smith et al., 1986). Companion animals
can be effectively treated by anthelmintic administration; however, veteri-
nary services and prescription drugs are generally inaccessible in the North
(Brook et al., 2010; Jenkins et al., 2011).
Rodents infected by T. canis may exhibit a variety of behavioural and
cognitive changes that impair survival and fitness relative to the intensity of
infection (Cox and Holland, 2001). These changes might increase vulnera-
bility to predation by canids and felids, ultimately completing the nematode
life cycle. Human hosts are known to experience adverse effects associated
with migrating larvae (pain, vision impairment, seizures), but it is unclear
whether animals are similarly affected. Postmortem examination of rats
Arctic Zoonoses 107

(Rattus norvegicus) experimentally infected by T. cati revealed L2-stage larvae

in a variety of tissues including the muscle, eye, liver, kidney, brain, and lung
(Santos et al., 2009).
Treatment and control of ascarids focuses on anthelmintic administra-
tion for definitive hosts (such as domestic dogs and cats), and on maintain-
ing high standards of hygiene with regard to pet faeces. Treatment of PHs
is unusual. A wide variety of commercial products are available to treat
Toxocara spp. in the definitive host. Formulations generally include one or
more of the following: pyrantel, piperazine, nictroscanate, and milbemycin
to target adult worms; and emodepside, ivermectin, moxidectin, selamectin,
and fenbendazole to treat both adult worms and larvae (Ramsey, 2011).
Fenbendazole, moxidectin, and the avermectins are used to prevent vertical
transmission of Toxocara in pregnant and lactating females. The Canadian
Parasitology Expert Panel recommends treating dogs with an anthelmintic
effective against roundworms at 2, 4, 6, and 8 weeks of age, followed by a
monthly regimen until 6 months of age, and then followed by annual, bi-
annual, or tri-annual treatment depending on the individual animal's risk
factors for exposure. The recommendation for cats is identical except that
kittens begin treatment at 3, 5, 7, and 9 weeks of age (Beck et al., 2009).

7.4. Transmission, Prevalence, and Public Health

Impact in the North
People become infected with larvae of Toxocara spp. through accidental
ingestion of embryonated eggs shed by definitive hosts, or through con-
sumption of uncooked meat from PHs (Fig. 2.15). Eggs shed by canids and
felids are not immediately infective for people or animals, and require a
period of maturation in the environment. Theoretically, people could come
into contact with embryonated eggs of Toxocara adhered to the peri-anal
region of cats and dogs (Overgaauw et al., 2009; Roddie et al., 2008). How-
ever, a number of studies focused on risk factor assessment have demon-
strated that pet ownership is, in fact, protective against exposure to T. canis
(Iddawela et al., 2003; Schantz et al., 1980; Won et al., 2008; Yang et al.,
1982). The prevalence of Toxocara spp. in people is directly proportional to
the rates of soil contamination with infective eggs of Toxocara, demonstrat-
ing that ingestion of eggs in a contaminated environment is the most com-
mon route of infection for people (Mizgajska, 2001).
Clinical disease associated with Toxocara spp. is characterised by visceral
or ocular larval migrans; however, some individuals remain asymptomatic
(‘covert toxocariasis’). In Canada, human cases are rare, and are most likely
108 Emily J. Jenkins et al.

to occur in children and those experiencing pica (Fanning et al., 1981;

Schantz et al., 1980). Larval migrans due to Toxocara spp. have not been
reported in people in the Canadian North, Alaska, or Greenland. In the
USA, there appears to be a southern bias, with 57% of 44 recent cases
of ocular toxocariasis occurring in residents of the southern U.S. states
Recent seroprevalence studies in Canada conducted between 2004 and
2012 demonstrate that exposure is low (<1–4%) in residents of NT, NL,
and QC (Table 2.11). In a recent study in Nunavik, QC, residents of the
Hudson Bay region were 3.5 times more likely to be seropositive than
those in the more northern Ungava Bay region (Messier et al., 2012). This
is a logical finding given the known sensitivity of Toxocara eggs to freez-
ing temperatures and the low prevalence of T. canis in wildlife and dogs at
Arctic latitudes.

Table 2.11  Seroprevalence [% (n)] of Toxocara canis for People Residing in Northern
Sampling Prevalence
Location Latitude Dates [% (n)] References
Inuvialuit Settle- 68–72°N 2007–2008 <1 (362) Egeland et al.
ment Region, (2010a)
Keewatin Yatthé 55–59°N 2011 13 (201) Schurer et al.
Health Region, (2013)
Nunavik, QC 55–62°N 1980s 11 (759) Tanner et al. (1987)
(Multiple sites)
Nunavik, QC 55–62°N 2004 4 (917) Messier et al.
(Multiple sites) (2012)
James Bay, QC 48–53°N 1980s 10 (436) Tanner et al. (1987)
(Multiple sites)
James Bay, QC 50°N 2005 4 (48) Lévesque et al.
(Mistissini) (2007)
James Bay, QC 52°N and 2007 3 (250) Campagna et al.
(Eastmain and 53°N (2011)
James Bay, QC 54°N and 2008 4 (266) Sampasa-Kanyinga
(Chisasibi and 51°N et al. (2012)
Nunatsiavut, NL 54–56°N, 2007–2008 1 (310) Egeland et al.
(Multiple sites) 58–62°W (2010b)
Abbreviations for states, provinces and territories as in Fig. 2.1.
Arctic Zoonoses 109

Diagnosis of human toxocariasis is based on ocular examination and/

or serology. It is important to note that serological tests for T. canis can cross-
react with other helmiths, such as T. leonina, which is the dominant ascarid
in domestic and wild canids at Arctic latitudes (Nicholas et al., 1984;
Park et al., 2002; Rausch and Fay, 2011). Cross-reactions may account
for higher seroprevalence (10–11%) reported in older studies with less-
specific tests (e.g. Tanner et al., 1987 in Table 2.11). In addition, there are
other parasitic causes of ocular larval migrans (such as larvae of Baylisascaris
and some trematode species), which may account for a recent finding that
30% of 20 patients clinically diagnosed with ocular toxocariasis in the
USA in 2009–2010 were seronegative on ELISA for antibody to Toxocara
spp. (
Treatment of toxocariasis in people differs according to the severity of
symptoms and the location of second-stage larvae. Patients with visceral
larval migrans are administered anti-parasiticides (such as albendazole, thia-
bendazole, and mebendazole), and may also be given anti-inflammatory
corticosteroids to relieve symptoms caused by severe allergic response. Cases
of ocular larval migrans are generally treated with corticosteroids, and may
also require ophthalmologic procedures (Despommier, 2003).

7.5. Future Impact of Climate and Landscape Change

Toxocara spp. nematodes may pose a greater risk of exposure for other DHs,
PHs, and people in the North if environmental conditions become more
suitable for eggs to survive and embryonate. In general, eggs require two
to six weeks at temperatures between 10 and 30 °C before the eggs reach
an infective stage, with accelerated development at warmer temperatures.
Therefore, warming temperatures in the North may lead to accelerated
embryonation in the environment. This may be offset by the fact that eggs
of T. canis do not embryonate in darkness (Feney-Rodriguez et al., 1988),
suggesting a relatively inflexible seasonal window of opportunity for eggs to
embryonate at northern latitudes.
In addition to influencing rate of embryonation, temperature is an
important limiting factor for survival of eggs of Toxocara, with both devel-
opment rates and viability decreasing with increasing time at freezing tem-
peratures; eggs of T. cati may be more freeze tolerant than those of T. canis
(Azam et al., 2012; O’Lorcain, 1995). At the other end of the spectrum, eggs
do not survive at temperatures above 37–40 °C for long (Gamboa, 2005);
however, in northern regions of North America, the lower temperature
threshold is likely the most important. The proposed lower temperature
110 Emily J. Jenkins et al.

threshold for survival of eggs of T. canis is approximately −15° C (Gillespie,

1988). Embryonated eggs can survive on the soil surface and/or beneath
snow cover, even at air temperatures reaching −26 to −29° C (Azam et al.,
2012; Ghadrian et al., 1976; Levine, 1968). Toxocara eggs are also sensitive to
arid conditions and desiccate quickly in direct sunlight (Mizgajska, 2001).
Therefore, warmer and wetter conditions in the North will likely favour
enhanced survival of eggs of Toxocara, especially in winter.
Scavenging of PHs may be an important route of transmission of Toxo-
cara spp., especially in sylvatic cycles. Second-stage larvae encysted in the
muscle tissue of dead PHs are sensitive to variations in temperature and
humidity. Larvae of T. cati encysted in the muscle tissue can survive refrig-
erator temperatures (∼4° C) for two weeks and remain infective for mice;
however, the larvae lose motility and viability after three weeks in a refrig-
erator and 12 h in a household freezer (−25° C) (Taira et al., 2012). Larvae
encysted in tissues of PHs for at least two to three weeks have increased
survival at freezing temperatures as compared to larvae in newly infected
PHs (Sprent, 1953). Therefore, freeze tolerance and age of infection may be
important factors for transmission through scavenging of PHs in adverse
northern conditions, as well as food safety aspects for northern residents, if
food preparation methods fail to inactivate encysted larvae.
The present geographic distribution of Toxocara rarely exceeds 60° lati-
tude in North America and the parasite is apparently absent in Greenland.
However, T. canis has recently been identified in northern dog popula-
tions where it was absent 35 years previously (Jenkins et al., 2011; Salb
et al., 2008; Unruh et al., 1973). This is likely due to the movement of
southern companion animals into northern communities, coupled with
warming temperatures that allow Toxocara eggs to embryonate and to sur-
vive for longer periods of time in the environment. In addition, as vertical
routes of transmission exist for both T. cati (transmammary) and T. canis
(transplacental), female pets brought into the North could create pock-
ets of infection, even under currently unfavourable climatic conditions.
Resource extraction opportunities and climate change may continue to
drive an influx of people and pets from temperate regions into the North,
where lack of veterinary services and canine overpopulation might facili-
tate human exposure to zoonotic species of Toxocara.
In addition to domestic dogs, wild canids may also be moving north.
Arctic fox in Canada are not currently reported as hosts for T. canis, but in
southern areas of the country, the prevalence of infection in red fox popula-
tions has been high (71–95%) (Baron, 1970; Eaton and Secord, 1979; Smith,
Arctic Zoonoses 111

1978). Climate change has resulted in the expansion of red fox north-
wards into what was previously arctic fox territory and the establishment
of sympatric arctic and red fox populations (Hersteinsson and Macdonald,
1992). Thus, natural range expansion of wildlife hosts could contribute to
establishment of T. canis in Arctic regions of North America, and possibly
Greenland, leading to a spillover into local wildlife. Previously uninfected
definitive host populations (e.g. wolves, arctic fox) shed eggs at higher rates
than previously exposed hosts, and given the right climatic conditions,
an environment can quickly become contaminated with eggs of Toxocara
(Overgaauw and van Knapen, 2008; Roddie et al., 2008). Adult female
T. canis nematodes can shed millions of eggs per day into the environment,
depending on infection intensity and host immune status (Glickman and
Schantz, 1981).
To summarise, climate change may drive the range expansion of Toxo-
cara spp. into Arctic areas where they are not currently well established.
In sub-Arctic regions of North America where Toxocara spp. are already
established, climate warming could lead to amplification of transmission
due to enhanced survival of eggs in the environment and larvae encysted in
muscles of dead PHs during winter, more rapid embryonation of eggs in the
environment during summer, and higher levels of egg shedding by previ-
ously uninfected hosts.

Anisakid nematodes are members of the Family Anisakidae, which
includes several zoonotic genera. Anisakids are present in aquatic environ-
ments worldwide, infecting invertebrates, fish, birds, and marine mammals.
The whaleworm (Anisakis simplex) and sealworm (Pseudoterranova decipiens)
are the most common zoonotic parasites in marine systems. Anisakis simplex
uses cetaceans as definitive hosts, whereas P. decipiens prefers seal species as
definitive hosts (Klimpel et al., 2004; Palm, 1999).
Within the definitive host, adult nematodes are present in the digestive
system, and the female nematodes release eggs into the marine environ-
ment through the faeces of the host (Fig. 2.17). Depending on the species,
eggs embryonate and larvae undergo two or three moults before hatching,
releasing second or third-stage larvae in the marine environment (Hays
et al., 1998; Køie et al., 1995). Copepods serving as PHs or IHs (depending
on species of anisakid nematode) ingest the larvae. In turn, copepods can
be eaten by larger invertebrates (such as isopods, amphipods, polychaetes,
112 Emily J. Jenkins et al.

Figure 2.17  Simplified, generic life cycle of anisakid nematodes such as Anisakis simplex
(whaleworm) and Pseudoterranova decipiens (sealworm). Definitive and paratenic hosts
(PH) can become infected by consumption of intermediate (IH) or PH at any point in
the life cycle. People are considered dead-end or accidental hosts, in which third-stage
larvae (L3) generally do not develop.

and mysids), fish, or cephalopods serving as PH. Larger pelagic and demersal
fish may act as PH by eating smaller benthic fish. In PH, third-stage larvae
migrate through the digestive system, and invade organs and flesh, where
they encapsulate (Anderson, 2000). The life cycle is completed when the
definitive hosts, such as marine mammals, eat infected PH (fish or inverte-

8.1. Geographic Distribution in the North

Anisakid nematodes have been detected in wildlife, predominantly marine
mammals, seabirds, and marine and anadromous fish, across northern North
America as far north as 70°N (Fig. 2.18; Table 2.12).

8.2. Species and Strains Present in the North

Species of Anisakis, Pseudoterranova (syn. Phocanema, Porrocaecum, Terranova),
Contracaecum, Phocascaris, and Hysterothylacium have been identified in the
Arctic Zoonoses 113

Figure 2.18  Published reports of anisakid nematodes in animals and people in Alaska,
northern Canada, and Greenland. (Animal data from Table 2.12).

North and Greenland (Table 2.12). In the 1990s, enzyme electrophoresis

research discovered genetically distinct siblings within species of Anisaki-
dae. For example, the A. simplex species complex is now recognised as
containing A. simplex C, A. pegreffii, A. physeteris and A. simplex sensu stricto
(Mattiucci et al., 1997).
In the North, a biogeographical model estimates that A. simplex (s. str.)
is present in the waters of the North Atlantic, Greenland, and up the Pacific
Coast to the Aleutian Islands of Alaska (Kuhn et al., 2011). The only other
Anisakis species present in the North is A. simplex C, located along the
coast of British Columbia (Mattiucci et al., 1997). In the North Atlantic,
P. decipiens A, B, and C are present in the marine food chain (Paggi et al.,
1991, 2000), whereas Contracaecum osculatum A, B, and C are present in Arc-
tic and boreal marine species (Mouritsen et al., 2010; Nascetti et al., 1993).
C. osculatum B and C have been described in grey seals (Halichoerus grypus),
and C. osculatum B in harbour seal (P. vitulina), harp seal (P. groenlandica),
and hooded seal (C. cristata) (Mattiucci and Nascetti, 2008). The develop-
ment and application of PCR techniques have led to the characterisation
Table 2.12  Prevalence [% (n)] of Anisakid Nematodes (Family Anisakidae) in Definitive Avian and Mammalian Hosts, and Fish PH, in northern
North America

Host Location(s) [% (n)] Parasite Identification References
Class Aves, Order Charadriiformes
Common Murre (Uria aalge) Northwest Atlantic <1 (667) Anisakis sp. Muzaffar (2009)
<1 (667) Contracaecum spp.
3 (667) C. spiculigerum
Thick billed Murre (Uria lomvia) Northwest Atlantic 6 (119) C. spiculigerum Muzaffar (2009)
Class Mammalia, Order Cetacea
Beluga Whale (Delphinapterus leucas) Mackenzie Delta, NT 20 (10) A. simplex Wazura et al. (1986)
100 (10) C. aduncum
Nunavik, QC 79 (19) Anisakidae spp. Pufall et al. (2012)
Churchill, NU 1 case A. simplex Doan and Douglas
Blue Whale (Balaenoptera musculus) Arctic and North At least 7 A. simplex, Anisakis sp., Measures (1993)
Pacific Oceans cases Pseudoterranova decipiens
Bowhead Whale (Balaena mysticetus) Barrow, AK 1 case Anisakis sp. Migaki et al. (1982)
Class Mammalia, Order Pinnipedia
Bearded Seal (Erignathus barbatus) Arviat, NU; Nain, NL 75 (16) Anisakidae spp. Pufall et al. (2012)
Fur Seal (Callorhinus ursinus) St-Paul Island, AK 2 (250) Anisakis spp. Spraker et al. (2003)
35 (250) Contracaecum spp.

Emily J. Jenkins et al.

92 (250) Pseudoterranova spp.
Harbour Seal (Phoca vitulina) Glacier Bay and Prince 85 (84) Anisakis spp. Herreman et al.
William, AK 8 (84) Contracaecum spp. (2011)
6 (84) P. decipiens
Ringed Seal (Phoca hispida) QC, NU, NL 18 (170) Anisakidae spp. Pufall et al. (2012)
Spotted Seal (Phoca largha) Bering Sea, AK 71 (55) C. osculatum Shults (1982)
25 (55) P. decipiens
Class Osteichthyes

Arctic Zoonoses
Arctic Char (Salvelinus alpinus) Nunavik, QC 18 (22) Anisakidae spp. Pufall et al. (2012)
Ungava Bay, QC 32 (62) Contracaecum spp. Desdevises et al. (1998)
Multiple, NL 9 (35) Anisakis sp. Hicks and Threlfall
3 (35) Contracaecum spp. (1973)
3 (35) C. aduncum
Multiple, Greenland 3 (348) A. simplex Due and Curtis
1 (348) Contracaecum spp. (1995)
2 (348) C. osculatum/C. phocae
1 (348) Hysterothylacium aduncum
<1 (348) P. decipiens
Atlantic Cod (Gadus morhua) Ungava Bay, QC 44 (313) Anisakis sp. Curtis (1984)
41 (313) Contracaecum or Phocascaris
West Greenland 24 (227) Anisakis sp. Mouritsen et al.
74 (227) C. osculatum (2010)
1 (227) H. aduncum
Atlantic Salmon (Salmo salar) Nunavik, QC 8 (36) Anisakidae spp. Pufall et al. (2012)
Multiple, NL 53 (71) Anisakis sp. Hicks and Threlfall
3 (71) C. aduncum (1973)
Atlantic Tomcod (Microgadus tomcod) Nain, NL 64 (25) Anisakidae spp. Pufall et al. (2012)
Atlantic Whitefish (Coregonus huntsmani) Nunavik, QC 8 (26) Anisakidae spp. Pufall et al. (2012)
Brook Trout (Salvelinus fontinalis) Multiple, NL 4 (124) Anisakis sp. Hicks and Threlfall
1 (124) Contracaecum sp. (1973)
Chum salmon (Onchorhynchus keta) Cordova, Nushagak, AK 100 (40) A. simplex Karl et al. (2011)
Fish, multiple species* Aleutians and SE AK 60 (124) Anisakis sp. Moles and Heintz
10 (124) Contracaecum spp. (2007)
27 (124) H. aduncum

15 (124) P. decipiens
Table 2.12  Prevalence [% (n)] of Anisakid Nematodes (Family Anisakidae) in Definitive Avian and Mammalian Hosts, and Fish PH, in

northern North America—cont’d
Host Location(s) [% (n)] Parasite Identification References
Greenland Cod (Gadus ogac) West Greenland 8 (64) A. simplex Mouritsen et al.
84 (64) C. osculatum (2010)
Greenland Halibut (Reinhardtius NL, Davis Strait, 10†, 43‡ (609) A. simplex Boje et al. (1997)
hippoglossoides) Greenland 45† (609) Contracaecum spp.
5† (609) H. aduncum
1†, 2‡ (609) P. decipiens
Lake Trout (Salvelinus namaycush) Multiple, NL 3 (31) C. aduncum Hicks and Threlfall
Pink Salmon (O. gorbuscha) Cordova, AK 100 (12) A. simplex Karl et al. (2011)
Polar Cod (Boreogadus saida) Nunavik, QC 69 (51) Anisakidae spp. Pufall et al. (2012)
Sable Fish (Anoplopoma fimbria) Sitka, AK 100 (25) Anisakidae spp. Heckmann and Otto
Sculpin, Longhorn (Myoxocephalus Nunavik, QC 86 (14) Anisakidae spp. Pufall et al. (2012)
Sculpin, Shorthorn (M. scorpius) Nunavik, QC 50 (26) Anisakidae spp. Pufall et al. (2012)
Sockeye Salmon (O. nerka) Puget Sound, AK 100 (NR) A. simplex Deardorff and Kent
Cordova, Nushagak, 100 (50) A. simplex Karl et al. (2011)
Naknek, AK

Emily J. Jenkins et al.

Abbreviations for states, provinces, and territories as in Fig. 2.1.
NR – Not recorded.
*Pacific sand lance (Ammodytes hexapterus), Pacific herring (Clupea pallasii), Pacific cod (Gadus macrocephalus), Dusky rockfish (Sebastes ciliatus), Pacific smelt (Tha-
leichthys pacificus), Alaska pollock (Theragra chalcogramma), Rock sole (Lepidopsetta bilineata), Capelin (Mallotus villosus), Arrowtooth flounder (Atherestes stomias), Atka
mackerel (Pleurogrammus monopterygius).
†Prevalence based on detection of larvae in alimentary tract.
‡Prevalence based on detection of larvae in fillets and/or body cavity.
Arctic Zoonoses 117

of Anisakis spp., Contracaecum spp., Hysterothylacium aduncum, and Porrocaecum

spp. in marine and freshwater fish, marine mammals and fish-eating birds
in the Circumpolar North from the Okhotsk, Bering and Norwegian Seas
(Kijewska et al., 2002).

8.3. Transmission, Prevalence, and Animal Health

Impact in the North
Anisakid nematodes were first reported in the North American Arctic as
early as 1899 (Stiles and Hassall, 1899). Anisakid nematodes have been docu-
mented in a wide range of definitive hosts, primarily marine mammals and
birds, and fish PHs in the North American Arctic and Greenland (Table
2.12). Anisakis sp. has also been reported in other mammals, such as sea otters
(Rausch et al., 2007) and a brown bear (U. arctos) in Alaska (Davey, 1971).
Reports of anisakid species from the Arctic generally stem from studies to
evaluate the potential impact on commercial fisheries (Boje et al., 1997;
Curtis, 1984; Deardorff and Kent, 1989; Desdevises et al., 1998; Heckmann
and Otto, 1985; Hicks and Threlfall, 1973; Karl et al., 2011; Moles and
Heintz, 2007), or are incidental reports during necropsy of stranded marine
mammals (Doan and Douglas, 1953; Measures, 1993; Migaki et al., 1982).
As well, Arctic bird studies have included helminth fauna as indicators of
climate change (Hoberg, 1996; Muzaffar, 2009). In the Eastern Canadian
Arctic, zoonotic anisakid species are present in marine fish species (such
as Atlantic tomcod, polar cod, and sculpins) and definitive hosts (such as
ringed seals, bearded seals, and beluga) that are consumed by Inuit (Pufall
et al., 2012). In the western Arctic (Alaska), salmon are important PHs
(Table 2.12) and larvae of A. simplex have been reported at low prevalence
(<1%) in krill IH (Euphausia pacifica and Thysanoessa raschii) in Prince Wil-
liam Sound, Alaska (Smith and Snyder, 2005).
Fauna and prevalence of anisakids in animals varies by region, as well
as age, sex, and dietary preferences of the host. For example, ringed seals
in two Inuit communities in the Hudson Bay region of Canada harbour
different species of anisakid nematodes, probably due to differences in diet
(M. Simard, unpublished data). Prevalence and abundance of anisakid nema-
todes in seals differed significantly depending on Arctic or Atlantic waters in
different Norwegian fjords, diet of seals, and fish age class (Johansen et al.,
2010). Adult male seals were more heavily infected than females or juveniles.
In fish, anadromous fish are less likely to be infected than estuarine fish
(Pufall et al., 2012). Prevalence of A. simplex in Atlantic and Greenland
cod increases with age, and peaks at age class 2 to 4 when the diet switches
118 Emily J. Jenkins et al.

from crustaceans (infected with one or two larvae) to capelin, that may har-
bour many anisakid larvae (Mouritsen et al., 2010). This shift has also been
demonstrated in Atlantic cod from the western Atlantic (McClelland, 2002).
Species of Anisakidae can show marked differences in regional abundance
and host specificity. Terranova decipiens (now P. decipiens) were most abundant
in Icelandic and Plateau cod, but almost absent in fisheries from Greenland,
Faroe Bank, and the Arctic sea of Norway (Platt, 1975). In contrast, Anisakis
sp. were present in all fisheries stock from all regions, with prevalence more
variable in North Atlantic cod (10–83%) than in cod from Arcto-Norwegian
waters (95%). In general, A. simplex has low definitive host specificity com-
pared to other Anisakidae (Klimpel et al., 2004). Anisakid nematodes also
differ in their IH preferences, with A. simplex detected in large, deep sea,
crustacean IHs (Copepoda and Euphausiacea), H. aduncum in planktonic and
benthic invertebrates, and Pseudoterranova in benthic Crustacea (Klimpel and
Rückert, 2005; Klimpel et al., 2006; Køie, 1993).
Anisakid nematodes can cause pathology in both definitive and paratenic
animal hosts, but the overall impact on health and fitness has not been
well described. In marine mammals, the majority of anisakid nematodes
are in the stomach: the fundic region in seals, and the anterior region in
cetaceans. Larvae or adults can be attached alone, or they may be found
in clusters. Pathology is variable and includes local granulomatous inflam-
matory responses, gastric nodules, and/or gastric ulcerations. Inflammation
(macrophages, leukocytes, and giant cells) may also be present as deep as the
muscularis externa (Bishop, 1979; Fleischman and Squire, 1970; McClelland,
1980; Migaki et al., 1971, 1982; Smith and Wootten, 1975; Spraker et al.,
2003; Wilson and Stockdale, 1970;Young and Lowe, 1969). Intestinal perfo-
ration associated with anisakid nematodes contributed to mortality in many
sea otters in Alaska (Rausch et al., 2007).There is one report of Contracaecum
sp. in the brain of a striped dolphin (Martin et al., 1970).
In fish PHs, depending on the parasite and fish species, anisakid larvae
can be recovered on organs, in the flesh, or both. Postmortem migration of
Anisakis sp. larvae from organs to flesh has been observed in herring (Clupea
harengus) (Smith, 1984; Smith and Wootten, 1975), although this was not
observed in salmon in Alaska (Karl et al., 2011). In Norway and England, A.
simplex is the cause of red vent syndrome in Atlantic salmon, where inflam-
mation and haemorrhage occurs around the vent. In severe cases, erosion
of the skin, scale loss, and moderate to severe haemorrhage may occur. The
cause of this syndrome is still unknown, but it does not seem to affect the
general body condition of the animal (Beck et al., 2008; Noguera et al.,
Arctic Zoonoses 119

2009). There are documented cases in Northern Quebec, Canada, raising

concerns that the parasite may be emerging (M. Simard, unpubl. data).

8.4. Transmission, Prevalence, and Public Health

Impact in the North
People are infected by anisakid nematodes through consumption of raw,
smoked, marinated, salted or undercooked fish or invertebrates. Ingested
larvae are thought to remain at the third stage (although see Ishikura et al.,
1995; Lichtenfels and Brancato, 1976), and people are generally considered
accidental or dead-end hosts (Fig. 2.17). Third-stage larvae of A. simplex
and P. decipiens are the most common causes of the disease called anisaki-
dosis (or anisakiasis), present in people worldwide. Other species such as A.
physeteris, A. pegreffii, Contracaecum spp. and Thynnascaris spp. can also cause
the disease (Audicana and Kennedy, 2008; Hochberg and Hamer, 2010;
Ishikura et al., 1990).
The passage of larvae in the oesophagus may create a tingling sensation
in the throat, and larvae may be coughed out or vomited. If the parasite is
retained, it can attach to the stomach or intestinal mucosa (Audicana and
Kennedy, 2008). Diagnosis can be confirmed by visualisation of nematodes
on endoscopy, followed by removal and morphological identification of
nematodes. A week after invasion of the anisakid nematode, patients may
experience nausea, vomiting, diarrhoea, abdominal pain, and hypersensi-
tivity reactions. Symptoms may last for several weeks to 2 years. In rare
cases, anaphylactic shock is possible. Allergic reactions have been reported
by consumption of infected cooked or raw fish and anchovies in vinegar.
Fishermen and workers in fish processing plants can become sensitive to
this nematode (Audicana and Kennedy, 2008).
Despite relatively high prevalence in fish consumed by people in the
North (in 102 Alaskan salmon examined, prevalence of infection with A.
simplex was 100% – Karl et al., 2011), human cases appear to be relatively
uncommon. As many cases may be asymptomatic or only mildly symp-
tomatic, it is likely that cases are underdiagnosed, and there is no formal
surveillance or reporting structure for human cases of anisakidosis. Clinical
cases have been reported in Alaska, including reports of human infections
with Pseudoterranova (Desowitz, 1986; Gyorkos et al., 2003; Lichtenfels and
Brancato, 1976; Myers, 1970). In one case, a fourth-stage larva was removed
from the throat of a patient (Lichtenfels and Brancato, 1976).Ten percent of
stools studied in Eskimos from the Bethel area were infected with imma-
ture larvae identified as Anisakis sp. and Porrocaecum (syn. Pseudoterranova)
120 Emily J. Jenkins et al.

sp. (Hitchcock, 1950). Outbreaks in Alaska have been associated with con-
sumption of undercooked salmon (6 people in Chitina), as well as raw
halibut (2 people in Glenallen) (
The only report of anisakidosis in Arctic Canada is in an Inuk woman
in Nunavik, QC, who had eaten raw Arctic char (Bhat and Clelland, 2010).
This person was referred to a southern specialist after complaining of epi-
gastric pain, weight loss, and fatigue to the local nursing station (Bhat and
Clelland, 2010). Her symptoms resolved upon endoscopic removal of a
single third-stage larva of Anisakis sp. Elsewhere in Canada, one case of Ani-
sakis sp. due to consumption of raw Pacific Salmon and a case of P. decipiens
in a person in Nova Scotia have been reported (Couture et al., 2003; Kates
et al., 1973). No clinical cases of anisakidosis have been reported in Green-
land. In the only serosurveillance study specific for anisakidosis in the Arctic,
Møller et al. (2007) reported a seroprevalence of 0.9% in 1012 children
from Greenland. These results were considered an underestimation due to
the short life of IgG antibodies.

8.5. Future Impact of Climate and Landscape Change

Anisakid species will react differently to climate change according to the
environmental tolerance of free-living stages and changes in fish host
populations. Eggs and newly hatched larvae are particularly dependent on
the temperature, pH, salinity, oxygen, and turbidity of their marine envi-
ronment (Rokicki, 2009). Therefore, enhanced coastal water melting and
freshwater run-off will alter the development of these stages. Water tem-
perature and salinity demonstrably influence egg hatching of P. decipiens.
Experimental laboratory research shows that larvae hatch faster in warmer
waters (5 °C–15 °C), and survive longer in brackish and salt waters com-
pared to freshwater (Measures, 1996). At −17 °C, development of eggs of
Contracaecum rudolphii is inhibited (Dziekońska-Rynko and Rokicki, 2007).
Declines of Anisakis sp. off the coast of Labrador coincided with different
climatic conditions and absence of capelin (Mallotus villosus) and cod (Gadus
morhua) in the coastal Labrador waters (Khan and Chandra, 2006). Decrease
in prevalence of P. decipiens and corresponding increase in prevalence of
C. osculatum in Atlantic cod, other groundfish and grey seals from the Gulf
of St Lawrence between 1988 and 1992 is believed to be due to warmer
water temperatures stemming from the Labrador current. This favoured
C. osculatum (in which eggs can hatch at 0 °C) as compared to cold-adapted
P. decipiens (Marcogliese, 2001). Therefore, climate change could lead to
Arctic Zoonoses 121

faunal shifts in anisakid nematodes. Furthermore, warmer water will favour

the northward migration of pelagic fish, and this may expand the range of
anisakids in the North and amplify endemic transmission of Anisakis sp.
(Marcogliese, 2001; Perry et al., 2005; Rokicki, 2009).
Final hosts such as marine mammals, especially those that are pagophilic
(dependent on floating ice), will be affected by warmer waters. It is pre-
dicted that feeding habits and diet will change due to reduction of available
ice habitat for resting, feeding, and breeding; changes in migration pat-
terns; and loss of substrate for prey (Burek et al., 2008; Rausch et al., 2007).
Changes in host migratory patterns can result in marked changes in sea-
sonal abundance of anisakid nematodes; for example, northward migration
of whales and a spring plankton bloom resulted in a peak in abundance of
A. simplex in saithe (Pollachius virens), cod (G. morhua), and redfish (Sebastes
marinus) in Norway coastal waters (Strømnes and Andersen, 2000).
From the perspective of Arctic residents, some of whom consume dried
marine mammal intestines and raw fish, amplified endemic transmission
and faunal shifts in anisakid nematodes to more temperate-adapted species
would likely result in altered risk of human exposure to zoonotic species.
Detection of the magnitude and direction of these changes will require
enhanced monitoring of prevalence in people and animals, as well as spe-
cies-level identification of larvae in fish to determine zoonotic potential.

Diphyllobothriids (the broad fish tapeworm and relatives) are well-
recognised zoonotic parasites, with an estimated 20 million people infected
throughout the world (Chai et al., 2005). Typical representatives of the order
Diphyllobothriidea (formerly Pseudophyllidea; see Kuchta et al., 2008) are
characteristic cestode parasites in piscivorous birds and mammals, and collec-
tively have widespread distributions globally in freshwater and marine envi-
ronments (Deliamure et al., 1985; Dick, 2008; Scholz et al., 2009). These are
among the largest cestodes in the world, with adults in some species attaining
up to 15–25 m in length, in excess of 4000 segments, and with infections
that may persist for over 20 years (Scholz et al., 2009). Evidence of a long
association with people is indicated by documentation of diphyllobothriosis
among coastal populations in Peru extending to 4500 years ago (Reinhard
and Urban, 2003). In North America, diphyllobothriids have been associated
with people since the earliest incursions out of Eurasia (Hoberg et al., 2012;
Rausch and Hilliard, 1970; Rausch et al., 1967; Scholz et al., 2009).
122 Emily J. Jenkins et al.

Among these cestodes, faunal structure has been determined by both nat-
ural events of expansion and isolation over the Quaternary (2.6 million years
ago) and more recent anthropogenic drivers for introductions and establish-
ment that may extend to the late Pleistocene linking Eurasia and North
America. Translocation and introduction during the last century have also
been significant mechanisms for establishment of species of Diphyllobothrium
in freshwater habitats (Adams and Rausch, 1997). Diphyllobothriids have
been associated with people coincidental with the earliest incursions out
of Eurasia into North America and in conjunction with diets rich in both
freshwater and anadromous fishes that serve as IHs and PHs (Hoberg et al.,
2012; Rausch and Hilliard, 1970; Rausch et al., 1967; Scholz et al., 2009).
These cycles are likely the sources for infection of early immigrants into
North America prior to European exploration and contact, and would have
driven circulation of cestodes coincidental with marine and aquatic fisheries
in freshwater habitats, coastal zones, and island archipelagos (Bouchet et al.,
1999, 2001; Hoberg et al., 2012). Diphyllobothrium latum in particular appears
to be primarily a parasite of people and historical occurrence of this spe-
cies in North America may reflect both late Pleistocene expansion across
Beringia, and later anthropogenic introductions associated with European
exploration and colonisation establishing focal distributions in the eighteenth
century resulting in a faunal mosaic (Dick, 2008; Hoberg et al., 2012; Rausch
and Hilliard, 1970).
Life cycles for diphyllobothriids are complex, involving one crusta-
cean and at least two vertebrates, generally a fish and a piscivorous avian
or mammalian definitive host (Adams and Rausch, 1997; Dubinina, 1966)
(Fig. 2.19). Among diphyllobothriids (zoonotic species of Diphyllobothrium,
Diplogonoporus, Pyramicocephalus, and Schistocephalus considered here), adult
tapeworms inhabit the small intestine of definitive hosts and release eggs
that are passed in host faeces. In marine environments, eggs have thick,
pitted shells, while in freshwater, eggs have thin, nonpitted shells (Hilliard,
1960). Eggs hatch in water to release a coracidium (ciliated oncosphere),
which is ingested by diaptomid or cyclopid copepods serving as first IHs.
Procercoid larval stages develop within the copepod, which is subsequently
ingested by a zooplanktivorous fish serving as a second IH. Within the fish,
development to the plerocercoid larval stage occurs either in the viscera or
musculature; plerocercoids may be encapsulated or free in the peritoneal
cavity depending on the species (Scholz et al., 2009). Infection of birds or
mammals may occur at this juncture through predation of infected fishes,
or further dissemination of parasites may involve circulation among PHs,
Arctic Zoonoses 123

Figure 2.19  Simplified, generic life cycle of diphyllobothriid cestodes (such as Diphyllo­
bothrium latum) in marine and freshwater cycles in the North. Adult cestodes are pres-
ent in the intestine of definitive hosts, including people, dogs, and pisicivorous wildlife.
Definitive hosts become infected by consumption of fish intermediate (IH) or paratenic
hosts (PH).

often larger predatory piscivorous fishes, which are most often the source of
human infection. The predilection site and behaviour of plerocercoids
in different hosts and tissues influences both geographic distribution
for assemblages of hosts and parasites, and potential sources for human
infections. Zoonotic and non-zoonotic species of diphyllobothriids may
circulate among mammalian, avian, and fish hosts in the same region
(Table 2.13), rendering species-level identifications critical to assessing
human risk (Andersen et al., 1987; Curtis and Bylund, 1991; Curtis et al.,
1988; Rausch and Hilliard, 1970).
There are four potential pathways for transmission of diphyllobothriids
in marine and freshwater environments (Table 2.13; Fig. 2.19). (1) Strictly
freshwater cycles, such as those for Diphyllobothrium dalliae, D. dendriticum,
D. latum and Schistocephalus solidus utilise freshwater fishes and piscivo-
rous birds or terrestrial mammals as definitive hosts, depending on the
­species involved. (2) Strictly marine cycles, including those for D. cordatum,
D. pacificum, D. hians and species of Diplogonoporus, involve marine mammals
Table 2.13  Location and Host Distribution for Diphyllobothriidae, Including Zoonotic Species of Diphyllobothrium, Diplogonoporus,

Pyramicocephalus, and Schistocephalus at high latitudes
Species Location Fish Hosts Definitive Hosts Transmission Reference
Diphyllobothrium spp.
D. alascense Western AK Burbot (Lota lota), Boreal Dog (Canis lupus Marine- Rausch and Wil-
smelt (Osmerus mordax), familiaris), Human Freshwater liamson (1958);
Diadromous forage Rausch et al.
fishes (1967); Rausch
and Adams
D. cordatum Circumpolar Unknown Phocid seals (Phoca spp.), Marine Leuckart (1863);
Bearded Seal (Erignathus Markowski
barbatus), Walrus (1952); Rausch
(Odobenus rosmarus), et al. (1967);
Dog, Human Rausch (2005)
D. dalliae Western AK, Eastern Blackfish (Dallia pectoralis), Dog, Arctic Fox (Vulpes Freshwater Rausch (1956a);
Chukhotka, AK Dolly Varden (Salvelinus lagopus), Human, Laridae Rausch and
malma) (Larus spp.) Hilliard (1970)
D. dendriticum Circumpolar Salmonidae (Salmoninae, Piscivorous birds Freshwater Rausch and
Coregoninae), Gasteros- (Laridae), Terrestrial Hilliard (1970);
teidae, Burbot mammals, Human Andersen et al.
(1987); McDon-

Emily J. Jenkins et al.

ald and Margolis
(1995); Dick
(2008); Scholz
et al. (2009)
D. ditremum Holarctic (Boreal) Salmonidae, Gasteroste- Piscivorous birds Freshwater Andersen et al.
idae, Osmeridae (1987)
Arctic Zoonoses
D. fayi Bering Sea, Arctic Unknown Pacific Walrus Marine Rausch (2005)
D. hians Circumpolar Unknown Ringed Seal (Phoca hispida), Marine Scholz et al.
Bearded Seal, Northern (2009)
Fur Seal (Callorhinus
ursinus), Human
D. lanceolatum Circumpolar Least cisco (Coregonus Bearded Seal, Harbour Seal Marine- Markowski (1952),
sardinella) (Phoca vitulina), Ringed Freshwater Rausch and
Seal, Ribbon Seal (Phoca Hilliard (1970)
fasciata), Dog, Human
D. latum Holarctic, Temperate Esocidae, Percidae, Human, Terrestrial Freshwater Plotnikof (1935);
to Sub-Arctic Burbot, Cottidae, ­mammals Rausch et al.
­Salmonidae (1967); Rausch
and Hilliard
Deliamure et al.
(1985); Dick
(2008); Scholz
et al. (2009);
Hoberg et al.
(In Press)
D. nihonkaiense N. Pacific basin, Salmonidae (Onchorhyn- Brown Bear (Ursus arctos), Freshwater- Scholz et al.
coastal/boreal chus spp.) Human Marine (2009)

Table 2.13  Location and Host Distribution for Diphyllobothriidae, Including Zoonotic Species of Diphyllobothrium, Diplogonoporus,
Pyramicocephalus, and Schistocephalus at high latitudes—cont’d
Species Location Fish Hosts Definitive Hosts Transmission Reference

D. pacificum Pacific Basin, Unknown Otariidae: Northern Fur Marine Rausch et al.
Temperate Seal, Steller Sea Lion (2010), Scholz
Northern/­ (Eumetopias jubatus), et al. (2009);
Southern California Sea Lion Rausch et al.
­Hemisphere (Zalophus californianus), (2010)
Juan Fernandez Fur
Seal (Arctocephalus
philippi), Human
D. orcini North Pacific basin Unknown Killer whale (Orcinus orca), Marine Kamo (1999);
Human Scholz et al.
D. roemeri Arctic Basin Unknown Walrus Marine Schmidt (1986),
Kamo (1999)
D. skrjabini Greenland, Bering Unknown Bearded seal Marine Iurakhno and
Strait Mal’tsev (1993)

Emily J. Jenkins et al.

D. stemmaceph- Holarctic, boreal Unknown Delphinidae, Human Marine Scholz et al.
alum (2009)
D. ursi NE Pacific, coastal/ Red salmon (O. nerka) Bear (U. arctos, U. Freshwater- Rausch (1954);
boreal-sub-Arctic Pacific salmon (Oncho- ­americanus), Human Marine Rausch and
rhynchus spp.) Hilliard (1970)
Arctic Zoonoses
Diplogonoporus spp.
D. balae- Circumpolar Engraulidae, Clupeidae Baleen Whales, Human, Marine Rausch (1964);
nopterae Japanese Anchovy Dog Adams and
(Engraulis japonica) Rausch (1997);
­Japanese Sardine Scholz et al.
(Sardinops melanostictus) (2009); Arizono
et al. (2008)
D. tetrapterus North Pacific basin Unknown Sea Otter (Enhydra lutra), Marine Margolis (1956);
Northern Fur Seal, Rausch (1964)
Steller Sea Lion
D. violettae Bering Sea Unknown Steller Sea Lion Marine Iurakhno (1986)
Pyramicocephalus spp.
P. phocarum Circumpolar Marine fishes, nearshore, Phocid seals, Human Marine- Rausch and
demersal, Cottidae, freshwater Hilliard (1970);
Gadidae Deliamure et al.
(1985); Rausch
and Adams
Schistocephalus spp.
S. solidus Circumpolar Nine-spined Stickleback Piscivorous Birds, Freshwater Rausch et al.
(Pungitius pungitius) ­Mammals, Human (1967);
Abbreviations for states, provinces, and territories as in Fig. 2.1.

128 Emily J. Jenkins et al.

and fishes in nearshore and oceanic habitats. (3) Marine-to-­freshwater cycles,

such as those for Diphyllobothrium alascense, D. lanceolatum, and Pyramico-
cephalus, occur when marine mammals indirectly infect diadromous for-
age fishes in the marine environment. For example, for D. lanceolatum
and D. alascense from western Alaska and Chukhotka, coracidia expelled
by ­pinniped definitive hosts result in plerocercoid infections in migratory
forage fishes including some osmerids and coregonids (but not appar-
ently salmonids) that serve as prey for freshwater PHs (Rausch and Adams,
2000; Rausch and Hilliard, 1970). Although cycles are initiated in marine
environments, transmission to dogs and humans apparently often occurs
through ingestion of infected fishes in freshwater. (4) Freshwater-­to-marine
cycles, such as those for D. ursi and D. nihonkaiense, occur when brown
bears (U. arctos) indirectly infect salmon IHs (­species of Onchorhynchus)
in freshwater environments prior to the migration of smolt downstream
to the ocean. Mature spawning salmon returning to natal streams carry
infective plerocercoids and life cycles are completed when foraging
bears (or humans) take these fish as prey (Rausch, 1954; Rausch and
Hilliard, 1970).
It is apparent that several mechanisms are associated with transfer of
marine diphyllobothriids and other helminths (such as anisakid nematodes)
into freshwater transmission cycles: (1) consumption of marine fishes by
freshwater piscivores transiently moving into estuarine/brackish water; (2)
consumption of marine fishes ascending a short distance into freshwater
environments; and (3) consumption of anadromous fishes ascending into
lotic (moving water; e.g. river) and lacustrine (e.g. lake) systems to spawn
(Rausch and Adams, 2000). For D. alascense and Pyramicocephalus, some spe-
cies of freshwater predatory fishes such as burbot (Lota lota) appear to be
important in facilitating linkages between the marine and lotic environ-
ments (Rausch and Adams, 2000). Interacting factors related to piscine and
homeotheric hosts, ecological context, and tolerance and resilience to tem-
perature and salinity during life history stages for these parasites serve to
determine the potential for human infection.

9.1. Species Present in the North

The most common zoonotic diphyllobothriid species in the Northern
Hemisphere are D. latum and D. dendriticum (Curtis and Bylund, 1991; Lan-
tis, 1981;Yera et al., 2006). Among the approximately 50 recognised species
of Diphyllobothrium, relatively few are known to occur at high latitudes,
and even fewer are restricted in distribution to the sub-Arctic and Arctic
Arctic Zoonoses 129

(Adams and Rausch, 1997; Deliamure et al., 1985; Scholz et al., 2009).
Although the overall diversity for zoonotic diphyllobothriids remains to be
completely resolved, globally 17 species (excluding species of Spirometra in
Asia and the tropics) have been identified in association with human infec-
tions (Adams and Rausch, 1997; Deliamure et al., 1985; Dick, 2008; Rausch
et al., 1967; Scholz et al., 2009). Among these, 15 species in terrestrial and
marine piscivores (including Diplogonoporus balaenopterae, Pyramicocephalus
phocarum, and S. solidus) have been documented in people across the circum-
polar north or in adjacent seas extending southward into boreal latitudes of
the North Pacific basin, including Japan and the North (Table 2.13). Lati-
tudinal gradients in diversity appear evident, with greatest species’ richness
in the sub-Arctic and temperate zones, with few species being restricted to
the Arctic (Deliamure et al., 1985; Dick, 2008; Rausch and Hilliard, 1970;
Scholz et al., 2009). Greenland has a particularly depauperate community
of diphyllobothriids, at least in terrestrial carnivores (Babbott et al., 1961;
Leuckart, 1863).

9.2. Geographic Distribution in the North

Diphyllobothriid cestodes are present in marine and freshwater systems
across the North. Some species have relatively limited geographic dis-
tributions (D. alascense and D. dalliae in western Alaska; D. nihonkianese,
D. pacificum, and D. ursi in the coastal North Pacific), whereas others
exhibit circumpolar distributions (D. dendriticum, D. latum, D. lanceola-
tum, and P. phocarum) (Table 2.13). Such associations reflect ecologically
defined patterns of transmission, mobility, and migratory behaviour of
fish, bird, and mammal hosts, and historical events of range expansion and
isolation (Hoberg et al., 2012). Anthropogenic translocations into North
America include introduction with immigrants across Beringia in the
late Pleistocene, and more recent introductions with European explora-
tion and contact since the eighteenth century (Adams and Rausch, 1997;
Bouchet et al., 1999, 2001; Dick, 2008; Hoberg et al., 2012; Rausch and
Hilliard, 1970).
Diphyllobothrium latum and D. dendriticum are distributed across boreal to
sub-Arctic North America (Fig. 2.20). Diphyllobothrium dendriticum, how-
ever, appears to be the dominant species north of 60°N in Canada and
Alaska (Dick, 2008), and may be the only species present in aquatic/ter-
restrial systems in Greenland (Kapel and Nansen, 1996; Rausch et al., 1983).
Plerocercoids of D. latum have been reported in fishes up to 61°N in the
Northwest Territories, as well as in northern Manitoba, Saskatchewan, and
130 Emily J. Jenkins et al.

Figure 2.20  Published reports of diphyllobothriid cestodes in animals and people in

Alaska, northern Canada, and Greenland. (Data from Tables 2.14 and 2.15).

Alberta (Ching, 1984; Dick, 2008; Dick and Poole, 1985; Dick et al., 2001),
and are present near the Arctic Circle (ca. 66°N) in Alaska (Rausch and
Hilliard, 1970).
Confusion about the distribution of D. latum in North America and
elsewhere has resulted from uncritical application of this name to diphyl-
lobothriids in humans and other mammals, absence of morphologically
identified specimens for comparison, and diagnoses based solely on eggs
in faecal samples (Adams and Rausch, 1997; Dick, 2008). The extraordi-
nary host range reported for D. latum by Deliamure et al. (1985) requires
confirmation (Scholz et al., 2009; Yera et al., 2006). The application of
molecular-based methods holds great promise to identify eggs in faecal
samples, morphologically similar adult tapeworms in birds and mammals,
and plerocercoid larvae in marine and freshwater fishes. Resolution of the
actual host and geographic range for D. latum must be established through
examination of adult cestodes and/or development of accurate molecular
foundations for identification and differentiation among morphologically
similar cestodes.
Arctic Zoonoses 131

9.3. Transmission, Prevalence, and Animal Health Impact

in the North
9.3.1. Prevalence in Terrestrial Piscivores
Reports of diphyllobothriids in domesticated and free-ranging terrestrial
carnivores across the North are predominately based on the presence of
characteristic eggs in faeces; in relatively few situations have adult cestodes
been examined or identified, nor have molecular techniques been applied
to surveys of wild and domestic carnivores in the North (Table 2.14).Thus,
substantial gaps may exist in our basic understanding about host associa-
tions, geographic distribution, and species diversity (Dick, 2008). Histori-
cally, prevalence in dogs has approached 50% in settlements adjacent to
marine or freshwater habitats. Fish are often a dietary mainstay for north-
ern dogs (Canis familiaris) (Rausch and Hilliard, 1970; Salb et al., 2008).
Terrestrial wild canids and bears are hosts for various diphyllobothriids;
however, prevalence in wild canids tends to be considerably lower than in
dogs (Table 2.14). This may reflect seasonal and geographical variation in
the proportions of marine, freshwater, and anadromous fishes and other
wildlife represented in the diet (Cameron et al., 1940; Kapel and Nansen,
1996; Rausch and Hilliard, 1970). Diphyllobothrium spp. cestodes were not
detected in 200 wolves (C. lupus) from the Copper River drainage, nor in
80 wolverine (G. gulo) from the Susitna River drainage and the Brooks
Range of Alaska in 1949–1959 (Rausch, 1959a; Rausch and Williamson,
A similar spectrum of fish shared in diets of domestic dogs and people
indicates that parasite faunas may have considerable overlap with respect
to species’ richness and diversity (Rausch and Hilliard, 1970; Rausch
et al., 1967). Demonstration of parasite diversity in canine populations
has been shown to be an accurate proxy with respect to the range of hel-
minth parasites likely to be derived by people from fishes in marine or
freshwater environments (Rausch and Hilliard, 1970; Rausch et al., 1967).
Indeed, in many remote and indigenous communities, free-ranging dogs
and sled dogs are often at higher risk of exposure than people (due to
consumption of uncooked fish) and may serve as excellent sentinels for
the presence of potentially zoonotic species of Diphyllobothrium ( Jenkins
et al., 2011; Rausch and Hilliard, 1970; Salb et al., 2008). For example, in
two communities in northern Quebec (Nunavik), only two of 87 people
were positive (Curtis et al., 1988), whereas concurrently 45% of 80 dogs
were shown to be shedding eggs of Diphyllobothrium spp. (Desrochers and
Curtis, 1987).
Table 2.14  Prevalence [% (n)] of Diphyllobothrium spp. in Representative Terrestrial and Marine Piscivores

Prevalence Parasite
Host Location(s) [% (n)] Identification Method References
Order Carnivora
Arctic Fox St. Lawrence Island, AK 3 (1579) D. dendriticum N Rausch et al. (1990a)
(Vulpes lagopus) St. Matthew Island, AK 32 (22) D. dendriticum, N Rausch and Rausch (1968);
D. dalliae Rausch and Hilliard (1970)
Brooks Range, AK 1 case D. latum N Rausch and Hilliard (1970)
Greenland 10 (38) D. dendriticum N Rausch et al. (1983)
8 sites, Greenland 6–15* (254) D. dendriticum N Kapel and Nansen (1996)
Black Bear Prince of Wales Island, AK 1 case D. ursi N Rausch and Hilliard (1970)
(Ursus americanus)
Valdez Island, AK 1 case D. ursi N Rausch and Hilliard (1970)
Peace River, AB 1 (91) NR N Dies (1979)
Brown Bear Karluk Lake, Kodiak Island, 1 case D. ursi N Rausch (1954)
(Ursus arctos) AK
Taku River Valley, BC and 14 (21) NR N Choquette et al. (1973)
Daring Lake, NT 18 (56) NR FF Gau et al. (1999)
Dog (Canis familiaris) Kotzebue, AK 1 (97) D. latum N Rausch and Hilliard (1970)
Western Alaska;   59 (97) D. alascense, D. dalliae, N Rausch et al. (1967); Rausch
Yukon-Kuskokwim D. dendriticum, and Hilliard (1970)

Emily J. Jenkins et al.

Delta D. lanceolatum
Assumption, AB; Fort 35 (327) D. latum FF, N Unruh et al. (1973)
Liard, Fort Rae, and
Snowdrift, NT
Fort Resolution, NT and 7 (129) NR FF Salb et al. (2008)
Fort Chipewyan, AB
Arctic Zoonoses
Fort Chipewyan, AB 47 (88) NR FS Saunders (1949)
Fox Lake, AB 6 (272) NR FF Unruh et al. (1973)
13 sites in SK 3 (3370) NR FF Allen and Mills (1971)
Loon Lake, La Ronge, SK 10 (106) NR FF Unruh et al. (1973)
29 sites in NT, AB, SK, NR NR FF Cameron et al. (1940)
Wolstenholme, QC and NR Diphyllobothrium N Cameron et al. (1940)
Nottingham, NU spp.
Kuujjuaq, QC 45 (80) NR FF Desrochers and Curtis
Greenland NR D. cordatum N Krabbe (1868)
Red Fox Ambler, AK 1 case D. latum N Rausch and Hilliard (1970)
(Vulpes vulpes)
Wolf (Canis lupus) Thelon River, NT 2 (61) Diphyllobothrium N Choquette et al. (1969)
Order Pinnipedia
Bearded Seal Bering Sea, AK and 0–21* (82) Diphyllobothriidae N Adams (1988)
(Erignathus barbatus) Sea of Okhotsk, 0–30* (82) Diphyllobothrium N Adams (1988)
4 sites 30–100* (82) D. lanceolatum N Adams (1988)
0–60* (82) Pyramicocephalus N Adams (1988)
Northern Fur Seal Northern Bering Sea NR D. pacificum N Rausch et al. (2010)
(Callorhinus ursinus)
Ringed Seal Hudson Strait, Salluit, 80 (5) Diplogonoporus N Measures and Gosselin
(Phoca hispida) QC tetrapterus (1994)
10 sites, Bering Sea to 0–33* (299) Diphyllobothrium N Adams (1988)
­Arctic coast, AK 0–40* (299) Diplogonoporus N Adams (1988)

0–39* (299) P. phocarum N Adams (1988)

Table 2.14  Prevalence [% (n)] of Diphyllobothrium spp. in Representative Terrestrial and Marine Piscivores—cont’d
Prevalence Parasite
Host Location(s) [% (n)] Identification Method References
Ribbon Seal Central Bering Sea, AK 6 (31) D. cordatum N Shults and Frost (1988)
(P. fasciata) Central Bering Sea, AK 3 (31) D. lanceolatum N Shults and Frost (1988)
Spotted Seal Bering Sea, AK 24 (55) D. tetrapterus N Shults (1982)
(P. largha) Bering Sea, AK 20 (55) D. cordatum N Shults (1982)
Anadyr, Bering Sea 2 (130) Diphyllobothrium N Deliamure et al. (1984)
Pribilof Island, AK 7 (57) Diphyllobothrium N Deliamure et al. (1984)
Steller Sea lion Bering Sea, AK 94 (67) D. tetrapterus N Shults (1986)
(Eumetopias jubatus) Gulf of Alaska, AK 28 (7) D. tetrapterus N Shults (1986)
Bering Sea, AK 31 (67) D. pacificum N Shults (1986)
Gulf of Alaska, AK 14 (7) D. pacificum N Shults (1986)
Walrus North Pacific/Bering 2–10* (306) D. cordatum N Adams (1988)
(Odobenus rosmarus) Sea, 3 sites, AK 0–2* (306) D. lanceolatum N Adams (1988)
1–10* (306) D. roemeri N Adams (1988)
Chukchi Sea, AK 10 (95) D. fayi N Rausch (2005)
Within a host species, reports move from west to east across the North. Abbreviations for states, provinces, and territories as in Fig. 2.1.

Emily J. Jenkins et al.

N – Necropsy, NR – Not recorded, FF– Faecal flotation, FS – Faecal smear.
*Range of site-specific prevalences.
Arctic Zoonoses 135

Diphyllobothrium spp. are thought to have little impact on the health of

mammalian definitive hosts, although there is a report of blockage of the
pancreatic duct in a captive black bear (U. americanus) in Alaska (Rausch,
1955). In fish, plerocercoids may be associated with pathology and may
have a detrimental influence on palatability and suitability of some piscine
­species as food (reviewed in Marcogliese, 2001).

9.3.2. Prevalence in Marine Piscivores

Although multiple genera and species of diphyllobothriids circulate among
pinnipeds and cetaceans, it is generally those species in pinnipeds (seals, sea
lions, and walruses) that have been shown to be zoonotic (Tables 2.13 and
2.14) (Deliamure et al., 1985; Kamo, 1999; Scholz et al., 2009). Diphyllo-
bothriids are not known in polar bears (U. maritimus), and this may reflect
a specialised diet of seals and carrion and associations with ice edge and
pack ice habitats. The apparent propensity of zoonotic species to circu-
late among pinnipeds may be indicative of linkages within near-shore food
webs, relatively focal sources due to breeding distributions and haul-outs,
and frequent involvement of large piscine prey (potential PH) that represent
a food resource for both marine mammals and people. For example, spotted
seals (Phoca largha) are generally associated with sea ice of the Bering Sea
during parturition early in the spring, but disperse into nearshore, coastal,
and estuarine habitats later in the summer (Deliamure et al., 1984). Among
species of pinnipeds, diphyllobothriids are often the most prevalent and
abundant tapeworms, and multiple species infections are not uncommon
(Table 2.14) – 11 species parasitise pinnipeds, with six being zoonotic (Table
2.13). In contrast, only three species with cetacean definitive hosts, Diphyl-
lobothrium orcini in killer whales (Orcinus orca) that specialise on salmonids,
Diphyllobothrium stemmacephalum in small delphinids, and D. balaenopterae in
baleen whales, are known in zoonotic infections (Deliamure et al., 1985;
Kamo, 1999).

9.4. Transmission, Prevalence, and Public Health

Impact in the North
Humans become infected with diphyllobothriid cestodes through
consumption of plerocercoids in fish IHs or PHs, and thus serve as
definitive hosts with adult cestodes in the small intestine. Transmission to
people occurs where fresh, undercooked fish (and possibly smoked, dried,
fermented, or salted fish) are consumed for cultural and nutritional reasons
(Adams and Rausch, 1997; Gyorkos et al., 2003; Rausch and Hilliard, 1970;
136 Emily J. Jenkins et al.

Rausch et al., 1967). In some communities, locally caught fish compose

approximately a third of all harvested country foods (Mackey, 1988; Ross
et al., 1989). Diphyllobothriid species in which plerocercoids localise in
the skeletal muscle (or migrate from the viscera into the muscle following
death of the fish) are more likely to be consumed by people. For example,
the usual predilection site for plerocercoids of D. ursi in the viscera may
preclude extensive infections in people, although at some localities such
as Kodiak Island, AK, nearly all returning salmon may be infected (Adams
and Rausch, 1997). In addition, Indigenous Arctic residents in some regions
consume the stomach and liver of fish (Ross et al., 1989). Plerocercoids
may have a detrimental influence on suitability and palatability of dietary
fish, although levels of traditional knowledge about the life cycle and sig-
nificance of this group of cestodes vary. Dogs and wild carnivores are not
a direct source of human exposure but may serve to amplify local cestode
populations if faeces are deposited near water (Adams and Rausch, 1997;
Scholz et al., 2009).
Most diphyllobothriids have zoonotic potential; only six of the 21
diphyllobothriid species distributed in northern environments of the
Western Hemisphere have not been documented in people (Table 2.13).
These associations indicate that the potential for dissemination to people is
strongly controlled by local ecology and fisheries. Only two diphylloboth-
riid species, D. dendriticum and D. latum, are commonly reported in people;
other species and genera of diphyllobothriids appear to be incidental in
people and companion animals such as dogs. Across Alaska, where there is
a diverse assemblage of species of Diphyllobothrium, records of D. latum are
almost always limited to infections in people (Rausch and Hilliard, 1970)
(Table 2.15). The diversity of other diphyllobothriids in people reflects dif-
ferences in local cycles, dietary preferences, and distributions for primary
definitive host species (Adams and Rausch, 1997; Rausch and Hilliard,
1970; Rausch et al., 2010). With the potential exception of D. latum, species
of Diphyllobothrium are maintained in endemic transmission cycles usually
independent of people as obligate definitive hosts. Consequently, diphyllo-
bothriosis can be regarded as a natural focal infection at landscape scales that
cannot simply be controlled by elimination of cestodes from the human
population (Adams and Rausch, 1997).
Transmission of diphyllobothriids in human communities appears to be
largely limited to isolated settlements scattered across northern latitudes
(Rausch, 1974). In Greenland, human infections with diphyllobothriids
appear to be rare; although D. cordatum has been reported (Leuckart, 1863),
Table 2.15  Prevalence [% (n)] of Diphyllobothriosis in People Based on Detection of Eggs in Faeces and/or Identification of Adult Cestodes

Arctic Zoonoses
Location Sampling Dates [% (n)] Identity References
Alaska, USA
Lower Kuskokwim River 1949 15 (100) Diphyllobothrium sp.* Hitchcock (1950)
Kotzebue 1950 6 (100) Diphyllobothrium sp.* Hitchcock (1951)
Hooper Bay 1957–1958 22 (1299) D. cordatum, D. alascense, Rausch et al. (1967)
D. dalliae
Chevak, Newtok, Nelson Island 1958 NR Schistocephalus solidus Rausch et al. (1967)
Southwestern Alaska 1958 11 (1680) Diphyllobothrium sp.* Fournelle et al. (1958)
Yukon-Kuskokwim Delta 1949–1970 NR D. alascense, D. dalliae, Rausch and Hilliard (1970)
D. dendriticum,
D. lanceolatum†
Kodiak Island/Ft.Yukon 1970 NR D. ursi † Rausch and Hilliard (1970)
Western Alaska (multiple villages) 1949–1970 53 (34) D. latum† Rausch and Hilliard (1970)
Fairbanks, Anchorage, Bethel, and 1981 6 cases D. latum‡ Alaska Epi. Bull. (1981)
King Salmon 1984 7 confirmed D. latum‡ Alaska Epi. Bull. (1984)
cases, 11 ill
Fort Chipewyan, AB 1945 11 (140) Diphyllobothrium sp.* Saunders (1949)
Southampton Island, NU 1947 29 (31) Diphyllobothrium sp.* Brown et al. (1948)
Igloolik, NU 1949 33 (97) Diphyllobothrium sp.* Brown et al. (1950)
MB, NT, ON, QC 1953 11.5 (426) Diphyllobothrium sp.* Wolfgang (1954)
Kuujjuaq, QC, (Ft. Chimo) 1959 28 (46) Diphyllobothrium sp.* Laird and Meerovitch (1961)

Table 2.15  Prevalence [% (n)] of Diphyllobothriosis in People Based on Detection of Eggs in Faeces and/or Identification of Adult
Location Sampling Dates [% (n)] Identity References

Inukjuaq, QC (Port Harrison) 1960 77 (328) Diphyllobothrium sp.* Arh (1960)

Igloolik, NU 1970–1971 2 (247) Diphyllobothrium sp.*, Freeman and Jamieson
D. dendriticum** (1976)
Northern Ontario 1974–1975 1.7 (536) Diphyllobothrium sp.* Watson et al. (1979)
Kuujjuaq, QC 1986 2 (87) Diphyllobothrium sp.* Curtis et al. (1988)
Greenland 1863 NR Diphyllobothrium cordatum Leuckart (1863)
Reports move from west to east, then chronologically within a state, province, or territory. Abbreviations for states, provinces, and territories as in Fig. 2.1.
NR – Not recorded.
*Identification of eggs in faeces possible only to genus level.
†Based on morphological identification of strobilate adults recovered from naturally infected people.
‡Associated with consumption of raw salmon; diphyllobothriid species identification uncertain. See:
**Based on morphological identification of strobilate adults recovered from experimentally infected human volunteer.

Emily J. Jenkins et al.

Arctic Zoonoses 139

no eggs were detected in 670 faecal samples from people in the Disko
Bay region tested in 1957 (Babbott et al., 1961). Diphyllobothriosis was
common among indigenous populations of Canada and Alaska into the
middle of the last century (prevalence generally around 30%, as high as
83%), but appears to have declined in the following decades (Gyorkos et al.,
2003). For example, in Igloolik in the eastern Canadian Arctic, prevalence
dropped from 33% in 1949 to 2% in 1970–1971, and in Kuujjuaq, preva-
lence dropped from 28% in 1959 to 2% in 1986 (Table 2.15). Prevalence
elsewhere in Canada appeared to be low (about 11%) in the 1940s and
1950s, and may also be declining. Between 1969 and 1978, 46 cases were
reported from the NT and what is now Nunavut, whereas between 1995
and 1998, only five cases of ‘tapeworm’ (either Diphyllobothrium or Echino-
coccus granulosus) were reported to territorial public health authorities.
During the 1960s in western Alaska, diphyllobothriosis was common
(up to 30% peaking in late winter or spring) and reflected seasonal diets
that by necessity were rich in small forage fishes such as pond smelt,
blackfish, and sticklebacks, which were often eaten partially frozen or raw
(Rausch et al., 1967). In contrast, prevalence was considerably lower in late
summer (16%), coinciding with opportunities for a more diversified diet.
More recently, individual cases or localised outbreaks at various localities
in Alaska during the early 1980s have been associated with consumption
of raw or undercooked salmon (Table 2.15). Overall, incidence appears to
be decreasing in the general North American population (Scholz et al.,
2009); however, surveillance is limited as diphyllobothriosis is not report-
able to public health authorities at the national level in North America. In
addition, factors hindering detection include reticence to report passing
of cestodes to medical personnel and to submit faecal samples for testing.
Declining levels of infection in people may reflect changes in traditional
diets over the past 50–60 years.
Diphyllobothriosis is rarely associated with detectable clinical disease
in North America. Pernicious anaemia associated with D. latum in Finland
appears to have a complex aetiology involving interactions among genetic
susceptibility and poor nutrition. This syndrome is seldom observed in
recent times, even in Finland, and has never been clinically prominent in
Canada or North America (Curtis and Bylund, 1991; Rausch et al., 1967).
Other species of Diphyllobothrium likely cause no or transient gastrointesti-
nal signs. Duration of infection with D. dendriticum is generally only four to
six months (Curtis and Bylund, 1991), although strobilate adults of D. latum
may persist for decades.
140 Emily J. Jenkins et al.

Globalisation of trade and rapid transport of fresh fish may lead to resur-
gence for diphyllobothriosis in people, even at sites far distant from local
transmission cycles for these parasites in the north. For example, the recogni-
tion of D. nihonkaiense as a zoonotic parasite from western North America was
based on molecular identification of proglottids passed by a patient in France
following the consumption of raw salmon (presumed to be Oncorhynchus keta)
from the Gulf of Alaska (Yera et al., 2006). Additional human infections for
species of Diphyllobothrium in western Europe have been related to impor-
tation of exotic fish (e.g. species of Pacific salmon) and new cuisines that
emphasise fresh and raw ingredients (Scholz et al., 2009). In addition, import-
ing new customs into the North may lead to localised outbreaks; in an out-
break in Alaska in 1984, the suspected source of infection was locally caught
salmon prepared using a recipe for ceviche brought to Naknek by a visitor
from California (

9.5. Diagnosis and Control

Diagnostic identification of strobilate (adult) diphyllobothriids in infections
of definitive hosts (people, mammals, and birds) can be achieved through
morphological or molecular means (Rausch and Hilliard, 1970; Scholz
et al., 2009;Yera et al., 2006). Diagnostic criteria have been well character-
ised for the genera and species recognised as zoonotic and for most species
that occur in terrestrial, aquatic, and marine piscivores (Deliamure et al.,
1985; Rausch et al., 2010). In patent infections, diphyllobothriosis in people
is still most often diagnosed based on the discovery of typical segments or
eggs in faeces, and such basic procedures are rapid and inexpensive. Recov-
ery of intact adults, however, remains the only established morphological
means for determining identity, but specimens must be in good condition,
and should retain the scolex to facilitate this process. Unfortunately many
human infections have simply been identified as D. latum by default.
Identification of infective plerocercoids in fish IHs and PHs continues as a
challenge, although for some species these larval stages are ­morphologically
distinct (Rausch and Hilliard, 1970). For example plerocercoids of D. ditremum,
D. dendriticum and D. latum circulating in freshwater fishes can often be rec-
ognised (Andersen and Gibson, 1989), and metacestodes of Pyramicocephalus
and D. lanceolatum in brackish and marine habitats are distinctive (Rausch and
Adams, 2000; Rausch and Hilliard, 1970). Application of molecular-based
methodologies has increasingly allowed many of these tapeworms to be differ-
entiated at the generic and species level, as sequence data across the assemblage
of diphyllobothriids continues to be developed (Scholz et al., 2009). Overall,
Arctic Zoonoses 141

these methods, based on either nuclear or mitochondrial DNA sequences, are

the most reliable tools for specific identification, and are appropriate for all
developmental stages in DHs, PHs, and IHs. Even though the apparent clini-
cal significance of diphyllobothriosis in people is often limited, specific iden-
tification remains important as a tool in epidemiology and in tracking the
sources of human infection at both local and regional scales. Such has become
increasingly important given the rapid and global transport and dissemination
of infected fish consumed in urban centres throughout the world.
Control of diphyllobothriosis is dependant on breaking the cycle for trans-
mission and can be achieved through treatment of infected people and dogs,
eliminating contamination of water sources (with human sewage treatment
especially relevant for D. latum), and limiting access to salmoniforms and other
fishes that harbour infective plerocercoids (Adams and Rausch, 1997; Rausch
et al., 1967; Scholz et al., 2009). Protocols for treatment are now well estab-
lished, and adult tapeworms are highly susceptible to either praziquantel or
niclosamide administered orally in well-determined dosage regimes (Scholz
et al., 2009); in dogs, it is important to note that the dose of praziquantel is
higher than that routinely used to eliminate other cestode infections. Reduc-
ing or eliminating exposure through safe food preparation practices, such as
adequate cooking of potentially infected fishes, are the most effective means of
prophylaxis. Fishes that are consumed raw, smoked, or pickled should first be
frozen for several days at minus 10 °C or colder to kill infective plerocercoids.
As noted, shifting diets for indigenous peoples in the north have tended to
reduce the levels of exposure and infections for species of Diphyllbothrium over
the past several decades. Salmon, however, continue to pose a risk of human
infection well beyond the borders of northern regions, and far from the locali-
ties where transmission is endemic for a number of species, including D. ursi
and Diphyllobothrium nihonkaiense. As Scholz et al. (2009) noted: ‘Salmon are
now transported worldwide only on ice, and this is the way that fish helminths
are usually introduced to new areas and may infect humans anywhere.’ Thus
interventions to limit the distribution of human infections by diphyllobothriids
must also involve education and discussion of the risks of consumption of raw
fish both across the villages of the north and in urban centres around the world.

9.6. Future Impact of Climate and Landscape Change

Climate warming and associated ecological perturbations are modifying the
structure of terrestrial, freshwater, and marine systems across high latitudes
of the north and globally (Burrows et al., 2011; Callaghan et al., 2004; Gilg
et al., 2012; Hoberg et al., in press; Post et al., 2009). For diphyllobothriids,
142 Emily J. Jenkins et al.

these changes will have an effect on patterns of distribution, seasonal tim-

ing of migration and reproduction of definitive hosts, and development
and survival of fish hosts (second IHs and PHs), invertebrate first IHs, and
free-living parasite stages (eggs and coracidia). Interactions and linkages
between abiotic and biotic drivers that unfold in terrestrial, freshwater, and
marine systems may fundamentally alter the distribution and abundance of
diphyllobothriids in the North.
In northern freshwater systems, current predictions suggest that fish-
ing practices, eutrophication, and temperature increases may have the most
profound effects on freshwater fish and their parasites (Marcogliese, 2001,
2008). Overall, freshwater systems are highly sensitive to water levels, ice
cover, flow rates, and changing patterns of primary and secondary produc-
tivity that influence ecosystem structure and potential prey diversity and
abundance for fish, birds, and some mammals (Marcogliese 2001, 2008).
These factors are central to the continuity of life cycles and potential for
transmission of Diphyllobothrium and Schistocephalus spp. The effects of cli-
mate change on diphyllobothriids in freshwater systems may be manifested
by: (1) shifts in development for invertebrates that involve tipping points
or transitions in life history from multiple to single-year cycles; (2) loss of
cold-water refugia leading to range reductions and extirpation of fishes
and their parasites endemic to the Arctic when tolerances and resilience
are exceeded; (3) changing distribution of wetland habitats; (4) northward
extension of the ranges for many host species (such as yellow perch, Perca
flavescens, and invertebrates) leading to introductions of parasite species pre-
viously unknown in the north (Reist et al., 2006); and (5) higher diversity
for fish and invertebrates (Schindler and Smol, 2006). For example, given the
current low diversity of freshwater diphyllobothriids in Greenland, climate
change may allow establishment of exotic species, if introduced through
anthropogenic translocation or movements of migratory hosts.
For diphyllobothriids currently common in freshwater systems in the
North (D. latum and D. dendriticum), environmental change will influence the
patterns of transmission and distribution. Increasing water temperatures and
expanded periods for ice-free conditions may relax biotic and abiotic con-
trols on the distribution of D. latum, which currently appears to be restricted
to the sub-Arctic and boreal zones ( Jenkins et al., 2011). If a different set of
fish second IH expands northward, this will represent new sources of human
infection in freshwater systems. Further, temperature has direct effects on the
development of D. dendriticum in the environment and in both invertebrate
and piscine IH. For example, warmer temperatures accelerate embryonation
Arctic Zoonoses 143

and hatching of eggs, while decreasing survival of coracidia (Hilliard, 1960).

Plerocercoids of D. dendriticum within fish IH are more active and grow
larger at warmer temperatures, probably causing more pathology in the fish
(reviewed in Marcogliese, 2001). Thus, at warmer temperatures, there will
be a trade-off between accelerated development of free-living stages and
stages within poikilothermic IH, and decreased survival of both free-living
­coracidia and infected fish hosts ( Jenkins et al., 2011).
Synchronicity in the occurrence and availability of infective para-
site stages and susceptible hosts is critical in the transmission dynamics of
diphyllobothriids. Climate change is predicted to result in substantial mis-
matches in timing of development for invertebrate prey (IH) and activity
patterns for fish, mammals, and migratory avian hosts (Hoberg et al., in
press). For example, transmission of D. dendriticum may be considerably dis-
rupted due to asynchrony between temperature-driven hatching of cora-
cidia and photoperiod-driven amplification of copepod populations, as well
as asynchrony between the availability of copepods and a susceptible popu-
lation of fish IH (Marcogliese, 2001). Shifts in seasonal timing (phenology)
for migratory birds serving as definitive hosts may include early migration
and nesting resulting in decreased food availability for breeding birds and
fledglings (Marcogliese, 2001). This may drive shifts to alternative prey spe-
cies (prey-switching), resulting in exposure to a broader spectrum of para-
sites. Mismatches in the seasonal timing of these multiple production cycles
are expected to disrupt patterns of parasite diversity. This may be reflected
through loss of typical parasites, or declines in their abundance and preva-
lence, and could also extend across migration corridors and staging areas.
Transmission of D. dendriticum to people also appears to be seasonally
defined (in part due to freezing susceptibility of pleroceroids), with egg shed-
ding in people peaking in late summer and fall (Curtis et al., 1988). As a con-
sequence, climate change might extend the season of transmission, as fresh
fish might be consumed by people (or fed to dogs) for a longer portion of
the year. Finally, climate change might alter the location of traditional fishing
grounds. If people transport fish for longer distances before processing, this
could allow more time for migration of greater numbers of plerocercoids of
D. dendriticum from the viscera to the musculature ( Jenkins et al., 2011).
In marine systems, environmental changes include variation in oceano-
graphic structure, regime shifts (oscillations from warm to cold conditions),
and range shifts for crustaceans, fish, and marine mammals. Directional cli-
mate change interacts with long-term oceanographic-atmospheric regime
shifts such as the Pacific Decadal Oscillation, and short-term variability,
144 Emily J. Jenkins et al.

particularly the North Atlantic Oscillation, which act as determinants of

production cycles, trophic structure, and ecology of invertebrates, fish, sea-
birds, and marine mammals in the Northern Hemisphere (Chavez et al.,
2003; Hurrell et al., 2003). Collectively, these processes serve to determine
the overall patterns of transmission, distribution, and abundance for diphyl-
lobothriids circulating among marine mammals and seabirds (Hoberg, 2005;
Hoberg and Adams, 2000; Hoberg et al., in press).
Decreases in sea ice in the Arctic basin are also predicted to have a perva-
sive effect on ecosystem structure and the biology of ice-associated marine
mammals, including walruses, seals, and whales that are primary hosts for
marine diphyllobothriids (Moore and Huntington, 2008). Changes in oce-
anic regimes, currents and water-mass structure, associated ice conditions,
freshwater melt and salinity will drive modifications in behaviour and diets
for marine mammals as distribution and species composition for inverte-
brate and vertebrate prey species respond to new environmental conditions
(Laidre et al., 2008; Marcogliese, 2001).The degree of sympatry and seasonal
overlap in distributions for cetaceans and pinnipeds are predicted to increase,
suggesting heightened opportunities for the exchange and d­ issemination of
parasites such as diphyllobothriids (Burek et al., 2008).


Echinococcus granulosus is a species complex of taeniid cestodes respon-
sible for cystic hydatid disease in people worldwide. According to the World
Health Organisation, hydatid disease is one of the most expensive parasitic
zoonoses to treat and prevent world-wide (Eckert et al., 2001). Life cycles of
E. granulosus involve carnivore DHs and herbivore IHs, and various species/
strains utilise different assemblages of domestic livestock, wildlife, and people
(Rausch, 1967). Adult cestodes, which are quite small (2–7 mm), reside in
the small intestines of definitive hosts and shed eggs that are immediately
infective for IHs. Ingested eggs release oncospheres that penetrate the intes-
tinal wall of the new host, undergo tissue migration, and eventually create
unilocular cysts containing larval protoscolices in organ tissue (most often
the liver or lung). People are considered accidental hosts, in which cysts
form but may not develop fertile protoscolices (Rausch, 2003).

10.1. Species and Strains Present in the North

There are at least 10 genotypes of the E. granulosus species complex that
circulate in different host assemblages worldwide (Thompson et al., 2006).
Arctic Zoonoses 145

The pastoral strains (G1-3, E. granulosus sensu stricto), which circulate among
domestic livestock and dogs, are not thought to be present in the North,
although they have been introduced into sheep rearing regions of the west-
ern continental USA (Rausch, 2003). In northern Canada, two genotypes
(G8 and G10) circulate in largely sylvatic cycles involving cervids and
wild canids (Fig. 2.21); only the G8 genotype has been reported in Alaska
(­McManus et al., 2002;  Thompson et al., 2006). It is possible that one or
both of these genotypes may have been introduced into the North American
Arctic along with infected reindeer imported from Siberia and Fennoscan-
dia in the early part of the twentieth century (Rausch, 2003; Thompson
et al., 2006); both G8 and G10 strains have been identified in Fennoscandia
(Saarma et al., 2009).
The taxonomic status of the E. granulosus species complex is somewhat
controversial. Initial phylogenetic analyses based on mitochondrial DNA
suggested that the G6–G10 genotypes be unified as the species E. canadensis
(Nakao et al., 2006; Thompson et al., 2006). However, more recent phylo-
genetic analyses based on nuclear DNA suggest that only the G8 and G10

Figure 2.21  Life cycle of the cervid strain of Echinococcus granulosus (E. canadensis)
in the North. The larval or metacestode stage takes the form of a unilocular hydatid cyst
(cystic hydatid).
146 Emily J. Jenkins et al.

cervid strains be unified under the name E. canadensis, and the G6, G7,
and G9 strains (in camels, pigs, and people, respectively) be unified as
E. intermedius (Saarma et al., 2009). Therefore, in this review, E. canadensis
will be used when referring to the cervid strain(s) present in North Amer-
ica, ­differentiated into the G8 and G10 genotypes where relevant.

10.2. Geographic Distribution in the North

Echinococcus canadensis is present across northern Canada and Alaska
(Fig. 2.22) but is not established in Greenland (Rausch, 2003). In Canada,
E. canadensis is present in all provinces and territories with the exception
of the East Coast (provinces of Nova Scotia, Prince Edward Island, New
Brunswick and the island of Newfoundland) where wolves (C. lupus) have
been historically absent (Sweatman, 1952). Indeed, E. canadensis remains
common in the North wherever wolves and ungulates co-exist (44–68°N);
however, it may be absent in the High Arctic islands due to the low year-
round density of ungulate IHs ( Jenkins et al., 2011; Miller, 1953; Sweatman,
1952). E. canadensis is not present on the island of Newfoundland due to

Figure 2.22  Published reports of cystic hydatid disease (Echinococcus canadensis) in

ungulates in the North. (Animal data from Table 2.16). Clinical cases have been d
­ ocumented
in people (Table 2.17), and serological surveys are reported in Table 2.18.
Arctic Zoonoses 147

the extirpation of wolves in the early part of the twentieth century, even
though ungulate IHs (moose, A. alces, and caribou, Rangifer tarandus) are
abundant. However, recent colonisation by coyotes (C. latrans) may enable
local ­transmission of E. canadensis.

10.3. Transmission, Prevalence, and Animal Health Impact

in the North
The sylvatic strains of E. canadensis cycle primarily between canid definitive
hosts and cervid IH via sympatric predator–prey relationships. In northern
Canada and Alaska, the larval cysts are detected most commonly in moose
and caribou/reindeer (Table 2.16); however, other ungulate IH have been
reported, including wapiti (Cervus canadensis) OMIT (C. elaphus), muskoxen
(O. moschatus), mountain goats (Oreamnos americanus),American bison (Bison
bison) and black-tailed deer (Odocoileus hemionus) (Cameron, 1960; Cho-
quette et al., 1957; Hadwen, 1932; Rausch and Williamson, 1959; Sweat-
man and Williams, 1963; Thomas, 1996). Earlier reports of hydatid cysts in
microtine rodents are most likely to be Echinococcus multilocularis (Rausch
and Schiller, 1951); grey squirrels (Sciurus carolinensis) have been experi-
mentally infected with E. granulosus (Sweatman and Williams, 1963). Adult
cestodes have been reported in the intestinal contents of wolves, coyotes,
and domestic dogs (C. lupus familiaris) (Choquette and Moynihan, 1964;
Jenkins et al., 2011; Jones and Pybus, 2001; Miller, 1953; Rausch and
Williamson, 1959; Sweatman, 1952). According to Rausch (1956b), historical
reports of E. granulosus in red fox (V. vulpes) and arctic fox (V. lagopus) in
Alaska and the Northwest Territories were more likely to be E. multilocularis.
Foxes are no longer considered to be natural hosts of E. ­granulosus/canadensis
(Rausch 1956b).
In sub-Arctic and Arctic regions of North America, the prevalence of
infected animals is highly variable among different host species and between
locations, and comparisons are difficult due to a range in detection effort and
methods. In IH, moose in northern Alaska were reported to have a higher
prevalence of infection than those in the south (24% and 4%, respectively),
and 0.5–6% of caribou were infected (Rausch, 1952, 1959b; Rausch and
Williamson, 1959) (Table 2.16). Between 3% and 5% of Alaskan reindeer
were reported infected with E. canadensis (Rausch, 2003; Sweatman and
Williams, 1963). In Canada, moose in the Yukon Territories were infected at
high prevalence (43%), as were caribou/reindeer in the Northwest Territories
(20–35%). In sub-Arctic and temperate regions of Canada, wapiti were infected
at a somewhat lower prevalence (6–21%) (Sweatman and Williams, 1963).
Table 2.16  Prevalence [% (n)] of Hydatid Cysts of Echinococcus canadensis as Determined Through Necropsy of Ungulates

(Order Artiodactyla) in Alaska and Northern Canada (from west to east, then chronologically within a host species)
Host Location Prevalence [% (n)] References
Black-tailed Deer (Odocoileus Baranof Island, AK 1 case Rausch and Williamson (1959)
­hemionus columbianus)
Caribou (Rangifer tarandus) Central Brooks Range, AK <1 (200) Rausch (1952)
Nelchina, AK 6 (67) Skoog in Rausch and
­Williamson (1959)
Central Brooks Range, AK 3 (79) Rausch (2003)
NR, AK 5 (63) Rausch (2003)
Northern SK and Wholdaia Lake, 21 (14) Harper et al. (1955)
Aklavik, NT 905 (1664) Choquette et al. (1957)
Fort Smith, NT 35 (17) Sweatman and Williams (1963)
Reindeer Station, NT 20 (517) Sweatman and Williams (1963)
Fort Smith, NT 3.9 (1258) Thomas (1996)
George River, NL 1.3 (159) Parker (1981)
Moose (Alces alces) Railbelt-Matanuska Valley, AK 24 (101) Rausch (1959b)
Anchorage,-Upper Kenai, AK 4 (23) Rausch (1959b)
Dawson City,YT 43 (154) Sweatman and Williams (1963)
Le Pas, MB 1 case Hadwen (1932)
Mountain Goat (Oreamnos americanus) Lynn Canal, AK 1 case Rausch and Williamson (1959)
Muskoxen (Ovibos moschatus) Thelon Game Sanctuary, NT 3 (3) Gibbs and Tener (1958)

Emily J. Jenkins et al.

Ellesmere Island, NU NR Tener, 1965 in Marquard-
Petersen (1997)
Abbreviations for states, provinces, and territories as in Fig. 2.1.
NR – not recorded.
Arctic Zoonoses 149

Sporadic cases in ungulates in northern regions of Saskatchewan, Manitoba,

and Labrador have also been reported (Hadwen, 1932; Harper et al., 1955;
Parker, 1981).
Detection of Echinococcus spp. infection in definitive hosts has historically
relied on collection of adult cestodes from the intestines during necropsy.
Identification of Echinococcus eggs detected in faeces is complex as eggs are
indistinguishable from other taeniid species; therefore, molecular meth-
ods are required for identification, which have only recently been applied
in North America. Using these methods, 6% of faecal samples from free-
ranging dogs in one community in the northern SK contained eggs of
E. canadensis (G10) (Himsworth et al., 2010a), but in other communities,
only eggs of Taenia spp. were detected (Schurer et al., 2012). Several Taenia
spp. have distributions in wild canids that overlap E. granulosus in the North,
including T. crassiceps, T. pisiformis, and T. polyacantha ( Jones and Pybus, 2001).
Taeniid eggs were detected in 5% of 423 wolves in Greenland, but were not
identified further (Marquard-Petersen, 1997).
In Alaska, based on recovery of adult cestodes at necropsy, 30% of 200
wolves were infected with adult cestodes of Echinococcus spp., with sled dogs
(10–22%) also reported as common hosts (Rausch, 1952, 2003; Rausch and
Williamson, 1959). A similar prevalence (also based on necropsy) is reported
in wolves in the Yukon Territory (22%; N = 89) as well as in the Northwest
Territories (24%; N = 21) (Choquette et al., 1973). One survey of dogs
culled from eight towns in Northwest Territories reported a 12% preva-
lence (4/33) of E. granulosus/canadensis (Miller, 1953).
The overall impact of E. canadensis infection on IHs is unknown, but
varies according to parasite load, cyst location, and host species. In moose
IHs, hydatid cysts (metacestodes) are present in various organs (the lung,
liver, spleen, heart, and kidneys), while in wild reindeer, cysts are generally
restricted to the lungs (Addison et al., 1979; Rausch, 2003). High intensity
of hydatid cysts in moose are thought to increase the likelihood of preda-
tion by wolves or human hunters, possibly due to decreased stamina and
pulmonary function as a result of space-occupying lung lesions ( Joly and
Messier, 2004; Rau and Caron, 1979). Infected canid definitive hosts do
not appear to be at risk of increased morbidity or mortality, and generally
experience no adverse effects.
Treatment and control programmes for E. granulosus/canadensis focus on
the regular administration of cestocidal drugs for definitive hosts, and on
good hygiene practices. The latter includes preventing dogs from ingesting
the viscera of infected IHs and ensuring proper disposal of canine faeces.
150 Emily J. Jenkins et al.

Praziquantel is the only drug currently labelled to remove adult cestodes

of E. granulosus from domestic dogs; however, nictroscanate has also proven
effective when administered at double the dose recommended for other
parasites (Ramsey, 2011). Veterinary practitioners in Canada and Alaska
would be unlikely to attempt treatment of the metacestode stage in cap-
tive cervids, as diagnosis is cost prohibitive and technologically challenging.
However, benzimidazoles such as albendazole and oxfendazole have effec-
tively inactivated protoscolices in IH (Blanton et al., 1998).

10.4. Transmission, Prevalence, and Public Health Impact

in the North
People are exposed to E. canadensis through the accidental ingestion of eggs
passed in the faeces of definitive hosts (wolves, coyotes, and dogs). These
eggs are immediately infective once they have passed into the environment,
and may adhere to the coat of an animal and a wide variety of surfaces
(Laws, 1968).Theoretically, hunters and trappers of wild carnivores could be
at risk due to their close contact with carnivore hides, faeces and intestines,
as well as dog owners who reside in endemic areas. Although the relative
significance of these exposure routes is currently unknown, it is likely that
people are predominantly infected though ingestion of contaminated sur-
face water, produce, and soil. The eggs of Echinococcus spp. and related tae-
niids are extremely resistant to extremes of temperature and humidity and
can persist in the environment for several years (Colli and Williams, 1972;
Eckert et al., 2001). Domestic or free-roaming dogs are considered impor-
tant ‘bridging hosts’ between people and wildlife due to their nonselective
diet and their close contact with people (Rausch, 2003). Subsistence hunt-
ing within a community, where dogs have access to offal and carcasses, is
also considered an important risk factor for human exposure to E. canadensis
(Himsworth et al., 2010a). However, people are not infected through con-
sumption of meat or organs from wild game but instead through contact
with faeces of dogs that have scavenged carcasses or been fed offal.
Cystic hydatid disease in people is most often characterised by unilocu-
lar fluid-filled cysts in the liver and lungs, although aberrant locations such
as the brain have also been documented (Himsworth et al., 2010a; Somily
et al., 2005; Wolfgang and Poole, 1956). Symptoms can include coughing,
anorexia, fever, shortness of breath, chest, or abdominal pain, and functional
neurological deficits if cysts are associated with the brain, nerves, or spi-
nal cord (Moore et al., 1994; Somily et al., 2005). Echinococcus canadensis
(or the cervid G8/G10 strains of the E. granulosus species complex) has been
Arctic Zoonoses 151

considered to be less likely to cause anaphylactic shock and secondary seed-

ing than the pastoral strain(s) (G1–G3) (Castrodale et al., 2002). Autochtho-
nous cases of cystic hydatid disease in Canada and Alaska do not commonly
result in fatality; however, infection with the G8 strain has been known
to cause severe clinical disease, and most recently, death (Castrodale et al.,
2002; McManus et al., 2002). Treatment options for hydatid disease include
surgical removal, benzimidazole chemotherapy, and puncture–aspiration–
injection–reaspiration therapy (Brunetti et al., 2010). In ideal circumstances
a physician might use a ‘watch-and-wait’ strategy to monitor and treat this
disease; however, the limited availability of medical imaging equipment
and geographic barriers to accessing medical care may make this approach
impractical in northern communities (Brunetti et al., 2010; Lamy et al.,
1993; Pinch and Wilson, 1973).
Human cystic hydatid disease did not appear in Canadian literature
until 1883, and until the 1950s (Table 2.17), most cases were detected in
immigrants from Iceland, an area historically endemic for the pastoral vari-
ant of E. granulosus (Cameron, 1960). In Alaska, the first human case was
recorded in 1941 (Rausch, 1968; Wilson et al., 1968). Human hydatid dis-
ease is reportable to Alaskan state public health authorities; peak numbers
of cases were detected from 1953 to 1973 (Fig. 2.23), nearly all of which
were Indigenous people (Rausch, 2003). Cases of autochthonous hydatid
infection were reported with increasing frequency in Canadian Indigenous
populations in the latter half of the twentieth century, mainly due to inci-
dental observation of cysts during tuberculosis screening (Lamy et al., 1993).
Similar to Alaska, 99% of 141 cystic hydatid cases in Canada in the 1950s
occurred in Indigenous people (Miller, 1953).
In 1952, Indian Health Services and the Institute of Parasitology in Can-
ada initiated efforts to determine the prevalence of infection in Indigenous
communities using the Casoni skin test. Initial efforts used antigen obtained
from Australian sheep cysts that was soon replaced by antigen obtained from
reindeer in Aklavik (YT), resulting in greater test sensitivity (Cameron,
1960; Wolfgang and Poole, 1956). Between 1954 and 1957, positive Casoni
skin test results were found in 6–52% of people across northern Canada
(N = 3429) (Table 2.18). This proportion was lower in Alaska where the
skin test employed did not use antigens of E. canadensis (Davis, 1957). Cul-
tural practices including food preparation, acquisition of locally acquired
foods, outdoor food storage, and the presence of large working dog popula-
tions may have significantly increased the risk of hydatid infection in the
middle of the twentieth century.
Table 2.17  Cases of Cystic Hydatid Disease in People in Alaska and Canada, Organised Chronologically

Location Sampling Dates Number of cases Reference
Alaska, USA
1941 1 Magath in Wilson et al. (1968)
1948 1 Williams in Wilson et al. (1968)
1949–1960 41 Rausch (1960)
1950–1966 101 Wilson et al. (1968)
1966–1973 25 Pinch and Wilson (1973)
1950–1990 >300* Castrodale (2003)
1991–2003 8 Castrodale (2003)
1999 2 Castrodale et al. (2002)
Central Canada Prior to 1883 8–10 Osler in Cameron (1960)
Northwestern Canada 1948–1955 At least 180 Miller (1953); Choquette and
Moynihan (1964)
ON 1967–1982 40 Langer et al. (1984)
NT and Northern AB 1970–1992 14 Moore et al. (1994)
Southern BC 1987–1991 5 Finlay and Speert (1992)
MB and ON 1987–1997 17 Al Saghier et al. (2001)
Northwestern Canada 1991–1993 3 Lamy et al. (1993)
NT, Northern AB 1991–2001 22 (+20 possible) Somily et al. (2005)

Emily J. Jenkins et al.

Canada 2001–2005 108 cases Gilbert et al. (2010)
SK 2008 1 Himsworth et al. (2010a)
Note that Alaskan cases are also captured in Fig. 2.23. Abbreviations for states, provinces, and territories as in Fig. 2.1.
*Includes the previous three citations.
Arctic Zoonoses 153

Figure 2.23  Cases of cystic hydatid disease in people in Alaska, 1940–2010, as reported
to the state public health authorities.

Today, imported and authochthonous cases of cystic hydatid disease

occur infrequently in North America, in part due to the eradication of
E. granulosus in Iceland, global efforts to control the disease, and the grad-
ual phasing out of sled dogs as a method of transportation in the North.
In Alaska, where human cases are reportable, zero to three cases per year
in Indigenous and other residents have been reported since 1973 (Fig.
2.23). In Canada, neither human nor animal cases are nationally reportable
(although laboratory confirmed cases in animals are annually notifiable to
the World Organisation for Animal Health), so surveillance is limited to case
reviews and serosurveillance.
A review of records in Edmonton hospitals, which act as referral cen-
tres for northern Alberta and the Northwest Territories, identified 42 cases
of suspected or confirmed cystic hydatid disease between 1991 and 2001
(Somily et al., 2005). Indigenous patients were over-represented in this
group, as 41% self-identified as Indigenous, compared with the 5% of Alber-
tans and 3% of Canadians who self-identified as Indigenous in 2001. These
results are supported by Gilbert et al. (2010), who reviewed hospital cases
Table 2.18  Prevalence [% (n)] of Exposure to Echinococcus granulosus/canadensis in People Residing in Alaska and Northern Canada

Location Sampling Dates Prevalence [% (n)] Method References
Alaska, USA
Fort Yukon 1957 16 (104) ST* Davis (1957)
Beaver, Tanana Stevens Village 1957 21 (168) ST† Tulloch in Davis (1957)
YK 1954 38 (293) ST‡ Wolfgang and Poole (1956)
Mackenzie Delta to Great Slave Lake, NT 1955 41.5 (1145) ST‡ Wolfgang and Poole (1956)
Great Slave Lake, NT 1955 13.5 (584) ST‡ Wolfgang and Poole (1956)
Inuvialuit Settlement Region, NT 2007–2008 <1 (362) SE** Egeland et al. (2010a)
Northeastern SK 2008 11 (106) SE Himsworth et al. (2010a)
Keewatin Yatthe Region, SK 2011 48 (201) SE Schurer et al. (2013)
Arviat, NU 1956–1957 52 (186) ST‡ Whitten in Cameron (1960)
Igoolik, NU 1956–1957 6 (63) ST‡ Whitten in Cameron (1960)
Nunavik, QC 1980s <1 (759) SE Tanner et al. (1987)
Nunavik, QC 2004 8.3 (917) SE Messier et al. (2012)
James Bay, QC 1980s <1 (436) SE Tanner et al. (1987)
James Bay, Eastmain and Wemindji, QC 2007 4 (250) SE Campagna et al. (2011)
James Bay, Chisasibi and Waskaganish, QC 2008 <1 (266) SE Sampasa-Kanyinga et al. (2012)

Emily J. Jenkins et al.

Nunatsiavut Health Survey, NL 2007–2008 <1 (310) SE Egeland et al. (2010b)
*Skin test = ST – with antigen acquired in New Zealand.
†Lilly skin test.
‡Casoni skin test with reindeer antigen.

Arctic Zoonoses 155

using ICD codes for Echinococcus/hydatid disease across Canada between

2001 and 2005 (N = 108). In this review, people living north of the 55th
parallel were 4.88 times (95% CI 2.52–9.44) more likely to be hospitalised
for cystic hydatid disease than the average Canadian (2.9 cases versus 0.72
cases per 1,000,000 people annually). Hospital records also indicate that
women may be at higher risk of developing hydatid disease than men (RR
1.92, 95% CI 1.29–2.87)(Gilbert et al., 2010; Langer et al., 1984; Somily
et al., 2005).
Casoni skin tests have been replaced with serological testing in the
northern and Indigenous communities based on IgG ELISA (Tanner et al.,
1987). Seroprevalence in Inuit and James Bay Cree, QC (0.1–4%) and First
Nations in Saskatchewan (11% and 48%) indicate that northern and Indig-
enous populations, especially in western Canada, continue to be at risk
for exposure to E. canadensis. However, the association between positive
serology and clinical cystic hydatid disease is unclear. As well, this disease is
underdiagnosed due to a variety of factors including many asymptomatic
cases, nonspecific symptoms, the long progression of the disease, and a wan-
ing awareness in the medical community. Therefore, these factors should be
considered when interpreting the apparent decline in prevalence of cystic
hydatid disease in human populations in North America.

10.5. Future Impact of Climate and Landscape Change

The worldwide distribution of strains in the E. granulosus species complex
demonstrates that this group of cestodes transmits well in different climates
and in a wide variety of hosts (Mas-Coma et al., 2008); however, species and
genotypes may vary in hardiness (Eckert et al., 2001; Jenkins et al., 2011).
Echinococcus canadensis is particularly well adapted to cold northern climates.
Eggs that passed in the faeces of definitive hosts can survive in the envi-
ronment for several years before infecting a new host; eggs and cysts may
survive even longer if encased within a protective barrier (e.g. snow, faeces,
sewage, or a host carcass) (Eckert et al., 2001). Temperatures above +35 °C
or below −30 °C can damage eggs, while temperatures above 60 °C or
below −70 °C completely inactivate them (Colli and Williams, 1972; Gem-
mell, 1973; Mas-Coma et al., 2008). Regardless of temperature, Echinococcus
eggs are sensitive to desiccation at low humidity and are inactivated within
one day at 0% relative humidity (RH) and within four days at 25% RH
(Eckert et al., 2001; Gemmell 1973). Diker et al. (2007) tested the viability
of hydatid cysts from sheep (E. granulosus) at a variety of temperature and
RH combinations in the laboratory, and estimated environmental survival
156 Emily J. Jenkins et al.

times for cysts in discarded carcasses: 3–36 days in winter (−10 to 0 °C),
12–28 days in spring/autumn (10–20 °C), and 3–4 days in summer
(30–40 °C) (Diker et al., 2007). This has limited application to the North,
where winter air temperatures drop far below −10 °C and the species
present is E. canadensis. Egg and cyst viability experiments demonstrate that
the duration of cold and freeze–thaw cycles are more important to inactiva-
tion than the magnitude of cold (Davis, 1957).
Density increases in moose populations are associated with increasingly
aggregated distributions and increases in prevalence of E. canadensis ( Joly
and Messier, 2004). The northern distribution of moose in Canada and
Alaska is thought to be limited by snow cover and vegetation; however,
warming trends that increase food availability could allow moose to move
further north (Darimont, 2005). Woodland and barren-ground caribou
populations are currently decreasing as a result of anthropogenic and natural
environmental changes, but could potentially be replaced by other ungu-
late hosts suitable for harbouring E. canadensis, such as moose and wapiti
(McLoughlin et al., 2002;Vors and Boyce, 2009). If the snow cover decreases
by 10–20%, as predicted, the High Arctic could become more supportive of
densely populated predator–prey food webs and might become a new area
for emergence of E. canadensis (Davidson et al., 2011).
Arctic temperatures over the last 2000 years were warmest in the period
between 1950 and 2000, despite a previous cooling period (Kaufman et al.,
2009). Mean annual precipitation in the Canadian Arctic has increased by
2–25% over the last 62 years (Furgal and Prowse, 2008). With regard to
effects on transmission of E. canadensis in the future, novel weather patterns
may alter sympatric territories of predator–prey systems or egg survival in
the environment, possibly resulting in the emergence of hydatid disease into
new areas, as well as retreat from warming areas (eggs have decreased sur-
vival in warmer temperatures).Warming winter temperatures could increase
the window of opportunity for hydatid cysts (which are freeze susceptible)
to survive before infecting a new definitive host. Increased precipitation
in the north is protective for eggs against desiccation, but could also limit
the accessibility of eggs on vegetation for ingestion by IHs ( Jenkins et al.,
2011). Climate change could cause breakdowns in sanitation infrastructure,
potentially reducing access to clean water through events such as water
contamination with eggs of Echinococcus (Parkinson and Evengard, 2009;
Schwabe, 1984). Finally, emergence of a related species (E. multilocularis) as
a result of increased globalisation, climate and landscape change, and altered
interfaces with wildlife reservoirs serves as an important reminder about the
Arctic Zoonoses 157

versatility of these cestodes (Davidson et al., 2012; Jenkins et al., 2011; Mas-
Coma et al., 2008; Schweiger et al., 2007).


Echinococcus multilocularis is a taeniid cestode responsible for alveolar
hydatid disease (also known as alveolar echinococcosis or alveolar hydatido-
sis) in people around the circumpolar North. Adults of this cestode are pres-
ent in the small intestine of wild carnivores, such as foxes, domestic canids,
and felids (Fig. 2.24). Eggs passed in the faeces are immediately infective for
rodent IHs. Ingested eggs release oncospheres that penetrate the intestinal
wall of the IH, undergo tissue migration, and eventually develop into alveo-
lar (=multilocular) hydatid cysts, which generally originate in the liver and
can fill the entire abdominal cavity. The life cycle is complete when a car-
nivore consumes the alveolar hydatid cyst in the rodent, whereupon proto-
scolices evert, attach to the intestinal wall, and begin to produce proglottids.
People and other mammals can serve as aberrant IHs, in which protoscolices
may not develop and the germinal membrane metastasises throughout the
liver and other organs.

Figure 2.24  Life cycle of Echinococcus multilocularis in the North. The larval or meta-
cestode stage takes the form of a multilocular hydatid cyst (alveolar hydatid).
158 Emily J. Jenkins et al.

11.1. Species and Strains Present in the North

Confusion over the identity and biological relationship of E. granulosus
and E. multilocularis was only resolved in the past 60 years (Tappe et al.,
2010). Resolution of a long and ongoing controversy about the biology of
these species only emerged following recognition and clarification of the
taxonomy for what we now regard as E. multilocularis in Alaska (Rausch
and Schiller, 1954). Up to that time, considerable contention existed as to
whether or not the distinct zoonoses attributable to these taeniids were
caused by variants of a single species. Final clarification of this significant
question emerged from the field and laboratory studies conducted in Alaska
by Robert Rausch and Everett Schiller, who were the first to unequivocally
complete the cycle for E. multilocularis from arvicoline IHs through arc-
tic fox definitive hosts (Rausch and Schiller, 1951). Although Rausch and
Schiller (1954) initially regard the forms found on St. Lawrence Island as a
distinct species, Echinococcus sibiricensis, it was later shown that these popula-
tions were conspecific with E. multilocularis, thus establishing a Holarctic
range for this parasite. Further, alveolar hydatid disease was documented in
the indigenous population of St. Lawrence Island, representing the first rec-
ognised cases for E. multilocularis as a zoonotic pathogen in North America.
Recent findings that E. multilocularis is not genetically uniform across its
distribution in the northern hemisphere have significance for understanding
pathogenicity, host specificity, and zoonotic potential (Knapp et al., 2009;
Nakao et al., 2009). Characterisation at multiple mitochondrial loci has
demonstrated distinct North America, Asian, and European haplotypes of
E. multilocularis (Nakao et al., 2009). On St. Lawrence Island, Alaska, there are
three known strains of E. multilocularis, a North American N1 haplotype and
two Asian strains, A2 and A4 (Nakao et al., 2009). The presence of two Asian
haplotypes in Alaska are likely due to the natural movement of arctic foxes
(Vulpes, formerly Alopex, lagopus), which travel extensive distances across the
ice (Dalen et al., 2005; Fay and Williamson, 1962; Hoberg et al., 2012). This
dispersal could lead to the eventual introduction of additional European or
Asian strains of E. multilocularis to North America and Greenland.
A second North American haplotype of E. multilocularis (N2), which is
distinct from those present on St Lawrence Island, Alaska, has been described
in the north central region (NCR) of North America (Nakao et al., 2009).
The NCR of North America corresponds to the southern portion of the
three Canadian prairie-provinces and contiguous American states. It is
unlikely that the N2 strain is present in the Arctic due to the lack of sup-
portive vegetation in the boreal region, which has created an area of low
Arctic Zoonoses 159

Figure 2.25  Published reports of alveolar hydatid disease (Echinococcus multilocularis)

in the North based on necropsy in animals (foxes, dogs, and rodents) and immunologi-
cal and clinical testing of people. (Data from Tables 2.19 and 2.20). Human cases have not
been described in northern Canada and the parasite is not thought to be present in Green­

rodent IH density, resulting in separate northern and southern populations of

E. multilocularis in North America (Nakao et al., 2009; Schantz et al., 1995).

11.2. Geographic Distribution in the North

There are two distinct populations of E. multilocularis in North America.The
northern population is found in the Arctic tundra region of Canada and
Alaska, and the second population is found in the North American NCR
(Eckert et al., 2001; Jenkins et al., 2011; Nakao et al., 2009). The southern
distributional limit of E. multilocularis in the Canadian Arctic is thought to
roughly follow the southern distribution of arctic foxes, which in turn,
roughly follows the northern border of the tree line. Actual reports of this
parasite in Arctic Canada are limited to one report on the mainland and two
in the high Arctic (Fig. 2.25). In Alaska, the distribution of E. multilocularis is
also thought to correspond to the distribution of the arctic fox and appears
to be largely limited to coastal regions of the northern Alaskan mainland
160 Emily J. Jenkins et al.

and the Alaskan Archipelagos (Fay and Williamson, 1962) (Fig. 2.25). Red
fox (V. vulpes) is also a suitable definitive host, whose distribution is now
sympatric with arctic fox in many regions of the Arctic mainland (Her-
steinsson and MacDonald, 1992; Rausch, 1956b). Although arctic foxes are
present in Greenland, to date, E. multilocularis has not been reported in any
hosts in Greenland (Braestrup, 1941; Kapel and Nansen, 1996).

11.3. Transmission, Prevalence, and Animal Health

Impact in the North
Definitive hosts for E. multilocularis in the North American Arctic include
canid species such as arctic fox, red fox, and domestic dogs (C. lupus familia-
ris) (Table 2.19). Wolves (C. lupus) may also serve as definitive hosts but are
more likely to be infected with E. granulosus (Rausch, 2003). Although the
domestic cat (Felis catus) and lynx (L. canadensis) may also serve as definitive
hosts for E. multilocularis, felids in general appear to be less suitable definitive
hosts (Kapel et al., 2006). In addition, lynx are not well-established north of
the boreal forest and free-ranging domestic cats are uncommon in northern
communities. Intermediate hosts in the North include arvicoline rodents
(lemmings, voles, and muskrats) and neotomine rodents (such as deer mice)
( Jones and Pybus, 2001). Other rodents, such as ground squirrels (Family
Sciuridae) and shrews (Family Soricidae), have been reported in a highly
endemic focus on St Lawrence Island (Table 2.19). In Greenland, the only
potential IH is the Greenland (collared) lemming (Dicrostonyx groenlandicus).
However, field and laboratory studies indicate that the collared lemming,
despite being a close relation to the brown lemming (Lemmus trimucronatus), is
not a suitable host for E. multilocularis (Ohbayashi et al., 1971; Rausch, 1995).
The prevalence of E. multilocularis in both definitive hosts and interme-
diate hosts on the Canadian Arctic islands and in the mainland North
American Arctic is relatively low. Surveys on the Arctic mainland have found
the prevalence of E. multilocularis in red and arctic foxes to be only 2–9%
(Table 2.19). In studies of rodent IHs on the mainland of Alaska, E. multilocu-
laris has not been found in excess of 1% despite multiple surveys (Holt et al.,
2005). Rausch (1956b) reported examining 2500 rodents, which he consid-
ered a ‘relatively small’ number, with no observed cysts.To our knowledge, IH
surveys have not been performed in the Canadian Arctic.
In contrast, St. Lawrence Island in the Bering Strait, as well as St. George
and Nunivak Islands in the Bering Sea, are considered hyperendemic foci
of transmission of E. multilocularis, with prevalence ranging from 32 to 100%
in arctic fox and 5–13% in dogs (Table 2.19). The discrepancy between
Table 2.19  Prevalence [% (n)] of Echinococcus multilocularis Identified at Necropsy of Carnivore Definitive Hosts and

Arctic Zoonoses
Rodent/Shrew IH in Alaska and Northern Canada
Host Location(s) Prevalence [% (n)] References
Order Carnivora
Arctic Fox (Vulpes lagopus) St. Lawrence Island, AK 71 (7) Rausch and Schiller (1951)
67 (6) Thomas et al. (1954)
40 (106) Rausch and Schiller (1956)
100 (40) Rausch and Schiller (1956)
75 (1527) Rausch (1967)
80 (1579) Rausch and Fay (2002)
St. George Island, AK 67 (5) Fay and Williamson (1962)
32 (28) Rausch (1967)
Nunivak Island, AK 73 (33) Rausch (1967)
Seward Peninsula, AK 2 (11) Rausch (1967)
Mainland, AK 4 (94) Rausch (1956b)
Mainland, AK 9 (207) Rausch (1967)
Banks Island, NT 2 (50) Eaton and Secord (1979)
Eskimo Point (Arviat), Resolute NR Choquette et al. (1962)
Bay, Cornwallis Island, NU
Dog (Canis lupus familiaris) St. Lawrence Island, AK 6 (89) Rausch (1960)
5 (110) Rausch (1967)
13 (31) Rausch and Fay (2002)
Red Fox (Vulpes vulpes) Nunivak Island and Point 2 (100) Rausch (1956b)
Barrow, AK
Nunivak Island and Brooks 55 (11) Rausch (1967)
Range, AK

Table 2.19  Prevalence [% (n)] of Echinococcus multilocularis Identified at Necropsy of Carnivore Definitive Hosts and

Rodent/Shrew IH in Alaska and Northern Canada—cont’d
Host Location(s) Prevalence [% (n)] References
Order Rodentia
Brown Lemming (Lemmus Mainland Alaska <1 (467) Holt et al. (2005)
Ground Squirrel (Citellus St Lawrence Island, AK 17 (12) Thomas et al. (1954)
Red-back Vole (Clethrionymus St Lawrence Island, AK 18 (22) Rausch and Schiller (1956)
12 (25) Rausch and Schiller (1956)
5 (22) Rausch and Schiller (1956)
Tundra Vole (Microtus oeconomus) St Lawrence Island, AK 2 (385) Rausch and Schiller (1951)
8 (905) Rausch and Schiller (1956)
16 (200) Rausch and Schiller (1956)
10 (320) Rausch and Schiller (1956)
5 (528) Rausch et al. (1990a)
28 (1115) Rausch et al. (1990b)
63 (329) Rausch and Fay (2002)
Voles St Lawrence Island, AK 17 (198) Thomas et al. (1954)
Order Soricomorpha

Emily J. Jenkins et al.

Shrew (Sorex jacksoni) St Lawrence Island, AK 25 (4) Thomas et al. (1954)
23 (13) Rausch and Schiller (1956)
Abbreviations for states, provinces, and territories as in Fig. 2.1.
NR – Not recorded.
Arctic Zoonoses 163

the mainland- and island infection rates may be due to the differences in
rodent population stability. The island host populations tend to remain
relatively stable from year to year while rodent populations on mainland
Alaska experience dramatic fluctuations (Rausch and Fay, 2002). In years
when infections in definitive hosts on St. Lawrence Island were between
76 and 100%, the prevalence of infection in rodent IHs did not exceed
20% (Rausch, 1956b). Although the published literature shows a range of
2–63% prevalence in rodents (primarily voles and shrews) on St. Lawrence
Island (Table 2.19), the prevalence of infection in rodents on the island has
at times exceeded 80% (Rausch et al., 1990a). Variation in infection rates
among definitive and intermediate host species serve to highlight the role
that definitive hosts play in parasite bioaccumulation. In fact, Fay and Wil-
liamson (1962) noted that an infection rate of less than 10% in tundra voles
(Microtus oeconomus) could yield almost 100% infection rates in Arctic foxes.
Prior to the implementation of an Echinococcus control programme, the
rate of infection on St. Lawrence Island was approximately 53% in voles
(Rausch et al., 1990b).The control programme, consisting of monthly doses
of praziquantel for local dogs near Savoonga, decreased the occurrence of
this parasite in voles by approximately 83% (Rausch et al., 1990b). These
control measures remain the recommended approach to controlling E. mul-
tilocularis in synanthropic cycles involving dogs (and cats) with access to
infected rodent IHs; praziquantel has good efficacy against adult cestodes
(Eckert and Deplazes, 2004; Eckert et al., 2001). Other recommended prac-
tices in endemic regions include dog population control, community efforts
to control free-roaming dogs, ‘poop scooping’, and thorough hand washing
following handling of dogs, trapped or hunted foxes and coyotes, and their
faeces. At the consumer/food handler level, thorough washing of fruits and
vegetables harvested in regions where this parasite is present, and effective
filtering of untreated surface water prior to consumption, are recommended.
Motivation for control programmes largely stems from public health
significance. Rarely, E. multilocularis can cause alveolar hydatid cysts in
dogs, resulting in severe disease similar to that observed in people (Eckert
and Deplazes, 2004). Treatment is similar to that recommended in peo-
ple with alveolar hydatid disease, involving an aggressive surgical removal
and long-term parasitostatic treatment with benzimidazoles (Peregrine
et al., 2012). Control in sylvatic cycles is more challenging than in synan-
thropic cycles. To reduce human risk of exposure, wildlife population con-
trol measures and good garbage management practices are recommended
in urban areas in endemic regions. In lieu of mass culling, regular doses
164 Emily J. Jenkins et al.

of praziquantel-containing baits for wild carnivores in endemic regions

may decrease the bioaccumulation of eggs in the environment (Eckert and
Deplazes, 2004; Eckert et al., 2001).

11.4. Transmission, Prevalence, and Public Health

Impact in the North
People may become infected with E. multilocularis by the accidental ingestion
of eggs shed in carnivore faeces. The sticky eggs may adhere to multiple sur-
faces in the environment including vegetation, fur and human skin and may
even float in water (Hildreth et al., 2000; Laws, 1968). In people, alveolar hyda-
tid disease behaves like an invasive neoplasm, most often originating in the
liver, with a case fatality rate that exceeds 90% within 10 years unless treated
early and aggressively (Kern et al., 2003). While detection of cysts smaller
than 10 mm is difficult, early detection and surgical resection of the infected
tissue is essential to survival (Eckert et al., 2001; Rausch and Wilson, 1985).
In North America, cases of human alveolar hydatid disease have occurred
mainly in Alaska, with only two cases in central North America (Minnesota,
USA and Manitoba, Canada) (Gamble et al., 1979; James and Boyd, 1937).
Autochthonous cases of human alveolar hydatid disease have been primarily
focused in the Alaskan Archipelagos with a few additional cases on the North
Slope of the Alaskan mainland (Wilson et al., 1995) (Table 2.20).
Since the 1950s, 54 human cases of alveolar hydatid disease have been
reported between 1947 and 1986 in Alaska (Castrodale, 2003) (Fig. 2.26).
Historically, the transition of the Inupiat Inuit to a sedentary way of life
negated the sanitary effects of a previously nomadic lifestyle, increasing the
rate of human infection (Rausch, 2003). Domestic dogs, replacing Arctic fox
as definitive hosts in villages, had access to stable and abundant populations
of infected IHs, which served to perpetuate the life cycle of E. multilocu-
laris and increase its prevalence in the immediate surroundings (Eckert and
Deplazes, 2004; Stehr-Green et al., 1988). Domestic dogs are considered the
most important source of transmission of this parasite to people primarily
due to close physical proximity (Rausch, 1956b; Wilson et al., 1995). Trap-
pers and hunters may also be at increased risk when handling infected foxes,
although trapping foxes was not a significant risk factor in adults in a case-
control study in Alaskan Eskimo (Rausch, 1956b; Stehr-Green et al., 1988).
Around the world, the highest incidence of human infections with alveolar
hydatid disease are primarily seen in rural areas where exposure is thought
to occur through the accidental ingestion of eggs on local produce and
vegetation (Hildreth et al., 2000). In some regions, consumption of surface
Arctic Zoonoses 165

Figure 2.26  Cases of alveolar hydatid disease (E. multilocularis) reported in people in
Alaska, 1940–2010. The last case was reported in 1986.

(vs. well) water is associated with increased risk of alveolar hydatid disease
(Yang et al., 2006).
At its peak, seropositivity for alveolar hydatid disease on St. Lawrence
Island reached 98/100,000 (Schantz et al., 1995; Wilson and Rausch, 1980).
However, there are significant challenges in the sensitivity and specificity of
immunological testing for exposure to E. multilocularis, including the pos-
sibility of cross-reaction with E. granulosus and related helminths. Therefore,
ultrasound examination of the liver is considered the method of choice for
detection of E. multilocularis infection in people, complemented by com-
puted tomography or medical imaging in some cases (Eckert and Deplazes,
2004; Eckert et al., 2001). The historical presence of E. multilocularis in both
human and animal hosts on the mainland of Alaska has been comparatively
low (Rausch and Fay, 2002). Since the successful implementation of educa-
tion and control programmes in 1986, there have been no reports of human
E. multilocularis infection in Alaska (Castrodale, 2003) (Fig. 2.26). There is,
however, the possibility of undiagnosed cases within Alaska and in other Arc-
tic regions, as alveolar hydatid disease can mimic other conditions, including
166 Emily J. Jenkins et al.

hepatic carcinoma (Hildreth et al., 2000; Webster and Cameron, 1967). This
may be particularly true in Arctic Canada, where there is little index of sus-
picion on the part of medical practitioners, hydatid disease is not notifiable at
the national level, and many records do not differentiate between alveolar (E.
multilocularis) and cystic (E. granulosus) hydatid disease (Gilbert et al., 2010).
North American strains may have lower zoonotic potential than the
European or Asian strains of E. multilocularis. If so, the majority of human
cases reported in western Alaska might have been infections with Asian hap-
lotypes (Nakao et al., 2009). While it is possible that the low prevalence of
human infection in the rest of North America is due to a decreased oppor-
tunity for human exposure, this seems unlikely given that many residents
of the North (especially Indigenous peoples) hunt, trap, consume untreated
surface water, and harvest wild foods. The transmission of cystic hydatid
disease continues to occur in northern and Indigenous communities within
the range of E. multilocularis in North America (Gilbert et al., 2010; Hil-
dreth et al., 2000; Himsworth et al., 2010a). This reinforces the idea that
parasite genetic differences might account for the lack of human cases of E.
multilocularis observed in North America outside of western Alaska, despite
relatively high prevalence in wild canids in the NCR.

11.5. Future Impact of Climate and Landscape Change

Climate alterations, including global warming, will affect the structure and
functioning of parasitic ecosystems (Hoberg, 2010; Hoberg et al., 2008a,
2008b; Parmesan and Yohe, 2003; Polley and Thompson, 2009). These
effects will be especially felt in the Arctic where average temperatures have
increased at double the rate of the global average in the last 100 years (Kutz
et al., 2009a). One consequence of climate change in the north is the altera-
tion of restrictive temperatures that limit survival and development times of
parasites (Kutz et al., 2009a). The current distribution of E. multilocularis is
restricted to the northern hemisphere where the impacts of climate change
are already being felt. The distributional restriction may therefore make E.
multilocularis highly susceptible to the effects of climate change (Jenkins et al.,
2011; Mas-Coma et al., 2008). Already, this parasite is emerging (increasing
in distribution and prevalence) in wildlife and human hosts elsewhere in the
circumpolar North and is colonising new regions through anthropogenic
and natural movements of wild and domestic hosts (Davidson et al., 2012;
Eckert et al., 2000; Jenkins et al., 2005, 2012; Schweiger et al., 2007).
The survival of infective eggs of E. multilocularis in the environment is
affected by both temperature and moisture. The eggs of E. multilocularis are
Arctic Zoonoses 167

susceptible to desiccation and warmer temperatures, which are currently

thought to limit the parasite to the northern hemisphere (Mas-Coma et al.,
2008). In a future of climate change, increased precipitation and enhanced
snow melting in the north may facilitate survival of the eggs of E. multilocu-
laris in the summer, while warmer temperatures may decrease overwinter
survival (Mas-Coma et al., 2008). In a warmer North America, the Arctic-
adapted strain(s) may see decreases at their southern limit, while the strain(s)
present in the NCR may expand northward into the Arctic along with
temperate-adapted wildlife hosts colonising northern habitats.
Alterations to the distribution of E. multilocularis may largely be medi-
ated through changes in rodent IH distribution and abundance. Climate
change may open up previously unsuitable areas (such as the boreal forest)
by clearing the way for early successional plant species, supporting higher
densities of rodent IHs. Climate change is also predicted to increase an
overall precipitation in northwestern North America, which will lead to
higher primary productivity and in turn, increased stability and density of
rodent populations, facilitating amplified transmission of E. multilocularis on
the Arctic mainland. Climate change is also predicted to increase extreme
weather events, which may in turn increase the frequency and amplitude of
fluctuations in arctic rodent populations. Fluctuating rodent numbers may
decrease overall transmission of E. multilocularis, or prevalence may be den-
sity-dependent (Rausch and Schiller, 1951). In North America, the preva-
lence of E. multilocularis is higher where deer mice were more abundant
(Holmes et al., 1971). Anthropogenic landscape changes such as deforesta-
tion may also lead to an IH-range expansion in North America. In Europe,
rodent and fox distributions are enhanced by deforestation and agricultural
practices that create a favourable habitat for rodent species, to which foxes
are attracted (Giraudoux et al., 2004; Romig et al., 2006; Viet et al., 1999).
In North America, warming temperatures may also increase interna-
tional shipping through the Northwest Passage, enabling further opportuni-
ties for translocation of infected rodents and dogs. This is supported by the
recent establishment of E. multilocularis on Svalbard in the Norwegian Arctic
and in Sweden, most likely by the introduction of suitable rodent hosts from
shipping, and infected domestic dogs, respectively (Henttonen et al., 2001;
Osterman Lind et al., 2011). The recent identification of a European strain
of E. multilocularis in central British Columbia, Canada (a previously non-
endemic region) may have occurred as a result of importation of infected
red foxes from Europe in the last century or the more recent translocation
of an infected dog (Jenkins et al., 2012). In Greenland, where Arctic fox
168 Emily J. Jenkins et al.

are already present, increased shipping coupled with warming temperatures

may provide an opportunity for more suitable rodent IHs to establish, com-
pleting the life cycle requirements of E. multilocularis.
In addition to altering the ecology of IHs, climate change may also affect
the distribution and abundance of sylvatic definitive hosts in Alaska, Canada,

Table 2.20  Prevalence [% (n)] of Alveolar Hydatid Disease in People in Alaska

Location Prevalence [% (n)] Method References
St. Lawrence 33 (233) Casoni skin test* Rausch and Schiller
Island (SLI) 16 (233) Casoni skin test† Rausch and Schiller
15 (233) CF Rausch and Schiller
8 (153) CF Rausch and Schiller
24 (232) SE Rausch and Schiller
Gambell, SLI 20 (126) Skin test Rausch and Schiller
2 (372) SE, X-ray, biopsy Wilson and Rausch
Savoonga, SLI 28 (106) Skin test Rausch and Schiller
2 (364) SE, X-ray, biopsy Wilson and Rausch
Little Diomede 1 (84) SE, X-ray, biopsy Wilson and Rausch
Wales 2 (131) SE, X-ray, biopsy Wilson and Rausch
Point Hope 2 (386) SE, X-ray, biopsy Wilson and Rausch
Noatak <1 (293) SE, X-ray, biopsy Wilson and Rausch
Kotzebue <1 (1696) SE, X-ray, biopsy Wilson and Rausch
Kiana <1 (278) SE, X-ray, biopsy Wilson and Rausch
NR 42 cases SE, X-ray Wilson et al. (1995)
From west to east, then chronologically within a location.
CF – complement fixation, SE – serology, NR – not recorded.
*Alveolar hydatid antigen.
†Cystic hydatid antigen.
Arctic Zoonoses 169

and Greenland. In the early part of the twentieth century in North America
and Greenland, red foxes moved north by successfully outcompeting the
Arctic fox for food and den sites, possibly as a result of climate alterations
(Hersteinsson and Macdonald, 1992; Post et al., 2009). With the encroach-
ment of the red fox into Arctic fox territory, there may be an opportu-
nity for mixing of the Arctic and southern strains of E. multilocularis, which
may differ in pathogenicity, zoonotic potential, and host specificity. Further
understanding of the genetic variability, distribution, and zoonotic potential
of strains of E. multilocularis is needed in the North and elsewhere in the
circumpolar North to assess risks posed by a future of climate and other
anthropogenic changes.

12.1. Zoonotic Parasites in the Traditional North
The transmission of zoonotic parasites among animals and people in
northern North America in the past has reflected close linkages between
northern residents and their environment, as well as relatively intact tro-
phic relationships among wildlife. For millennia, the harvesting of fish
and wildlife for food, together with traditional methods of food prepa-
ration, has carried with it risks of food-borne pathogens: for example,
Trichinella, Toxoplasma, diphyllobothriid cestodes, and anisakid nematodes.
Prior to European colonisation, Indigenous peoples of the Arctic demon-
strated traditional knowledge protective against food-borne transmission
of parasites, even though historically the specific threat was not identi-
fied. For example, bear meat was eaten thoroughly cooked, and wildlife
with visible lesions were avoided for human consumption (Rausch, 1968).
Interestingly, the last practice might have perpetuated the transmission of
E. canadensis in the North if viscera deemed unfit for human consumption
were deliberately fed to dogs, the definitive hosts and sources of human
infection. In general, close association between people and dogs in the
North (sled dogs and free-ranging populations) facilitated human infec-
tions with Echinococcus spp. and T. canis (the latter in sub-Arctic regions).
Other risk factors for environmentally transmitted parasites in the North
included consumption of surface water, harvesting of wild berries, and
trapping. Underdeveloped water treatment and sewage infrastructure in
the North have likely increased transmission of enteric parasites such as
Cryptosporidium and Giardia. Many of these risk factors remain under cur-
rent conditions in the North today, and there is evidence that northern
170 Emily J. Jenkins et al.

residents remain at higher risk of infection with some parasites than the
general North American population (Gilbert et al., 2010).

12.2. Risk Assessment for Zoonotic Parasites in the North

As predicted by Rausch (1968), the prevalence of zoonotic helminths, such
as Trichinella spp. and anisakid nematodes, as well as Echinococcus spp. and
diphyllobothriid cestodes, in Indigenous peoples of the North has declined,
likely as a result of improving socioeconomic status, increasing reliance on
store-bought foods, and changing dietary preferences (Rausch, 1968, 1972,
1974). However, some zoonotic parasites in the North can have important
consequences for the individuals affected due to severity of the disease (e.g.
Trichinella, Echinococcus spp.) or health status of the individual (e.g. Toxo-
plasma in pregnant women). In addition, surveillance for enteric protozoan
parasites (Giardia and Cryptosporidium) in people has only recently been
implemented in the USA and Canada, and therefore the public health sig-
nificance of these protozoan parasites in the North is largely unknown.
The comprehensive nature of this review provides an unprecedented
opportunity for an evidence-based, qualitative risk assessment for the cur-
rent public health significance of zoonotic parasites in the North. We have
assigned priorities to the nine parasites reviewed (Table 2.21), ranking each
parasite from 1 to 4 using the following categories:
• Zoonotic potential: intrinsic ability of the parasite to cross the species
barrier. Groups with high host specificity rated lower.
• Human exposure: how commonly northern residents are exposed (cor-
responds to prevalence in animals and in people, as well as demographic
and behavioural risk factors). For example, those parasites that only have
opportunities to infect a portion of northern residents, either due to
focal geographic distribution or local dietary preferences, rated lower.
• Severity of human disease: severity of clinical disease in immunocom-
petent people. Parasites that are commonly asymptomatic, or have self-
resolving gastrointestinal signs or mild flu-like illness rated lower. Parasites
associated with anaphylaxis, abortion, and mortality rated higher.
• Difficulty of diagnosis (dx) and treatment (tx): parasitic diseases for
which treatments are effective and available in the North rated lower,
as are those that could be readily diagnosed in the North or by sending
samples to southern laboratories. Diseases that require diagnostic equip-
ment (such as ultrasound, endoscopy) or procedures (surgery) not read-
ily available in the North, sometimes requiring evacuation of the patient,
rated higher.
Arctic Zoonoses 171

• L
 ikelihood of emergence (increase in prevalence and/or distribution)
in a changing North: parasites that are likely to remain restricted geo-
graphically and those with life cycles disrupted by environmental change
rated lower. Parasites with environmentally susceptible life stages that are
likely to benefit in a warmer, wetter North rated higher, as are those that
currently show evidence of emergence.
Based on this subjective review process, the zoonotic parasites of most
importance in the North from a public health perspective are E. ­multilocularis,
T. gondii, Trichinella spp., and Giardia spp. Alveolar hydatid disease caused
by E. multilocularis was prioritised primarily because of severity of disease
and difficulty of diagnosis and treatment, especially in remote regions. This
parasite is rare outside of western Alaska; however, in a future of climate
change, strains of this parasite currently present in western Alaska or in
Eurasia might expand their range, or endemic strains might undergo ampli-
fication as a result of increased stability and abundance of rodent popula-
tions. Elsewhere in the circumpolar North, this parasite is emerging as
a result of climate and landscape changes, globalisation, and altered wildlife-
pet-people interfaces (Davidson et al., 2012; Eckert et al., 2000; Jenkins
et al., 2011; Schweiger et al., 2007).
Based on a low-IH specificity and current evidence of high levels of
human exposure in some regions of the North, T. gondii may well be ‘the
most important parasitic infection in the North American Arctic’ (Hotez,
2010). However, the prevalence of toxoplasmosis is not uniform across the
North; indeed, in most regions other than Nunavik, Canada, prevalence in
people is on par or lower than the North American average (Table 2.5).
Despite its potential public health importance, transmission of T. gondii
remains enigmatic at high latitudes.The role of oocyst transmission of Toxo-
plasma (relative to food-borne routes) is not clear in tundra regions where
wild and domestic felids are uncommon; however, residents of coastal
communities could become infected with oocysts contaminating marine
environments. There is some evidence in the Norwegian Arctic that cli-
mate change may be enhancing the transmission of toxoplasmosis in Arctic
marine systems due to enhanced survival of oocysts transported from sub-
Arctic regions and amplification of filter-feeding invertebrate populations,
which serve as transport hosts for oocysts ( Jensen et al., 2010).
Giardia and Trichinella together ranked third in terms of public health
priority. Giardia was prioritised due to the disproportionately high number
of cases reported in people in the North, and the high probability of under-
diagnosis due to the mild or asymptomatic nature of infection (Scallan et al.,
172 Emily J. Jenkins et al.

2011). It is not known how many outbreaks and cases of giardiasis are of
animal versus human origin; however, pets and ‘urban’ wildlife may play a
role in maintaining and transmitting zoonotic genotypes of Giardia within
human communities. Trichinella remains an important public health consid-
eration due to the possibility of large outbreaks resulting from food-sharing,
severe and even fatal consequences of disease, and evidence of ongoing
exposure across the North. Likewise, cystic hydatid disease (E. canadensis)
was ranked moderately high because of the potential severity of the disease,
difficulty in diagnosis and treatment in remote areas, and evidence of ongo-
ing exposure across the North.
For two environmentally transmitted parasites, Toxocara and Cryptospo-
ridium, both human and animal cases currently appear to be rare in the
Arctic. For Toxocara, development and survival of environmental stages has
likely been limited historically by abiotic conditions in the North. For
Cryptosporidium, there may be also be environmental tolerance limitations;
alternatively, there may not have been sufficient densities of human and
livestock populations to support high levels of amplification of this pro-
tozoan in the North. Both these parasites are flagged to emerge in a more
permissive and populated northern environment. Anisakidosis and diphyl-
lobothriosis ranked the lowest for concern due to evidence of low levels
of human transmission, mild disease, and the possibility that climate change
may disrupt marine cycles of transmission. It is important to note that this
risk assessment was primarily based on public health significance versus
animal health or trade criteria. Both of these fish-borne parasites may be of
increasing concern as fish are marketed for export from the North, and visi-
tors come into the North and sample local foods without local knowledge
of food safety considerations.

12.3. Risk Mitigation

Risk mitigation for some of these diseases in northern communities is already
in place and showing evidence of success. For endemic helminth zoono-
ses, exposure in people in the North appears to be declining. In Alaska, this
holds true for diseases for which there are physician-reporting systems and
laboratory-based surveillance (trichinellosis, alveolar and cystic hydatid disease
– Figs. 2.13, 2.23, and 2.26). In Canada, recent serosurveys over the last decade
in Nunavik and the James Bay Cree regions of QC, Nunatsiavut in NL, and
the Inuvialuit settlement region in the NT, collectively suggest that exposure
to Trichinella and Echinococcus is low and/or declining in northeastern Canada
(Tables 2.9, 2.11, and 2.18) (Campagna et al., 2011; Egeland et al., 2010a,
Arctic Zoonoses 173

2010b; Lévesque et al., 2007; Messier et al., 2012; Sampasa-Kanyinga et al.,

2012). Other than reported cases of cystic hydatid disease in the 1950s, little
surveillance has occurred in people in sub-Arctic regions in western Canada,
including the northern half of the Prairie Provinces. A recent serosurvey for
zoonotic parasites in one Dene community in northern SK suggests that these
diseases may persist in these communities at levels higher than those currently
reported in Inuit and Cree in northeastern Canada (Schurer et al., 2013).
Declines in these endemic helminth zoonoses are in part a consequence
of changes in dietary preference and availability of processed foods, and the
passing of sled dogs as a primary method of transportation in the North.
However, some of these declines may be a result of public health messaging
and programming, such as the NTPP (Nunavik Trichinellosis Prevention
Programme), which screens harvested walrus for trichinellosis prior to con-
sumption, and screening of pregnant Nunavik women for toxoplasmosis
(Lavoie et al., 2008; Proulx et al., 2002). Another success story is the impact
of regular anthelminthic treatment of dogs on St Lawrence Island, Alaska,
which led to significant reductions in prevalence of alveolar hydatid cysts in
rodents as an indicator of environmental egg contamination (Rausch et al.,
1990b). In many northern and Indigenous communities, however, access
to veterinary medical and veterinary public health services remains a chal-
lenge (Brook et al., 2010; Jenkins et al., 2011). In addition, evaluation of the
success of these interventions is seldom performed and critically needed to
motivate funding for and focus on such programmes.
Public education and targeted interventions are key to mitigating risks
of zoonotic parasites (Schwabe, 1986). The most successful approaches have
taken into account the undeniable benefits of wildlife as high-quality main-
stays of northern diets, and the ongoing challenges of maintaining security
and safety of food and water in a remote and harsh environment. Public health
interventions for the control of environmentally transmitted parasites include
drinking water and sewage treatment, as well as environmental hygiene and
dog population control. As true of today as it was 4 decades ago, ‘control of
zoonotic diseases in arctic regions can best be achieved through education
and improvement of the standard of living, but because some customs change
only with difficulty, rapid progress is not to be expected’ (Rausch, 1968).

12.4. Zoonotic Parasites in a North in Transition

Rapid and accelerating environmental change may already be altering the
distribution and transmission of zoonotic diseases currently present in the
North. For example, T. canis has now been reported at latitudes greater than
174 Emily J. Jenkins et al.

Table 2.21  Qualitative Risk Assessment From a Public Health Perspective for the Nine
Parasitic Zoonoses in the North Considered in this Review
Zoonotic Human Disease Difficulty
potential exposure severity of dx/tx Emergence Total
Alveolar 2 1 4 4 3 14
Anisakidosis 2 1 1 3 2 9
Cryptospo- 3 2 1 2 3 11
Cystic 2 2 3 3 1 11
Diphylloboth- 2 2 1 1 2 8
Giardiasis 3 4 1 1 3 12
Toxocariasis 2 1 2 2 3 10
Toxoplasmosis 4 3 2 2 2 13
Trichinellosis 3 2 3 3 1 12
For each criterion, diseases were ranked from 1 (lowest) to 4 (highest).
dx – diagnosis, tx – treatment.
*Echinococcus multilocularis.
†E. canadensis (cervid strain of E. granulosus).

60°N in areas of western Canada where it was not detected in studies

35 years previously ( Jenkins et al., 2011; Salb et al., 2008; Unruh et al.,
1973). While there are uncertainties about the magnitude and variability of
climate changes in northern Canada, the overall direction of change in the
terrestrial Arctic appears to be warmer, wetter, with an increased severity
and frequency of extreme climatic events, especially for the western Arctic.
Changes in marine systems appear to be greater than those in terrestrial sys-
tems, with enhanced velocity of change as well as shifts in phenology (Bur-
rows et al., 2011). When considering the effects of climate and landscape
changes, as well as other drivers of emerging diseases, on the ecology of
zoonotic diseases in the North, some common themes are apparent among
the mechanisms of disease emergence.
For parasites with largely food-borne transmission routes in the North
(such as Trichinella, Toxoplasma, anisakid nematodes, and diphyllobothriid
cestodes), effects of climate change will be largely linked to changes in
the distribution and abundance of wildlife reservoirs and altered interfaces
between wildlife and people. These changes are happening against a com-
plex backdrop of social and cultural change that may decrease zoonotic risks
due to these parasites, independently of the effects of environmental change
on transmission in sylvatic cycles. In contrast, environmentally transmitted
Arctic Zoonoses 175

parasites (such as Giardia, Cryptosporidium, Toxocara, and oocysts of Toxo-

plasma) may now be coming into their own in an increasingly connected
and hospitable North. Parasites that undergo water-borne transmission
(Giardia, Cryptosporidium, and possibly Toxoplasma) will be influenced greatly
by changes in regional hydrology and frequency of extreme rainfall events;
human exposure to water-borne diseases will largely rely on the resilience
of water treatment infrastructure and availability of treated water. Pathogens
with life stages that undergo mandatory and often temperature-dependent
development in the environment (such as Toxoplasma, Toxocara, anisakid
nematodes, and diphyllobothriid cestodes) will likely undergo accelerated
development in endemic areas, although this may trade off against decreased
survival at warmer temperatures in summer.
This review process has enabled more accurate determination of north-
ern distributions of parasites and their distributional limits based on the
best available knowledge in the published literature, and allows us to
describe current and future vulnerabilities for northern North America.
For ­example, parasites with environmental life stages that are currently
excluded from Arctic regions of mainland North America (D. latum, T. canis,
and possibly Cryptosporidium) might well move north, along with domestic
livestock, pets, and wildlife that are currently better established in sub-Arc-
tic and temperate regions. In addition, Greenland appears to be currently
free of several zoonotic parasites (including E. granulosus, E. multilocularis,
and T. canis). Echinococcus multilocularis has recently been identified in newly
endemic regions in the circumpolar North, likely as a result of importation
of domestic dogs (Davidson et al., 2012). Given the connectivity of once
remote northern locations and an increasingly permissive climate, main-
tenance of country freedom status might well rely on import regulations
mandating ­prophylactic treatment and screening of imported animals.

12.5. Future Needs for Research and Surveillance of Zoonotic

Parasites in the North
Perhaps the most important outcome of this review process is identification
of knowledge gaps regarding the diversity and health significance of zoo-
notic parasites in the North. Until recently, many were thought to be the
same parasite species as those in animals and people at temperate latitudes
(i.e. freeze-susceptible T. spiralis versus freeze-tolerant northern Trichinella
species). Until 1960, E. multilocularis and E. granulosus, which we now know
to have very different clinical syndromes and prognoses, were thought to be
the same species, and genetic diversity across the circumpolar distribution
176 Emily J. Jenkins et al.

of E. multilocularis has only recently been recognised. Protozoans, especially

Giardia spp., may be one of the most important causes of enteric disease
in northern human populations; however, molecular and epidemiologi-
cal characterisation to determine source of infection is seldom performed.
Such investigations are necessary to determine zoonotic potential and to
aid in source attribution in human clinical cases and outbreaks. In addition,
molecular databases and ‘fingerprints’ are needed to detect the emergence
of new zoonoses and to track movements of strains and species of parasite
zoonoses around the globe (Davidson et al., 2012; Jenkins et al., 2012). This
in turn provides compelling evidence to motivate and prioritise risk mitiga-
tion measures, such as targeted food safety recommendations, or regulations
for import and export of animals and animal products. Basic survey and
inventory of parasites present in the North, and those poised on its doorstep,
are critically needed in order to detect and predict changes in patterns of
distribution and transmission of zoonotic parasites (Hoberg, 2010; Hoberg
et al., 2008a, 2008b, 2012, in press).
While this review has focused on the public health significance of zoo-
notic parasites, the impact of endemic and potentially introduced parasites
on the health of northern wildlife populations important for ecological,
cultural, and socioeconomic reasons is almost completely unknown. We
have also identified gaps in surveillance for zoonotic parasites in different
human populations in the North. For example, most surveillance efforts
have focused on Indigenous groups; non-indigenous northern residents
might experience different risk factors and would be a useful out-group
for comparison. In addition, non-Indigenous residents may be at increased
risk of exposure due to lack of protective traditional knowledge, and may
experience more severe outcomes of infection with northern parasites for
which they have had little historical exposure, such as E. canadensis (McMa-
nus et al., 2002; Rausch, 2003).
Compelling evidence (such as cost-benefit analyses) is needed to moti-
vate public health policy makers to prioritise parasites in the light of other
infectious and chronic diseases facing the North. In many ways, the obser-
vations of Robert Rausch, to whom this review is dedicated, are as relevant
today as they were 60 years ago, when his early publications led to the first
recognition of the importance of Arctic zoonoses. Prior to this, the focus in
the medical literature on infectious diseases in the North was almost entirely
on diseases directly transmissible from person to person (Rausch, 1968).
This trend is still observable today; for example, at the 14th International
Congress on Circumpolar Health in 2009, infectious diseases of northern
Arctic Zoonoses 177

importance on the agenda were tuberculosis, respiratory and reproductive

diseases, hepatitis, Helicobacter pylori, and antibiotic resistant bacteria (http:// The importance
of these infectious diseases, along with chronic diseases such as diabetes,
cancer, and cardiovascular dysfunction, is undeniable. We forget parasitic
zoonoses at our peril, however, as they are more likely to emerge, or re-
emerge, in northern populations challenged by other infectious and chronic
diseases. In addition, the perceived threat of parasitic zoonoses cannot be
allowed to drive Indigenous and northern residents away from their ties
to the land. Maintaining this relationship requires an increased focus on
the preventable nature of zoonotic transmission of parasites through public
education, and interventions that address critical determinants of health in
northern peoples. Finally, there is a need to explore the potential for emer-
gence of zoonotic parasites in tandem with the potential for adaptation
on the part of northern residents and wildlife in a North at the interface
between tradition and transition.

We acknowledge the contributions of Brent Wagner, Juliane Deubner, Aaron Genest, Lena
Measures, Kimberlee Beckmen, Kelly Konecsni (curator of the Canada Database of Animal
Parasites maintained at the Canadian Food Inspection Agency Centre for Food-borne and
Animal Parasites), and the Notifiable Diseases and Field Surveillance Section, Surveillance
and Epidemiology Division, Centre for Communicable Diseases and Infection Control,
Public Health Agency of Canada. Funding for this project was provided by: Canadian
Foundation for Innovation Leaders Opportunity Fund, Natural Sciences and Engineering
Research Council, Public Health and the Agricultural Rural Ecosystem Training Program
(Canadian Institutes of Health Research Strategic Training Initiative in Health Research),
Public Health Agency of Canada, Saskatchewan Health Research Foundation, University
of Saskatchewan, and the Western College of Veterinary Medicine, Saskatoon, SK, Canada.

ACIA, 2005. Arctic Climate Impact Assessment. Cambridge University Press, New York.
Adams, A.M., 1988.Taxonomy, Systematics and Ecology of Helminth Parasites of the Ringed
Seal, Phoca Hispida Schreber, in Alaskan Waters. Doctoral Dissertation, University of
Washington, Seattle.
Adams, A.M., Rausch, R.L., 1997. Diphyllobothriasis. In: Connor, Chandler, Schwartz,
Manz (Eds.), Pathology of Infectious Diseases, Vol 2. Appleton and Lang, Stamford,
pp. 1377–1389.
Addison, E.M., Fyvie, A., Johnson, F.J., 1979. Metacestodes of moose, Alces alces, of the Chap-
leau Crown Game Preserve, Ontario. Can. J. Zool. 57, 1619–1623.
Adams, D.A., Gallagher, K.M., Jajosky, R.A., Ward, J., Sharp, P., 2012. Summary of notifiable
diseases – United States, 2010. MMWR 59 (53), 1–111.
Al Saghier, M., Taylor, M.C., Greenberg, H.M., 2001. Canadian-acquired hydatid disease:
a case report. Can. J. Infect. Dis. 12, 178–182.
178 Emily J. Jenkins et al.

Allen, J.R., Mills, J.H., 1971. Alaria arisaemoides in Saskatchewan dogs. Can.Vet. J. 12, 24–28.
Alvarez, F.J.D.L.P., Gallardo, A.M.P.,Vazquez, A.T., Rivera, M.U., Molina, A.M., 2007. Acute
renal failure due to sulfadiazine crystalluria. An. Med. Interna. 24 (5), 235–238.
Ancelle, T., De Bruyne, A.E., Dupouy-Camet, J., 2005. Outbreak of trichinellosis due to
consumption of bear meat from Canada, France. Euro. Surveill. 10 (41) pii = 2809.
Andersen, K., Ching, H.L.,Vik, R., 1987. A review of freshwater species of Diphyllobothrium
with redescriptions and distribution of D. dendriticum (Nitzsch, 1824) and D. ditremum
(Creplin, 1825) from North America. Can. J. Zool. 65, 2216–2228.
Andersen, K., Gibson, D.I., 1989. A key to three species of larval Diphyllobothrium Cobbold,
1858 (Cestoda: Pseudophyllidea) occurring in European and North American freshwa-
ter fishes. Syst. Parasitol. 13, 3–9.
Anderson, R.C., 2000.Their development and transmission. In Nematode Parasites of V   erte­
brates, second ed. CAB International, New York.
Appelbee, A.J., 2006. Giardia and Cryptosporidium in Pinnipeds from the Gulf of St. Lawrence,
Canada. Ph.D. Thesis. Murdoch University, Murdoch, Western Australia, pp. 218.
Appelbee, A.J., Thompson, R.C.A., Olson, M.E., 2005. Giardia and Cryptosporidium in mam-
malian wildlife – current status and future needs. Trends Parasitol. 21, 370–376.
Appelbee, A.J., Thompson, R.C.A., Measures, L.M., Olson, M.E., 2010. Giardia and Crypto-
sporidium in harp and hooded seals from the Gulf of St. Lawrence, Canada.Vet. Parasitol.
173, 19–23.
Appleyard, G.D., Gajadhar, A.A., 2000. A review of trichinellosis in people and wildlife in
Canada. Can. J. Public Health 91, 293–297.
Arh, I., 1960. Fish tapeworm in Eskimos in the Port Harrison area, Canada. Can. J. Public
Health 51, 268–271.
Arizono, N., Fukomoto, S., Tademoto, S., Yamada, M., Uchikawa, R., Tegoshi, T., et al.,
2008. Diplogonoporiasis in Japan: genetic analysis of 5 clinical isolates. Parasitol. Int.
57, 212–216.
Audicana, M.T., Kennedy, M.W., 2008. Anisakis simplex: from obscure infectious worm to
inducer of immune hypersensitivity. Clin. Microbiol. Rev. 1 (2), 360–379.
Azam, D., Ukpai, O.M., Said, A., Abd-Allah, G.A., Mogan, E.R., 2012. Temperature and the
development and survival of infective Toxocara canis larvae. Parasitol. Res. 110, 649–656.
doi: 10.1007/s00436-011-2536-8.
Babbott Jr., F.L., Frye, W.W., Gordon, J.E., 1961. Intestinal parasites of man in Arctic Green-
land. Am. J. Trop. Med. Hyg. 10, 185–190.
Bailey,T.M., Schantz, P.M., 1990.Trends in the incidence and transmission patterns of trichi-
nosis in humans in the United States: comparisons of the periods 1975–1981 and 1982–
1986. Rev. Infect. Dis. 12, 5–11.
Ballweber, L.R., Xiao, L.H., Bowman, D.D., Kahn, G., Cama, V.A., 2010. Giardiasis in dogs
and cats: update on epidemiology and public health significance. Trends Parasitol. 26 (4),
Baron, R.W., 1970. The occurrence of Echinococcus multilocularis Leuckart, 1863 and of other
helminths in the red fox, Vulpes vulpes, in southern Manitoba. Can. J. Zool. 48, 1132.
Beck, K., Conboy, G., Gilleard, J., Mauffete, M.-E., Peregrine, A., Polley, L., Villeneuve, A.,
Wagner, B., 2009. Canadian guidelines for the treatment of parasites in dogs and cats.
Canadian Parasitology Expert Panel (CPEP) p. 21.
Beck, M., Evans, R., Feist, S.W., Stebbing, P., Longshaw, M., Harris, E., 2008. Anisakis simplex
sensu lato associated with red vent syndrome in wild adult Atlantic salmon Salmo salar in
England and Wales. Dis. Aquat. Org. 82 (1), 61–65.
Bemrick, W.J., Erlandsen, S.L., 1988. Giardiasis – is it really a zoonosis? Parasitol. Today 4,
Berkes, F., Jolly, D., 2001. Adapting to climate change: social-ecological resilience in a Cana-
dian western Arctic community. Conserv. Ecol. 5 (2), 18.
Arctic Zoonoses 179

Bhat, M., Cleland, P., 2010. Gastric anisakiasis. Clin. Gastroenterol. Hepatol. 8, 1.
Bishop, L., 1979. Parasites-related lesions in a bearded seal. Erignathus barbatus. J. Wildl. Dis.
15, 265–293.
Blanchet, C., Rochette, L., 2008. Nunavik Inuit Health Survey 2004/Qanuipittaa? How are
we? Nutrition and food consumption among the Inuit of Nunavik: Institut national
de santé publique du Québec (INSPQ) et Nunavik Regional Health Board and Social
Services (NRHBSS) p. 143.
Blanton, R.E., Wachira, T.M., Zeyhle, E.E., Njoroge, E.M., Magambo, J.K., Schantz, P.M.,
1998. Oxfendazole treatment for cystic hydatid disease in naturally infected animals.
Antimicrob. Agents Chemother. 42 (3), 601–605.
Boje, J., Riget, F., KØie, M., 1997. Helminth parasites as biological tags in population studies
of Greenland halibut (Reinhardtius hippoglossoides) (Walbaum) in the north-west Atlantic.
ICES J. Mar. Sci. 54, 886–895.
Born, E.W., Henriksen, A.A., 1990. Prevalence of Trichinella sp. in polar bears (Ursus mariti-
mus) from northeastern Greenland. Polar. Res. 8 (2), 313–315.
Born, E.W., Clausen, B., Henriksen, S.A., 1982. Trichinella infection in a hunting community
in East Greenland. Z. Saugetierkd. 47, 246–251.
Bouchet, F., Lefèvre, C., West, D., Corbett, D., 1999. First paleoparasitological analysis of a
midden in the Aleutian Islands (Alaska): results and limits. J. Parasitol. 85, 369–372.
Bouchet, F.,West, D., Lefèvre, C., Corbett, D., 2001. Identification of parasitoses in a child burial
from Adak Island (Central Aleutian Islands, Alaska). C.R. Acad. Sci. III 324, 123–127.
Bowie, W.R., King, A.S., Werker, D.H., Isaac-Renton, J.L., 1997. Outbreak of toxoplasmosis
associated with municipal drinking water. Lancet 350, 173–177.
Braestrup, F.W., 1941. A study on the Arctic fox in Greenland: immigrations, fluctuations in
numbers based mainly on trading statistics. Medd Grønl. 131 (4), 1–101.
Brandly, P.J., Rausch, R., 1950. A preliminary note on Trichinosis investigations in Alaska.
Arctic 3 (2), 105–107.
Brassard, P., Hoey, J., Ismail, J., Gosselin, F., 1985. The prevalence of intestinal pathogens and
enteropathogenic bacteria in James Bay Cree Indians, Quebec. Can. J. Public Health 76,
Britov,V.A., 1962. On the role played by fishes and crustaceans in the transmission of trichi-
nosis to marine animals. Zool. Zh. 41 (5), 776–777 [Russian]. Canadian Translation of
Fisheries and Aquatic Sciences No. 5617, 1994.
Britov,V.A., Boev, S.N., 1972. Taxonomic rank of various strains of Trichinella and their cir-
culation in nature.Vestn. Akad. Nauk. SSSR 28, 27–32 [In Russian].
Brook, R.K., Kutz, S.J., Millins, C.,Veitch, A.M., Elkin, B.T., Leighton, F.A., 2010. Evaluation
and delivery of domestic animal health services in remote communities in the North-
west Territories: a case study of status and needs. Can.Vet. J. 51 (10), 1115–1122.
Brown, M., 1949. Medical investigation at Southampton Island. Arctic 2 (1), 70–71.
Brown, M., Cronk, B., Desinner, F., Green, J.E., Gibbons, J.E., Kuitunen-Ekbaum, E., 1949.
Trichinosis on Southhampton Island, N.W.T. Can. J. Public Health 40, 508–514.
Brown, M., Sinclair, R.G., Cronk, L.B., Clark, G.C., Kuitunen-Ekbaum, E., 1948. Intesti-
nal parasites of Eskimos on Southampton Island, Northwest Territories. Can. J. Public
Health 39, 451–454.
Brown, M., Green, J.E., Boag, T.J., Kuitunen-Ekbaum, E., 1950. Parasitic infections in the
Eskimos at Igloolik, N.W.T. Can. J. Public Health 41, 508–512.
Brunetti, E., Kern, P., Vuitton, D.A.Writing Panel for the WHO-IWGE, 2010. Expert con-
sensus for the diagnosis and treatment of cystic and alveolar echinococcosis in humans.
Acta Trop. 114, 1–16.
Bryan, H.M., Darimont, C.T., Paquet, P.C., Ellis, J.A., Goji, N., Gouix, M., Smits, J.E., 2011.
Exposure to infectious agents in dogs in remote coastal British Columbia: possible sen-
tinels of diseases in wildlife and humans. Can. J.Vet. Res. 75 (1), 11–17.
180 Emily J. Jenkins et al.

Burek, K.A., Gulland, F.M.D., O’Hara, T.M., 2008. Effects of climate change on Arctic
marine mammal health. Ecol. Appl. 18 (2) Supplement, S126–S134.
Burrows, M.T., Schoeman, D.S., Buckley, L.B., Moore, P., Poloczanska, E.S., Brander, K.M.,
2011. The pace of shifting climate in marine and terrestrial ecosystems. Science 334,
Butler, C.E., Khan, R.A., 1992. Prevalence of Trichinella spiralis in black bears (Ursus america-
nus) from Newfoundland and Labrador, Canada. J. Wildl. Dis. 28, 474–475.
Callaghan, T.V., Björn, L.O., Chernov, Y., Chapin, T., Christensen, T.R., Huntley, B., Ims,
R.A., Johansen, M., Jolly, D., Jonasson, S., Matveyeva, N., Panikov, N., Oechel,W., Shaver,
G., Heikki, H., 2004. Effects on the structure of Arctic ecosystems in the short- and
long-term perspectives. Ambio 33, 436–447.
Cameron, T.W.M., 1960. The incidence and diagnosis of hydatid cyst in Canada. Echinococcus
granulosus var. canadensis. Parassitologia 2, 381–390.
Cameron, T.W.M., Parnell, I.W., Lyster, L.L., 1940. The helminth parasites of sledge-dogs in
northern Canada and Newfoundland. Can. J. Res. 18, 325–332.
Campagna, S., Lévesque, B., Anassour-Laouan-Sidi, E., Côté, S., Serhir, B.,Ward, B.J., Libman,
M.D., Drebot, M.A., Makowski, K., Andonova, M., Ndao, M., Dewailly, E., 2011. Serop-
revalence of 10 zoonotic infections in 2 Canadian Cree communities. Diagn. Microbiol.
Infect. Dis. 70 (2), 191–199.
Capo, V., 1996. Clinical aspects of infection with Trichinella spp. Clin. Microbiol. Rev. 9,
Castrodale, L., 2003. Echinococcosis in Alaska. State of Alaska epidemiology bulletin. In:
Middaugh, J. (Ed.), State of Alaska Epidemiology,
Castrodale, L.J., Beller, M., Wilson, J.F., Schantz, P.M., McManus, D.P., Zhang, L.-H., Fallico,
F.G., Sacco, F.D., 2002. Two atypical cases of cystic echinococcosis (Echininococcus granu-
losus) in Alaska, 1999. Am. J. Trop. Med. Hyg. 66, 325–327.
Chadee, K., Dick, T.A., 1982. Designation and freezing resistance of isolates of Trichinella
spiralis from wild carnivores. J. Wildl. Dis. 18, 169–173.
Chai, J.Y., Murrell, K.D., Lymbery, A.J., 2005. Fish-borne parasitic zoonoses: status and issues.
Int. J. Parasitol. 35, 1233–1254.
Chan, H., Fediuk, K., Hamilton, S., Rostas, L., Caughey, A., Kuhnlein, H., Egeland, G.,
­Loring, E., 2006. Food security in Nunavut, Canada: barriers and recommendations. Int.
J. Circumpolar Health 65 (5), 416–431.
Chavez, F.P., Ryan, J., Lluch-Cota, S.E., Miguel Ñiquen, C., 2003. From anchovies to sardines
and back: mutildecadal change in the Pacific Ocean. Science 299, 217–221.
Ching, H.L., 1984. Fish tapeworm infections (diphyllobothriasis) in Canada, particularly
British Columbia. Can. Med. Assoc. J. 130, 1125–1127.
Chomel, B.B., Zarnke, R.L., Kasten, R.W., Kass, P.H., Mendes, E., 1995. Serologic survey of
Toxoplasma gondii in grizzly bears (Ursus arctos) and black bears (Ursus americanus) from
Alaska, 1998 to 1991. J. Wildl. Dis. 31 (4), 472–479.
Chomel, B.B., Kasten, R.W., Chappuis, G., Soulier, M., Kikuchi, Y., 1998. Serological
survey of selected canine viral pathogens and zoonoses in grizzly bears (Ursus arc-
tos horribilis) and black bears (Ursus americanus) from Alaska. Rev. Sci. Tech. 17 (3),
Choquette, L.P.E., Moynihan,W.A., 1964. Control of disease in dogs in the Canadian North.
Can.Vet. J. 5, 262–267.
Choquette, L.P.E., Whitten, L.K., Rankin, G., Seal, C.M., 1957. Notes on parasites found in
reindeer (Rangifer tarandus) in Canada. Can. J. Comp. Med. 21, 199–203.
Choquette, L.P.E., Macpherson, A.H., Cousineau, J.G., 1962. Note on the occurrence of
Echinococcus multilocularis Leuckart, 1863 in the Arctic fox in Canada. Can. J. Zool. 40
(6), 1167.
Arctic Zoonoses 181

Choquette, L.P.E., Gibson, G.G., Pearson, A.M., 1969. Helminths of the grizzly bear, Ursus
arctos L., in northern Canada. Can. J. Zool. 47, 167–170.
Choquette, L.P.E., Gibson, G.G., Kuyt, E., Pearson, A.M., 1973. Helminths of wolves, Canis
lupus L., in the Yukon and Northwest Territories. Can. J. Zool. 51, 1087–1091.
Clark, P.S., Brownsberger, K.M., Saslow, A.R., Kagan, I.G., Noble, G.R., Maynard, J.E., 1972.
Bear meat trichinosis: epidemiologic, serologic, and clinical observations from two Alas-
kan outbreaks. Ann. Intern. Med. 76, 951–956.
Clausen, B., Hjort, P., 1986. Survey for antibodies against various infectious disease agents in
muskoxen (Ovibos moschatus) from Jamesonland, Northeast Greenland. J. Wildl. Dis. 22
(2), 264–266.
Coffey, J.E., Wigglesworth, F.W., 1956. Trichinosis in Canadian Eskimos. Can. Med. Assoc.
J. 75, 295–299.
Colli, C.W., Williams, J.F., 1972. Influence of temperature on the infectivity of Echinococcus
granulosus in laboratory rodents. J. Parasitol. 58, 422–426.
Connell, F.H., 1949. Trichinosis in the Arctic: a review. Arctic 2, 98–107.
Couture, C., Measures, L., Gagnon, J., Desbiens, C., 2003. Human intestinal anisakiosis due
to consumption of raw salmon. Am. J. Surg. Pathol. 27, 1167–1172.
Cox, D.M., Holland, C.V., 2001. Relationship between three intensity levels of Toxocara
canis larvae in the brain and effects on exploration, anxiety, learning and memory in the
murine host. J. Helminthol. 75, 33–41.
Curtis, M.A., 1984. A report on the results of parasite survey on cod (Gadus morhua) from
the Killiniq experimental fishery. Institute of Parasitology, McDonald College, McGill
Curtis, M.A., Bylund, G., 1991. Diphyllobothriasis: fish tapeworm disease in the circumpolar
north. Arctic Med. Res. 50, 18–24.
Curtis, M.A., Rau, M.E., Tanner, C.E., Prichard, R.K., Faubert, G.M., Olpinski, S., et al.,
1988. Parasitic zoonoses in relation to fish and wildlife harvesting by Inuit communities
in northern Quebec, Canada. Arctic Med. Res. 47, 693–696.
Dalen, L., Fuglei, E.V.A., Hersteinsson, P., M.O Kapel, C., D Roth, J., Samelius, G., Tanner-
feldt, M., Angerbjorn, A., 2005. Population history and genetic structure of a circumpo-
lar species: the Arctic fox. Biol. J. Linn. Soc. 84 (1), 79–89.
Darimont, C.T., 2005. Range expansion by moose into coastal temperate rainforests of Brit-
ish Columbia, Canada. Divers. Distrib. 11, 235–239.
Daszak, P., Cunningham, A.A., Hyatt, A.D., 2000. Emerging infectious diseases of wildlife–
threats to biodiversity and human health. Science 287 (5452), 443–449.
Dau, J., 1981. Toxascaris and Toxocara. In Alaskan Wildlife Diseases. University of Alaska, Fair-
banks 128–131.
Davey, J.T., 1971. A case of Anisakis sp. infection in a brown bear from Alaska. Trans. R. Soc.
Trop. Med. Hyg. 65 (4), 433–434.
Davidson, R.K., Handeland, K., Kapel, C.M., 2008. High tolerance to repeated cycles of
freezing and thawing in different Trichinella nativa isolates. Parasitol. Res. 103, 1005–1010.
Davidson, R., Simard, M., Kutz, S.J., Kapel, C.M.O., Hamnes, I.S., Robertson, L.J., 2011.
Arctic parasitology: why should we care? Trends Parasitol. 27 (6), 239–245.
Davidson, R.K., Romig, T., Jenkins, E.J., Tryland, M., Robertson, L.J., 2012. The impact of
globalization on the distribution of Echinococcus multilocularis. Trends Parasitol. 28 (6),
Davies, L.E.C., Cameron, T.W.M., 1961. Trichinosis in Northwest Territories. Medical Ser-
vices Journal Canada 17, 99–104.
Davies, R.B., Hibler, C.P., 1979. Animal reservoirs and cross-species transmission of Giardia.
In: Jakubowski, W., Hoff, J.C. (Eds.), Waterborne Transmission of Giardiasis, Environ-
mental Protection Agency, Cincinnati, USA, pp. 104–126.
Davis, T.R.A., 1957. Hydatid disease in Alaska. Am. J. Med. 23, 99–106.
182 Emily J. Jenkins et al.

Deardorff, T.L., Kent, M.L., 1989. Prevalence of larval Anisakis simplex in pen-reared and
wild-caught salmon (Salmonidae) from Puget Sound, Washington. J. Wildl. Dis. 25,
Delecluse, P., 2008. The origin of climate changes. World Organization for Animal Health
(OIE). Rev. Sci. Tech. OIE 27 (2), 309–317.
Deliamure, S.L., Yurakhno, M., Popov, V.N., Shults, L.M., Fay, F.H., 1984. Helminthological
comparison of subpopulations of Bering Sea spotted seals, Phoca largha Pallas. In: Fay,
F.H., Fedoseev, G.A. (Eds.), Soviet-American Cooperative Research on Marine mam-
mals, vol. 1. NOAA Tech Report, National Marine Fisheries 12, Washington, D.C.
pp. 61–65.
Deliamure, S.L., Skriabin, A.S., Serdiukov, 1985. Difillobotriidy-lentochnye gel’minty che-
loveka, mlekopitaiushchikh i ptits. vol. 11. Osnovy Tsestodologii. Akademiia Nauk
SSSR, Nauka, Moskva, USSR.
Desdevises,Y., Arthur, R.J., Pellerin-Massicotte, J., 1998. Parasites of Anadromous Arctic Char
(Salvelinus alpinus) from two sites in Ungava Bay (Quebec, Canada). J. Helminthol. Soc.
Wash. 65 (1), 87–90.
Desowitz, R.S., 1986. Human and experimental anisakiasis in the United States. Hokkaido
Igaku Zasshi. 61 (3), 358–371.
Despommier, D., 2003. Toxocariasis: clinical aspects, epidemiology, medical ecology, and
molecular aspects. Clin. Microbiol. Rev. 16 (2), 265–272.
Desrochers, F., Curtis, M.A., 1987.The occurrence of gastrointestinal helminths in dogs from
Kuujjuaq (Fort Chimo), Quebec, Canada. Can. J. Public Health 78 (6), 403–406.
Dick, T.A., 1983. Infectivity of isolates of Trichinella and the ability of an arctic isolate to sur-
vive freezing temperatures in the raccoon, Procyon lotor, under experimental conditions.
J. Wildl. Dis. 19, 333–336.
Dick, T., 2008. Diphyllobothriasis: the Diphyllobothrium latum human infection conundrum
and reconciliation with a worldwide zoonosis. In: Murrell, K.D., Freid, B. (Eds.), Food-
borne Parasitic Zoonoses: Fish and Plant-borne Parasites (world class parasites), vol. 11.
Springer, London, pp. 151–184.
Dick,T.A., Belosovic, M., 1978. Observations on a Trichinella spiralis isolate from a polar bear.
J. Parasitol. 64, 1143–1145.
Dick, T.A., Poole, B.C., 1985. Identification of Diphyllobothrium dendriticum and Diphylloboth-
rium latum from some freshwater fishes of central Canada. Can. J. Zool. 63, 196–201.
Dick, T.A., Pozio, E., 2001. Trichinella spp. and trichinosis. In: Samuel, W.M., Pybus, M.J.,
Kocan, A.A. (Eds.), Parasitic Diseases of  Wild Mammals, second ed. Iowa State Univer-
sity Press, Ames, Iowa, pp. 380–396.
Dick, T.A., Nelson, P.A., Choudhury, A., 2001. Diphyllobothriasis: update on human cases,
foci, patterns and sources of human infections and future considerations. SE Asia J. Trop.
Med. Publ. Hlth. 32, 59–76.
Dies, K.H., 1979. Helminths recovered from black bears in the Peace River region of north-
western Alberta. J. Wldlf. Dis. 15, 49–50.
Dies, K., 1980. Survival of Trichinella spiralis larvae in deep-frozen wolf tissue. Can.Vet. J. 21, 38.
Diker, A.J., Tinar, R., Senlik, B., 2007. Viability of Echinococcus granulosus protoscolices at
different conditions.Vet. Parasitol. 150, 84–87.
Dixon, B., Parrington, L., Parenteau, M., Leclair, D., Santin, M., Fayer, R., 2008. Giardia
duodenalis and Cryptosporidium spp. in the intestinal contents of ringed seals (Phoca
hispida) and bearded seals (Erignathus barbatus) in Nunavik, Quebec, Canada. J. Parasitol.
94, 1161–1163.
Doan, K., Douglas, C.W., 1953. Beluga of the Churchill Region of Hudson Bay. Fish. Res.
Bd. Can. Bull. 98, 27.
Doyle, P.M., Beuchat, L.R. (Eds.), 2007. Food Microbiology: Fundamentals and Frontiers,
ASM Press, Washington D.C.
Arctic Zoonoses 183

Dubey, J.P., 2009. Toxoplasmosis of Animals and Humans. CRC Press.

Dubey, J.P., Miller, N.L., Frenkel, J.K., 1970. Characterization of the new fecal form of Toxo-
plasma gondii. J. Parasitol. 56, 447–456.
Dubey, J.P., Lewis, B., Beam, K., Abbitt, B., 2002. Transplacental toxoplasmosis in a reindeer
(Rangifer tarandus) fetus.Vet. Parasitol. 110 (1–2), 131–135.
Dubey, J.P., Zarnke, R., Thomas, N.J., Wong, S.K., Van Bonn, W., Briggs, M., Davis, J.W.,
Ewing, R., Mensea, M., Kwok, O.C.H., Romand, S.,Thulliez, P., 2003. Toxoplasma gondii,
Neospora caninum, Sarcocystis neurona, and Sarcocystis canis-like infections in marine mam-
mals.Vet. Parasitol. 116, 275–296.
Dubey, J.P., Quirk, T., Pitt, J.A., Sundar, N., Velmurugan, G.V., Kwok, O.C.H., Leclair, D.,
Hill, R., Su, C., 2008. Isolation and genetic characterization of Toxoplasma gondii from
raccoons (Procyon lotor), cats (Felis domesticus), striped skunk (Mephitis mephitis), black bear
(Ursus americanus), and cougar (Puma concolor) from Canada. J. Parasitol. 94 (1), 42–45.
Dubey, J.P., Rajendran, C., Ferreira, L.R., Kwok, O.C., Sinnett, D., Majumdar, D., Su, C.,
2010. A new atypical highly mouse virulent Toxoplasma gondii genotype isolated from a
wild black bear in Alaska. J. Parasitol. 96 (4), 713–716.
Dubey, J.P., Velmurugan, G.V., Rajendran, C., Yabsley, M.J., Thomas, N.J., Beckmen, K.B.,
Sinnett, D., Ruid, D., Hart, J., Fair, P.A., McFee, W.E., Shearn-Bochsler, V., Kwok,
O.C.H., Ferreira, L.R., Choudhary, S., Faria, E.B., Zhou, H., Felix, T.A., Su, C., 2011.
Genetic characterisation of Toxoplasma gondii in wildlife from North America revealed
widespread and high prevalence of the fourth clonal type. Int. J. Parasitol. 41, 1139–1147.
Dubinina, M.N., 1966. Tapeworms (Cestoda, Ligulidae) of the fauna of the USSR. Nauka
Publishers, Moscow [English Translation (1980), Amerind Publishing Company, New
Due, T.T., Curtis, M.A., 1995. Parasites of freshwater resident and anadromous Arctic charr
(Salvelinus alpinus) in Greenland. J. Fish Biol. 46, 578–592.
Dunams-Morel, D.B., Richard, M.V., Toretti, L., Zarlenga, D.S., Rosenthal, B.M., 2012.
Discernible but limited introgression has occurred where Trichinella nativa and the T-6
genotype occur in sympatry. Infect. Genet. Evol. 12, 530–538.
Dupouy-Camet, J., Kociecka, W., Bruschi, F., Bolas-Fernandez, F., Pozio, E., 2002. Opinion
on the diagnosis and treatment of human trichinellosis. Expert Opin. Pharmacother. 3,
Dziekońska-Rynko, J., Rokicki, J., 2007. Life cycle of the nematode Contracaecum rudolphii
Hartwig, 1964 (sensu lato) from northern Poland under laboratory conditions. Helmin-
thologia 44 (3), 95–102.
Eaton, R.D.P., 1976. Endemic Giardiasis in Northern Canada. Canada Diseases Weekly
Report 2–32, pp. 125–126.
Eaton, R.D., Meerovitch, E., 1982.The changing face of parasitism among Canadian aborig-
ines. In: Meerovitch, E. (Ed.), Aspects of Parasitology: A Festschrift Dedicated to the
Fiftieth Anniversary of the Institute of Parasitology of McGill University, 1932–1982,
The Institute of Parasitology, Montreal, pp. 71–90.
Eaton, R.D.P., Secord, D.C., 1979. Some intestinal parasites of arctic fox, Banks Island. N.W.T.
Can. J. Comp. Med. 43, 229–230.
Eckert, J., Deplazes, P., 2004. Biological, epidemiological, and clinical aspects of Echinococ-
cosis, a zoonosis of increasing concern. Clin. Microbiol. Rev. 17 (1), 107–135.
Eckert, J., Conraths, F.J., Tackmann, K., 2000. Echinococcosis: an emerging or re-emerging
zoonosis? Int. J. Parasitol. 30 (12–13), 1283–1294.
Eckert, J., Schantz, P.M., Gasser, R.B., Torgerson, P.R., Bessonov, A.S., Movsessian, S.O.,
Thakur, A., Grimm, F., Nikogossian, M., 2001. Chapter 4: Geographic Distribution and
Prevalence. In WHO/OIE Manual on Echinococcosis in Humans and Animals. World
Organisation for Animal Health (Office International des Epizooties) and World Health
Organization, Paris, France 100–142.
184 Emily J. Jenkins et al.

Egeland, G.M.Inuvialuit Settlement Region Steering Committee, 2010a. Inuit Health Sur-
vey 2007–2008. Inuvialuit Settlement Region. McGill University, Ste-Anne-de-Bel-
levue, QC
Egeland, G.M.Nunatsiavut Steering Committee, 2010b. Inuit Health Survey 2007–2008
Nunatsiavut. McGill University, Ste-Anne-de-Bellevue, QC.
Elmore, S.A., Jenkins, E.J., Huyvaert, K.P., Polley, L., Root, J.J., Moore, C.G., 2012. Toxo-
plasma gondii in people and wildlife of the circumpolar North. Vector-borne Zoonot.
12 (1), 1–9.
Elwin, K., Hadfield, S.J., Robinson, G., Crouch, N.D., Chalmers, R.M., 2012. Cryptospo-
ridium viatorum n. sp. (Apicomplexa: Cryptosporidiidae) among travellers returning to
Great Britain from the Indian subcontinent, 2007–2011. Int. J. Parasitol. 42 (7), 675–682.
Emmott, F., Eaton, R.D.P., 1977. Trichinosis in the Northwest Territories. Can. Dis. Wkly.
Rep. 3, 14–15.
Emson, H.E., Baltzan, M.A., Wiens, H.E., 1972. Trichinosis in Saskatchewan: an outbreak
due to infected bear meat. Can. Med. Assoc. J. 106, 897–898.
Fanning, M., Hill, A., Langer, H.M., Keystone, J.S., 1981.Visceral larva migrans (toxocariasis)
in Toronto. Can. Med. Assoc. J. 124, 21–27.
Fay, F.H., 1960. Carnivorous walrus and some Arctic zoonoses. Arctic 13 (2), 111–122.
Fay, F.H., 1968. Experimental transmission of Trichinella spiralis via marine amphipods. Can.
J. Zool. 46, 597–599.
Fay, F.H.,Williamson, F.S.L., 1962. Studies on the helminth fauna of Alaska: XXXIX. Echino-
coccus multilocularis Leuckart, 1863, and other helminths of foxes on the Pribilof Islands.
Can. J. Zool. 40 (5), 767–772.
Fay, F.H., Sease, J.L., Merrisck, R.L., 1990. Predation on a ringed seal, Phoca hispida, and a
black guillemot, Cepphus grylle, by a Pacific walrus, Odobenus rosmarus divergens. Mar.
Mamm. Sci. 6 (4), 348–350.
Fayer, R., 2010. Taxonomy and species delimitation in Cryptosporidium. Exp. Parasitol. 124,
Fayer, R., Dubey, J.P., Lindsay, D.S., 2004. Zoonotic protozoa: from land to sea. Trends Para-
sitol. 20, 531–536.
Feldman, H.A., 1974. Toxoplasmosis: an overview. Acad. Med. 50 (2), 110–127.
Feney-Rodriguez, S., Ceullar del Hoyo, C., Guillen Llera, J.L., 1988. Comparative study of
the influence of light on embryonization of Toxocara canis, Toxascaris leonina and Ascaris
suum. Revista Iberica De Parasitologia 48, 395–401.
Feng, Y., Xiao, L., 2011. Zoonotic potential and molecular epidemiology of Giardia species
and giardiasis. Clin. Microbiol. Rev. 24 (1), 110. doi: 10.1128/CMR.00033-10.
Finlay, J.C., Speert, D.P., 1992. Sylvatic hydatid disease in children: case reports and review
of endemic Echinococcus granulosus infection in Canada and Alaska. Pediatr. Infect. Dis.
J. 11, 322–326.
Fleischman, R.W., Squire, R.A., 1970. Verminous pneumonia in the California sea lion
(Zalophus californianus). Pathol.Vet. 7, 89–101.
Forbes, L., 2000.The occurrence and ecology of Trichinella in marine mammals.Vet. Parasitol.
93 (3–4), 321–334.
Forbes, L.B., Measures, L., Gajadhar, A., Kapel, C., 2003. Infectivity of Trichinella nativa in
traditional northern (country) foods prepared with meat from experimentally infected
seals. J. Food Prot. 66, 1857–1863.
Fortuine, R., 1961. Current status of animal-borne diseases among the Eskimos. Can.
J. Comp. Med.Vet. Sci. 25 (7), 185–189.
Fournelle, H.J., Wallace, I.L., Rader,V., 1958. A bacteriological and parasitological survey of
enteric infections in an Alaskan Eskimo area. Am. J. Public Health 48, 1489–1497.
Fournelle, H.J., Rader, V., Allen, C., 1959. Seasonal study of enteric infections in Alaskan
Eskimos. Public Health Rep. 74, 55–59.
Arctic Zoonoses 185

Franzén, O., Jerlström-Hultqvist, J., Castro, E., Sherwood, E., Ankarklev, J., Reiner, D.S.,
Palm, D., Andersson, J.O., S D. Palm, J.O., Svärd, S.G., 2009. Draft genome sequencing of
Giardia intestinalis Assemblage B isolate GS: is human giardiasis caused by two different
species? PLoS Pathog. 5 (8), e1000560.
Frechette, J.E., Rau, M.E., 1977. Helminths of the black bear in Quebec. J. Wildl. Dis. 13,
Freeman, R., Jamieson, J., 1976. Parasites of Eskimos at Igloolik and Hall Beach, Northwest
Territories. Proceedings of the 3rd International Symposium on Circumpolar Health,
U of  Toronto Press,Yellowknife, NT.
Frenkel, J.K., Dubey, J.P., 1973. Effects of freezing on the viability of Toxoplasma oocysts.
J. Parasitol. 59 (3), 587–588.
Frenkel, J.K., Dubey, J.P., Miller, N.L., 1970. Toxoplasma gondii in cats: fecal stages identified
as coccidian oocysts. Science 167 (3919), 893–896.
Frenkel, J.K., Nelson, B.M., Nelson, M.D., Alarias-Stella, J., 1975. Immunosuppression and
toxoplasmic encephalitis: clinical and experimental aspects. Hum. Pathol. 6, 97–111.
Furgal, C., Prowse,T.D., 2008. Northern Canada. In: Lemmen, D.S. (Ed.), From Impacts to Adap-
tation: Canada in a Changing Climate, Government of Canada, Ottawa, ON, pp. 57–118.
Gajadhar, A.A., Forbes, L.B., 2010. A 10-year wildlife survey of 15 species of Canadian car-
nivores identifies new hosts or geographic locations for Trichinella genotypes T2, T4, T5,
and T6.Vet. Parasitol. 168, 78–83.
Gajadhar, A.A., Bisaillon, J.R., Appleyard, G.D., 1997. Status of Trichinella spiralis in domestic
swine and wild boar in Canada. Can. J.Vet. Res. 61, 256–259.
Gamble,W.G., Segal, M., Schantz, P.M., Rausch, R.L., 1979. Alveolar hydatid disease in Min-
nesota: first human case acquired in the contiguous United States. J. Am. Med. Assoc.
241 (9), 904–907.
Gamboa, M.I., 2005. Effects of temperature and humidity on the development of eggs of
Toxocara canis under laboratory conditions. J. Helminthol. 79, 327–331.
Gau, R.J., Kutz, S., Elkin, B.T., 1999. Parasites in grizzly bears from the central Canadian
Arctic. J. Wildl. Dis. 35, 618–621.
Gaulin, C., Picard, I., Huot, M., Proulx, J.-F., 2006. Outbreak of Trichinellosis, in French
hunters who ate Canadian black bear meat. CCDR 32 (9), 109–112.
Gaydos, J.K., Conrad, P.A., Gilardi, K.V., Blundell, G.M., Ben-David, M., 2007. Does human
proximity affect antibody prevalence in marine-foraging river otters (Lontra canadensis)?
J. Wildl. Dis. 43 (1), 116–123.
Gemmell, M.A., 1973. Surveillance of Echinococcus granulosus in dogs with arecoline hydro-
bromide. Bull. Wld. Hlth. Org. 48, 649–652.
Ghadrian, E., Viens, P., Strykowski, H., Dubreuil, F., 1976. Epidemiology of toxocariasis in
the Montreal area. Prevalence of Toxocara and other helminth ova in dogs and soil. Can.
J. Public Health 67, 495–498.
Gibbs, H.C., Tener, J.S., 1958. On some helminth parasites collected from the muskox
(Ovibos moschatus) in the Thelon Game Sanctuary, Northwest Territories. Can. J. Zool.
36, 529–532.
Gilbert, N.L., Oluwayemisi, K.D., Libman, M.D., Muchaal, P.K., Ogden, N.H., 2010.
­Hospitalization for trichinellosis and echinococcosis in the Canadian Arctic, 2001–2005:
the tip of the iceberg? Can. J. Public Health 101 (4), 337–340.
Gilg, O., Moreau, J., Aars, J., Gauthier, G., Gremillet, D., Ims, R.A., et al., 2012. Climate change
and the ecology and evolution of Arctic vertebrates. Ann. N.Y. Acad. Sci. 1249, 166–190.
Gillespie, S.H., 1988. The epidemiology of Toxocara canis. Parasitol. Today 4, 180–182.
Giraudoux, P., Craig, P.S., Delattre, P., Bao, G., Bartholomot, B., Harraga, S., Quere, J.-P.,
Raoul, F., Wang,Y., Shi, D.,Vuitton, D.A., 2004. Interactions between landscape changes
and host communities can regulate Echinococcus multilocularis transmission. Parasitology
127 (S1), 121–131.
186 Emily J. Jenkins et al.

Gjertz, I., 1990. Walrus predation of seabirds. Polar Rec. 26 (159), 317.
Glickman, L.T., Schantz, P.M., 1981. Epidemiology and pathogenesis of zoonotic toxocaria-
sis. Epidemiol. Rev. 3, 230–250.
Goldstein,T., Gill,V.A.,Tuomi, P., Monson, D., Burdin, A., Conrad, P.A., Dunn, J.L., Field, C.,
Johnson, C., Jessup, D.A., Bodkin, J., Doroff, A.M., 2011. Assessment of clinical pathology
and pathogen exposure in sea otters (Enhydra lutris) bordering the threatened population
in Alaska. J. Wildl. Dis. 47 (3), 579–592.
Gottstein, B., Pozio, E., Nöckler, K., 2009. Epidemiology, diagnosis, treatment, and control of
Trichinellosis. Clin. Microbiol. Rev. 22, 127–145.
Graczyk, T.K., Fayer, R., Trout, J.M., Lewis, E.J., Farley, C.A., Sulaiman, I., Lal, A.A., 1998.
Giardia sp. cysts and infectious Cryptosporidium parvum oocysts in the feces of migratory
Canada Geese (Branta canadensis). Appl. Environ. Microbiol. 64 (7), 2736–2738.
Graczyk, T.K., Majewska, A.C., Schwab, K.J., 2008. The role of birds in dissemination of
human waterborne enteropathogens. Trends Parasitol. 4 (2), 55–59.
Gyorkos, T.W., Faubert, G., 1980. Serological investigations for five selected parasitic infec-
tions in Inuvik and Arctic Bay/Strathcona Sound, Northwest Territories. Can. Dis.Wkly.
Rep. 6, 134–136.
Gyorkos, T.W., MacLean, J.D., Serhir, B., Ward, B., 2003. Prevalence of parasites in Can-
ada and Alaska; epidemiology, past and present. In: Akuffo, H., Linder, E., Ljungstrom,
Wahlgren, M. (Eds.), Parasites of the Colder Climates, Taylor and Francis, London,
pp. 77–88.
Hadwen, S., 1932. Untitled note on parasites of moose. In Proceedings of the Helminth
Society of  Washington, J. Parasitol. 19, 83.
Hall-Baker, P.A., Nives, H., Jajosky, R.A., Adams, D.A., Sharp, P., Anderson, W.J., et al., 2010.
Summary of notifiable diseases – United States, 2008. MMWR 57 (54), 1–94.
Hall-Baker, P.A., Groseclose, S.L., Adams, D.A., Sharp, P., Anderson, W.J., et al., 2011. Sum-
mary of notifiable diseases – United States, 2009. MMWR 58 (53), 1–100.
Hanni, K.D., Mazet, J.A., Gulland, F.M., Estes, J., Staedler, M., Murray, M.J., Miller, M., Jessup,
D.A., 2003. Clinical pathology and assessment of pathogen exposure in southern and
Alaskan sea otters. J. Wildl. Dis. 39 (4), 837–850.
Harper, T., Ruttan, R., Benson, W., 1955. Hydatid Disease (Echinococcus granulosus) in Sas-
katchewan big game. Trans. 20th N. Am. Wildl. Conf, 198–208.
Hays, R., Measures, L.N., Huot, J., 1998. Euphausiids as intermediate hosts of Anisakis sim-
plex in the St. Lawrence estuary. Can. J. Zool. 76, 1226–1235.
Heckmann, R., Otto, T., 1985. Occurrence of anisakid larvae (Nematoda: Ascaridida) in
fishes from Alaska and Idaho. Great Basin Nat. 45 (3), 427–431.
Heinzig, L., 1996. A case of trichinosis. EpiNorth 8, 7.
Henttonen, H., Fuglei, E., Gower, C.N., Haukisalmi, V., Ims, R.A., Niemimaa, J., Yoccoz,
N.G., 2001. Echinococcus multilocularis on Svalbard: introduction of an intermediate host
has enabled the local life-cycle. Parasitology 123 (06), 547–552.
Herreman, J.K., McIntosh, A.D., Dziuba, R.K., Blundell, G.M., Ben-David, M., Greiner,
E.C., 2011. Parasites of harbor seals (Phoca vitulina) in Glacier Bay and Prince William
Sound, Alaska. Mar. Mamm. Sci. 27 (1), 247–253.
Hersteinsson, P., Macdonald, D.W., 1992. Interspecific competition and the geographical
distribution of red and arctic foxes Vulpes vulpes and Alopex lagopus. Oikos 64, 505–515.
Herwaldt, B.L., Craun, G.F., Stokes, S.L., Juranek, D.D., 1992. Outbreaks of waterborne dis-
ease in the United States, 1989 – 1990. J. Am. Wat. Wks. Assoc. 84, 129–135.
Hicks, F.J., Threlfall, W., 1973. Metazoan parasites of salmonids and coregonids from coastal
Labrador. J. Fish. Biol. 5, 399–415.
Hildreth, M.B., Sriram, S., Gottstein, B., Wilson, M., Schantz, P.M., 2000. Failure to identify
alveolar echinococcosis in trappers from South Dakota in spite of high prevalence of
Echinococcus multilocularis in Wild Canids. J. Parasitol. 86 (1), 75–77.
Arctic Zoonoses 187

Hilliard, D.K., 1960. Studies on the helminth fauna of Alaska. XXXVIII. The taxonomic
significance of eggs and coracidia of some diphyllobothriid cestodes. J. Parasitol. 46,
Himsworth, C.G., Jenkins, E.J., Hill, J.E., Nsungu, M., Thompson, R.C.A., Covacin, C.,
Ash, A., Wagner, B.A., McConnell, A., Leighton, F.A., Skinner, S., 2010a. Emergence
of sylvatic Echinococcus granulosus as a parasitic zoonosis of public health concern in an
Indigenous community in Canada. Am. J. Trop. Med. Hyg. 82 (4), 643–645.
Himsworth, C.G., Skinner, S., Chaban, B., Jenkins, E., Wagner, B.A., Harms, N.J., Leighton,
F.A., Thompson, R.C.A., Hill, J.E., 2010b. Multiple zoonotic pathogens identified in
canine feces collected from a remote Canadian indigenous community. Am. J.Trop. Med.
Hyg. 83 (2), 338–341.
Hitchcock, D.J., 1950. Parasitological study on the Eskimos in the Bethel area of Alaska.
J. Parasitol. 36, 232–234.
Hitchcock, D.J., 1951. Parasitological study on the Eskimos in the Kotzebue area of Alaska.
J. Parasitol. 37, 309–311.
Hoberg, E.P., 1996. Faunal diversity among avian parasite assemblages: the interaction of
history, ecology, and biogeography in the marine realm. Bull. Scand. Soc. Parasitol. 6,
Hoberg, E.P., 2005. Marine birds and their helminths. In: Rohde, K. (Ed.), Marine Parasitol-
ogy, CSIRO Publishing, Collingwood, pp. 414–420.
Hoberg, E.P., 2010. Invasive processes, mosaics and the structure of helminth parasite faunas.
Rev. Sci. Tech. OIE 29, 255–272.
Hoberg, E.P., Adams, A., 2000. Phylogeny, history and biodiversity: understanding faunal
structure and biogeography in the marine realm. Bull. Scand. Soc. Parasitol. 10, 19–37.
Hoberg, E.P., Polley, L., Jenkins, E.J., Kutz, S.J., 2008a. Pathogens of domestic and free rang-
ing ungulates: global climate change in temperate to boreal latitudes across North Amer-
ica. Rev. Sci. Tech. OIE 27, 511–528.
Hoberg, E.P., Polley, L., Jenkins, E.J., Kutz, S.J., Veitch, A.M., Elkin, B.T., 2008b. Integrated
approaches and empirical models for investigation of parasitic diseases in northern wild-
life. Emerg. Infect. Dis. 14, 10–17.
Hoberg, E.P., Galbreath, K.E., Cook, J.A., Kutz, S.J., Polley, L., 2012. Northern host–parasite
assemblages: history and biogeography on the borderlands of episodic climate and envi-
ronmental transition. Adv. Parasitol. 79, 1–97.
Hoberg, E.P., Kutz, S.J., Cook, J.A., Galaktionov, K., Haukisalmi, V., Henttonen, H., Laak-
sonen, S., Makarikov, A., Marcogliese, D.J. Parasites in terrestrial, freshwater and marine
systems. In: Meltofte H. (Ed.), Arctic Biodiversity Assessment-Status and Trends in Arctic
Biodiversity. Conservation of Arctic Floral and Fauna, Arctic Council, in press.
Hochberg, N.S., Hamer, D.H., 2010. Anisakidosis: perils of the deep. Clin. Infect. Dis. 51,
Hochleim, K., Barber, D.G., Luchovich, J.V., 2010. Changing sea ice conditions in Hudson
Bay, 1980–2005. In: Ferguson, S.H., Liseto, L.L., Mallory, M.L. (Eds.), A Little less ­Arctic:
Top Predators in the World’s Largest Northern Inland Sea, Hudson Bay, Springer,
pp. 39–52.
Hockin, J., Meerovitch, E., 1982. Trichinellosis – prevalence in Labrador, Newfoundland.
Can. Dis. Wkly. Rep. 8, 201–203.
Hodgins, S., 1997. Health and what affects it in Nunavik: how is the situation changing?
Department of Public Health, Nunavik Regional Board of Health and Social Services,
Kuujjuaq, Quebec, Canada, p. 321.
Holmes, J.C., Podesta, R., 1968. The helminths of wolves and coyotes from the forested
regions of Alberta. Can. J. Zool. 46, 1193–1204.
Holmes, J.C., Mahrt, J.L., Samuel, W.M., 1971. The Occurrence of Echinococcus multilocularis
Leuckart, 1863 in Alberta. Can. J. Zool. 49 (4), 575–576.
188 Emily J. Jenkins et al.

Holt, D.W., Hanns, C., O’hara, T., Burek, K., Frantz, R., 2005. New distribution records of
Echinococcus multilocularis in the Brown lemming from Barrow, Alaska, USA. J. Wildl. Dis.
41 (1), 257.
Hotez, P.J., 2010. Neglected infections of poverty among the Indigenous peoples of the
Arctic. PLoS Negl. Trop. Dis. 4 (1), 1–6 (e606).
Hotop, A., Hiobil, H., Gross, U., 2012. Efficacy of rapid treatment initiation following pri-
mary Toxoplasma gondii infection during pregnancy. Clin. Infect. Dis. 54 (11), 1545–1552.
Houzé, S., Ancelle, T., Matra, R., Boceno, C., Carlier, Y., Gajadhar, A.A., Dupouy-Camet, J.,
2009.Trichinellosis acquired in Nunavut, Canada in September 2009: meat from grizzly
bear suspected. Euro. Surveill. 14 (44) pii = 19383.
Hueffer, K., Holcomb, D., Ballweber, L.R., Gende, S.M., Blundell, G., O'Hara, T.M., 2011.
Serologic surveillance of pathogens in a declining harbor seal (Phoca vitulina) popula-
tion in Glacier Bay National Park, Alaska, USA and a reference site. J. Wildl. Dis. 47 (4),
Hughes-Hanks, J.M., Rickard, L.G., Panuska, C., Saucier, J.R., O'Hara, T.M., Dehn, L., Rol-
land, R.M., 2005. Prevalence of Cryptosporidium spp. and Giardia spp. in five marine
mammal species. J. Parasitol. 91, 1225–1228.
Huleback, K.L., 1980. Mechanical transmission of larval Trichinella by arctic crustacea. Can.
J. Zool. 58, 1388–1390.
Hunter, P.R.,Thompson, R.C.A., 2005.The zoonotic transmission of Giardia and Cryptospo-
ridium. Int. J. Parasitol. 35, 1181–1190.
Hurrell, J.W., Kushnir,Y., Ottersen, G.,Visbeck, M., 2003. A overview of the North Atlantic
oscillation. In: Hurrell, J.H. (Ed.), The North Atlantic Oscillation: Climatic Significance
and Environmental Impact, Geophysical Monograph, vol. 134. American Geophysical
Union, pp. 1–35.
Hutchison, W.M., Dunachie, J.F., Siim, J.C., Work, K., 1969. The life cycle of Toxoplasma
gondii. Brit. Med. J. 4, 806.
Iddawela, D.R., Kumarasiri, P.V.R., Wijesundera, M., 2003. A seroepidemiological study of
toxocariasis and risk factors for infection in children in Sri Lanka. Southeast Asian J.Trop.
Med. Public Health 34, 7–15.
Irvine, J., Quinn, B., Stockdale, D., 2011. Northern Saskatchewan Health Indicators Report
2011. Athabasca Health Authority and Keewatin Yatthé and Mamawetan Churchill
River Regional Health Authorities. Population Health Unit, La Ronge.
Ishikura, H., Kikuchi, K., Nagasawa, K., Ooiwa, T., Tamiya, H., Sato, N., Sugane, K., 1990.
Anisakidae and anisakidosis. In: Sun, T. (Ed.), Progress in Clinical Parasitology, vol. 3.
Springer-Verlag, New York, pp. 43–102.
Ishikura, H., Kikuchi, K., Akao, N., Doutei, M.,Yagi, K., Takahashi, S., Sato, N., 1995. Parasi-
tologic significance of the alteration of the causative Anisakidae worm and of the Pseudo-
terranova decipiens female immature adult worm, casting off the old cuticles, and excreted
from human in Kanazawa City. Hokkaido Igaku Zasshi 70 (5), 667–685.
Iurakhno, M.V., 1986. Novyi vid tsestod Diplogonoporus violettae sp. n. (Cestoda, Diphyllo-
bothriidae) parazit beringovomorskogo sivucha (Eumetopias jubatus Schreb). Parazitolo-
giia 20, 39–45.
Iurakhno, M.V., Mal’tsev,V.N., 1993. Diphyllobothrium skrjabini sp. n. (Cestoda: Diphylloboth-
riidae) parazit morskogo zaitsa (Erignathus barbatus Erx). Parazitologiia 27, 84–89.
James, E., Boyd, W., 1937. Echinococcus alveolaris:(with the report of a case). Can. Med. Assoc.
J. 36 (4), 354–356.
Jenkerson, S.A., Middaugh, J., 1987. Prevalence of enteric pathogens in two Alaska day care
centers. Alaska Med. 29 (4), 130–133.
Jenkerson, S.A., Middaugh, J., 1990. Epidemiologic surveillance of enteric diseases in Alaska-
value of case investigation. Alaska Med. 32 (1), 9–18.
Arctic Zoonoses 189

Jenkins, D.J., Romig, T., Thompson, R.C.A., 2005. Emergence/re-emergence of Echinococcus

spp.– a global update. Int. J. Parasitol. 35 (11–12), 1205–1219.
Jenkins, E.J., Schurer, J.M., Gesy, K.M., 2011. Old problems on a new playing field: helminth
zoonoses transmitted among dogs, wildlife, and people in a changing northern climate.
Vet. Parasitol. 182, 54–69.
Jenkins, E.J., Peregrine, A.S., Hill, J.E., Somers, C.M., Gesy, K.M., Barnes, B., Gottstein, B.,
Polley, L., 2012. Detection of a European strain of Echinococcus multilocularis in North
America. Emerg. Infect. Dis. 18 (6), 1010–1012.
Jensen, S.K., Aars, J., Lydersen, C., Kovacs, K.M., Åsbakk, K., 2010. The prevalence of Toxo-
plasma gondii in polar bears and their marine mammal prey: evidence for a marine trans-
mission pathway? Polar Biol. 33 (5), 599–606.
Johansen, C.E., Lydersen, C., Aspholm, P.E., Haug,T., Kovacs, K.M., 2010. Helminth parasites
in ringed seals (Pusa hispida) from Svalbard, Norway with special emphasis on nema-
todes: variation with age, sex, diet, and location of host. J. Parasitol. 96 (5), 946–953.
Johnson, D., Harms, N.J., Larter, N.C., Elkin, B.R., Tabel, H., Wei, G., 2010. Serum bio-
chemistry, serology, and parasitology of boreal caribou (Rangifer tarandus caribou) in the
Northwest Territories, Canada. J. Wildl. Dis. 46 (4), 1096–1107.
Joly, D.O., Messier, F., 2004.The distribution of Echinococcus granulosus in moose: evidence for
parasite-induced vulnerability to predation by wolves? Oecologia 140, 586–590.
Jones, A., Pybus, M.J., 2001. Taeniasis and echinococcosis. In: Samuel, W.M., Pybus, M.J.,
Kocan, A.A. (Eds.), Parasitic Diseases of Wild Mammals, second ed. Iowa State University
Press, Ames, Iowa, pp. 150–192.
Jones, J.L., Kruszon-Moran, D., Wilson, M., McQuillan, G., Navin, T., McAuley, J.B., 2001.
Toxoplasma gondii infection in the United States: seroprevalence and risk factors. Am.
J. Epidemiol. 154 (4), 357–365.
Kamo, H., 1999. Guide to Identification of Diphyllobothriid Cestodes. Gendai Kikaku,
Tokyo [In Japanese].
Kapel, C.M.O., 1997. Trichinella in Arctic, subarctic and temperate regions: Greenland,
the Scandinavian countries and the Baltic states. SE. Asian J.Trop. Med. Public Health
28 (Suppl. 1), 14–19.
Kapel, C.M.O., Nansen, P., 1996. Gastrointestinal helminths of Arctic foxes (Alopex lagopus)
from different bioclimatological regions of Greenland. J. Parasitol. 82 (1), 17–24.
Kapel, C.M.O., Henrikson, S.A., Berg, T.B., Nansen, P., 1995. Trichinella infection in arc-
tic foxes from Greenland: studies and reflections on predilection sites of muscle larvae.
J. Helminthol. 69, 325–330.
Kapel, C.M.O., Pozio, E., Sacchi, L., Prestrud, P., 1999. Freeze tolerance, morphology, and
RAPD-PCR identification of Trichinella nativa in naturally infected arctic foxes. J. Para-
sitol. 85, 144–147.
Kapel, C.M., Measures, L., Møller, L.N., Forbes, L., Gajadhar, A., 2003. Experimental Trichi-
nella infection in seals. Int. J. Parasitol. 33, 1463–1470.
Kapel, C.M.O.,Torgerson, P.R.,Thompson, R.C.A., Deplazes, P., 2006. Reproductive poten-
tial of Echinococcus multilocularis in experimentally infected foxes, dogs, raccoon dogs and
cats. Int. J. Parasitol. 36 (1), 79–86.
Kapperud, G., Jenum, P.A., StrayPedersen, B., Melby, K.K., Eskild, A., Eng, J., 1996. Risk fac-
tors for Toxoplasma gondii infection in pregnancy – results of a prospective case–control
study in Norway. Am. J. Epidemiol. 144 (4), 405–412.
Karl, H., Baumann, F., Ostermeyer, U., Kuhn, T., Klimpel, S., 2011. Anisakis simplex (s.s.)
larvae in wild Alaska salmon: no indication of post-mortem migration from viscera into
flesh. Dis. Aquat. Org. 94 (3), 201–209.
Kates, S., Wright, K.A., Wright, R., 1973. A case of human infection with the cod nematode
Phocanema sp. Am. J. Trop. Med. Hyg. 22, 606–608.
190 Emily J. Jenkins et al.

Kaufman, D.S., Schneider, D.P., McKay, N.P., Ammann, C.M., Bradley, R.S., Briffa, K.R.,
et al., 2009. Recent warming reverses long term Arctic cooling. Science 325, 12369.
Kaye, A., 2011. Toxoplasmosis: diagnosis, treatment and prevention in congenitally exposed
infants. J. Pediatr. Health Care 25 (6), 355–364.
Kennedy, E.E., Hall, R.L., Montgomery, S.P., Pyburn, D.G., Jones, J.L., 2009. Trichinellosis
surveillance – United States, 2002–2007. MMWR Surveill. Summ. 58 (SS09), 1–7.
Kern, P., Bardonnet, K., Renner, E., Auer, H., Pawlowski, Z., Ammann, R.W., Vuitton,
D.A., Kern, P., 2003. European echinococcosis registry: human alveolar echinococcosis,
Europe, 1982–2000. Emerg. Infect. Dis. 9 (3), 343–349.
Khan, R.A., Chandra, C.V., 2006. Influence of climatic changes on the parasites of Atlantic
cod Gadus morhua off coastal Labrador, Canada. J. Helminthol. 80, 193–197.
Kijewska, A., Rokicki, J., Sitko, J., Węgrzyn, G., 2002. Ascaridoidea: a simple DNA assay for
identification of 11 species infecting marine and freshwater fish, mammals, and fish-
eating birds. Exp. Parasitol. 101, 35–39.
Kirk, C.M., Amstrup, S., Swor, R., Holcomb, D., et al., 2010. Morbillivirus and Toxoplasma
exposure and association with hematological parameters for Southern Beaufort Sea polar
bears: potential response to infectious agents in a sentinel species. Ecohealth 7, 321–331.
Klimpel, S., Rückert, S., 2005. Life cycle strategy of Hysterothylacium aduncum to become the
most abundant anisakid fish nematode in the North Sea. Parasitol. Res. 97, 141–149.
Klimpel, S., Palm, H.W., Rückert, S., Piatkowski, U., 2004. The life cycle of Anisakis simplex
in the Norwegian Deep (northern North Sea). Parasitol. Res. 94 (1), 1–9.
Klimpel, S., Palm, H.W., Busch, M.W., Kellermanns, E., Rückert, S., 2006. Fish parasites in
the Arctic deep-sea: poor diversity in pelagic fish species vs. heavy parasite load in a
demersal fish. Deep-sea Res. 53, 1167–1181.
Knapp, J., Bart, J.M., Maillard, S., Gottstein, B., Piarroux, R., 2009. The genomic Echinococcus
microsatellite EmsB sequences: from a molecular marker to the epidemiological tool.
Parasitology 137 (03), 439–449.
Kocan, A.A., Barron, S.J., Fox, J.C., Franzmann, A.W., 1986. Antibodies to Toxoplasma gondii
in moose (Alces alces) from Alaska. J. Wildl. Dis. 22 (3), 432.
Køie, M., 1993. Aspects of the lifecycle of Hysterothylatium aduncum (Rudolphi, 1802) (Nem-
atoda: Ascaridoidae, Anisakidae). Can. J. Zool. 71, 1289–1296.
Køie, M., Berland, B., Burt, D.B., 1995. Development to third-stage larvae occurs in the eggs
of Anisakis simplex and Pseudoterranova decipiens (Nematoda, Ascaridoidea, Anisakidae).
Can. J. Fish. Aquat. Sci. 52, 134–139.
Kozlov, D.P., 1971. Sources of Trichinella infection in pinnipeds. Trudy Gel'mintologicheskoi
Laboratroii Akademii Nauk SSSR. 21, 36–40. [Russian]. Translated by Kabata, Z. and
Margolis, L. Fisheries Research Board of Canada. Translation Series No. 3010 (1974).
Krabbe, H., 1868. Helminthologiske undersøgelser i Danmark og på Island, med saerligt
hensyn til blaereormslidelser på Island. vol. 7. Kongelige Danske Videnskabernes Selkabs
Skrifter fior Naturvidenskab, Matematisk Afdeling, 345–408.
Kruse, H., Kirkemo, A.M., Handeland, K., 2004. Wildlife as source of zoonotic infec-
tions. Emerg. Infect. Dis. 10, 2067–2072.
Kuchta, R., Scholz, T., Brabec, J., Bray, R.A., 2008. Supression of the tapeworm order Pseu-
dophyllidea (Platyhelminthes: Eucestoda) and the proposal of two new orders, Bothrio-
cephalidea and Diphyllobothriidea. Int. J. Parasitol. 38, 49–55.
Kuhn, T., García-Màrquez, J., Klimpel, S., 2011. Adaptive radiation within marine anisakid
nematodes: a zoogeographical modeling of cosmopolitan, zoonotic parasites. PLoS One
6 (12), e28642.
Kuitunen-Ekbaum, E., 1950.Trichinosis in the Canadian north. Can. J. Public Health 41, 34.
Kuitunen-Ekbaum, E., 1954.Walrus meat as a source of trichinosis in Eskimos. Can. J. Public
Health 45, 30.
Arctic Zoonoses 191

Kutz, S.J., Elkin, B., Gunn, A., Dubey, J.P., 2000. Prevalence of Toxoplasma gondii anti-
bodies in muskox (Ovibos moschatus) sera from Northern Canada. J. Parasitol. 86 (4),
Kutz, S.J., Elkin, B.T., Panay, D., Dubey, J.P., 2001. Prevalence of Toxoplasma gondii antibod-
ies in barren-ground caribou (Rangifer tarandus groenlandicus) from the Canadian Arctic.
J. Parasitol. 87 (2), 439–442.
Kutz, S.J., Jenkins, E.J., Veitch, A.M., Ducrocq, J., Polley, L., Elkin, B., Lair, S., 2009a. The
Arctic as a model for anticipating, preventing, and mitigating climate change impacts on
host–parasite interactions.Vet. Parasitol. 163 (3), 217–228.
Kutz, S.J., Thompson, R.C.A., Polley, L., 2009b. Wildlife with Giardia: villain or victim and
vector? In: Ortega-Pierres, G., Caccio, S., Fayer, R., Mank,T.G., Smith, H.V.,Thompson,
R.C.A. (Eds.), Giardia and Cryptosporidium: From molecules to disease, CABi Walling-
ford, UK, pp. 94–106.
Kutz, S.J., Thompson, R.C.A., Polley, L., Kandola, K., Nagy, J., Wielinga, C.M., Elkin, B.T.,
2008. Giardia assemblage A: human genotype in muskoxen in the Canadian Arctic. Para-
sit.Vectors 1, 32.
Kutz, S.J., Ducrocq, J., Verocai, G.G., Hoar, B.M., Colwell, D.D., Beckmen, K.B., Polley, L.,
Elkin, B.T., Hoberg, E.P., 2012. Parasites in ungulates of Arctic North America and
Greenland: a view of contemporary diversity, ecology, and impact in a world under
change. Adv. Parasitol. 79 (1), 99–252.
La Rosa, G., Pozio, E., 1990. Biochemical characterization of Trichinella in Greenland. Acta
Vet. Scand. 31, 381–383.
La Rosa, G., Marucci, G., Zarlenga, D.S., Casulli, A., Zarnke, R.L., Pozio, E., 2003.
Molecular identification of natural hybrids between Trichinella nativa and Trichinella
T6 provides evidence of gene flow and ongoing genetic divergence. Int. J. Parasitol.
33, 209–216.
Labelle, P., Dubey, J.P., Mikaelian, I., Blanchette, N., Lafond, R., St-Onge, S., Martineau, D.,
2001. Seroprevalence of antibodies to Toxoplasma gondii in lynx (Lynx canadensis) and
bobcats (Lynx rufus) from Quebec, Canada. J. Parasitol. 87 (5), 1194–1196.
Laidre, K.L., Stirling, I., Lowry, L.F., Wiig, Ø., Heide-Jørgensen, M.P., Ferguson, S.H., 2008.
Quantifying the sensitivity of Arctic marine mammals to climate-induced habitat
change. Ecol. Appl. 18, S97–S125.
Laird, M., Meerovitch, E., 1961. Parasites from northern Canada: I. Entozoa of Fort Chimo
Eskimos. Can. J. Zool. 39, 63–67.
Lambden, J., Receveur, O., Marshal, J., Kuhnlein, H.V., 2006. Traditional and market food
access in Arctic Canada is affected by economic factors. Int. J. Circumpolar Health 65
(4), 331–340.
Lambden, J., Receveur, O., Kuhnlein, H.V., 2007. Traditional food attributes must be
included in studies of food security in the Canadian Arctic. Int. J. Circumpolar Health
66 (4), 308–319.
Lamy, A.L., Cameron, B.H., LeBlanc, J.G., Culham, G., Blair, G.K., Taylor, G.P., 1993. Giant
hydatid lung cysts in the Canadian Northwest: outcome of conservative treatment in
three children. J. Pediatr. Surg. 28, 1140–1143.
Langer, J.C., Rose, D.B., Keystone, J.S.,Taylor, B.R., Langer, B., 1984. Diagnosis and manage-
ment of hydatid disease of the liver. A 15-year North American experience. Ann. Surg.
199, 412–417.
Lantis, M., 1981. Zoonotic diseases in the Canadian and Alaskan North. Inuit Studies 5 (2),
Larrat, S., Simardý, M., Lairý, S., Bélangerý, D., Proulx, J.-F., 2012. From science to action and
from action to science: the Nunavik Trichinellosis prevention program. Int. J. Circumpo-
lar Health 71 (18595)
192 Emily J. Jenkins et al.

Larter, N.C., Forbes, L.B., Elkin, B.T., Allaire, D.G., 2011. Prevalence of Trichinella spp. in
black bears, grizzly bears, and wolves in the Dehcho Region, Northwest Territories,
Canada, including the first report of T. nativa in a grizzly bear from Canada. J. Wildl. Dis.
47 (3), 745–749.
Lasek-Nesselquist, E., Welch, D.M., Sogin, M.L., 2010. The identification of a new Giardia
duodenalis assemblage in marine vertebrates and a preliminary analysis of G. duodenalis
population biology in marine systems. Int. J. Parasitol. 40, 1063–1074.
Laurence, R.A., Desgens, M., Trudel, L., 1983. Trichinosis in Nouveau Quebec. Can. Dis.
Wkly. Rep. 9, 209–210.
Lavoie, E., Lévesque, B., Proulx, J.-F., Grant, J., Ndassebe, A.D., Gingras, S., Hubert, B.,
Libman, M., 2008. Evaluation of the efficacy of the Toxoplasma gondii screening pro-
gram among pregnant women in Nunavik, 1994–2003. Can. J. Public Health 99 (5),
Laws, G.F., 1968. Physical factors influencing survival of taeniid eggs. Exp. Parasitol. 22,
Leclair, D., Doidge, D.W., 2001. Seroprevalence survey for Toxoplasma gondii in arctic wildlife
from Nunavik. Progress report 12–349 submitted to Nunavik Regional Board of Health
and Social Services. Nunavik Research Centre. Makivik Corporation, Kuujjuaq p. 44.
Leclair, D., Forbes, L., Suppa, S., Gajadhar, A.A., 2003. Evaluation of a digestion assay and
determination of sample size and tissue for the reliable detection of Trichinella larvae in
walrus meat. J.Vet. Diagn. Invest. 15, 188–191.
Leuckart, R., 1863. Die menschlichen Parasiten und die von ihnen herrührenden
Krankheiten. Winter’sche Verlaghandlund, Leipzig und Heidelberg.
Lévesque, B., Messier,V., Bonnier-Viger,Y., Couillard, M., Côté, S., Ward, B.J., Libman, M.D.,
Gingras, S., Dick, D., Dewailly, E., 2007. Seroprevalence of zoonoses in a Cree commu-
nity (Canada). Diagn. Microbiol. Infect. Dis. 59 (3), 283–286.
Lévesque, B., Barthe, C., Dixon, B.R., Parrington, L.J., Martin, D., Doidge, B., Proulx, J.F.,
Murphy, D., 2010. Microbiological quality of blue mussels (Mytilus edulis) in Nunavik,
Quebec: a pilot study. Can. J. Microbiol. 56, 968–977.
Levine, N.D., 1968. Nematode Parasites of Domestic Animals and Man, second ed. Burgess,
Lichtenfels, J.R., Brancato, F.P., 1976. Anisakid larva from the throat of an Alaskan Eskimo.
Am. J. Trop. Med. 25 (5), 691–693.
Lindsay, D.S., Dubey, J.P., 2009. Long-term survival of Toxoplasma gondii sporulated oocysts in
seawater. J. Parasitol. 95 (4), 1019–1020.
Lindsay, D.S., Blagburn, B.L., Dubey, J.P., 2002. Survival of nonsporulated Toxoplasma gondii
oocysts under refrigerator conditions.Vet. Parasitol. 103, 309–313.
Lindsay, D.S., Collins, M.V., Mitchell, S.M., Wetch, C.N., Rosypal, A.C., Flick, G.J., Zajac,
A.M., Lindquist, A., Dubey, J.P., 2004. Survival of Toxoplasma gondii oocysts in eastern
oysters. (Crassostrea virginica). J. Parasitol. 90 (5), 1054–1057.
Lindsay, D.S., Phelps, K.K., Smith, S.A., Flick, G., Sumner, S.S., Dubey, J.P., 2005. Removal
of Toxoplasma gondii oocysts from sea water by eastern oysters (Crassostrea virginica).
J. Eukaryot. Microbiol. 48 (1), 197–198.
Lowry, L.F., Fay, F.H., 1984. Seal eating by walruses in the Bering and Chukchi Seas. Polar
Biol. 3, 11–18.
Mackey, M.G.A., 1988. The impact of imported foods on the traditional Inuit diet. Arctic
Med. Res. 47 (1), 128–133.
MacLean, J.D.,Viallet, J., Law, C., Staudt, M., 1989. Trichinosis in the Canadian Arctic: report
of five outbreaks and a new clinical syndrome. J. Infect. Dis. 160 (3), 513–520.
MacLean, J.D., Poirier, L., Gyorkos, T.W., Proulx, J.-F., Bourgeault, J., Corriveau, A., Illisituk,
S., Staudt, M., 1992. Epidemiologic and serologic definition of primary and secondary
trichinosis in the Arctic. J. Infect. Dis. 165, 908–912.
Arctic Zoonoses 193

Madsen, H., 1961. The distribution of Trichinella spiralis in sledge dogs and wild mammals in
Greenland. Medd. Grönl. 159, 1–125.
Mallory, M.L., Woo, K., Gaston, A.J., Davies, W.E., Mineau, P., 2004. Walrus (Odobenus rosma-
nus) predation on thick-billed murres (Uria lumvia) on Coats Island, Nunavut, Canada.
Polar Res. 23 (1), 111–114.
Manning, T.H., 1960. Comments on carnivorous walrus and some Arctic zoonoses. Arctic
14, 76–77.
Marcogliese, D.J., 2001. Implications of climate change for parasitism of animals in the
aquatic environment. Can. J. Zool. 79, 1331–1352.
Marcogliese, D.J., 2008.The impact of climate change on the parasites and diseases of aquatic
animals. Rev. Sci. Tech. OIE 27, 467–484.
Margolis, L., 1956. Parasitic helminths and arthropods from Pinnipedia of the Canadian
Pacific coast. J. Fish. Res. Bd. Can. 13, 489–505.
Margolis, H.S., Middaugh, J.P., Burgess, R.D., 1979. Arctic trichinosis: two Alaskan outbreaks
from walrus meat. J. Infect. Dis. 139 (1), 102–105.
Markowski, S., 1952. The cestodes of pinnipeds in the Arctic and other regions. J. Helmin-
thol. 26, 171–214.
Marquard-Petersen, U., 1997. Endoparasites of arctic wolves in Greenland. Arctic 50, 349.
Martin, W.E., Haun, C.K., Barrows, H.S., Cravioto, H., 1970. Nematode damage to brain of
striped dolphin, Lagenorhynchus obliquidens. T. Am. Microsc. Soc. 89 (2), 200–205.
Mas-Coma, S.,Valero, M.A., Margues, M.D., 2008. Effects of climate change on animal and
zoonotic helminthiasis. Rev. Sci. Tech. OIE 27, 443–452.
Massie, G.N., Ware, M.W., Villegas, E.N., Black, M.W., 2010. Uptake and transmission of
Toxoplasma gondii oocysts by migratory, filter-feeding fish. Vet. Parasitol. 169 (3–4),
Masuoka, P.M., Burke, R., Colaccico, M., Razuri, H., Hill, D., Murrell, K.D., 2009. Predicted
geographic ranges for North American sylvatic Trichinella species. J. Parasitol. 95 (4),
Mattiucci, S., Nascetti, G., 2008. Advances and trends in the molecular systematics of ani-
sakid nematodes, with implications for their evolutionary ecology and host–parasite co-
evolutionary processes. Adv. Parasitol. 66, 47–148. 10.1016/S0065-308X(08)00202-9.
Mattiucci, S., Nascetti, G., Clanchi, R., Paggi, L., Arduino, P., Margolis, L., Brattey, J.,Webb, S.,
D'Amelio, S., Orecchia, P., Bullini, L., 1997. Genetic and ecological data on the Anisakis
simplex complex, with evidence for a new species (Nematoda, Ascaridoidea, Anisaki-
dae). J. Parasitol. 83 (3), 401–416.
Maynard, J.E., Pauls, F.P., 1962. Trichinosis in Alaska. Am. J. Hyg. 76, 252–261.
McAuley, J.B., Michelson, M.K., Schantz, P.M., 1991. Trichinella infection in travelers.
J. Infect. Dis. 164 (5), 1013–1016.
McClelland, G., 1980. Phocanema decipiens: pathology in seals. Exp. Parasitol. 49, 405–419.
McClelland, G., 2002.The trouble with sealworms (Pseudoterranova decipiens species complex,
Nematoda): a review. Parasitology 124 (7), 183–203.
McDonald, J.C., Gyorkos, T.W., Alberton, B., MacLean, J.D., Richer, G., Juranek, D., 1990.
An outbreak of toxoplasmosis in pregnant women in Northern Quebec. J. Infect. Dis.
161, 769–774.
McDonald, T.E., Margolis, L., 1995. Synopsis of the parasites of fishes of Canada. Supple-
ment (1978–1993) NRC Research Press.
McLoughlin, P.D., Dzus, E.,Wynes, B., Boutin, S., 2002. Declines in populations of woodland
caribou. J. Wildl. Manage. 67, 755–761.
McManus, D.P., Zhang, L.-H., Castrodale, L.J., Le, T.H., Pearson, M., Blair, D., 2002. Short
report: molecular genetic characterization of an unusually severe case of hydatid disease
in Alaska caused by the cervid strain of Echinococcus granulosus. Am. J. Trop. Med. Hyg.
67, 296–298.
194 Emily J. Jenkins et al.

Measures, L.N., 1993. Annotated list of metazoan parasites reported from the blue whale,
Balaenoptera musculus. J. Helminthol. Soc. Wash. 60 (1), 62–66.
Measures, L.N., 1996. Effect of temperature and salinity on development and survival of eggs
and free-living larvae of sealworm (Pseudoterranova decipiens). Can. J. Fish. Aquat. Sci. 53,
Measures, L.N., Gosselin, J.F., 1994. Helminth parasites of ringed seals, Phoca hispida, from
northern Quebec, Canada. J. Helminthol. Soc. Wash. 61, 240–244.
Measures, L.N., Olson, M.E., 1999. Giardiasis in pinnipeds of eastern Canada. J. Wildl. Dis.
35, 779–782.
Messier,V., Lévesque, B., Proulx, J.-F., Rochette, L., Libman, M., Ward, B., Serhir, B., Couil-
lard, M., Ogden, N., Dewailly, E., Hubert, B., Déry, S., Barthe, C., Murphy, D., Dixon,
B., 2009. Seroprevalence of Toxoplasma gondii among Nunavik Inuit (Canada). Zoonoses
Public Health 56, 188–197.
Messier,V., Lévesque, B., Proulx, J.-F., Rochette, L., Srehir, B., Couillard, M., Ward, B.J., Lib-
mand, M.D., Dewailly, E., Déry, S., 2012. Seroprevalence of seven zoonotic infections in
Nunavik, Quebec (Canada). Zoonoses Public Health 59 (2), 107–117.
Migaki, G., Van Dyke, D., Hubbard, R.C., 1971. Some histopathological lesions caused by
helminthes in marine mammals. J. Wildl. Dis. 7, 281–289.
Migaki, G., Heckmann, R.A., Albert,T.F., 1982. Gastric nodules caused by "Anisakidae type"
larvae in the bowhead whale (Balaena mysticetus). J. Wildl. Dis. 18 (3), 353–357.
Miller, M.A., Conrad, P.A., James, E.R., Packham, A., Toy-Choutka, S., Murray, M.J., Jessup,
D., Grigg, M., 2008. Transplacental toxoplasmosis in a wild southern sea otter (Enhydra
lutris nereis).Vet. Parasitol. 153 (1–2), 12–18.
Miller, M.J., 1953. Hydatid Infection in Canada. Can. J. Med. Assoc. 68, 423–434.
Mitreva, M., Jasmer, D.P., 2006. Biology and Genome of Trichinella spiralis, WormBook,
ed. The C. elegans Research Community, WormBook, doi: 10.1895/wormbook.1.124.1.
Mizgajska, H., 2001. Eggs of Toxocara spp. in the environment and their public health impli-
cations. J. Helminthol. 75, 147–151. doi: 10.1079/JOH200170.
Moles, A., Heintz, R.A., 2007. Parasites of forage fishes in the vicinity of Stellar sea lion
(Eumetopias jubatus) habitat in Alaska. J. Wildl. Dis. 43 (3), 366–375.
Møller, L.N., Petersen, E., Kapel, C.M.O., Melbye, M., Koch, A., 2005. Outbreak of trichi-
nellosis associated with consumption of game meat in West Greenland.Vet. Parasitol. 132
(1–2), 131–136.
Møller, L.N., Krause, T.G., Koch, A., Melbye, M., Kapel, C.M.O., Petersen, E., 2007. Human
antibody recognition of Anisakidae and Trichinella spp. in Greenland. Clin. Microbiol.
Infect. 13 (7), 702–708.
Møller, L.N., Koch, A., Petersen, E., Hjuler, T., Kapel, C.M.O., Andersen, A., Melbye, M.,
2010. Trichinella infection in a hunting community in East Greenland. Epidemiol. Infect.
138, 1252–1256.
Montoya, J.G., Rosso, F., 2005. Diagnosis and management of toxoplasmosis. Clin. Prenatol.
32 (3), 705–726.
Moore, R.D., Urschel, J.D., Fraser, R.E., Nakai, S.S., Geeraert, A.J., 1994. Cystic hydatid lung
disease in northwest Canada. Can. J. Surg. 37, 20–22.
Moore, S.E., Huntington, H.P., 2008. Arctic marine mammals and climate change: impacts
and resilience. Ecol. Appl. 18, S157–S165.
Moorhead, A., Grunenwald, P.E., Dietz,V.J., Schantz, P.M., 1999.Trichinellosis in the United
States: declining but not gone. Am. J. Trop. Med. Hyg. 60, 66–69.
Morgan, U.M., Xiao, L., Hill, B.D., O’Donoghue, P., Limor, J., Lal, A., Thompson, R.C.A.,
2001. Detection of the Cryptosporidium parvum ‘human’ genotype in a Dugong (Dugong
dugon). J. Parasitol. 86, 1352–1354.
Mouritsen, K.N., Hedeholm, R., Schack, H.B., Møller, L.N., Storr-Paulsen, M., Dzido, J.,
Rokicki, 2010. Occurrence of anisakid nematodes in Atlantic cod (Gadus morhua) and
Greenland cod (Gadus ogac), West Greenland. Acta Parasitol. 55 (1), 81–89.
Arctic Zoonoses 195

Murphy, N.J., 1981. Giardiasis in Alaska 1969–1979: a descriptive epidemiological study.

Alaska Med. 23 (2), 22–27.
Murrell, K.D., Lichtenfels, R.J., Zarlenga, D.S., Pozio, E., 2000. The systematics of the genus
Trichinella with a key to species.Vet. Parasitol. 93, 293–307.
Muzaffar, S.B., 2009. Helminths of murres (Alcidae: Uria spp.): markers of ecological change
in the marine environment. J. Wildl. Dis. 45 (3), 672–683.
Myers, B.J., 1970. Nematodes Transmitted to Man by Fish and Aquatic Mammals. J. Wildl.
Dis. 6, 266–271.
Nakao, M., McManus, D.P., Schantz, P.M., Craig, P.S., Ito, A., 2006. A molecular phylogeny
of the genus Echinococcus inferred from complete mitochondrial genomes. Parasitology
134, 713–722.
Nakao, M., Xiao, N., Okamoto, M., Yanagida, T., Sako, Y., Ito, A., 2009. Geographic pattern
of genetic variation in the fox tapeworm Echinococcus multilocularis. Parasitol. Int. 58 (4),
Nascetti, G., Cianchi, R., Mattiucci, S., D’Amelio, S., Orecchia, P., Paggi, L., Brattey, J.,
Berland, B., Smith, J.W., Bulling, L., 1993. Three sibling species within Contracaecum
osculatum (Nematoda, Ascaridida, Ascaridoidea) from the Atlantic Arctic-Boreal region:
reproductive isolation and host preferences. Int. J. Parasitol. 23, 105–120.
Nicholas,W.L., Stewart, A.C., Mitchell, G.F., 1984. Antibody responses to Toxocara canis using
sera from parasite-infected mice and protection from toxocariasis by immunisation with
ES antigens. Aust. J. Exp. Biol. Med. Sci. 62, 619–626.
Noguera, P., Collins, C., Bruno, D., Pert, C., Turnbull, A., McIntosh, A., Lester, K., Bricknell,
I., Wallace, S., Cook, P., 2009. Red vent syndrome in wild Atlantic salmon Salmo salar in
Scotland is associated with Anisakis simplex sensu stricto (Nematoda: Anisakidae). Dis.
Aquat. Org. 87, 199–215.
Nozais, J.P., Mannevy,V., Danis, M., 1996. Two cases of trichinosis from polar bear (Thalarctos
maritimus) meat. 1996. Med. Mal. Inf. 26, 732–733.
O’Lorcain, P., 1995.The effects of freezing on the viability of Toxocara canis and T. cati embry-
onated eggs. J. Helminthol. 69, 169–171.
Ohbayashi, M., Rausch, R.L., Fay, F.H., 1971. On the ecology and distribution of Echinococ-
cus spp. (cestoda: taeniidae), and characteristics of their development in the intermediate
host. II. Comparative studies on the development of the larval E. multilocularis Leuckart,
1863, in the intermediate host. Jpn. J.Vet. Res. 19, 1–53.
Oksanen, A., Asbakk, K., Prestrud, K.W., Aars, J., Derocher, A.E., Tryland, M., Wiig, Ø.,
Dubey, J.P., Sonne, C., Dietz, R., Andersen, M., Born, E.W., 2009. Prevalence of antibod-
ies against Toxoplasma gondii in polar (Urusus maritimus) from Svalbard and East Green-
land. J. Parasitol. 95 (1), 89–94.
Olson, M.E., Roach, P.D., Stabler, M., Chan, W., 1997. Giardiasis in ringed seals from the
western Arctic. J. Wildl. Dis. 33, 646–648.
Olson, M.E., O’Handley, R.M., Ralston, B.J., McAllister, T.A., Thompson, R.C.A., 2004.
Update on Cryptosporidium and Giardia infections in cattle.Trends Parasitol. 20, 185–191.
Osterman Lind, E., Juremalm, M., Christensson, D., Wildgren, S., Hallgren, G., Agren, E.O.,
Uhlhorn, H., Lindberg, A., Cedersmyg, M.,Wahlstrom, H., 2011. First detection of Echino-
coccus multilocularis in Sweden, February to March 2011. Euro. Surveill. 16 (14) pii = 19836.
Overgaauw, P.A.M., van Knapen, F., 2008. Toxocariasis, an important zoonoses. European
Journal of Companion Animal Practices 18, 259–266.
Overgaauw, P.A.M., van Zutphen, L., Hoek, D., Yaya, F.O., Roelfsema, J., Pinelli, E., van
Knapen, F., Kortbeek, L.M., 2009. Zoonotic parasites in faecal samples and fur from dogs
and cats in the Netherlands.Vet. Parasitol.doi: 10.1016/j.vetpar.2009.03.
Paggi, L., Mattiucci, S., Gibson, D.I., Berland, B., Nascetti, G., Cianchi, R., Bullini, L., 2000.
Pseudoterranova decipiens species A and B (Nematoda, Ascaridoidea): nomenclatural des-
ignation, morphological diagnostic characters and genetic markers. Syst. Parasitol. 45
(3), 185–197.
196 Emily J. Jenkins et al.

Paggi, L., Nascetti, G., Cianchi, R., Orecchia, P., Mattiucci, S., D’Amelio, S., Berland, B.,
Brattey, J., Smith, J.W., Bullini, L., 1991. Genetic evidence for three species within Pseu-
doterranova decipiens (Nematoda, Ascaridida, Ascaridoidea) in the North Atlantic and
Norwegian and Barents seas. Int. J. Parasitol. 21 (2), 195–212.
Palm, H.W., 1999. Ecology of Pseudoterranova decipiens (Krabbe, 1878) (Nematoda: Anisaki-
dae) from Antarctic waters. Parasitol. Res. 85 (8–9), 638–646.
Park, H.Y., Lee, S.-U., Kong,Y., Magnaval, J.F., 2002. A seroepidemiological survey for toxo-
cariasis in apparently healthy residents in Gangwon-do, Korea. Korean J. Parasitol. 40,
Parker, G.R., 1981. Physical and reproductive characteristics of an expanding woodland
caribou population (Rangifer tarandus caribou) in northern Labrador. Can. J. Zool. 59,
Parkinson, A.J., Butler, J.C., 2005. Potential impacts of climate change on infectious diseases
in the arctic. Int. J. Circumpolar Health 64, 478–486.
Parkinson, A.J., Evengard, B., 2009. Climate change, its impact on human health in the Arctic
and the public health response to threats of emerging infectious diseases. Global Health
Action. doi: 10.3402/gha.v2i0.2075.
Parmesan, C., Yohe, G., 2003. A globally coherent fingerprint of climate change impacts
across natural systems. Nature 421, 37–42.
Parnell, I.W., 1934. Animal parasites of north east Canada. Canad. Field. Nat. 18, 111–115.
Pars, T., Osler, M., Bjerregaard, P., 2001. Contemporary use of traditional and imported food
among Greenland Inuit. Arctic 54 (1), 22–31.
Peregrine, A.S., Jenkins, E.J., Barnes, B., Johnson, S., Polley, L., Barker, I.K., De Wolf, B.,
Gottstein, B., 2012. Alveolar hydatid disease (Echinococcus multilocularis) in the liver of a
Canadian dog in British Columbia, a newly endemic region. Can.Vet. J. 53 (8), 870–874.
Perry, A.L., Low, P.J., Ellis, J.R., Reynolds, J.D., 2005. Climate change and distribution shifts
in marine fishes. Science 308, 1912–1915.
Peterson, D.R., Cooney, M.K., Beasley, R.P., 1974. Prevalence of antibody to Toxoplasma
among Alaskan natives: relation to exposure to the felidae. J. Infect. Dis. 130 (6), 557–563.
Pinch, L.W.,Wilson, J.F., 1973. Non-surgical management of cystic hydatid disease in Alaska:
a review of 30 cases of Echinococcus granulosus infection treated without operation. Ann.
Surg. 178, 45–48.
Platt, N.E., 1975. Infestation of cod (Gadus morhua L.) with larvae of codworm (Terranova
decipiens Krabbe) and herringworm, Anisakis sp. (Nematoda Ascaridata), in North Atlan-
tic and Arctic waters. J. Appl. Ecol. 12 (2), 437–450.
Plotnikof, N.N., 1935. On the spread of the plerocercoids of Diphyllobothrium latum in fishes
of rivers Irtysh and Tobol. Med. Parasitol. Parazit. Bolezni. 4, 330.
Polley, L., Thompson, R.C.A., 2009. Parasite zoonoses and climate change: molecular tools
for tracking shifting boundaries. Trends Parasitol. 25 (6), 285–291.
Polley, L., Gaschler, C., Gajadhar,  A.A., 2000. National occurrence reporting of Trichinella
and trichinellosis using a computerized database.Vet. Parasitol. 93 (3–4), 351–363.
Poole, B.C., Chadee, K., Dick, T.A., 1983. Helminth parasites of pine marten, Martes ameri-
cana (Turton), from Manitoba, Canada. J. Wildl. Dis. 19 (1), 10–13.
Porter, K., Provo, G., Franklin, T., Ross, K., A new strategy for understanding giardiasis in
Alaska. State of Alaska Epidemiology Bulletin 21
docs/b2011_21.pdf 2011.
Post, E., Forchhammer, M.C., Bret-Harte, M.S., Callaghan, T.V., Christensen, T.R., Elber-
ling, B., Fox, A.D., Gilg, O., Hik, D.S., Hoye, T.T., Ims, R.A., Jeppesen, E., Klein, D.R.,
Madsen, J., McGuire, A.D., Rysgaard, S., Schindler, D.E., Stirling, I.,Tamstorf, M.P.,Tyler,
N.J.C., van der Wal, R., Welker, J., Wookey, P.A., Schmidt, N.M., Aastrup, P., 2009. Eco-
logical dynamics across the Arctic associated with recent climate change. Science 325
(5946), 1355–1358.
Arctic Zoonoses 197

Pozio, E., 2000. Factors affecting the flow among domestic, synanthropic and sylvatic cycles
of Trichinella.Vet. Parasitol. 93 (3–4), 241–262.
Pozio, E., 2005. The broad spectrum of Trichinella hosts: from cold- to warm-blooded ani-
mals.Vet. Parasitol. 132, 3–11.
Pozio, E., Hoberg, E., La Rosa, G., Zarlenga, D.S., 2009. Molecular taxonomy, phylogeny
and biogeography of nematodes belonging to the Trichinella genus. Infect. Genet. Evol.
9, 606–616.
Prestrud, K.W., Kjetil, A., Sbakk, E., Fuglei, E., Mørk, T., Stien, A., Ropstad, E., Tryland, M.,
Gabrielsen, G.W., Lydersen, C., Kovacs, K.M., Loonen, M.  J.E., Sagerup, K., Oksanen, A.,
2007. Serosurvey for Toxoplasma gondii in arctic foxes and possible sources of infection in
the high Arctic of Svalbard.Vet. Parasitol. 150, 6–12.
ProMED, 2003. Trichinellosis – Canada (Repulse Bay) 20030212.0374.
Proulx, J.F., MacLean, J.D., Gyorkos, T.W., Leclair, D., Richter, A.K., Serhir, B., Forbes, L.,
Gajadhar, A., 2002. Novel prevention program for trichinellosis in Inuit communities.
Clin. Infect. Dis. 34, 1508–1514.
Public Health Agency of Canada, 2007. Laboratory Surveillance Data for Enteric Pathogens
in Canada. Annual Summary 2006. Enteric Diseases Program, National Microbiology
Laboratory, Winnipeg, Manitoba, Canada.
Pufall, E., Jones Bitton,A.Q., McEwen, S.A., Brown,T.M., Edge,V.L., Rokicki, J.A., Peregrine,
A.S., Simard, M., 2012. Prevalence of zoonotic anisakid nematodes, and risk factors for
abundance, in Inuit-caught fish and marine mammals from Nunavik and Nunatsiavut,
Canada. Foodborne Pathog. Dis. 9 (11), 1002–1009. doi: 10.1089/fpd.2012.1186.
Rah, H., Chomel, B.B., Kasten, R.W., Hew, C.H., Farver, T.B., Follmann, E.H., Garner,
G.W., Amstrup, S.C., 2005. Serosurvey of selected zoonotic agents in polar bears (Ursus
maritimus).Vet. Rec. 156 (1), 7–13.
Ramsey, I., 2011. BSAVA Small Animal Formulary, seventh ed. British Small Animal Veteri-
nary Association, Gloucester, England.
Rau, M.E., Caron, F.R., 1979. Parasite-induced susceptibility of moose to hunting. Can.
J. Zool. 57, 2466–2468.
Rausch, R.L., 1951. Notes on the Nunamiut Eskimo and mammals of the Anaktuvuk Pass
region, Brooks Range, Alaska. Arctic 4, 147–196.
Rausch, R.L., 1952. Hydatid disease in boreal regions. Arctic 5, 157–174.
Rausch, R.L., 1954. Studies on the helminth fauna of Alaska. XXI. Taxonomy, morpho-
logical variation, and ecology of Diphyllobothrium ursi n. sp. provis. on Kodiak Island.
J. Parasitol. 40, 540–563.
Rausch, R.L., 1955. Unusual pathogenicity of Diphyllobothrium sp. in a black bear. Proc.
Helm. Soc. Wash. 22, 95–97.
Rausch, R.L., 1956a. Studies on the helminth fauna of Alaska. XXVII. The description and
occurrence of Diphyllobothrium dalliae n. sp. Trans. Am. Micrscp. Soc. 75, 180–187.
Rausch, R.L., 1956b. Studies on the helminth fauna of Alaska. XXX. The occurrence of
Echinococcus multilocularis Leukart, 1863, on the mainland of Alaska. Am. J. Trop. Med.
Hyg. 5 (6), 1086–1092.
Rausch, R.L., 1959a. Studies on the helminth fauna of Alaska. XXXVI. Parasites of the
wolverine, Gulo gulo L., with observations on the biology of Taenia twitchelli Schwartz,
1924. J. Parasitol. 45, 465–484.
Rausch, R.L., 1959b. Notes on the prevalence of hydatid disease in Alaskan Moose. J. Wildl.
Manage. 23, 122–123.
Rausch, R.L., 1960. Recent studies on hydatid disease in Alaska. Parassitologia 2 (3),
Rausch, R.L., 1964. Studies on the helminth fauna of Alaska XLI. Observations on ces-
todes of the genus Diplogonoporus Lönnberg, 1892 (Diphyllobothriidae). Can. J. Zool.
42, 1049–1069.
198 Emily J. Jenkins et al.

Rausch, R.L., 1967. On the ecology and distribution of Echinococcus spp. (cestoda: taeniidae),
and characteristics of their development in the intermediate host. Ann. Parasitol. 42 (1),
Rausch, R.L., 1968. Zoonotic diseases in the changing Arctic. Environ. Health Prev. Occup.
Aero. Med. 17 (4), 627–630.
Rausch, R.L., 1972. Observations on some natural-focal zoonoses in Alaska. Arch. Environ.
Health 25 (4), 246.
Rausch, R.L., 1974. Tropical problems in the Arctic: infectious and parasitic diseases, a com-
mon denominator. In: Pelizzon (Ed.), Industry and Tropical Health VIII, Harvard School
of Public Health, Cambridge, pp. 63–70.
Rausch, R.L., 1995. Life cycle patterns and geographic distribution of Echinococcus species,
Echinococcus and Hydatid Disease. first ed. CAB International, Oxfordshire, UK.
Rausch, R.L., 2003. Cystic echinococcosis in the Arctic and sub-Arctic. Parasitology 127
(S1), S73–S85.
Rausch, R.L., 2005. Diphyllobothrium fayi n. sp. (Cestoda: Diphyllobothriidae) from the
Pacific walrus, Odobenus rosmarus divergens. Comp. Parasitol. 72, 129–135.
Rausch, R.L., Adams, A.M., 2000. Natural transfer of helminths of marine origin to freshwa-
ter fishes, with observations on the development of Diphyllobothrium alascense. J. Parasitol.
86, 319–327.
Rausch, R.L., Fay, F.H., 2002. Epidemiology of alveolar echinococcosis with refer-
ence to St. Lawrence Island, Bering Sea. In: Craig, P., Pawlowski, Z. (Eds.), Cestode
Zoonoses: Echinococcosis and Cysticercosis, IOS Press, Seattle, Washinton, USA,
pp. 309–324.
Rausch, R.L., Fay, F.H., 2011. Toxascaris leonina in rodents, and relationship to eosinophilia in
a human population. Comp. Parasitol. 78, 236–244.
Rausch, R.L., Hilliard, D.K., 1970. Studies of the helminth fauna of Alaska. XLIX. The
occurrence of Diphyllobothrium latum (Linnaeus, 1758) (Cestoda: Diphyllobothriidae) in
Alaska, with notes on other species. Can. J. Zool. 48, 1201–1219.
Rausch, R.L., Rausch,V.R., 1968. On the biology and systematic position of Microtus abbre-
viatus Miller, a vole endemic to St. Matthew Island, Bering Sea. Zeitschrift für Säuget-
ierkunde 33, 65–99.
Rausch, R.L., Schiller, E.L., 1951. Hydatid disease (echinococcosis) in Alaska and the impor-
tance of rodent intermediate hosts. Science 113, 57–58.
Rausch, R.L., Schiller, E.L., 1954. Studies on the helminth fauna of Alaska XXIV. Echinococ-
cus sibiricensis n. sp. from St. Lawrence Island. J. Parasitol. 40, 659–662.
Rausch, R., Schiller, E.L., 1956. Studies on the helminth fauna of Alaska XXV. The ecology
and public health significance of Echinococcus sibiricensis Rausch and Schiller, 1954, on
St. Lawrence Island. Parasitology 46, 396–418.
Rausch, R.L., Williamson, F.S.L., 1958. Studies on the helminth fauna of Alaska XXXIII.
The description and occurrence of Diphyllobothrium alascense n. sp. (Cestoda). Z. Tro-
penmed. Parasitol. 8, 64–72.
Rausch, R.L., Williamson, F.S.L., 1959. Studies on the helminth fauna of Alaska. XXXIV.
The parasites of wolves, Canis lupus L. J. Parasitol. 45, 395–403.
Rausch, R.L., Wilson, J.F., 1985. The current status of alveolar hydatid disease in northern
regions. In: Fortuine., R. (Ed.), Proceedings of the Sixth International Symposium on
Circumpolar Health 84, University of  Washington Press, Seattle, pp. 245–247.
Rausch, R., Babero, B.B., Rausch, R.V., Schiller, E.L., 1956. Studies on the helminth fauna
of Alaska. XXVII. The occurrence of larvae of Trichinella spiralis in Alaskan mammals.
J. Parasitol. 42, 259–271.
Rausch, R.L., Scott, E.M., Rausch, V.R., 1967. Helminths in Eskimos in western Alaska,
with particular reference to Diphyllobothrium infection and anaemia. Trans. Roy. Soc.
Trop. Med. Hyg. 61, 351–357.
Arctic Zoonoses 199

Rausch, R.L., Fay, F.H., Williamson, F.S.L., 1983. Helminths of the arctic fox, Alopex lagopus
(L.), in Greenland. Can. J. Zool. 61, 1847–1851.
Rausch, R.L., Fay, F.H., Williamson, F.S.L., 1990a. The ecology of Echinococcus multilocularis
(Cestoda: Taeniidae) on St. Lawrence Island, Alaska. II Helminth populations in the
definitive host. Ann. Parasitol. Hum. Comp. 65, 131–140.
Rausch, R.L.,Wilson, J.F., Schantz, P.M., 1990b. A programme to reduce the risk of infection
by Echinococcus multilocularis: the use of praziquantel to control the cestode in a village in
the hyperendemic region of Alaska. Ann. Trop. Med. Parasitol. 84 (3), 239–250.
Rausch, R.L., George, J.C., Brower, H.K., 2007. Effect of warming on the Pacific walrus, and
potential modification of its helminth fauna. J. Parasitol. 93 (5), 1247–1251.
Rausch, R.L., Adams, A.M., Margolis, L., 2010. Identity of Diphyllobothrium spp. (Cestoda:
Diphyllobothriidae) from sealions and people along the Pacific coast of South America.
J. Parasitol. 96, 359–365.
Reichard, M.V., Torretti, L., Garvon, J.M., Dubey, J.P., 2008a. Prevalence of antibodies to
Toxoplasma gondii in wolverines from Nunavut, Canada. J. Parasitol. 94 (3), 764–765.
Reichard, M., Torretti, L., Snider, T., Garvon, J., Marucci, G., Pozio, E., 2008b. Trichinella T6
and Trichinella nativa in wolverines (Gulo gulo) from Nunavut, Canada. Parasitol. Res.
103 (3), 657–661.
Reinhard, K.J., Urban, O., 2003. Diagnosing ancient diphyllobothriasis from Chinchorro
mummies. Mem. Inst. Oswaldo Cruz 98, 191–193.
Reist, J.D., Wrona, F.J., Prowse, T.D., Power, M., Dempson, J.B., Beamish, R.J., King, J.R.,
Carmichael,T.J., Sawatzky, C.D., 2006. General effects of climate change on Arctic fishes
and fish populations. Ambio 35, 370–380.
Rengifo-Herrera, C., Ortega-Mora, L.M., Álvarez-García, G., Gómez-Bautista, M., Gar-
cía-Párraga, D., García-Peña, F.J., Pedraza-Díaz, S., 2012. Detection of Toxoplasma gondii
antibodies in Antarctic pinnipeds. Vet. Parasitol. doi: 10.1016/j.vetpar.2012.05.020
Ahead of Print.
Reynoldson, J.A., Behnke, J.M., Gracey, M., Horton, R.J., Spargo, R., Hopkins, R., Con-
stantine, C.C., Gilbert, F., Stead, C., Hobbs, R.P., Thompson, R.C.A., 1998. Efficacy of
albendazole against Giardia and hookworm in a remote aboriginal community in the
north of Western Australia. Acta Trop. 171, 27–44.
Richardson, E., Branigan, M., Calvert, W., Cattet, M., Derocher, A.E., Doidge, W., Hedman,
D., Lunn, N.J., McLoughlin, P., Obbard, M.E., Stirling, I., Taylor, M., 2005. Research on
Polar Bears in Canada 2001–2004. Report to the 14th Working Meeting of the IUCN/
SSC Polar Bear Specialist Group, June 2005, Seattle, Washington, U.S.A., p. 21.
Roach, P.D., Olson, M.E.,Whitley, G.,Wallis, P.M., 1993.Waterborne Giardia cysts and Cryp-
tosporidium oocysts in the Yukon, Canada. Appl. Environ. Microbiol. 59, 67–73.
Robertson, L.J., 2007. The potential for marine bivalve shellfish to act as transmission vehi-
cles for outbreaks of protozoan infections in humans: a review. Int. J. Food Microbiol.
120, 201–216.
Robinson, R.A., Catley, A., Hird, D., 2003. Significance of participatory epidemiology in
veterinary public health community-based systems. In Final Report Expert Consulta-
tion on Community Based Veterinary Public Health (VPH) Systems. UN Food and
Agriculture Organization, Rome, Italy, pp. 22–32.
Roddie, G., Stafford, P., Holland, C.,Wolfe, A., 2008. Contamination of dog hair with eggs of
Toxocara canis.Vet. Parasitol. 152, 85–93.
Rokicki, J., 2009. Effects of climatic changes on anisakid nematodes in polar regions. Polar
Sci. 3, 197–201.
Romig,T.,Thoma, D.,Weible, A.K., 2006. Echinococcus multilocularis – a zoonosis of anthropo-
genic environments? J. Helminthol. 80 (2), 207–212.
Ross, P., Olpinski, S., Curtis, M., 1989. Relationships between dietary practice and parasite
zoonoses in Northern Quebec Inuit communities. Études/Inuit/Studies 13 (2), 33–47.
200 Emily J. Jenkins et al.

Roth, H., 1949. Trichinosis in arctic animals. Nature 163, 805–806.

Roth, H., 1950. Trichinosis in the Arctic. Bull. Off. Int. Epizoot. 34, 197–220.
Roth, H., Madsen, H., 1953. Die Trichinose in Gronlands, abschliessender Bericht der
Jahre 1948–1953. Proceedings of the 14th International Congress on Zoology, vol. 10.
Copenhagen, pp. 340–341.
Roy, S.L., Lopez, A.S., Schantz, P.M., 2003. Trichinellosis surveillance – United States,
1997–2001. MMWR Surveill. Summ. 52 (SS06), 1–8.
Saarma, U., Jogisalu, I., Moks, E.,Varcasia, A., Lavikainen, A., Oksanen, A., Simsek, S., Andre-
siuk,V., Denegri, G., Gonalez, L.M., Ferrer, E., Garate, T., Rinaldi, L., Maravilla, P., 2009.
A novel phylogeny for the genus Echinococcus, based on nuclear data, challenges relation-
ships based on mitochondrial evidence. Parasitology 136, 317–328.
Salb, A.L., Barkema, H.W., Elkin, B.T., Thompson, R.C., Whiteside, D.P., Black, S.R., Dubey,
J.P., Kutz, S.J., 2008. Dogs as sentinels of parasites in humans and wildlife, northern
Canada. Emerg. Infect. Dis. 14 (1), 60–63.
Sampasa-Kanyinga, H., Lévesque, B., Anassour-Laouan-Sidi, E., Côté, S., Serhir, B., Ward,
B.J., Libman, M.D., Drebot, M.A., Ndao, M., Dewailly, É., 2012. Zoonotic infections
in native communities of James Bay, Canada. Vector-borne Zoonot. 12 (6), 473–481.
Santín, M., Dixon, B.R., Fayer, R., 2005. Genetic characterization of Cryptosporidium isolates
from ringed seals (Phoca hispida) in northern Quebec, Canada. J. Parasitol. 91, 712–716.
Santos, S.V., Lescano, S.Z., Castro, J.M., Chieffi, P.P., 2009. Larval recovery of Toxocara cati in
experimentally infected Rattus norvegicus and analysis of the rat as potential reservoir for
this ascarid. Mem. Ins. Oswaldo Cruz 104, 933–934.
Saunders, L.G., 1949. A survey of helminth and protozoan incidence in man and dogs at Fort
Chipewyan, Alberta. J. Parasitol. 35 (1), 31–34.
Savioli, L., Smith, H., Thompson, R.C.A., 2006. Giardia and Cryptosporidium join the
‘Neglected Diseases Initiative. Trends Parasitol. 22, 203–208.
Scallan, E., Hoekstra, R.M., Angulo, F.  J., Tauxe, R.V., Widdowson, A., Roy, S.L., Jones, J.L.,
Griffin, P.M., 2011. Foodborne illness acquired in the United States – major pathogens.
Emerg. Infect. Dis. 17 (1), 7–15.
Schantz, P.M., Weis, P.E., Pollard, Z.F., White, M.C., 1980. Risk factors for toxocaral ocular
larva migrans: a case–control study. Am. J. Public Health 70, 1269–1272.
Schantz, P.M., Chai, J., Craig, P.S., Eckert, J., Jenkins, D.J., Macpherson, C.N.L., Thakur, A.,
1995. Epidemiology and control of hydatid disease. In Echinococcus and Hydatid Dis-
ease. CAB International, Wallingford, U.K, 233–332.
Schellenberg, R.S.,Tan, B.J.K., Irvine, J.D., Stockdale, D.R., Gajadhar, A.A., Serhir, B., Botha,
J., Armstrong, C.A., Woods, S.A., Blondeau, J.M., McNab, T.L., 2003. An outbreak of
trichinellosis due to consumption of bear meat infected with Trichinella nativa in 2
northern Saskatchewan communities. J. Infect. Dis. 188, 835–843.
Schiller, E.L., 1952. Studies on the helminth fauna of Alaska. V. Notes on Adak rats (Rattus
norvegicus Berkenhout) with special reference to helminth parasites. J. Mammal. 33 (1),
Schindler, D.W., Smol, J.P., 2006. Cummulative effects of climate warming and other human
activities on freshwaters of Arctic and Subarctic North America. Ambio 35, 160–168.
Schmidt, G.D., 1986. CRC Handbook of Tapeworm Identification. CRC Press, Boca Raton.
Scholz, T., Garcia, H.H., Kuchta, R., Wicht, B., 2009. Update on the human broad tape-
worm (Genus Diphyllobothrium), including clinical relevance. Clin. Microbiol. Rev. 22,
Schurer J.M., Ndao, M., Skinner, S., Irvine, J., Elmore, S.A., Epp, T., Jenkins, E.J., 2013.
Parasitic zoonoses: one health surveillance in northern Saskatchewan. PLoS Negl.
Trop. Dis. 7(3): e2141. doi:10.1371/journal.pntd.0002141.
Arctic Zoonoses 201

Schurer, J., Hill, J., Fernando, C., Jenkins, E., 2012. Sentinel surveillance for zoonotic parasites
in companion animals in Indigenous communities of Saskatchewan. Am. J. Trop. Med.
Hyg. 87 (3), 495–498.
Schuster, C.  J., Ellis, A.G., Robertson, W.J., Charron, D.F., Aramini, J. J., Marshall, B.J.,
Medeiros, D.T., 2005. Infectious disease outbreaks related to drinking water in Canada,
1974–2001. Can. J. Public Health 96 (4), 254–258.
Schwabe, C.W., 1984.Veterinary medicine and human health, third ed.Williams and Wilkins,
Baltimore, Maryland.
Schweiger, A.R.W., Ammann, D., Candinas, P.A., Clavien, J., Eckert, B., Gottstein, N., et al.,
2007. Human alveolar echinococcosis after fox population increase, Switzerland. Emerg.
Infect. Dis. 13 (6), 878–882.
Serhir, B., MacLean, J.D., Healey, S., Segal, B., Forbes, L., 2001. Outbreak of trichinellosis
associated with Arctic walruses in northern Canada. Can. Commun. Dis. Rep. 27, 31–36.
Shults, L.M., 1982. Helminths of the spotted seal, Phoca largha, from the Bering Sea. J. Wildl.
Dis. 18 (1), 59–62.
Shults, L.M., 1986. Helminth parasites of the Steller sea lion, Eumetopias jubatus, in Alaska.
Proc. Helm. Soc. Wash. 53, 68–73.
Shults, L.M., Frost, K.J., 1988. Helminth parasites of ribbon seals, Phoca fasciata, in the Bering
Sea and their intermediate hosts. Proc. Helm. Soc. Wash 55, 68–73.
Siefker, C., Rickard, L.G., Pharr, G.T., Simmons, J.S., O’Hara, T.M., 2002. Molecular charac-
terization of Cryptosporidium sp. isolated from northern Alaskan caribou (Rangifer taran-
dus). J. Parasitol. 88 (1), 213–216.
Simon, A., Chambellant, M., Ward, B., Simard, M., Proulx, J., Lévesque, B., Bigras-Poulin,
M., Rousseau, A., Ogden, N., 2011. Spatio-temporal variations and age effect on Toxo-
plasma gondii seroprevalence in seals from the Canadian Arctic. Parasitology 138 (11),
Slough, B., 2003. COSEWIC Assessment and Update Status Report on the Wolverine Gulo
gulo Eastern Population and Western Population in Canada. COSEWIC Committee on
the status of endangered wildlife in Canada, p. 28.
Smith, J.D., Addison, E.M., Joachim, D.G., Smith, L.M., 1986. Helminth parasites of Canada
lynx (Felis canadensis) from northern Ontario. Can. J. Zool. 64, 358–364.
Smith, J.W., 1984. The abundance of Anisakis simplex L3 in the body cavity and flesh of
marine teleosts. Int. J. Parasitol. 14, 491–495.
Smith, J.W., Snyder, J.M., 2005. New locality records for third-stage larvae of Anisakis simplex
(sensu lato) (Nematoda: Ascaridoidea) in euphausiids Euphausia pacifica and Thysanoessa
raschii from Prince William Sound, Alaska. Parasitol. Res. 97 (6), 539–542.
Smith, J.W., Wootten, R., 1975. Experimental studies on the migration of Anisakis sp. larvae
(Nematoda: Ascaridida) into the flesh of herring, Clupea harengus L. Int. J. Parasitol. 5,
Smith, H.J., 1978. Parasites of red foxes in New Brunswick and Nova Scotia. J. Wildl. Dis.
14, 366–370.
Smith, H.  J., 1985. Infectivity of Canadian isolates of Trichinella spiralis nativa for swine, rats
and carnivores. Can. J. Comp. Med. 49 (1), 88–90.
Smith, H.  J., Snowden, K.E., 1988. Sylvatic trichinosis in Canada. Can. J. Vet. Res. 52 (4),
Somily, A., Robinson, J.L., Miedzinski, L.J., Bhargava, R., Marrie, T.J., 2005. Echinococcal
disease in Alberta, Canada: more than a calcified opacity. BMC Infect. Dis. 5, 34.
Sorensen, K.K., Mork, T., Siguroardottir, O.G., Asbakk, K., Akerstedt, J., Bergsjo, B., Fuglei,
E., 2005. Acute toxoplasmosis in three wild arctic foxes (Alopex lagopus) from Svalbard;
one with co-infections of Salmonella enteritidis PT1 and Yersinia pseudotuberculosis sero-
type 2b. Res.Vet. Sci. 78 (2), 161–167.
202 Emily J. Jenkins et al.

Spraker, T.R., Lyons, E.T., Tolliver, S.C., Bair, H.D., 2003. Ascaridoid nematodes and associ-
ated lesions in stomachs of subadult male northern fur seals (Callorhinus ursinus) on
St. Paul Island, Alaska: (1987–1999). J.Vet. Diagn. Invest. 15, 432–437.
Sprent, J.F.A., 1953. On the migratory behaviour of the larvae of various ascaris species in
white mice: II. Longevity. J. Infect. Dis. 92, 114–117.
Stefansson, V., 1914. The Stefansson-Anderson arctic expedition of the American Museum.
Preliminary ethnological report. Anthropology Papers American Museum of Natural
History 14 (1) 386, 445–458.
Stehr-Green, J.K., Stehr-Green, P.A., Schantz, P.M., Wilson, J.F., Lanier, A., 1988. Risk fac-
tors for infection with Echinococcus multilocularis in Alaska. Am. J. Trop. Med. Hyg. 38 (2),
Stieve, E., Beckmen, K., Kania, S.A., Widner, A., Patton, S., 2010. Neospora caninum and Toxo-
plasma gondii antibody prevalence in Alaska wildlife. J. Wildl. Dis. 46, 348–355.
Stiles, C.W., Hassall, A., 1899.VII. Internal Parasites of the Fur Seal. In:The Fur Seals and Fur
Seal Islands of the North Pacific Ocean (David Starr pp. 99–177 Jordan Report 1899).
part 3, U.S. Treasury Department, Washington, DC.
Strømnes, E., Andersen, K., 2000. ‘Spring rise’ of whaleworm (Anisakis simplex; Nematoda,
Ascaridoidea) third-stage larvae in some fish species from Norwegian waters. Parasitol.
Res. 86 (8), 619–624.
Stronen, A.V., Sallows,T., Forbes, G.J.,Wagner, B.A., Paquet, P.C., 2011. Diseases and parasites
in wolves of the Riding Mountain National Park region, Manitoba, Canada. J. Wildl.
Dis. 47, 222–227.
Sweatman, G.K., 1952. Distribution and incidence of Echinococcus granulosus in man and
other animals with special reference to Canada. Parasitology 43, 480–485.
Sweatman, G.K., Williams, J.F., 1963. Comparative studies on the biology and morphology
of Echinococcus granulosus from domestic livestock, moose and reindeer. Parasitology 53,
Taira, K., Saitoh, Y., Sugiyama, H., Kapel, C.M.O., 2012. Tolerance to low temperatures
of Toxocara cati larvae in chicken muscle tissue. Vet. Parasitol. (May 9) http://dx.doi.
Tanner, C.E., Staudt, M., Adamowski, R., Lussier, M., Bertrand, S., Prichard, R.K., 1987.
Seroepidemiological study for five different zoonotic parasites in northern Quebec. Can.
J. Public Health 78 (4), 262–266.
Tappe, D., Kern, P., Frosch, M., Kern, P., 2010. A hundred years of controversy about the
taxonomic status of Echinococcus species. Acta Trop. 115, 167–174.
Taylor, M., Larsen, T., Schweinsburg, Z.R.E., 1985. Observations of intraspecific aggression
and cannibalism in polar bears (Ursus maritimus). Arctic 3 (4), 303–309.
Tenter, A.M., Heckeroth, A.R.,Weiss, L.M., 2000. Toxoplasma gondii: from animals to humans.
Int. J. Parasitol. 30 (12–13), 1217–1258.
Thing, H., Clausen, B., Henriksen, S.A., 1976. Finding of Trichinella spiralis in a walrus
(­Odobenus rosmarus L.) in the Thule district, Northwest Greenland. Nord.Vet. Med. 28, 59.
Thomas, D.C., 1996. Prevalence of Echinococcus granulosus and Taenia hydatigena in caribou in
north-central Canada. Rangifer 9, 331–335.
Thomas, L.J., Babero, B.B., Gallicchio,V., Lacey, R.  J., 1954. Echinococcosis on St. Lawrence
Island, Alaska. Science 120, 1102–1103.
Thompson, R.C.A., 2011. In: Zoonoses Palmer, S.R., Soulsby, E.J.L., Torgerson, P., Brown,
D. (Eds.), Giardia Infections, Oxford University Press, Oxford.
Thompson, R.C.A., Monis, P.T., 2011. Taxonomy of Giardia species. In: Lujan, H.D., Svärd,
S. (Eds.), Giardia: A Model Organism, Springer, pp. 3–15.
Thompson, R.C.A., Monis, P.T., 2012. Giardia – from genome to proteome. Adv. Parasitol.
78, 57–95.
Thompson, R.C.A., Smith, A., 2011. Zoonotic enteric protozoa.Vet. Parasitol. 182, 70–78.
Arctic Zoonoses 203

Thompson, R.C.A., Lymbery, A.J., Meloni, B.P., 1990. Genetic variation in Giardia Kun-
stler, 1882: taxonomic and epidemiological significance. Review article. Protozoological
Abstracts 14, 1–28.
Thompson, R.C.A., Reynoldson, J.A., Garrow, S.J., McCarthy, J.S., Behnke, J.M., 2001.
Towards the eradication of hookworm in an isolated Australian community. Lancet 357,
Thompson, R.C.A., Boxell, A.C., Ralston, B.J., Constantine, C.C., Hobbs, R.P., Shury, T.,
et al., 2006. Molecular and morphological characterization of Echinococcus in cervids
from North America. Parasitology 132, 439–447.
Thompson, R.C.A., Palmer, C.S., O'Handley, R., 2008. The public health and clinical
significance of Giardia and Cryptosporidium in domestic animals.Vet. J. 177, 18–25.
Thompson, R.C.A., Kutz, S.J., Smith, A., 2009. Parasite zoonoses and wildlife: emerging
issues. Int. J. Environ. Res. Publ. Health 6, 678–693.
Thompson, R.C.A., Lymbery, A.J., Smith, A., 2010. Parasites, emerging disease and wildlife
conservation. Int. J. Parasitol. 40, 1163–1170.
Thorborg, N.B., Tulinius, S., Roth, H., 1948. Trichinosis in Greenland. Acta. Pathol. Micro-
biol. Scand. 25 (6), 778–794.
Thorshaug, K.N., Rosted, K.F., 1956. Researches on the prevalences of trichinosis in animals
in Arctic and Antarctic waters. Nord.Vet. Med. 8, 115–129.
Unruh, D.H.A., King, J.E., Eaton, R.D.P., Allen, J.R., 1973. Parasites of dogs from Indian
settlements in northwestern Canada: a survey with public health implications. Can.
J. Comp. Med. 37, 25–32.
van Zyll de Jong, C.G., 1966. Parasites of the Canada lynx, Felix (lynx) canadensis (Kerr). Can.
J. Zool. 44, 499–509.
Viet, J.F., Giraudoux, P., Abrial, V., Bresson-Hadni, S., 1999. Water vole (Arvicola Terrestris
Scherman) density as risk factor for human alveolar echinococcosis. The Am. J. Trop.
Med. Hyg. 61 (4), 559–565.
Vors, L.S., Boyce, M.S., 2009. Global declines of caribou and reindeer. Glob. Change Biol.
15, 2626–2633.
Wallis, P.M., Erlandsen, S.L., Isaac-Renton, J.L., Olson, M.E., Robertson, W.J., van Keulen,
H., 1996. Prevalence of Giardia cysts and Cryptosporidium oocysts and characterization
of Giardia spp. isolated from drinking water in Canada. Appl. Environ. Microbiol. 62 (8),
Watson,T.G., Freeman, R.S., Staszak, M., 1979. Parasites in native people of the Sioux Look-
out Zone, Northwestern Ontario. Can. J. Public Health 70, 179–182.
Wazura, K.W., Strong, J.T., Glenn, C.L., Bush, A.O., 1986. Helminths of the beluga whale
(Delphinapterus leucas) from the Mackenzie River Delta, Northwest Territories. J. Wildl.
Dis. 22 (3), 440–442.
Webster, G.A., Cameron, T.W.M., 1967. Epidemiology and diagnosis of echinococcosis in
Canada. Can. Med. Assoc. J. 96 (10), 600–607.
Wilson, J.F., Rausch, R.L., 1980. Alveolar hydatid disease – a review of clinical features of 33
indigenous cases of Echinococcus multilocularis infection in Alaskan Eskimos. Am. J. Trop.
Med. Hyg. 29 (6), 1340–1355.
Wilson, J.F., Diddams, A.C., Rausch, R.L., 1968. Cystic hydatid disease in Alaska: a review of
101 autochthonous cases of Echinococcus granulosus infection.Am. Rev. Respir. Dis. 98, 1–15.
Wilson, J.F., Rausch, R.L., Wilson, F.R., 1995. Alveolar hydatid disease. Review of the surgi-
cal experience in 42 cases of active disease among Alaskan Eskimos. Ann. Surg. 221 (3),
Wilson, R., 1967. Bear meat trichinosis. Profound serum protein alterations, minor eosino-
philia, and response to thiabendazole. Ann. Intern. Med. 66 (5), 965–971.
Wilson, T.M., Stockdale, P.H., 1970. The harp seal, Pagophilus groenlandicus (Erxleben, 1777)
XI. Contracaecum sp. infestation in a harp seal. J. Wildl. Dis. 6, 152–154.
204 Emily J. Jenkins et al.

Wolfgang, R.W., 1954. Indian and Eskimo Diphyllobothriasis. Can. Med. Assoc. J. 70, 536.
Wolfgang, R.W., Poole, J.B., 1956. Distribution of Echinococcus disease in northwestern Can-
ada. Am. J. Trop. Med. Hyg. 5, 869–871.
Won, K.Y., Druszon-Moran, D., Schantz, P.M., Jones, J.L., 2008. National seroprevalence
and risk factors for zoonotic Toxocara spp. infection. Am. J. Trop. Med. Hyg. 79, 552–557.
Wood, H., 1835. Observations on the Trichina spiralis with a case. London Medical Gazette
16, 190–191 Retrieved on May 24th, 2012 from
Wu, J., Kutz, S., Checkley, S., 2010. Health survey of selected veterinary and zoonotic disease
in muskox of Victoria Island, Nunavut, Canada. Abstract in the Proceedings of the John
waters zoonotic disease workshop, November 18–19, Calgary, Alberta, Canada.
Xiao, L., Fayer, R., 2008. Molecular characterisation of species and genotypes of Crypto-
sporidium and Giardia and assessment of zoonotic transmission. Int. J. Parasitol. 38 (11),
Xiao, L., Feng, Y., 2008. Zoonotic cryptosporidiosis. FEMS Immunol. Med. Microbiol. 52,
Xiao, L., Fayer, R., Ryan, U., Upton, S.J., 2004. Cryptosporidium taxonomy: recent advances
and implications for public health. Clin. Microbiol. Rev. 17 (1), 72–97.
Yang, J., Keystone, J.S., McIntyre, L., Spence, H., 1982. Toxocara antibodies in veterinary per-
sonnel. Can.Vet. J. 23, 126–128.
Yang,Y.R., Sun,T., Li, Z., Zhang, J.,Teng, J., Liu, X., et al., 2006. Community surveys and risk
factor analysis of human alveolar and cystic echinococcosis in Ningxia Hui autonomous
region, China. Bull. World Health Organ. 84 (9), 714–721.
Yera, H., Estran, C., Delaunay, P., Gari-Toussaint, M., Dupouy-Camet, J., Marty, P., 2006.
Putative Diphyllobothrium nihonkaiense acquired from a Pacific salmon (Oncorhynchus keta)
eaten in France; genomic identification and case report. Parasitol. Int. 55, 45–49.
Yoder, J.S., Harral, C., Beach, M.J., 2010a. Cryptosporidiosis Surveillance – United States,
2006–2008. Morb. Mortal. Wkly. Rep. 59 (SS06), 1–14.
Yoder, J.S., Harral, C., Beach, M.J., 2010b. Giardiasis Surveillance United States, 2006–2008.
Morb. Mortal. Wkly. Rep. 59 (SS06), 15–25.
Young, P.C., Lowe, D., 1969. Larval nematodes from fish of the subfamily Anisakinae and
gastro-intestinal lesions in animals. J. Comp. Pathol. 79, 301–313.
Zarlenga, D.S., Chute, M.B., Martin, A., Kapel, C.M.O., 1999. A multiplex PCR for unequiv-
ocal differentiation of all encapsulated and non-encapsulated genotypes of Trichinella. Int.
J. Parasitol. 29 (11), 1859–1867.
Zarlenga, D.S., Rosenthal, B.M., La Rosa, G., Pozio, E., Hoberg, E.P., 2006. Post-Miocene
expansion, colonization, and host switching drove speciation among extant nematodes
of the archaic genus Trichinella. Proceed. Natl. Acad. Sci. U. S. A. 103 (19), 7354–7359.
Zarnke, R.L., Dubey, J.P., Kwok, O.C.H., Ver Hoef, J.M., 1997. Serologic survey for Toxo-
plasma gondii in grizzly bears from Alaska. J. Wildl. Dis. 33, 267–270.
Zarnke, R.L., Worley, D.E.,Ver Hoef, J.M., McNay, M.E., 1999. Trichinella sp. in wolves from
interior Alaska. J. Wildl. Dis. 35 (1), 94–97.
Zarnke, R.L., Dubey, J.P., Kwok, O.C.H., Ver Hoef, J.M., 2000. Serologic survey for Toxo-
plasma gondii in selected wildlife species from Alaska. J. Wildl. Dis. 36 (2), 219–224.
Zarnke, R.L., Dubey, J.P., Ver Hoef, J.M., McNay, M.E., Kwok, O.C.H., 2001. Serologic
survey for Toxoplasma gondii in lynx from Interior Alaska. J. Wildl. Dis. 37 (1), 36–38.
Zhou, L., Kassa, H., Tischler, M.L., Xiao, L., 2004. Host-adapted Cryptosporidium spp. in
Canada geese (Branta canadensis). Appl. Environ. Microbiol. 70 (7), 4211–4215.
Zimmerman, W.J., Hubbard, E.D., Mathews, J., 1959. Studies on fecal transmission of Trichi-
nella spiralis. J. Parasitol. 45, 441–445.

The Malaria Transition on the

Arabian Peninsula: Progress
toward a Malaria-Free Region
between 1960–2010
Robert W. Snow*,†,1, Punam Amratia*, Ghasem Zamani‡,
Clara W. Mundia*, Abdisalan M. Noor*,†, Ziad A. Memish§,
­Mohammad H. Al Zahrani§, Adel Al Jasari¶, Mahmoud Fikri§§,
Hoda Atta¶¶,1
*Malaria Public Health Department, Kenya Medical Research Institute–Wellcome Trust–University
of Oxford Programme, GPO, Nairobi, Kenya
†Center for Tropical Medicine, Nuffield Department of Clinical Medicine, University of Oxford, Oxford, UK
§Ministry of Health, Kingdom of Saudi Arabia
¶Malaria Control Programme, Ministry of Public Health and Population,Yemen
§§Ministry of Health, United Arab Emirates
¶¶Malaria Control & Elimination, Division of Communicable Diseases Control, World Health Organization

Regional Office for the Eastern Mediterranean, Cairo, Egypt

1Corresponding authors: E-mail:;

1. Background and Context 206
2. Kingdom of Saudi Arabia 210
3. Republic of Yemen 216
4. Sultanate of Oman 224
5. United Arab Emirates 229
6. Kingdom of Bahrain 233
7. Qatar236
8. State of Kuwait 237
9. Discussion238

The transmission of malaria across the Arabian Peninsula is governed by the diversity of
dominant vectors and extreme aridity. It is likely that where malaria transmission was
historically possible it was intense and led to a high disease burden. Here, we review the
speed of elimination, approaches taken, define the shrinking map of risk since 1960 and
discuss the threats posed to a malaria-free Arabian Peninsula using the archive mate-
rial, case data and published works. From as early as the 1940s, attempts were made

Advances in Parasitology, Volume 82 © 2013 Elsevier Ltd.

ISSN 0065-308X, All rights reserved. 205
206 Robert W. Snow et al.

to eliminate malaria on the peninsula but were met with varying degrees of success
through to the 1970s; however, these did result in a shrinking of the margins of malaria
transmission across the peninsula. Epidemics in the 1990s galvanised national malaria
control programmes to reinvigorate control efforts. Before the launch of the recent
global ambition for malaria eradication, countries on the Arabian Peninsula launched a
collaborative malaria-free initiative in 2005. This initiative led a further shrinking of the
malaria risk map and today locally acquired clinical cases of malaria are reported only in
Saudi Arabia and Yemen, with the latter contributing to over 98% of the clinical burden.


The Arabian Peninsula has a diverse malaria epidemiology and an
important historical contribution to the understanding of successes and fail-
ures of malaria elimination. Writings from travellers to the Arabian Peninsula
during the previous two centuries make reference to periodic fevers and
deaths from fever at oases and along the inhospitable Tihama region on the
western border with the Red Sea (Rogan, 2011). It is thought that during the
Prophet Mohammad's migration from Mecca to Medina in the year 622, an
epidemic of  ‘Yethrib’ fever attacked his followers; Y   ethrib was subsequently
named Medina and was regarded as a ‘dangerously unhealthy place’ (Farid,
1956, 1996). The presence of the established human red cell polymorphisms,
protective against malaria, such as haemoglobin S and Glucose-6-Phosphate
Dehydrogenase deficiency, across the region suggests a long-term selective
pressure through a significant malaria burden (Lehman et al., 1963; Gelpi,
1965; El Hamzi et al., 2011). It is likely that malaria occurred across populated
areas of most of the present day territories of Saudi Arabia, Kuwait, Qatar,
United Arab Emirates (UAE), Bahrain, Oman and Yemen at the turn of the
last century, where transmission was limited only in its extent by the availabil-
ity of breeding sites for dominant vectors and the presence of human hosts.
Altitude and deserts have been used to define the absence of malaria
transmission in most previous iterations of global malaria maps (Boyd, 1930;
Dutta and Dutt, 1978; Lysenko and Semashko, 1968). Ambient temper-
ature determines the likelihood of transmission of human malaria based
on its relationship with the duration of sporogony of the parasite in the
mosquito. Extreme aridity effects Anopheline development and survival
(Shililu et al., 2004). Using recently developed models of temperature suit-
ability based on long-term climate data (Gething et al., 2011) and remotely
sensed proxies of extreme aridity (Guerra et al., 2006, 2008), it is possible
to distinguish the biological limits of transmission across the peninsula. Low
ambient ­temperatures identify the mountains of Jebel el Nabi Shu'ayb and
a spine of high altitude areas around the capitol city of Sana'a in Yemen that
Malaria Transition in the Arabian Peninsula 207

probably cannot support transmission of either Plasmodium vivax or Plas-

modium falciparum. Aridity limits transmission across the vast deserts of the
Rub' al-Khali or ‘empty quarter’ in Saudi Arabia and bordering territories
of UAE and Qatar, the desert coasts of Bahrain, Hadramaut Governorate
in the Republic of Yemen and the focal nature of transmission as a result
of aridity in northern Oman. The presence of human hosts is important
for the continued transmission of the malaria parasite. There are ‘climate-
suitable’ areas of the Arabian Peninsula where for decades people have not
lived, and these can be identified using long-term human settlement models
(Goldewijik et al., 2010).The combined effects of low ambient temperature,
aridity and human population density are likely to represent the biologically
maximal limits of malaria risk (Fig. 3.1).
The sub-region encompasses three eco-epidemiological zones of
malaria (palaearctic, oriental and afrotropical) lending itself to large varia-
tion in vectors and parasite transmissions. The distribution of malaria vec-
tors across the Arabian Peninsula is complex and one of the main drivers
of variations in the transmission intensity and the success of control within
and between countries (Zahar, 1974; Beljaev, 2002; EMRO, 1990). Some
of the earliest descriptions of vector-species distribution across the region
come from Buxton (1944), and since then many authors have investi-
gated the presence of Anopheline species across the peninsula as part of
detailed epidemiological investigations (Sinka et al., 2010) or as a pri-
mary function of control activities (Zahar, 1974). Primary malaria vectors
include Anopheles sergentii, Anopheles stephensi, Anopheles arabiensis, Anoph-
eles superpictus and Anopheles culicifacies; less important roles are played by
‘secondary’ vectors including Anopheles claviger, Anopheles d’thali, Anopheles
fluviatilis and Anopheles pulcherrimus. Of the dominant vectors An. sergen-
tii is the most ubiquitous across the region and referred to as the ‘desert
malaria vector’. It makes use of a range of larval habitats, including streams,
oases, date palm groves, irrigation channels, springs, rice fields, and found
in moderately brackish habitats. Anopheles stephensi is located on the east-
ern side of the peninsula along the Gulf of Kuwait, Saudi Arabia, Qatar,
Bahrain, UAE and Oman. In Oman and UAE, the secondary vector asso-
ciated with An. stephensi distributions is mainly An. culicifacies except in
two regions of Oman: Dhofar (An. sergentii) and Musandam (An. fluviatilis).
Anopheles stephensi breeds in various artificial containers in homes and
collections of water associated with construction sites and other industrial
developments. In rural areas, An. stephensi larvae utilise fresh water pools,
stream margins and stream beds, catch basins, seepage canals, wells and
domestic water storage containers. Anopheles arabiensis is located in the
208 Robert W. Snow et al.

Figure 3.1  Map showing the aridity and temperature masks that do not support malaria
transmission (light grey) and areas able to support some degree of stable transmission
(dark grey) on the Arabian Peninsula. Dark lines represent national boundaries; light
grey lines represent sub-national provinces or governorates. Areas unsuitable for stable
malaria transmission represented in light grey developed from temperature, aridity and
population density masks. A temperature suitability index was used to provide a means
to exclude the possibilities of transmission based on the average vector's life-span,
monthly ambient temperature and the duration of sporogony (Gething et  al., 2011).
For extreme aridity, the enhanced vegetation index (EVI) from 12 monthly surfaces has
been used in previous global malaria risk maps to classify into areas unlikely to support
transmission, areas without two or more consecutive months of an EVI >0.1 (Guerra
et al., 2006; Guerra et al., 2008). The history database of the global environment (HYDE)
population dataset provides a modelled projection of population distributions and
densities at a 9 km × 9 km resolution for every decade (Goldewijik et al., 2010). The HYDE
dataset uses national and sub-national population numbers from multiple, time-series
sources and every historical source adjusted to match the current sub-national bound-
aries. Here, we have used a mask to identify those areas in 2000 with population density
less than 1 person per 100 km2. These biological receptive limits are adjusted according
to temporal information on elimination status, medical intelligence and reported case
data for the years 1960, 1970, 1980, 1990, 2000 and 2010, as shown in Fig. 3.10.

west along the Red Sea coast extending from Aden in Yemen to Mecca in
Saudi Arabia. Anopheles arabiensis larval habitats are generally small, tempo-
rary, sunlit fresh water environments. Anopheles superpictus is found only in
the northern territories of Saudi Arabia bordering Iraq and easily adapts
Malaria Transition in the Arabian Peninsula 209

to human-influenced habitats making use of irrigation channels and stor-

age tanks and pools formed from their leakage, rice fields, ditches and
construction sites; it is generally a zoophilic species but opportunistic in
its feeding habits. Anopheles culicifacies is a complex of species within the
Funestus group, highly zoophilic and found in Oman, UAE, Yemen and
Bahrain. Larval habitats include irrigated canals, stream margins, borrow
pits, ponds, domestic wells, tanks and gutters.
Territories across the Arabian Peninsula before the Second World War,
despite rich culturally significant civilisations, were some of the eco-
nomically poorest in the world. Most countries had no functioning road
networks, infrastructure or health care system. The discovery of oil trans-
formed the region within a few decades into a region of rapidly grow-
ing economies able to change their nations into modern societies with
a significant global political influence. By the late 1970s, most countries
were able to expand free medical care and education to their predomi-
nantly young populations and rapidly develop cities and commercial cen-
tres resulting in some of the highest rates of urbanisation worldwide. This
economic growth and requirements for labour brought an influx of foreign
nationals to meet the needs in the oil and gas industries, construction and
support services.
There were limited efforts to control malaria before the Second World
War in the region and largely managed by the colonial medical authorities
in southern Yemen and Bahrain. The exploration and extraction of oil in
Saudi Arabia in the 1940s highlighted the economic impact on the labour
force posed by malaria around oases and signalled the beginnings of aggres-
sive attempts to eliminate malaria. Malaria elimination began in various
parts of the peninsula from the 1960s and was met with varying degrees of
success over the next 40 years. In 2007, the international community reas-
serted a commitment to global malaria eradication (BMGF, 2007; RBM,
2008) by iteratively shrinking the malaria map (Feachem et al., 2010a,b).
Before the launch of the global business plan for control and elimination,
the Eastern Mediterranean Regional Office of the World Health Organiza-
tion (EMRO) introduced the concept of a ‘malaria-free Arabian Peninsula’
in 2005 (EMRO, 2007; Atta and Zamani, 2009), which was endorsed in
2006 at a meeting of Health Ministers of Gulf Cooperation Council (GCC)
States (Atta, 2006; Meleigy, 2007).
Here we present a review of the historical distribution and control of
malaria, pre-1960 to the present day.The review provides an insight into the
context and challenges of malaria elimination and the future threats posed
for the realisation of a malaria-free Arabian Peninsula.
210 Robert W. Snow et al.


The Kingdom was established in 1932 and until the discovery of oil
in 1941 was one of the poorest countries in the world. Oil now accounts for
more than 90% of exports and 75% of government revenue that supports a
free welfare state for its nationals and immigrant labour force including all
funding for domestic malaria control and support for control activities in
neighbouring countries.
In 1935, malaria accounted for 45% of all out-patient attendances in Jed-
dah (Buxton, 1944). It was not until 1947 that attempts were made to docu-
ment infection prevalence at Qatif and Al-Hassa oases on the Gulf coast
and smaller surveys in the interior at Yabrin and Al-Kharj, south of Riyadh
(Daggy, 1959). This area supports breeding sites for An. sergentii and An.
stephensi and is separated from the Najd interior by the Dahna sand dunes.
Oil exploration by the Arabian–American Oil Company began in 1938 and
malaria presented a major public health threat to the 13,000 Saudi employ-
ees. An estimated clinical attack rate was reported of 160 per 1000 popula-
tion per year between 1941 and 1947, with almost equivalent contributions
of P. vivax and P. falciparum. Malaria was also the cause of approximately 12%
of all deaths among the Saudi employee population.The surveys at the Qatif
and Al-Hassa oases showed parasite rates among children aged 0–14 years
between 14% and 100% (Daggy, 1959). In 1948, aggressive efforts to con-
trol malaria were mounted in this area using annual indoor residual spray-
ing (IRS) with dichloro-diphenyltrichloroethane (DDT) and continued
through to 1955 when deildrin replaced DDT, prompted by a rise in case
incidence and suspected DDT resistance. By 1957, cases of clinical malaria
among the employee population had declined considerably; from over 2000
clinical cases in 1947 to 54 cases by 1957, 88% of cases being P. vivax. The
success of the programme was measured using annualised infant and child-
hood parasite rates; by 1956, infant parasite rates were zero (Daggy, 1959).
The Qatif area became a demonstration area for further malaria control
training from 1966.
The success of the Qatif malaria-elimination effort led to the estab-
lishment of the Malaria Control Service (MCS) in 1956. In collaboration
with the World Health Organization (WHO), the MCS launched a pre-­
eradication programme in 1963 and delineated the country into prepa-
ratory, attack, consolidation and preoperational areas (Ministry of Health,
Kingdom of Saudi Arabia, 1963). Over the next 10 years, the programme
Malaria Transition in the Arabian Peninsula 211

began systematically reducing the foci of risks in the eastern and central
regions of the country through IRS using DDT and dieldrin. During the
1960s, locally acquired malaria cases continued to be reported at Qatif; there
were 35 cases in 1964, but rose to between 54 and 231 cases between 1965
and 1969 and declined to only 30 and 12 cases in 1970 and 1971 respec-
tively; the last foci being Awwamiyah. There were no autochthonous cases
from 1972 at Qatif and none from Al-Hassa from 1973 (Sebai, 1988; Jalal
and Lin, 1972). Resistance to both DDT and dieldrin prompted a change
in attack methods that increasingly included larval control with Paris Green
(copper acetoarsenite) and mass drug administration using chloroquine
(Anon, 1984; Amara, 1988) at the other oases and coastal towns of the east-
ern province. In this region, malaria declined significantly, and transmission
was largely interrupted by 1975, despite a continued threat posed by rising
numbers of imported cases and the continued presence of the ­vector (Sebai,
1988; Al Tawfiq, 2006).
There is some reference to parasitological surveys undertaken in the
northern provinces during the 1950s, an area where transmission is sup-
ported by An. superpictus. Infant parasite surveys at Qurayat (1957) and Al
Jouf (1958) showed infection rates of 6 and 12% respectively (Amara, 1988).
From 1965, larviciding, first with Paris Green and then temephos, began
at Al Jouf, Sikakaand and Qurayat. DDT IRS was introduced later, and
by 1971 malaria was reduced significantly through widescale active-case
detection and mass-drug administration in all northern regions and areas
bordering Jordan and Iraq.The vector was thought to have been eliminated
in this region and the parasite reservoir removed. However, in August 1982
An. superpictus reappeared at Doumat Al-Jandal Oasis in the Jouf area but
aggressive larviciding and case-detection ensured that no local transmission
occurred by 1984 (Anon, 1984).
By the mid-1970s, the principal risk areas remained along the Red Sea
coast from the north to the southern borders with Yemen. In these regions,
the dominant vectors were An. sergentii in the north and An. arabiensis along
the southern Red Sea coastal areas. In the north western region, threats
of malaria had always posed a public health risk to pilgrims on the Hajj
(Farid, 1956). Between March 1950 and February 1951, the hospital at
Medina treated 4876 clinical malaria events and reported 343 deaths from
malaria (Farid, 1956). From the 1950s, the control of malaria in Medina and
­Khayber (1957) followed by Mecca and Jeddah (early 1960s) was mounted to
protect the pilgrimage routes travelled by Hajjis. Larviciding in urban areas
and IRS with DDT in households located in rural areas gradually increased
212 Robert W. Snow et al.

in the scope and coverage; in 1971, temephos was introduced to replace

Paris Green as the larvicide, and DDT was stopped as it had failed to inter-
rupt transmission in Khayber and Medina (Amara, 1988). Malaria control
was largely successful in the northern areas of the Red Sea coast and was
finally supported with active, epidemiological case surveillance to identify
the last foci in the most northerly reaches. However, residual foci persisted
and proved harder to control in the lower reaches of the Hijaz Mountains,
where An. sergentii maintained transmission and the persistent An. arabiensis
foci in the foothills of Mecca (Magzoub, 1980; Sebai, 1988). In 1984–1985,
a cross-sectional survey among 3834 children at 18 primary schools in the
Mecca region found 2.1% infected with malaria, 90% due to P. falciparum
(Hammouda et al., 1986), and throughout the early 1980s, malaria contin-
ued to be a cause of severe, life-threatening hospital admissions near Mecca
(El Sebai and Makled, 1987).
By the mid-1970s, the Kingdom had successfully eliminated transmission
from the oil-rich areas of the east, where competence of dominant vectors
for transmission was lowest and the risks from transmission across borders
was minimal (north east). Nevertheless in 1974, it was recognised that eradi-
cation of malaria across the country was not immediately feasible, largely
due to the entrenched active transmission areas of the south western regions
bordering Yemen and the Red Sea coast, areas dominated by An. arabiensis
(Abdoon and Alshahrani, 2003; Al-Sheikh, 2004; Al Zahrani, 2007). In con-
sultation with the WHO, the national malaria programme changed from a
‘pre-eradication’ to a ‘control’ programme based on clearly defined epidemi-
ological annual targets (Amara, 1988).The first attempts at malaria control in
the Asir region began with successful DDT house-­spraying at Wadi Najran
in 1954 and showed a reduction in infant parasite rates from 43% to 0% by
1955 (Chuang, 1986). The DDT programme extended to Wadi Habouna,
Wadi Tathleeth, Wadi Bisha and Wadi Tabala and successfully reduced infant
parasite rates by the late 1950s in this low lying valley to below 1% (Chuang,
1986). In 1974, a malaria station was established at Abha covering the east-
ern and western slopes of the Asir Mountains to ­support reconnaissance of
breeding sites in the low lying areas of this region. Between 1973 and 1976,
IRS with DDT began in some areas of Jizan, Al Lith, Mohayil and Bisha;
however, lack of human resources meant that ­coverage was poor (Amara,
1988).The National Malaria Control (NMC) established a malaria station in
Qunfudha in 1980 and a national malaria training centre in Jizan in 1981,
supporting eight malaria reconnaissance centres along the Tihama straits
from 1983. Since the mid-1980s, an optimistic vector control programme
Malaria Transition in the Arabian Peninsula 213

was mounted in this region using annual DDT residual house spraying in
areas of hyper-endemicity and larviciding with temephos in persistent foci
covering 791 villages in Jizan, and approximately 70 villages in Mohayil,
Qunfudha, Al Lith and Abha (Malaria Control Service-MoH, 1986).
At Shuqayri in Jizan, between 1982 and 1983, combined vector control
approaches were found most effective, with infant parasite rates declining
from 8%-11% under single rounds of DDT to less than 1% when IRS was
combined with weekly temephos larviciding (Anon, 1984). In addition,
Ultra-Low Volume (ULV) spraying was undertaken using the pyrethroid
Reslin in some selected persistent foci in the mid-1980s (Anon, 1986). In
the southern region, DDT resistance, identified in 1986, hampered vector
control and was replaced for IRS with fenitrothion in 1987 (Amara, 1988).
From the mid-1980s, the main attack tools appear to have been weekly
larviciding with temephos and some success was evident with a reduction
in P. falciparum prevalence from 36% (1977) to 7% (1987) reported during
annual mass blood surveys (Amara, 1988).
Contrasting the successes in the rest of the country, malaria control
efforts in the southern region had never achieved a sustained interruption
of transmission. The highest risks between 1980 and the early 1990s have
included focal areas in Qunfudha and Al Lith sectors of Mecca Province,
Asir in the southern region and the most intense transmission covering
much of Jizan Province (Farid, 1992).The 1990s were a period when inter-
vention efficacies were failing, intervention coverage declining and a time
of increased domestic threats posed by terrorism. From 1990, malaria con-
trol remained a vertical programme under the directorate of the MCS with
the aim of maintaining the malaria-free areas safe from local transmission,
combat outbreaks early and reduce disease incidence in highly endemic
areas. During the 1990s, attempts were made to integrate case management
within an expanded Primary Health Care (PHC) scheme. Chloroquine-
resistant case reports began to emerge in the early 1990s (Kinsara et al.,
1997; Malik et al., 1997) with documented treatment failure rates of 12% in
Jizan by 1998 (Ghalib et al., 2001). Overall, the attention given to malaria
control waned. Despite earlier successes in reducing case incidence in the
south during the early 1980s, malaria began to rise in the 1990s and resulted
in a series of epidemic outbreaks in 1992, 1996 and 1998 mainly in Jizan
and Asir. Within one area of Al Baha, a serious epidemic led to over 400
P. falciparum cases in a few months in 1996 (Al Abdullalatif et al., 1996).
From 1986 to 1998, locally acquired malaria cases began to increase in Jizan
Province (Fig. 3.2). The epidemics between 1992 and 1998 affected Jizan,
214 Robert W. Snow et al.

Figure 3.2  Locally acquired, slide-confirmed cases of malaria in Jizan province 1986–
2010. (Data provided in Anon, 1994 and by Dr Ahmed Sahli).

and the epidemiology during these ‘wet years’ changed leading to rising
infection risks. The biggest malaria threats in Jizan exist along the border
with Yemen, and this was seen in 1994 as a major challenge to the future
malaria status of the province given the lack of control activities on the
Yemeni side (Anon, 1994). The border was porous; in 1985, more than 15%
of detected malaria cases were among the Yemenis and their follow-up and
radical treatment was incomplete (Chuang, 1986). In 2003, more than 70%
of total national case burden occurred in the southern region (mainly Jizan
and Asir), of which about 90% of cases were caused by P. falciparum.
The 1998 epidemic resulted in 31,925 local cases of which 61% were
detected in Jizan.This epidemic served to strengthen control efforts and led to
the adoption of the Roll Back Malaria (RBM) initiative as part of a regional
consultation that included stronger intersectoral collaboration, partnerships
and cross-border collaborations. As a result of political commitment, local
support and a general development (infrastructure, housing and electricity),
the number of malaria cases significantly decreased in the southern provinces.
An interesting development was the integration of vector control approaches
in 2000 including surveillance and response to Rift Valley Fever, which was
contained through the intersectoral collaboration between the Agriculture
Department and Malaria Control Programme, and resulted in collateral
­benefits through an abrupt fall in malaria incidence (Al-Seghayer and ­Alattas,
2005). In 2003 Saudi Arabia re-expressed its elimination ambitions.
The objectives of the National Malaria Strategy 2004–2007 were laid
out to re-establish a pathway to pre-elimination with a concentrated effort
Malaria Transition in the Arabian Peninsula 215

in the Southern region and enhanced surveillance in other previously

controlled areas to sustain a malaria-free state. The elimination strategy
emphasises strengthened case management, including the provision of free
artemisinin-based combination therapy to all locally acquired and imported
cases; improved, quality-assured laboratory confirmation of all cases, vector
control (IRS, insecticide-treated nets and space spraying when required),
enhanced geographical information system (GIS) of breeding sites to
­support larviciding, improved surveillance (with active detection and epi-
demiological investigation of all cases) and special emphasis on the threats
posed by cross border movement from Yemen with biannual meetings to
plan and monitor the border coordination activities. Political commitment
remains high with the King and important members of the Saudi govern-
ment involved in promoting the strategy and a provision of US$ 30 million
per year to the ambitions laid out in the strategy. The objectives were
­specifically to prevent reintroduction of local transmission in areas where it had
been interrupted (eastern, northern and central regions); reduce the num-
ber of indigenous cases by 50% between 2005 and 2007 and subsequently
by 100% by 2010; thereafter mount a maintenance phase to ensure that the
country remains malaria-free (Kondrachine, 2004). In 2001, the National
Malaria Control Programme in Yemen was re-established and a collabora-
tive programme to control cross-border malaria was resurrected and revised
since it was first established in 1979. An agreement to support efforts for a
malaria-free Arabian Peninsula was signed by Ministers from both countries
and a cross-border initiative was launched in 2007 (Meleigy, 2007). Cross-
border activities included sharing plans, information, spraying activities
within a 10 km range of the border in Yemen, within and establishing 22
border ‘malaria posts’ offering free screening and treatment. It was estimated
that these activities would target approximately 3,000 border migrants per
day; however, the illegal migrants continue to pose a significant contribu-
tion to transmission as they remain undetected and are often s­ emi-immune
therefore do not seek treatment.
Malaria-elimination interventions intensified between 2007 and 2009;
over 0.5 million long-lasting insecticide treated nets (ITN) were distrib-
uted in the southern region; detailed mapping and reconnaissance of larval
breeding sites served to supported temephos larviciding; and passive, active
and case investigation formed the basis of treating infected people and their
contacts. Following the escalation of falciparum chloroquine resistance
(Kinsara et al., 1997; Ghalib et al., 2001), it was replaced as a first-line
treatment in 2007 with the ACT artesunate-sulphadoxine-pyrimethamine
216 Robert W. Snow et al.

and artemether-lumefanthrine was reserved for a second-line treatment.

Chloroquine plus primaquine continued to be used for radical treatment of
P. vivax malaria. During the second phase of the strategy (2007–2010), the
specific goal was to “…reduce malaria incidence to the level of less 0.5 per
100 000 people, or about 100–120 indigenous cases annually, reported in
the residual active foci only.” A plan was envisaged to develop an “inventory
of malaria foci, identification of their epidemiological status, selection and
application of measures and evaluation. For monitoring the status of foci,
it will be absolutely essential that every case of malaria detected should be
epidemiologically classified. The outcome of epidemiological classification
of cases will serve as a basis for identification of the type of malaria focus”
(Kondrachine, 2004). The Kingdom was then classified by the WHO as a
country “with focal transmission and targeting elimination” (EMRO, 2007).
By 2005, there were no reported local cases from Al Baha and Taif
regions and only four active transmission foci in Asir resulting in 13 locally
acquired cases during that year, four local cases were reported in Qunfudha
from three active foci of transmission, local transmission was identified at
only two foci at Wadi Al Furra, outside city limits of Medina that resulted
in six cases. In 2005, the majority of residual transmission foci (66) were
located in Jizan and led to 125 locally acquired cases (Kondrachine, 2006).
By 2010, only 29 locally acquired cases were detected in the Kingdom
with 11 from Asir and 18 from Jizan (Al Zahrani, 2010). In 2010, there
were however 1912 imported cases across the Kingdom, 30% were from
Yemen. The changing annual incidence of autochthonous malaria cases in
the Kingdom of Saudi Arabia between 1970 and 2010 is shown in Fig. 3.3.

The boundaries of the present day Republic of Yemen have changed
subject to regional power struggles over the last 150 years. In 1937, the city
of Aden and its surrounding villages was renamed the Colony of Aden and
the remaining areas of South Yemen became the British Aden Protector-
ate (Gavin, 1975). In 1963, the Colony of Aden and Protectorate joined
to form the Federation of South Arabia, and in 1967, became the inde-
pendent country of the People's Democratic Republic of Yemen (PDRY)
(Dresch, 2000). In 1918, North Yemen was declared independent of the
Ottoman Empire. From 1962, civil war ravaged the region until 1972 when
North and South Yemen declared they would take steps towards unification,
completed in May 1990 as the Republic of Y   emen. Today the country is
Malaria Transition in the Arabian Peninsula 217

Figure 3.3  Annual incidence of slide-confirmed, locally acquired malaria cases between
1979 and 2010 in the Kingdom of Saudi Arabia per 100,000 population per annum.
Reports of slide-confirmed, locally acquired cases used for 1975–1979 (Malaria Control
Service Ministry of Health, 1980); 1990–2010 EMRO database. Population data have
been sourced from several publications: 1992, 2004, 2007 and 2010 (Central Depart-
ment of Statistics and Information, Kingdom of Saudi Arabia, 2011); 2009 (Saudi Arabian
Monetary Agency, 2011). All other years have been estimated using intercensal growth

the poorest and least developed of all its neighbours on the peninsula and
­continues to face civil unrest and conflict.
Records of malaria risks are available from the earliest periods following
the occupation of Aden by the British. In 1933, Colonel Phipson conducted
a medical survey across the Aden Colony and Protectorate discovering that
malaria was practically nonexistent around the Aden port and its surround-
ing villages. Extremely low levels of mosquitoes were detected and the use
of bed-nets was thought unnecessary. The few patients that were diagnosed
with malaria came from the inland areas of the protectorate and presented
with P. falciparum on most occasions (Phipson, 1933; Buxton, 1944). A few
kilometres north of the port of Aden at the oasis of Sheikh Othman, malaria
was of more serious concern, and cases were regularly documented at the
Keith Falconer Mission Hospital (Fig. 3.4). In 1909, Lt. Colonel Wightwick
began an antimalarial scheme based on the approaches of environmental
management, using kerosene of mapped larval breeding sites advocated by
Sir Ronald Ross.There was a protracted period through to the 1940s where
water pools in mosques and ponds were sprayed with Gammexane dispers-
ible powder (WHO-Aden, 1956). Malaria re-established itself as a major
218 Robert W. Snow et al.

Figure 3.4  Malaria admissions to Keith Falconer Mission Hospital, Sheikh Othman,
Aden 1907–1933 (Phipson, 1933). At the Mission Hospital, case incidence dropped from
over 1900 cases in 1907 to 460 locally acquired cases by 1915 following environmen-
tal management and larviciding. During the First World War, the control of malaria was
interrupted but resumed in 1922 with increasing success at mapping breeding sites in
surrounding villages (including Dar-al-amir, Lahej and Halwan) and cases reported at
the mission hospital declined to very low levels by 1933 (Phipson, 1933).

cause of admission to the renamed Sheikh Othman Hospital in 1943 and

spleen rates were recorded among children living at Wadi Milah, Musiemir
and Tom el Baha exceeding 75% (Petrie and Seal, 1943). In North Yemen
including most of the area from Ta'iz to the Saudi border, some antimalarial
measures were implemented prior to 1956; construction of canals, renewal
of water in the ponds at mosques, removal of stagnant water, regular aerosol
DDT spraying, periodic distribution of quinine at military barracks and
schools in Sana'a and Al Hudaydah (WHO-Yemen, 1956).
After the Second World War, the Abyan Cotton Board was established to
help improve irrigation across the Abyan district in the Aden Protectorate.
During the construction period, high levels of morbidity and mortality were
recorded due to malaria amongst labourers, which prompted antimalarial mea-
sures to be established between 1949 and 1954. Larviciding using 5% DDT
occurred across the entire district operated by a health assistant, 8 spray men,
8 labourers and 8 donkeys. As a result of intense larviciding, malaria transmis-
sion was reportedly interrupted; however, the entire scheme cost US$ 28,000
a year. To make it more cost-effective, in 1954, the programme changed to
residual spraying with the organochloride benzene hexachloride in all houses
in the district four times a year. Due to lack of insecticide, spraying was rarely
Malaria Transition in the Arabian Peninsula 219

completed by 1961. An increase in malaria cases was observed after the con-
trol was stopped (Colbourne and Smith, 1964). At this time, the malaria pro-
gramme lacked skilled leadership, the highest qualified member of 65 staff was
a technician and the WHO-trained medical officer left the country.
Prior to 1941, it was believed that Sana'a was malaria-free and that the
majority of cases came from the lowlands of the Tihama plains. During the
Second World War, cases of malaria in Sana'a remained low, but in June 1946,
a malaria outbreak occurred with a sharp rise in the malaria mortality rate
(4.3 per 1000 residents); cases were considered local as the majority of cases
lived less than 10 km away from the city of Sana'a (Audisio de Marchi
and Audisio, 1952). In 1951, a general medical survey was conducted to
assess the health and sanitary conditions in the three western regions of
Yemeni Arab Republic (YAR): 289 thick and thin films were examined for
malaria parasites as part of the survey revealing positivity rates of 28% at Ta'iz
(P. falciparum and P. vivax), 2% at Al Hudaydah (P. falciparum and ­Plasmodium
malariae), and 1.5% at Sana'a (P. vivax only) (Mount, 1953).
From the 1970s, the epidemiology of malaria across Yemen was charac-
terised according to topographical criteria (Thuriaux, 1971; Kouznetzov,
1976; Kravchenko, 1978) and loosely linked to a spleen survey of 35,000
people undertaken in the mid-1970s (Kravchenko, 1978) and other parasite
prevalence data (Mount, 1953; Thuriaux, 1971; Kravchenko, 1978). These
strata continue to be used today (NMCP Yemen, 2006) to define priority
control areas and include: the mesoendemic coastal plains, including Tihama,
characterised by low rainfall and extensive wadis; foothill regions between
200 and 2000 m above the sea level of hypo-mesoendemicity; the epidemic
prone desert areas including Hadramaut Governorate; the dry, mountainous
highland plateau (above 2000 m) where large parts are malaria-free (includ-
ing Sana'a); and Socotra Island that was meso-hyperendemic and a unique
separate ecology. In the 1970s, 95% of all infections were due to P. falciparum,
4% due to P. malariae and less than 1% due to P. vivax (Kravchenko, 1978).
Plasmodium ovale was conspicuous by its absence in most reports and the
first case of P. ovale was detected at Beni-Hussan village, in Bajil district, Al
Hudaydah Governorate in 1998 (Al-Maktari and Bassiouny, 1999).
In collaboration with the WHO, the first national malaria control plan
was established in 1969 with the PDYR, with a base at Aden. In 1978, a
similar plan was established with the YAR that led to the establishment of
the Malaria Control Programme (MCP) at Al Hudaydah to support larval
control using temephos and IRS using DDT across the Tihama plains, a
project jointly supported by WHO, to serve as a pilot project to expand
220 Robert W. Snow et al.

nationally with time (Shidrawi, 1980a). In 1979, health centres and hospitals
were encouraged to routinely collect blood slides from febrile outpatients
and report to the MCP but institutionalised more rigorously at nine sentinel
centres across Al Hudaydah Governorate. Baseline cross-sectional data showed
that the Al Hudaydah Governorate was mesoendemic with higher prevalence
rates in the foothills near the Ta'iz Governorate, parasite rates ranging from
28% to 38% (Shidrawi, 1980a). The national malaria control plan proposed
the expansion of field sites to include six malaria units, 12 malaria posts and
three entomology units, including staff and commodity costs; it was estimated
that US$ 400,000 would be necessary to implement the plan from the gov-
ernment and WHO funds (MoPH, 1981). However, lack of administrative
support, unsatisfactory organisation of a special budget for malaria, delays in
salaries and travel expenses led to a halt in the entire programme by the end
of 1980 (Shidrawi, 1980a). Between 1978 and 1988, in both the PDRY and
YAR, most control activities focussed on attacking larval and adult forms
of the vector using larvivorous fish (Aphanius dispar) in wadis across Abyan
Governorate (Amini, 1988) and the use of temephos alone or in combina-
tion with DDT IRS in the Thiama plains area and foothill regions (Shidrawi,
1980a; Assabri, 1989). In 1989, 30,000 people were protected by DDT IRS
(concentrated at Wadi Rima) and 67,000 people were living in areas where
temephos was used in wadis (Moar, Toor, Siham, Sardood, Zabid) (MoH
Yemen, 1989). Between 1983 and 1988, overall national fever-tested slide
positivity remained unchanged (Anon, 1988; Assabri, 1989), although some
reductions were noted at the sentinel sites of Zabid and Al Zohra, attributed
to IRS and larval control respectively (MoH Yemen, 1989). Towards the end
of the 1980s, as part of the third national health plan, malaria became inte-
grated within a programme of PHC, and 722 village health guides were
trained to presumptively treat fevers (Delfini, 1986; Anon, 1988).
By 1992, funding for residual spraying and larval control stopped as a
direct result of political unrest during this period (Beljaev, 1997).This coin-
cided with the spread of chloroquine resistance, first detected at Al Makatra,
Ta'iz Governorate in 1987 (Berga, 1999; Abdel-Hameed, 2003). By 1997,
the Republic of Yemen had the highest malaria case burdens of the entire
Arabian Peninsula with over 380,000 reported cases (highest incidences in
Al Hudaydah, Abyan, Hajjah and Mahwet Governorates) and endemicity
levels comparable to large parts of Africa in some areas (Mashaal et al., 1998).
In June 1996, unexpected heavy rains led to flooding in several parts of the
country, particularly in traditionally arid areas, that resulted in over 24,000
clinical cases and 475 malaria deaths within a few months (Beljaev, 1997).
Malaria Transition in the Arabian Peninsula 221

Two years later, the El Nino 1998 epidemic doubled the national slide posi-
tivity from previous years, and it was estimated that approximately 1 million
cases might have occurred during this year, with a very rough estimate of
between 5000 and 10,000 deaths (Souleimanov, 1999). In November 1998,
1175 school children were examined for infection across the Tihama region
of Al Hudaydah Governorate, the slide positivity rate was 48% (Mashaal,
1998). The epidemic had one positive consequence – it served to galvanise
government action to strengthen the malaria control programme.
In March 2001, the National Malaria Control Programme (NMCP)
was established under the presidential appointment of a Supreme National
Malaria Control Committee. The NMCP moved back to Sana'a, from
small offices based at Jaar in Abyan Governorate, to take forward a National
Malaria Strategic Plan (2001–2005), developed following adoption of the
global RBM initiative (NMCP-Yemen, 2001). The government increased
its annual budgetary allocation from US$ 0.25 to 2 million at the launch
of the strategy; the Global Fund (second round) approved US$ 12 million
for 5 years from 2002, and Yemen received additional financial support from
some Gulf countries (Saudi Arabia, Oman and UAE). The organisation of
malaria control across the country was so dysfunctional that the programme
started building the infrastructure and capacity from scratch. The expanded
delivery of integrated vector control began in areas of highest risk – the
Tihama coast from the Saudi border to Ta'iz, selected districts in foothill
and mountain areas and Socotra Island. The control approaches included
larviciding with temephos (approximately 400 l used per month in 2002),
lambda-cyhalothrin IRS (514 tons used in 2002) and biological control
using A. dispar at a small scale in Tihama region and Socotra Island. In 2005,
coverage increased to over 40,000 households receiving IRS, 48,000 ITN
distributed and 2180 km2 potential breeding sites covered with larvicides
(Ali, 2005). By 2002, acceptable clinical responses to chloroquine were only
43–54% at three drug sensitivity-monitoring sites at Bajil, Musemir and
Udayn (NMCP Yemen, 2006), and this prompted a transition in Novem-
ber 2005 to artesunate-sulfadoxine/pyrimethamine as a first-line treatment
for uncomplicated falciparum cases, supported by a second-line treatment
using artemether-lumefantrine (Anon, 2007). There has been no system-
atic review of the morbidity impact of the increased intervention coverage;
however, compared to the November 1998, Tihama plains school malaria
infection surveys showing 48% infection prevalence recorded at its maxi-
mum post-epidemic peak, school surveys undertaken in Tihama in March
2003 showed prevalence rates of only 7% (NMCP Yemen, 2003).
222 Robert W. Snow et al.

Socotra Island, with a small population of 43,000 people living on

3650 km2 about 400 km from the Yemeni coastline, had one of the highest
recorded transmission intensities in Yemen. Clinical cases transmitted by a sin-
gle vector (An. culicifacies) presented as both P. falciparum and P. vivax. During the
mid-1980s, DDT IRS was deployed on the island but discontinued following
recommendations to adopt temephos as an approach to target larval stages in
1989 (Farid, 1988). Control was sporadic and unregulated on this inaccessible
island, until 2000. In September 2000, an elimination demonstration project
was established using extensive larviciding with temephos across the island,
followed in 2002 by IRS spraying using lambda-cyhalothrin (Kondrachine,
2009). No locally acquired cases were reported on the island from 2006 (Fig.
3.5) (EMRO, 2008). Socotra's success was a boost for the National Malaria
Control Programme to initiate those efforts into the mainland.
The second National Malaria Strategic Plan was launched in 2006 to
cover the period up to 2010, using similar approaches to control and similar
ambitions to the previous five-year strategic plan, reducing 2000 morbidity

Figure 3.5  Monthly slide confirmed cases 2000–2010 on Socotra island (Anon, 2009).
According to the census in 2004, Socotra Island had a population of 43,000 people. 50%
of the population live in two settlements, Hudaibo and Qalansia. The rest of the popula-
tion live in scattered villages across three ecological zones: Coastal (0–400 m above sea
level), foothills (400–700 m) and hills (above 700 m). Anopheles culicifacies is believed to
be the major malaria vector in all geographical areas of the island. In September 2000,
the Plan of Action for Malaria Control in Socotra was launched and implemented with
funding from the government, Oman, Italy and WHO. Operational personnel included a
director, team leaders in operations, supervision, malaria case management and health
education, six supervisors and 37 spray-men. Larviciding with temephos across over
5000 mapped breeding sites began in 2001. Over 5000 ITN were distributed between
2002 and 2005. Between 2004 and 2008, 25,000–30,000 people were protected with
­bi-annual IRS using lambda-cyhalothrin (Kondrachine, 2009).
Malaria Transition in the Arabian Peninsula 223

by 75% by 2010 by sustaining the gains and improving progress towards

coverage targets established in 2001. In addition, the 2006 strategy pledged
to support the regional vision of a malaria-free Arabian Peninsula by 2015
(NMCP Yemen, 2006) and reaffirmed its commitment to work with Saudi
Arabia to control malaria along their borders; an initiative first launched in
1993 (EMRO, 1993) but restarted in February 2004. In 2008, the Global
Fund approved US$ 27 million to provide support to the second national
strategic plan. During a national household sample survey in 2009, 11%
of households had received IRS in the preceding 12 months and 27% of
households owned at least one ITN. Overall slide positivity from 12,902
persons sampled was only 1.5% (NMCP Yemen, 2009). Despite the limita-
tions of accuracy and coverage of reporting, the rise and fall of presumed
malaria burdens in Yemen since 1979 is shown in Fig. 3.6.

Figure 3.6  Annual presumed malaria case incidence between 1979 and 2010 per
100,000 population per annum across the combined territories that constitute the
present day Republic of Yemen. (Data sourced from Anon (1981), Jamal Amran unpub-
lished data (2006), Anon (2010) and EMRO Database (2012)). No distinction is made in
the available reports between locally acquired/imported infections nor is it possible
to define slide confirmed/presumptively treated for the entire surveillance period, and
therefore cases included are regarded as presumed malaria diagnoses. However, by the
mid-1980s, it is thought that reported cases were confirmed cases only. From the 1980s
onwards, it is not possible to distinguish the slide-confirmed and presumptively treated
malaria cases. The national malaria indicator survey in 2009 reported that only 56% of
all fevers sought any form of treatment, and therefore it is additionally likely that many
fever cases that are malaria go undetected (NMCP Yemen, 2009). Population has been
estimated from several projections (Yemen Central Statistics Organization, 2010), com-
bining YAR and PDYR estimates and based on the first census of the Republic in 1994
where nonreported years computed from intercensal growth rates, including pre-1994
census using the intercensal growth rate (2.91%).
224 Robert W. Snow et al.

The recently launched national strategy (2011–2015) states that by the

end of 2015, the burden of the malaria disease in Yemen will be reduced,
through the adoption and wide implementation of evidence-based malaria
control interventions, to levels that warrant the embarkation of the NMCP
on malaria pre-elimination (MoPH and P, 2011). Particular emphasis in
the revised strategy is given to establishing a much stronger epidemiologi-
cal platform to deliver control, including an adapted stratification to guide
integrated vector control methods and improving access to treatment, diag-
nosis and case-reporting in the revised strategy. Consistent with strategic
trends in Saudi Arabia over the last decade,Yemen also recognises the need
to embrace intersectoral collaboration, strengthen partnerships and sustain
cross-border collaborations to achieve its ambitions by 2015.

The Sultanate of Oman is characterised by a large desert plain that
covers most of central and southern regions of the country interspersed with
wadis. Mountain ranges are found along the north (Al Hajar Mountains) and
southeast coast, and the country's main cities are also located at high altitude
including the capital city Muscat, Sohar and Sur in the northern mountain
regions and Salalah in the south. The peninsula of Musandam is a strategic
location on the Strait of Hormuz but separated from the rest of Oman by
the UAE. Early Sultans sought to extend their influence along the East Afri-
can coast as far south as Mozambique, and most notable was the relocation
of the Sultan to the Island of Zanzibar (Horton, 1987). Thousands of Oma-
nis today can trace their lineage, and continue to have links with, East Africa.
Oil exploration began in 1967 that heralded the country's modern devel-
opment, and the Omani economy has been radically transformed over a
series of development plans since 1976. Before 1970, there were few asphalt
roads and no ministry of health. About 50% of the 2.6 million population
lives in Muscat and the Batinah coastal plain northwest of the capital; about
200,000 people live in the Dhofar (southern) region, and about 30,000 live
in the remote Musandam Peninsula.
Buxton (1944) cites work by Gill in 1916 who reports that fever was a
common debilitating illness among troops stationed at Muscat with admis-
sion rates between 100 and 400 cases per 1000 soldiers per month and that
the cases were predominantly P. falciparum. Over 90% of infections in the
1970s were a result of P. falciparum; P. vivax and P. malariae were rare and only
one case of P. ovale had been documented by 1979 (PHD, MoH, 1979).
Malaria Transition in the Arabian Peninsula 225

Parasitological surveys undertaken across Oman during the early 1970s sug-
gest that most of the northern areas were mesoendemic with the highest
rates of infection recorded in the Batinah (13% infection prevalence among
school children) and the islands (including Masira) and the southern regions
were either malaria-free, hypoendemic or had high epidemic potential at
wells, oases and wadis (Farid et al., 1973). It seems reasonable therefore to
regard Dhofar and the Omani Islands as unstable transmission areas in 1970.
The National Central Malaria Control Section (CMCS) of the Preventa-
tive Medicine Department, Ministry of Health, began work in 1970 (PHD,
MoH, 1979; MoH, Oman, 2011a). Following a nationwide malaria survey
that showed parasite rates between 3% and 49%, a control programme was
started in January 1975 with financial assistance from the United Nations
Development Programme (UNDP). By the middle of 1978, 17 malaria
units had been established in the northern region and the malaria control
staff had increased from 14 to 100. A malaria training centre, to overcome
shortages in trained staff, was established in 1979. The principal aim of the
first control programme was to target source reduction through biologi-
cal control with indigenous larvivorous fish (A. dispar) but met with only
partial success. The programme moved to larviciding with temephos fol-
lowing the pilot projects along the coastal strip at Seeb and extended from
1977 to 1979 to include Samayel, Bahla, Mudarib, Sohar, Saham, Khasab,
Jue, Buraimi, Nizwa, Bahia, Hamia, Qurayat and limited areas in Bani Bou
Hassan, Bilad, Bilad Sur and Jalan. A key feature of the vector control pro-
gramme in Oman was the very detailed mapping of risk areas from aerial
photography to guide larval control from early in the programme's history
in 1975 (Zahar et al., 1982).Weekly chloroquine prophylaxis of school chil-
dren during the months of September to May in highly endemic areas was
undertaken in collaboration with the Ministry of Education between 1973
and 1979 (Shidrawi, 1980b; Matta, 1984). This programme was stopped in
Muscat in 1980 and in Salalah in 1981. By 1982, in areas protected by DDT,
prophylaxis was stopped in part due to fears of emerging resistance, and
chloroquine was reserved for use by pregnant women and young children
(Matta, 1984).
From 1976, DDT residual spraying was expanded following a trial at
Shinas in Batinah Province to areas of Dank and along the Buraimi ­border
area with the UAE (Zahar et al., 1982). Between 1976 and 1992, it was
estimated that approximately 0.14 million tons of DDT were used for IRS
in Oman (Al-Wahabi and Parvez, 2002). However, the IRS campaign never
really reached a maximal coverage; for example in Batinah Province, annual
226 Robert W. Snow et al.

rounds of DDT house spraying declined from 1976, where more than 90%
of houses were sprayed, to less than 50% by 1981 (Shidrawi, 1982). DDT
resistance was first detected in larvae of An. culicifacies in 1980 (Zahar et al.,
1982). The use of DDT was finally stopped and replaced with Fenitothion
in 1993, partly because of the technical difficulties in maintaining high
coverage (Al-Wahabi and Parvez, 2002) and because of recorded escalat-
ing resistance. By 2003, An. culicifacies was resistant to both insecticides
(Al-Wahabi et al., 2003).
The programmes in the 1970s and early 1980s had only partial suc-
cess, largely because of shortages of staff, funding and transport (Shidrawi,
1980b). Summarising the malaria situation in 1981, Zahar and colleagues
described most of the northern populated areas as experiencing hypomeso-
endemic transmission with the coastal strip of Batinah province having the
highest transmission and the southern area of Dhofar province suffered only
sporadic outbreaks (Zahar et al., 1982). By 1983, parasite prevalence among
school children in the Batinah, Musandam, Buraimi and all other provinces
remained between 3% and 10%, at Wadi Jizzi parasite rates were above 10%
and overall it was felt that the DDT spraying campaigns had little impact
since they started in 1976 (UNDP, 1987).
The malaria action plan covering the period 1981–1985 was managed
by a newly formed intersectoral Malaria Control Coordinating Board and
the programme largely funded by UNDP and the Cooperative Funds of the
Gulf Health Secretariat. This five-year plan focused more on DDT IRS in
rural areas supported by the mass drug administration (using chloroquine)
provided during spraying times. One single round per year was planned
for the coastal area during September/October and for the interior and
mountainous areas in February/March. Priority for IRS was given to the
border areas with UAE. Temephos larviciding continued in the urban areas
and rural suburbs for 8 months a year with the possibility of using larvivorous
fish and engineering methods for larval control in priority breeding sites as
defined by the CMCS. Drug prophylaxis to school children in rural areas
was suspended during this period of control. By 1985, it was hoped that the
expansion of malaria control in the Oman Sultanate would result in almost
negligible transmission along the borders with UAE and a yearly reduction
of 35% in malaria prevalence among school children aged 6–9 years. Notable
risks of infection continued through the 1980s along the border with
UAE and both countries agreed in the late 1980s to supervise each other's
control efforts and maintain a coordinated effort to eliminate the vector-
breeding sites in these areas. This coordinated effort led to only marginal
Malaria Transition in the Arabian Peninsula 227

success and cases detected in UAE were often labelled as originating from
the Omani side of the border.
The programme was re-evaluated in 1991 and the Ministry of Health
launched its programme of Eradication, with the ambition of completely
interrupting transmission and eliminating the reservoir of infected cases
(MoH Oman, 2011b; Delfini and Abdel-Majeed, 1993; Mashaal, 1998).
Malaria was made the only disease in Oman to be treated free of charge
(Mashaal, 1998). Special attention was continued to be given to the border
areas with the UAE who saw Oman as a threat to their elimination agenda.
The revised malaria plan organised the country according to eco-epide-
miological criteria and defined coastal, foothills, desert oasis areas, islands
and Dhofar to guide its selection of targeted control approaches (Matta,
1984). The first phase began with a technical, administrative and practical
feasibility of the programme and a pilot project in Sharquiya region. After
the 1991 pilot, the elimination strategy was extended to neighbouring areas
of Qurayat in Muscat Governorate in 1992 before extending to Batinah
Governorate in 1994 and the programme was extended spatially with time
to all of Muscat Governorate (1995), Musandam Governorate (1996) and
the Dhahia region (1997).
The programme continued to build its intelligence of risk using
detailed geographic reconnaissance based on larval survey mapping and
school based infection prevalence surveys. The strategies used as part of
the elimination strategy were almost entirely anchored on source reduc-
tion using temephos and the passive and active detection of malaria cases.
Supplementary vector control measures included imagociding operations,
­biological, ­environmental management measures and occasional IRS using
lambda-cyhalothrin were implemented as required. All suspected cases were
­parasitologically diagnosed under a quality assured programme of upgraded
laboratory services. Vivax patients were treated with chloroquine and
­primaquine and imported falciparum cases with a combination of quinine,
Fansidar and primaquine. In the last few years, treatment policy for the
falciparum cases has changed to artemether-lumefantrine for all imported
cases. A policy of chemoprophylaxis was introduced for all travellers to East
Africa, where many imported cases from Zanzibar continued to be detected.
One of the main pillars of the elimination programme was the combined
passive and active surveillance of new cases and case investigation. Passive
surveillance included all the 231 peripheral health facilities maintained by
the ­government, an engagement with the over 500 private sector health
providers to improve parasitological diagnosis and reporting and a public
228 Robert W. Snow et al.

awareness campaign. Active case detection included screening of all travellers

arriving from East Africa at Seeb Airport and the follow-up of all positive
cases to screen neighbourhood contacts and periodic school surveys.
During the late 1980s, it was estimated that there were up to 300,000
clinical malaria cases of malaria each year (MoH Oman, 2011b). Between
1994 and 1999, the annual incidence of locally acquired malaria dropped
from 21.5 per 10,000 population to 0.1 per 10,000 population (Fig. 3.7). By
1999, 77% of the population was under an elimination strategy while the
remaining areas of the country were under a phase of control; there were
no malaria deaths reported, and malaria infection prevalence among school

Figure 3.7  Annual locally acquired, slide-confirmed malaria cases both locally
acquired and imported in Oman 1976–2011 per 100,000 resident populations; insert
shows only locally acquired notified case incidence 1995–2011. Before 1994, malaria
was not a notifiable disease and imported versus locally acquired cases were not
distinguished. The graph shows all slide-confirmed cases of malaria detected in the
Sultanate of Oman between 1976 and 2011 as dark bars. Various authors and reports
have assembled estimates of locally acquired slide-positivity rates from clinic records
before 1994 including the periods 1976–1979 (Zahar et al., 1982), 1980–1985 (EMRO,
1987), 1986–1988 (WHO, 1989) and data 1988–1993 from the Omani MoH Statistics
office (MoH Oman, 2009). Data for the period 1994–2011 are from the EMRO database.
The insert is from 1995 to 2011 showing the incidence of only locally acquired cases
all foci rapidly identified and EMRO regard Oman as malaria-free today. Population has
been sourced from several publications: 1993–2002, 2004 and 2006–2010 (Sultanate
of Oman Ministry of National Economy, 2012); 2003 (MoH, Oman, 2003) and 2011 (UN
population projections, 2011). All population estimates prior to 1993 have been calcu-
lated using intercensal growth rates.
Malaria Transition in the Arabian Peninsula 229

children had declined from 2.2% in 1990 to 0.003% in 1998 (Khalifa, 1999).
In 1996, a focal epidemic occurred in Nizwa in Dakhliya affecting 16 chil-
dren and at Debba in Musandam affecting 10 people (Mashaal, 1998). After
1999, school infection prevalence surveys were suspended in 2000 due to
their insensitive nature at very low transmission intensity. By 1999, only 29
of all identified cases were considered local, of which 14 were detected near
the Bilad mountainous areas in Musandam province (Mashaal, 2006). By
2000, there were no locally acquired cases (Al Zedjali, 2010). Threats from
unregulated, illegal migration continued to challenge the programme, nota-
bly in the mountainous areas of North Batinah (Mashaal, 2000). Between
2000 and 2003, a total of 20 cases were detected; between 2004 and 2006,
there were no cases. In 2007 and 2008, 4 and 8 autochthonous cases were
detected in Dakhliya and North Batinah regions respectively (EMRO,
2010). In 2010 and 2011, 24 and 13 locally acquired cases were identified as
part of combined active and passive case detection (Fig. 3.7).
There continues to be outbreaks of locally acquired cases following
importation since 2007 and the challenge has been to maintain strong
surveillance for early detection and treatment of all cases – proper timely
epidemiological investigation of cases and foci especially with increasing
vulnerability. While receptive risks have probably reduced substantially by
targeting vector larval sites rather than reducing adult vectors, vectors con-
tinue to be identified, and vigilant larval control is necessary to protect
against the highly vulnerable nature of imported infections from East Africa
and the Indian sub-continent. Almost 30% of Oman's population today
comprise foreign nationals. Monitoring of breeding sites and their man-
agement with temephos remain a priority. There was no documented evi-
dence of temephos resistance by 2006, but reduced mortalities (80%) were
observed in bioassays of An. stephensi larvae in Dhahira in 2010. Recom-
mendations have been made to begin using biological agents such as Bacillus
­thuringiensis (Andreason, 2006). Figure 3.7 shows the declining incidence of
locally acquired cases in the Sultanate of Oman since 1994 when epidemio-
logical investigations of reported cases distinguished between imported and
local infections. Given the sporadic nature of new cases over the last 10 years,
all rapidly contained, EMRO considers Oman ostensibly malaria-free today.


UAE has approximately 200 small islands in the Gulf and a sea bor-
der of 650 km that encompasses coastal salt flats (‘sabkha’). Approximately
230 Robert W. Snow et al.

80% of the country is desert merging with the Rub' al-Khali of Saudi
Arabia; however, there are oases, notably the large oasis settlements at Al
Ain, Liwa and several others towards the borders of Qatar and Saudi Ara-
bia. Fertile plains are fed by mountain ranges in Ras Al-Khaimah Emirate.
The sea and the desert provide natural barriers to malaria transmission in
the UAE. Oil was discovered in the early 1960s and revenues were used to
accelerate development. In 1971, the Trucial States became the UAE and
today is constitutionally run by a federation of seven emirates: Abu Dhabi,
Ajman, Dubai, Fujeirah, Ras Al-Khaimah, Shariqah, and Umm Al-Quwain.
Abu Dhabi is the largest of the seven emirates, and Abu Dhabi City is the
capital of the UAE.
During the early 1970s, the country was divided into two main epide-
miological strata (Farid, 1977). The first stratum was the highly endemic
areas, including the emirates of Ras Al-Khaimah, Shariqah, Fujeirah, the
east along the Omani border and the central plateau. Across Fujeirah, in
April 1969, P. falciparum parasite rates among children were 43% and 12%
for P. vivax; at Shariqah corresponding figures were 26% P. falciparum and
14% P. vivax; and across Ras Al-Khaimah prevalence was 12% P. falciparum
and 4% P. vivax (Zahar, 1969). The dominant vector reported for this stra-
tum was Anopheles culicifaces (Farid, 1977). The second dominant stratum
was the low-risk region encompassing the coastal strip from Abu Dhabi to
Umm Al Quwain and Ajman and included the oasis areas of Al Ain where,
in 1977, spleen rates among school children were 6% and the dominant
vector was An. stephensi (Farid, 1977). The rapidly growing economy in the
1970s led to major construction works requiring imported labour from the
Indian sub-continent that transformed the epidemiological risks, including
increased transmission of P. vivax (Farid, 1977).
Malaria control began across the emirates in 1970. Annual rounds of
DDT spraying were mounted at labour camps, space spraying in densely
populated areas or near breeding sites and fortnightly temephos larviciding
across all rural areas. Occasionally, the school health department distributed
chloroquine as part of mass drug administration, as practised in areas within
neighbouring Oman, but this was not coordinated with the malaria service
and little information is available on the extent of this practice. An attempt
to devolve control responsibility to district levels in 1975 did not provide
harmonised and complete coverage, DDT was stopped during this year
and a lack of central leadership meant that drugs, insecticides and support-
ing commodities were not ordered; peripheral malaria staff then undertook
other non-malaria activities. The parasitological diagnosis of malaria was
Malaria Transition in the Arabian Peninsula 231

incomplete and inadequate at most peripheral health facilities and there was
no functioning health information system by 1976 that hampered effective
malaria planning (Farid, 1977). A series of malaria epidemics were reported
between 1975 and 1977 and prompted the re-establishment of the Central
Malaria Department (CMD) in 1977.
Between 1977 and 1984, DDT IRS was the mainstay of malaria control
as part of a vertical programme to reduce malaria risk in the high-risk strata,
complimented with larviciding and reports of ULV space spraying with
neopyburthrin in urban areas of focal risk. The programme was directed
to cover operational zones under the leadership of a federal, vertical pro-
gramme that received 1.2% of the national health budget in 1979 equivalent
to US$ 300,000 (Farid, 1981). By 1979, a system of malaria reporting had
been introduced that assisted in planning the control programme, although
it was recognised that the reported cases were likely to be less than the
actual cases (Farid, 1981). In addition, entomological mapping, surveillance
and a census of construction sites helped guide intervention. By 1980, the
number of malaria cases had declined; Al Ain, Dubai and Abu Dhabi were
reported as malaria-free without any vectors; however, resistant foci contin-
ued to pose a problem for control in Ras Al-Khaimah and along the Omani
border at Debba where communities refused larviciding (Farid, 1981).
Meetings between the malaria programmes of the Sultanate of Oman and
UAE were held twice a year to coordinate activities in this area. From 1984,
IRS was gradually replaced, following detection of DDT resistance, by the
detection of vector-breeding sites and their weekly or fortnightly treatment
with temephos, including later with larvivorous fish (A. dispar and Tilapia),
and improved surveillance. By 1987, the malaria funding provided from the
federal health budget increased to US$ 2.5 million.
In 1990, a more intensive case-register surveillance system was intro-
duced combining active and passive-case detections, treatment of confirmed
malaria cases, epidemiological investigation of cases and foci, and posttreat-
ment follow-up of the malaria cases. Active case detection was gradually
phased out as comprehensive health facility coverage across the country
became established. The proportion of cases originating from autochtho-
nous malaria transmission in 1990 was 0.46% but declined to 0.04% by
1997. The last autochthonous case of vivax malaria was recorded at Mas-
foot in the Central Plateau, in 1997 (Kondrachine, 2001; MoH-UAE, 2002,
2007; Fikiri, 2010;Wernsdorfer, 2004; Fig. 3.8). Despite the heavy rainfall in
1998 and 2004 across the receptive central plateau region, no local transmis-
sion occurred. In 1998, the national malaria plan was redesigned from the
232 Robert W. Snow et al.

Figure 3.8  Annual, locally acquired case incidence per 100,000 population in the
United Arab Emirates 1990–2005. Locally acquired case data provided by MoH-UAE
(2002). The last case of locally acquired malaria was vivax and reported in 1997.
UAE was certified malaria-free in 2007. Annual population estimates derived from
UAE National Bureau of Statistics (2006) and all noncensus years have been esti-
mated using intercensal growth rates.

one supporting control to elimination, and within a few years the CMD
staff across the country was 240 full-time employees with 47 based at the
headquarters in Sharjah.
UAE managed to escape the threats posed by chloroquine resistance
elsewhere, and given the increasing numbers of P. vivax cases from India,
Bangladesh and Pakistan continued to use chloroquine and the 14-day treat-
ment regimen primaquine from 1990s. In 2006, the drug policy changed to
support the use of artemether-lumefanthine for uncomplicated falciparum
imported malaria cases, in-line with regional policy, while chloroquine and
primaquine continued to be used for vivax cases.
Strategies to maintain the malaria-free status in the UAE from 1999
included surveillance at clinics runs by both the public and private sec-
tors, detailed case investigation, traveller advisory awareness on the need for
prompt fever investigation, vector-breeding surveillance including a detailed
GIS reconnaissance, continued use of temephos and larvivorous fish, the
monitoring of insecticide resistance and high profile, politically supported
malaria-free awareness days on 28 December. A request for the certification
of malaria-free status in the UAE was submitted in 2002. There followed
Malaria Transition in the Arabian Peninsula 233

three review visits by the WHO, which included a review of records, pro-
gramme efficiencies (including the ability to detect all cases) and other sup-
porting data. This official approach for certification stimulated a renaissance
in the certification process for the WHO.
On 27 March 2007, UAE was declared malaria-free, with a cautionary
note that while UAE had managed to reduce its receptivity of local trans-
mission, by targeting the larval stages of the vector and rapid urbanisation,
vectors had not been eliminated and combined with high vulnerability
risks from imported infections meant that the CMD needed to remain
vigilant. In 2010, there were 3239 imported infections of which 85% were
P. vivax and 90% originated from Pakistan and India. A framework was
proposed for the postelimination phase including continued notification of
all imported cases, free diagnosis and treatment (including prophylaxis for
travellers outside of UAE), toll-free help lines, case and breeding site epide-
miological investigations and sustained public awareness campaigns. It was
also recommended that the CMD be incorporated within a wider vector
control department (MoH-UAE, 2007).

Bahrain is an archipelago of 33 islands, with the largest island of Bah-
rain Island being only 652 km2 where over 90% of the land mass is a low
lying desert, with a single mountain, Jabal ad Dukhan, rising to 134 m above
sea level. Bahrain Island is connected to Saudi Arabia by the King Fahd
Causeway. Muharraq Island is much more barren and smaller in size and the
only fresh water supply comes from the Zimma Spring near Hidd village.
After protracted periods of international disagreement and national unrest,
the Emirate of Bahrain became a self-governed nation state in 1970.The oil
boom of the 1970s led to rapid financial prosperity and a period of diver-
sification of its economy into offshore banking facilities. In 2002, Bahrain
changed its name from the State of Bahrain to the Kingdom of Bahrain
with five Governorates, Capital, Central, Muharraq, Northern and South-
ern. In 2010, Bahrain had 1.2 million residents, including 517,000 foreign
nationals, the largest majority (290,000) from India.
Malaria is likely to have existed on the islands for hundreds of years.
­Belgrave (1935) wrote that in 1529, 400 Portuguese men stationed at
Manama Fort suffered from an epidemic of fevers. Harrison (1924), writ-
ing about his experiences while practising at Manama Hospital, refers to
the area as “full of fever, all along the coast the efficiency of the population
234 Robert W. Snow et al.

is reduced by malaria to a mere fraction of what it ought to be”. Data on

malaria cases between 1920 and 1937 presenting to the Victoria Memorial
Hospital at Manama were assembled as part of a detailed malaria survey
across Bahrain by the Malaria Institute of India, indicating at least 1000
cases per year up to 1927 when cases began to rise to over 3000 by 1937
(Afridi and Majid, 1938). The malaria survey identified An. stephensi as the
dominant vector followed by Anopheles fluvatilis, An. culicifacies, An. pulcher-
rimus and An. sergentii. Among 249 school children sampled for parasitology,
4% were positive for P. falciparum, 4% were positive for P. malariae and 5% for
P. vivax (Afridi and Majid, 1938). In 1938, recommendations were made by
the survey team to improve drainage, manage the irrigations systems, ban
water storage tanks around households and introduce larvivorous fish.
DDT was introduced for adult vector control in 1946 and led to a
dramatic decline in malaria incidence within a year and expanded in 1953
to cover all towns and villages across the islands. By 1957 An. fluvatilis had
almost disappeared but An. stephensi remained prolific. In 1953, there were
only 169 locally acquired cases dropping to 38 cases by 1958; however, an
epidemic occurred in 1959 due to flooding resulting in 329 cases (Hamza
et al., 2006; Mahmood, 1992). The systematic documentation of imported
malaria cases began in 1963 (Amin, 1989) and was recognised early on
as a major threat to effective control in Bahrain. Twice yearly, DDT IRS
remained the main vector control measure for many years, despite growing
reluctance of the population to allow spray men into their houses (Delfini,
1977). Locally acquired malaria cases dropped to single digits by 1975. In
1976, there was an interruption in the downward trend, an epidemic of 35
P. vivax cases, felt largely to be a result of indiscriminate blockage of drains
and a proliferation of landfills (Mahmood, 1992; Delfini, 1977; Oddo and
Payne, 1982; Fig. 3.9). Under the guidance of WHO, the Ministry of Health
began its elimination phase in 1977 with the introduction of active case
detection and investigation to compliment the passive case-detection meth-
ods, presumptive treatment of immigrant labour and radical treatment of all
parasite positive detected cases using chloroquine and primaquine (Delfini,
1977). In 1977, 111,000 inhabitants were protected by bi-annual house
spraying with fenitrothion, and diesel oil was used for larval control every
8–10 days and occasional space spraying with pybuthrin in densely popu-
lated areas, which had started in 1968. Coincidental with vector control,
rapid urbanisation across the island was felt to contribute to the decline in
larval breeding sites (Oddo and Payne, 1982). The last autochthonous case
was identified in 1979. Throughout the elimination attack phase malaria
Malaria Transition in the Arabian Peninsula 235

Figure 3.9  Annual locally acquired malaria case incidence 1953–1990 in the Kingdom
of Bahrain per 100,000 resident populations. (Data assembled from Amin (1989)). Bahrain
was declared malaria-free in 1979. Population data sourced from census years between
1950 and 1985 (State of Bahrain Central Statistics Organization, 2002). ­Intercensal
growth rates used to compute noncensus year population size.

was integrated within other departments and divisions of the Ministry of

Health; for example, epidemiological surveillance was part of the commu-
nicable disease section and vector control initiative as part of environmental
health section – latterly a unit of malaria, insects and rodent control man-
aged from six regional centres. As such, at no time was there a single malaria
control or eradication department.
From 1980, all fever cases screened at health clinics, the Salmaniya ­Medical
Centre and the Public Health Laboratory cases were investigated by a health
inspector including the screening of household and neighbourhood con-
tacts. From 1976, imported cases remained relatively stable between 200
and 300 cases each year, mostly from India. Imported cases were detected
at a time coincidental with returning travel to and emigration from the
sub-continent during peak months of transmission in India (Fernandes
and Mahmood, 1987). Between 1992 and 2001, no cases of indigenous
malaria in Bahrain were reported, and the number of imported cases began
to show a steady decline from 282 to 54 cases by 2001 with five countries,
India, Pakistan, Sri Lanka, Bangladesh and Sudan, as the major importation
origins (Ismaeel et al., 2004). Between 2005 and 2010, there have been
528 imported infections – 471 from India and Pakistan. The predominance
of latent P. vivax infections from the Indian sub-continent continues to
pose threats to reintroduction of malaria in Bahrain as An. stephensi remains
236 Robert W. Snow et al.

present. Between 1992 and 2004, 792 active breeding sites were identified,
despite regular larval control activities and thus there remains a potential for
the reintroduction of indigenous malaria transmission (Ismaeel et al. 2004).
Currently, vector control is maintained using diesel oil and where this is
not appropriate temephos has been used since 1983 (Amin, 1989; Alsitrawi,
2003). There are also reports of continued use of IRS. Bahrain has been
malaria-free since 1979 but has not sought certification from the WHO.

Qatar has a small land border with Saudi Arabia but is otherwise sur-
rounded by the Gulf. Combined with several islands, Qatar covers approxi-
mately 11,437 km2, with a hilly region known as the Dukhan hills in the
west and salt flats along large parts of coastline. Oil was discovered in 1930s
and the off-shore natural gas field is largest in the world. Of Qatar's 1.5 mil-
lion people, 60% live in Doha, a large part of rest of population now live in
the fast-growing cities of Al Khor, Ras Laffan and Dukhan.
Not much is known about the historical risks of malaria in Qatar. In
the early 1960s, the WHO classified Qatar as at risk of malaria. The princi-
pal vectors have been identified as An. stephensi and Anopheles multicolor. In
1977, only 116 cases were reported to the central laboratory, and most were
thought to be imported although there was little systematic investigation
or follow-up of detected cases during this period (Shidrawi, 1976). Arte-
sian wells, irrigation areas, swamps and farms investigated for breeding sites
in 1977 identified very few vectors, and it was felt that overall conditions
were not favourable to dominant vectors of the region so while imported
infections were high receptivity remained low (Shidrawi, 1976). In the early
1980s, a malaria unit was established under the division of infectious dis-
eases and epidemic control. Their functions were to survey and control
vector-breeding sites and undertake insecticide spraying in areas where
Anopheles larvae were identified, mostly at farms in the northern reaches
of the peninsula (El Manieh, 1982). It is not clear when local transmission
was interrupted but it is likely that there were no locally acquired malaria
infections since the 1970s and the Qatari government has never sought the
official WHO certification. Imported infections varied between 100 and
450 cases per year since 1997 (Al-Kuwari, 2009). In 2011, there were 673
imported infections and 98% were P. vivax.
Presently, there is no well-formed national strategy to maintain a malaria-
free status. Responsibilities for malaria are integrated across departments
Malaria Transition in the Arabian Peninsula 237

of preventative health and primary health care in the ministry of public

health, the ministry of municipal affairs and the Hamad Medical Corpora-
tion, based in Doha that diagnoses all cases, maintains register of imported
cases and advises on drug policy (Kondrachine, 2002). Despite attempts to
include the private sector in case detection and reporting these have been
inadequate and many cases are thought to go undetected and not radically
cured. Immigrants from 46 malaria endemic countries and blood donors
are screened and radically treated, including chloroquine and primaquine
for vivax cases. By 2002, there was no evidence of active case detection
or epidemiological investigation of passively detected cases. Vector con-
trol is under the responsibility of the ministry of municipal affairs, which
employs the varied agriculture and pest control departments to supervise
the weekly identification and elimination, using temephos, of larval breed-
ing sites, largely with a focus on swamp areas on periphery of Doha.The last
reported observation of An. stephensi larvae was in 2000.

Kuwait covers approximately 18,000 km2 and is mostly a desert. Its
oil fields were discovered in the late-1930s and today has the fifth largest
oil reserves worldwide. After Kuwait gained independence from the United
Kingdom in 1961, the country witnessed rapid economic growth. In 2007,
Kuwait's population is estimated to be between 3 and 3.5 million people,
including 2 million foreign nationals.
Some reports suggest that malaria transmission has never occurred in
Kuwait (Hira et al. 1985; EMRO, 1990). Malaria cases reported between
1971 and 1981 showed that approximately 200 cases were identified and
investigated each year but that none of the cases were locally acquired infec-
tions and the Ministry of Health reported that malaria vectors were absent
from Kuwait (Al-Kilidar, 1982). However, the presence of An. stephensi lar-
vae has been reported in Kuwait (Mamser, 1984). Screening of larval habi-
tats is the responsibility of the Medical Insects Division of the Ministry of
Public health, who rarely identify malaria vector-breeding sites, and any
suspected sites are treated with temephos (Salem, 1999). At no time has
there been a malaria control department.
More than 200,000 immigrants come to Kuwait every year for residence
or work and all checked for infectious diseases including malaria. Of 921,012
slides taken during screening between 1991 and 1999, 1366 were positive
(0.15%), the majority from the Indian sub-continent (Sher et al., 2004) a
238 Robert W. Snow et al.

situation very similar to a decade previously but in much lower frequencies

(Hira et al., 1985). Of 1446 patients screened as acute febrile admissions to
Al-Jahra hospital between 1996 and 1999, 183 P. vivax cases were identified,
15 P. falciparum and 4 mixed infections all imported and mostly from India,
Bangladesh and Sri Lanka (Shweiki et al., 2002).

For centuries, malaria has plagued large parts of the Arabian Peninsula
although the likelihood of natural, uncontrolled transmission has been gov-
erned by the abilities of dominant vectors to maintain transmission under
harsh environmental conditions. The intensity of malaria transmission has
varied enormously across the peninsula from a likely absence of transmis-
sion in Kuwait to an intense parasite exposure, similar to conditions in many
parts of Africa, among residents of the south western reaches of the pen-
insula in Saudi Arabia and Yemen. The spatial extents of malaria risk have
contracted through aggressive control and elimination efforts beginning
during the 1940s but only managing to dramatically reshape national risk
profiles since the 1980s, a period coincidental with rapid economic growth.
Using the information provided in narratives of published and unpublished
reports, it is possible to map the changing margins of malaria risk from its
likely natural extent (Fig. 3.1), and from 1960 by decade through to 2010
(Fig. 3.10).
The most easterly regions of the peninsula located along the Gulf and
the interior of the Rub' al-Khali are regions occupied by the dominant
vectors An. sergentii, An. stephensi, An. culicifacies and An. fluviatilis. In these
regions, the elimination of transmission was rapid. By 1980, Qatar, Bahrain
and the eastern and central provinces of the Kingdom of Saudi Arabia were
malaria-free following intensive control efforts mounted over a relatively
short period. Over the same period, malaria remained entrenched along the
western and southern reaches of Saudi Arabia and Yemen and notably along
their borders. On the Gulf during this time, the UAE and Oman continued
to struggle with risks posed by local transmission in difficult foci and along
their respective borders. The An. arabiensis ecological niche of the penin-
sula has proved the most resilient to elimination efforts and is congruent
with some of the poorest and politically volatile regions. It is not surprising
therefore that the most southerly provinces of Saudi Arabia only began to
witness real success in shrinking the extents of malaria with a recognition
of the national economic potential of the region and a need for investment.
Malaria Transition in the Arabian Peninsula 239

Yemen has been less fortunate. Despite a concerted effort to contain and
control the epidemic resurgence of malaria during the 1990s that affected
the entire sub-region following exception rainfall patterns and emerging
chloroquine resistance, Yemen remains one of the poorest countries in the
region that continues to suffer a civil conflict making concerted and ubiq-
uitous control efforts difficult.
There are several features related to the organisation of malaria con-
trol that characterise the elimination success where this has occurred on
the peninsula. First, areas that responded most rapidly to increased invest-
ment in vector control were areas already under rapid economic and urban
growth.The expanding modern cities along the Gulf transformed the natu-
ral ecology and receptivity of malaria risk. It is hard to imagine that cities
such as Abu Dhabi and Doha would experience the same risks of malaria
transmission today compared to 30 years ago. The rapid decline in malaria
incidence in Bahrain, Qatar and UAE is likely to have been a combined
result of urban growth, social investment of oil revenues and vector con-
trol. Second, a political commitment was necessary to move from a status
quo of sustained control to one that embraced an ambition of elimina-
tion. Control programmes in the UAE, Oman, Yemen and south western
Saudi Arabia met with only limited success during the 1970s when politi-
cal commitment was lacking resulting in inadequate funding and staff for
control programmes. Progress towards elimination was reversed when a
­commitment was revived. This may seem an obvious prerequisite but it is
worth highlighting as an essential part of elimination success. Thirdly, at
different stages in the control to elimination pathway, attempts have been
made to integrate malaria activities into broader primary health care initia-
tives in every country on the peninsula. There have been mixed responses
to this; at one extreme Mashaal's view is that “the integration of malaria
control and eradication into the health services is the first step to failure”
(Mashaal, 2005). However, during maintenance phases, postelimination the
detection of malaria cases and their investigation becomes a broad health
service and infectious disease surveillance agenda as is currently the case
in Qatar and UAE. Maintaining political interest and dedicated malaria
staff with adequate resources postelimination is harder to sustain, with
some fears that malaria-free certification promptly leads to the demise of
any malaria programme. It is notable that resurgent risks in the 1970s in
UAE and dramatic epidemics in the mid-1990s in Saudi Arabia and Yemen
were necessary to refocus government support around malaria. Ironically,
epidemics galvanise political commitments to malaria-specific initiatives.
Robert W. Snow et al.
Figure 3.10  Changing limits of malaria transmission 1960–2010 across the Arabian Peninsula showing the aridity and temperature masks
that do not support malaria transmission or where malaria transmission has been eliminated (light grey) and areas able to support some
degree of stable transmission (dark grey). Temperature, aridity and population density masks are applied according to the rule outlined in
text and legend to Fig. 3.1 and reflect the population density changes with time from 1960 to 2000 (Goldewijik et al., 2010). 1960: Kuwait:

Malaria Transition in the Arabian Peninsula

While the potential for transmission exists, there is no evidence that locally acquired infections have occurred in Kuwait and therefore
regarded as malaria-free since 1960 (Hira et al., 1985; EMRO, 1990; Al-Kilidar, 1982). Yemen: During the 1940s, it was documented that local
transmission was absent from the Aden Colony and the only cases detected were imported cases found on the ships entering the port or
from surrounding areas (WHO-Aden, 1956). By 1980, Aden remained a town thought only to report cases of malaria acquired outside the lim-
its of the town (MoPH, 1981). The city limits of Sana'a had experienced an epidemic in 1946 but have been regarded as malaria-free since the
1960s with most cases from low-lying areas outside the city. 1970: Saudi Arabia: The last case of autochthonous malaria was detected in the
eastern region at Awwamiyah in 1973. By early late 1970s, active transmission in the north western areas was interrupted by the eradication
of An. superpictus. All central areas were free of active transmission by before 1974. Qatar: Probably malaria-free from 1970 (Shidrawi, 1976).
1980: Saudi Arabia: By the 1980s, the north western regions were under active surveillance for the last foci and were largely malaria-free by
early 1980s. Jazan city and Farasan Island were also reported malaria-free at this time (Farid et al., 1980; Anon, 1994). Oman: Muscat city limits
were free from active transmission in 1980, respectively. In Dhofar, epidemiological surveys between 1983 and 1986 included slides taken
from 15,418 individuals of whom only one was found positive (Delfini and Abdel-Majeed, 1993) and a survey of three areas in October 1987
among 1513 people found no one positive (Muiz, 1989). During the 1990s, the WHO regarded the border area with Yemen as malaria-free
(Anon, 1993); however, sporadic epidemics from imported infections were reported in 1998 initiated by infected Somali immigrants (Baomar
and Mohamed, 2000). While reasonable to presume that this area was malaria free in the 1990s, it does have a receptive risk making it vul-
nerable to imported infections. UAE: In 1976, there were no locally acquired cases in Dubai and all of the 2432 cases detected in Abu Dhabi
Emirate were classified as imported in 1976 (Farid, 1977). In November 1996, no infant was found positive for malaria infection and a survey
of 6–9 year-old school children identified 26 children with enlarged spleens and the three P. vivax slide positive cases had come from Oman
and one P. falciparum case from Bangladesh (Farid, 1977). Al Ain, Dubai and Abu Dhabi were reported as malaria-free by 1980 (Farid, 1981).
Bahrain: was reported as malaria-free in 1979. 1990: Saudi Arabia: The focal risks in 1990 were documented largely at Qunfudha and Al Lith
sectors of Mecca province, Asir in the southern region and much of Jizan province (Farid, 1992). UAE: In 1990, there were a few dominant
residual foci identified: Menaey, Lolya, Al Foa, Rashidia, Hili, Kattara, Khorfakkan, Dibbal Hisan, Medha and Masfoot, and these led to 18 cases
of malaria in 1990. Oman: Risks only in most northerly coastal governorates. 2000: Saudi Arabia: Cases detected only in Asir, Quadanfun
and Jizan provinces. Oman: By 2000, foci in the five most northerly provinces; UAE: Last locally acquired case detected in 1997 and by 2000
malaria-free. 2010: Saudi Arabia: By 2010, only 29 locally acquired cases were detected in the Kingdom with 11 from Asir resumed at south-
erly edge with Jizan province and 18 from Jizan at two localities close to Yemeni border, Kkauba and Samta (Al Zahrani, 2010). Yemen: The
last reported case on Socotra Island was in 2005 and regarded malaria-free since this date. Oman: Foci detected between 2005 and 2011 in
Dakhliya and north Batinah all rapidly controlled and Oman regarded as malaria-free by EMRO.

242 Robert W. Snow et al.

Fourth, the success of elimination depended heavily on a mapped intelli-

gence of risk.The UAE, Oman and Saudi Arabia developed an early malaria
risk cartography based on vectors, intensity of transmission and ecology.
These national atlases and stratification served as frameworks to develop a
nationally staggered approach to shrinking the limits of transmission and
defining appropriate combinations of intervention. The resolution of this
risk mapping intensified as vector control was mounted sub-nationally,
and detailed maps were developed of regions and locations of households
to mount targeted IRS and larval control. As the target of elimination
approached, the precise mapping of cases became imperative to contain the
onward transmission. Geographic reconnaissance was used to guide all levels
of control to elimination from national to village scales and the skill and use
of malaria risk mapping to guide elimination strategies contributed to its
success. Finally, and perhaps uniquely to this region, larval control appeared
to be a successful means of reducing vector abundance and remains widely
practised. Attribution of individual vector control approaches to declining
malaria incidence is not possible with the data available. Nevertheless, the
use of temephos linked to the high-resolution reconnaissance of breeding
sites dominated much of the elimination efforts in all countries on the pen-
insula. With the exception of An. arabiensis, most vectors in the region have
identifiable breeding sites and when larval control was used in several areas
from the 1940s malaria incidence declined and later when combined with
IRS were thought to have a larger impact on community infection preva-
lence than when IRS was used alone. Where vectors are no longer present,
the receptive risks have been diminished to such low levels that these areas
are no longer vulnerable.
The threats posed by imported infections remain significant. A large
immigrant labour force travels to and from their home countries and the
Arabian Peninsula every year. This work force comes predominantly from
India, Pakistan and Bangladesh with lesser representation from other nations
across the malaria endemic world. During the 1970s through to the 1990s,
they came to build the new cities and provide labour in the growing service
industries. By the early 1990s, this growth in immigration coincided with
the global epidemic of malaria and led to the importation of chloroquine
resistance (Al-Farsi et al., 2012), contributing to the rise in malaria incidence
in countries where transmission remained entrenched (Saudi Arabia,Yemen
and Oman). Despite the continued increases in economic labour migration
into the peninsula today, the patterns of receptivity and vulnerability are very
different compared to the 1990s. Risks are lower in originating countries,
Malaria Transition in the Arabian Peninsula 243

vector-breeding sites along the Gulf have been reduced and receptivity is
considerably lower and countries who have reached zero locally acquired
cases are more vigilant about detecting imported infections and treating
with more effective drugs. However, the patterns of migration, the risks
they pose to areas of continued receptive risk and the likelihood of contain-
ment remain poorly defined and quantified.
Two countries have yet to achieve a malaria-free state, Yemen and the
Kingdom of Saudi Arabia, with approximately 2.1 million people at risk of
malaria in 2010 living in an area of 188,000 km2 (Fig. 3.10); 91% of whom
are Yemeni. In Saudi Arabia, the costs required to maintain surveillance and
contain the active foci of transmission remain high per case – 29 cases in
2010.The counterfactual without sustained financial investment; however, is
in the order of thousands of cases in Jizan Province of Saudi Arabia (Fig. 3.2).
Yemen remains the largest threat to a malaria-free peninsula.The long-term
future of elimination in Saudi Arabia depends critically upon the ability to
contain imported infections from neighbouring Yemen.This was recognised
as early as 1979 and re-asserted in 2007 with agreements between govern-
ments to collaborate and institute cross-border activities. Such initiatives are
not easy to manage when resources (financial and human) and government
priorities and policies differ across a single political boundary shared by
people connected by family ties and history. Cooperation was maintained to
achieve elimination in the UAE with its neighbour Oman but this required
regular bi-annual meetings, negotiation and resolution despite both having
equivalent ambitions but disparate resources.Yemen shares many ecological
similarities with Jizan Province in Saudi Arabia but also with neighbours
across the Red Sea on mainland Africa (Somalia, Eritrea and Ethiopia) who
are highly mobile as a result of combined regional conflict and economic
pressures. Despite successes on the unique malaria ecology of Socotra Island
(Fig. 3.5), Yemen contributes over 98% of the malaria burden of the Arab
Peninsula today. Yemen has emerged from a recent political crisis but con-
tinues to face an uncertain future. Without a concerted regional effort to
tackle malaria in Yemen over the next 5–10 years, the Arabian Peninsula will
not enjoy a malaria-free status.

RWS is supported by the Wellcome Trust as Principal Research Fellow (# 079080) that also
supports PA and CM. AMN is supported by the Wellcome Trust as an Intermediate Research
Fellow (# 095127).The authors wish to acknowledge all the current and past malaria control
programme managers of countries on the peninsula who have generously provided annual
information to the WHO and have documented in detail their efforts towards elimination.
244 Robert W. Snow et al.

We are also grateful to Nahla Ibrahim, Amir Kamal Aman and the library and archive staff
at the WHO-EMRO offices in Cairo; Marie Sarah Villemin Partow of the World Health
Organization Archives in Geneva; the library staff at The Wellcome Institute, London;
Caroline Kabaria of the KEMRI-Wellcome Trust programme for help with developing the
maps; Dr Jamal Amran (ex-Yemeni head of NMCP), Dr Ahmed Sahli (ex-Jizan Province
head of malaria programme) for detailed spatial information; and Professor Kevin Marsh for
reading an early draft of the manuscript.

Abdel-Hameed, A.A., 2003. Antimalarial drug resistance in the Eastern Mediterranean
region. East. Mediterr. Health J. 9, 492–509.
Abdoon, A.M.M.O., Alshahrani, A.M., 2003. Prevalence and distribution of Anopheline
mosquitoes in malaria endemic areas of Asia region, Saudi Arabia. East. Mediterr. Health
J. 9, 240–247.
Afridi, M.K., Majid, S.A., 1938. Malaria in Bahrain Islands (Persian Gulf  ). J. Mal. Inst. India
1, 428–452.
Al Abdullalatif, Z., Fontaine, R.E., Saeed, A.B., Al Hamdan, N., Al Sagheer, S., 1996. Malaria
outbreak in Gellwa, Al Baha, Saudi Arabia, January to March 1996. Saudi Epidemiol.
Bull. 3, 27–29.
Al Tawfiq, J.A., 2006. Epidemiology of travel-related malaria in a non-malarious area in
Saudi Arabia. Saudi Med. J. 27, 86–89.
Al Zahrani, M.H., 2007. Impact of Irrigation Systems on Malaria and Rift Valley Fever
Transmission in Jazan, Saudi Arabia. PhD Thesis University of Liverpool, UK.
Al Zahrani, M.H., 2010. Malaria situation in Kingdom of Saudi Arabia. Presentation given at
EMRO malaria regional meeting, Marrakech, Kingdom of Morocco, 22–24 September
Al Zedjali, M., 2010. Malaria situation in Oman, 2009. Presentation given at EMRO malaria
regional meeting, Marrakech, Kingdom of Morocco, 22–24 September 2010.
Ali, O.M., 2005. Consultants Report from Progress Review of RBM in Yemen January–
November 2005. World Health Organization, Eastern Mediterranean Regional Office
archive, Cairo.
Al-Farsi, H.M., Al-Hashami, Z.S., Bin Dajem, S.M., Al-Sheikh, A.A., Al-Qahtani, A., Beja-
Pereira, A., Idris, M.A., Babiker, H.A., 2012. Source of drug resistant Plasmodium falci-
parum in a potential malaria elimination site in Saudi Arabia. Infect. Genet. Evol. 12,
Al-Kilidar, A.A., 1982. Malaria in Kuwait, 1981. Ministry of Public Health Report. World
Health Organization, Eastern Mediteranean Regional Office archive, Cairo.
Al-Kuwari, M.G., 2009. Epidemiology of imported malaria in Qatar. J. Travel Med. 16,
Al-Maktari, M.T., Bassiouny, H.K., 1999. Ovale malaria: a case report from the Republic of
Yemen. East. Mediterr. Health J. 5, 826–827.
Al-Seghayer, S.M, Alattas, M.S., 2005. Roll back malaria in Saudi Arabia. Fifth Inter-Country
Meeting of National Malaria Programme Managers Countries of Moderate to High
Malaria Endemicity Cairo, Egypt, 29–31 May 2005.
Al-Sheikh, A.A.H., 2004. Studies on the Ecology, Vectorial Role and Population Structure
of Anopheles arabiensis in the Tihama Region of Saudi Arabia and Yemen. PhD Thesis
University of Liverpool, UK.
Al-Wahabi, S.S., Parvez, S.D., 2002. Malaria in the Sultanate of Oman, past, present and
future. World Health Organization informal consultation on elimination of residual
foci and prevention of re-introduction of malaria. Rabat, Kingdom of Morocco, 18–20
June 2002.
Malaria Transition in the Arabian Peninsula 245

Al-Wahabi, S.S., Hallaj, Z., Abdel-Rahim, I.M., Majori, G., Onwujekwe, O., Atta, H.,
Mnzava, A., 2003. Malaria eradication in Oman: An analysis of processes, costs and
impact. In: Report of the Inter-Country Workshop on Developing a Regional Strat-
egy for Integrated Vector Management (IVM) for Malaria and Other Vector-Borne
Diseases. Khartoum, Sudan, 21–23 January 2003.
Alsitrawi, A.A., 2003. Malaria in Bahrain 2002. Report to the third inter-country of national
malaria programme managers, EMRO Meeting Lahore, Pakistan 12–15 May 2003.
Amara, H.A., 1988. Assignment report Malaria Control Programme, Kingdom of Saudi Ara-
bia covering period 21 August 1981–15 May 1988. World Health Organization, Eastern
Mediterranean Region report; SAA/MPD/001.
Amin, O.M., 1989. The status of malaria in Bahrain, Arabian Gulf. J. Univ. Kuwait (Sci.) 16,
Amini, A., 1988. Report on a field visit to Subba area in the Abiyan Governorate. World
Health Organization, Eastern Mediterranean Region report; YEA/MAL/001, Aden,
December 1988.
Andreason M.H., 2006. Emerging resistance to temephos in Anopheles stephensi in the Al-
Dahihia region of Oman. Assignment report 6–10 May 2006. World Health Organiza-
tion, Eastern Mediterranean Region report; EM/MAL/328/E/R/6.06.
Anon, 1981. World malaria situation 1979. WHO-PAHO Bull. 15, 278–284.
Anon, 1984. Saudi Arabia: the present malaria situation. Report published by National
Malaria Control Service, Saudi Arabia.
Anon, 1986. Joint Government/WHO Malaria Review Mission to Saudi Arabia 5–23
July 1986. World Health Organization, Eastern Mediterranean Region report; SAA/
Anon, 1988. Malaria Control Project Yemen. World Health Organization, Eastern Mediter-
ranean Region report;YEA/MAL/001, Aden, December 1988.
Anon, 1993. Report on the malaria border meeting between Oman, Saudi Arabia, the United
Arab Emirates and the Republic of Yemen. Muscat, Oman, 5–8 September 1993. World
Health Organization, Eastern Mediterranean Region report;WHO-EM/MAL/229-E/L.
Anon, 1994. Status of Malaria Control in Gizan 1988–1993. World Health Organization,
Eastern Mediterranean Regional Office archive, Cairo.
Anon, 2007. Malaria Epidemiological Situation in Yemen. 7th Inter-country meeting of
national malaria programme managers, Dubai, UAE, 10–12 June, 2007.
Anon, 2009. Progress towards Malaria Elimination in Socotra Island, Yemen: Intervention
Coverage and Health Impact. World Health Organization, Eastern Mediterranean
Regional Office archive, Cairo.
Anon. Patent Progress and Challenges of Malaria Control in Republic of Yemen. Presen-
tation given at EMRO malaria regional meeting, Marrakech, Kingdom of Morocco,
22–24 September 2010.
Assabri, A.M., 1989. Malaria as a Major Public Health Problem in the Yemen Arab Republic.
Consultation on epidemiological malaria information at national and regional levels.
Amman, Jordon, 25–30 November 1989. World Health Organisation, Eastern Mediter-
ranean Regional Office report; EH/CNS.EHI.NAT.REG/13.
Atta, H., 2006. Report on Malaria Programme in Eastern Mediterranean Region. Sixth
Inter-country meeting of National Malaria Control Programme Managers. Cairo,
Egypt, 3–6 July 2006.
Atta, H., Zamani, G., 2009. The progress of roll back malaria in the Eastern Mediterranean
region over the past decade. East. Mediterr. Health J. 14, S82–S89.
Audisio de Marchi, M.L.A., Audisio, G., 1952. La malaria nel Yemen. Giorn. Med. Milit. 102,
Baomar, A.T., Mohamed, A.G., 2000. Malaria outbreak in a malaria-free region of Oman
1998: unknown impact of civil war in Africa. Public Health 114, 480–483.
246 Robert W. Snow et al.

Belgrave, C.D., 1935. The Portuguese in the Bahrain islands, 1521–1602. J. R. Cent. Asian
Soc. 22, 617–630.
Beljaev, A.E., 1997. Report on a Visit to Yemen, 12–26 February 1997. World Health Orga-
nization, Eastern Mediterranean Region archives, Cairo.
Beljaev, A.E., 2002. Determinants of malaria in the Middle East and North Africa. In: Cas-
man, E.A., Dowlatabadi, H. (Eds.), The Contextual Determinants of Malaria, Resources
for the Future Press, Washington, DC, pp. 137–166.
Berga, D.K., 1999. Assignment Report: Monitoring Therapeutic Efficacy of Chloroquine in
Republic of Yemen 21 December 1998–18 January 1999. World Health Organization,
Eastern Mediterranean Region report; EM/MAL/261/E/R/02.99/23.
Bill and Melinda Gates Foundation, 2007. Malaria Forum Keynote Address by Melinda Gates,
October16, 2007. Available from:
tary/Pages/melinda-french-gates-2007-malaria-forum.aspx (accessed 30.07.12.).
Boyd, M.F., 1930. An Introduction to Malariology. Harvard University Press, Cambridge,
Buxton, P.A., 1944. Rough notes: Anopheles mosquitoes and malaria in Arabia. Trans. R. Soc.
Trop. Med. Hyg. 38, 205–214.
Central Department of Statistics and Information Kingdom of Saudi Arabia, 2011. Popula-
tion Statistics Database. (accessed 30.04.12.).
Chuang, C.H., 1986. Assignment Report on Malaria Control in Saudi Arabia. Covering
period 17 December 1977 to 31 July 1986. World Health Organization, Eastern Medi-
terranean Region archive, Cairo.
Colbourne, M.J., Smith, S.A., 1964. Problems of Malaria in the Aden Protectorate (report on
a visit). World Health Organization report; WHO/MAL/442.
Daggy, R.H., 1959. Malaria in oases of eastern Saudi Arabia. Am. J. Trop. Med. Hyg. 8,
Delfini, L.F., 1977. Report on a Visit to Bahrain. 29 January–4 February 1977. World Health
Organization, Eastern Mediterranean Region archive, Cairo.
Delfini, L.F., 1986. Assignment Report on Malaria Control in Yemen 14 September–25
November 1985. World Health Organization, Eastern Mediterranean Region; WHO-
EM/MAL/212-E, March 1986.
Delfini, L.F., Abdel-Majeed, M.S., 1993. For Malaria Control in Sultanate of Oman. Malaria
Control Section, Directorate of Preventative Medicine, Ministry of Health, Sultanate of
Dresch, P., 2000. A History of Modern Yemen. Cambridge University Press, Cambridge.
Dutta, H.M., Dutt, A.K., 1978. Malarial ecology: a global perspective. Soc. Sci. Med. 12,
El Hazmi, M.A.F., Al-Hazmi, A.M., Warsy, A.S., 2011. Sickle cell disease in Middle East Arab
countries. Indian J. Med. Res. 134, 597–610.
El Manieh, K.M., 1982. Report on the Malaria Epidemiological Situation in 1981. Ministry
of Public Health, State of Qatar, March 1982.
El Sebai, M.M., Makled, M.K., 1987. Malaria in El-Taif, Saudi Arabia. J. Egypt. Soc. Parasitol.
17, 373–375.
EMRO, 1987. Regional Technical Consultation on Malaria Control and Primary Health
Care, June 1987, Ammana, Jordon. World Health Organization, Eastern Mediterranean
Regional Office report; EM/MAL/216-E.
EMRO, 1990. Consultation on Epidemiological Malaria Information at National and
Regional Levels. World Health Organization, Eastern Mediterranean Regional Office
report; WHO-EM/MAL/217E, Amman, Jordan, November 1989.
EMRO, 1993. Report on the Malaria Border Meeting between Oman, Saudi Arabia, the United
Arab Emirates and Republic of Yemen, Muscat, Oman 5–8 September 1993.World Health
Organization, Eastern Mediterranean Regional Office report;WHO-EM/MAL/229-E/L.
Malaria Transition in the Arabian Peninsula 247

EMRO, 2007. Strategic Plan for Malaria Elimination in the WHO Eastern Mediterranean
Region 2006–2010.World Health Organization Regional Office for the Eastern Medi-
EMRO, 2008. Technical discussion on malaria elimination in the Eastern Mediterranean
region: vision, requirements and strategic outline. Regional committee for the Eastern
Mediterranean Fifty-fifth session, Agenda item 7 (b). EM/RC55/Tech.Disc.2.
EMRO, 2010. IVM Strategic Plan for Oman (2010–2016).World Health Organization, East-
ern Mediterranean Regional Office report;VBC.8/2. OMA/HCE/020.
Farid, M.A., 1956. The pilgrimage and its implications in a regional malaria eradication pro-
gramme.WHO/EMRO inter-regional conference on malaria for the Eastern Mediterranean
and European regions, April 1956.World Health Organization report;WHO/MAL/168.
Farid, M.A., 1977. Long-term Malaria Control Programme in the United Arab Emirates.
Assignment report 1 February–25 April 1977. World Health Organization, Eastern
Mediterranean Regional Office report; EM/UAE/MPD/001/RB.
Farid, M.A., 1981. The Anti-Malaria Programme United Arab Emirates. Assignment report
27 October–28 November 1980. World Health Organization, Eastern Mediterranean
Regional Office report; EM/UAE/MPD/001.
Farid, M.A., 1988. Malaria in Socotra Island, Democratic Yemen. World Health Organiza-
tion, Eastern Mediterranean Regional Office archive, Cairo.
Farid, M.A., 1992. Report on a Field Visit to Saudi Arabia 31 July–10 August 1992. World
Health Organization, Eastern Mediterranean Regional Office archive, Cairo.
Farid, M.A., 1996. An attempt to illustrate the malaria situation in Arabia at the time of the
Prophet Muhammad. East. Mediterr. Health J. 2, 531–537.
Farid, M.A., Nasir, A.S., Benthein, F.G.E., 1973. Assignment Report, WHO Malaria Survey
Team, Sultanate of Oman, 13 April–8 June 1973. World Health Organization, Eastern
Mediterranean Regional Office report; EM/MAL/118.
Farid, M.A., Akeel, A.-R., Abul-Naga, F., 1980. The Indispensible Role of a Special Malaria
Service in the Context of an Intensive Socio-economic Development Programme
in Jizan Province (Saudi Arabia). World Health Organization, Eastern Mediterranean
Regional Office archive, Cairo.
Feachem, R.G.A., Phillips, A.A., Hwang, J., Cotter, C.,Weilgosz, B., Greenwood, B.M., et al.,
2010a. Shrinking the malaria map: progress and prospects. Lancet 376, 1566–1578.
Feachem, R.G.A., Phillips, A.A., Targett, G.A., Snow, R.W., 2010b. Call to action: priorities
for malaria elimination. Lancet 376, 1517–1521.
Fernandes, E.L., Mahmood, R.A.H., 1987. Hibernation of the malaria parasite in Bahrain.
Bahrain Med. Bull. 9, 22–25.
Fikiri, M., 2010. Malaria Free Status in United Arab Emirates: Story of Success. Inter-
Country Meeting of National Malaria Programme Managers, Marrakech, Kingdom of
Morocco, 24–26 September 2010.
Gavin, R.J., 1975. Aden under British Rule 1839–1967. C Hurst and Co Publishers Ltd.
Gelpi, A.P., 1965. Glucose-6-phosphate dehydrogenase deficiency in Saudi Arabia: a survey.
Blood 25, 486–493.
Gething, P.W., Van Boeckel, T.P., Smith, D.L., Guerra, C.A., Patil, A.P., Snow, R.W., et al.,
2011. Modelling the global constraints of temperature on transmission of Plasmodium
falciparum and P. vivax. Parasite Vector 4, e92.
Ghalib, H.W., Al-Ghamdi, S., Akood, M., Haridi, A.E., Ageel, A.A., Abdalla, R.E., 2001.Ther-
apeutic efficacy of chloroquine against uncomplicated, Plasmodium falciparum malaria in
south-western Saudi Arabia. Ann. Trop. Med. Parasitol. 95, 773–779.
Goldewijik, K., Beusen, A., Janssen, P., 2010. Long-term dynamic modeling of global popula-
tion and built-up area in a spatially explicit way: HYDE 3.1.The Holocene 20, 565–573.
Guerra, C.A., Snow, R.W., Hay, S.I., 2006. Defining the global limits of malaria transmission
in 2005. Adv. Parasitol. 62, 157–179.
248 Robert W. Snow et al.

Guerra, C.A., Gikandi, P.W., Tatem, A.J., Noor, A.M., Smith, D.L., Hay, S.I., et al., 2008. The
limits and intensity of Plasmodium falciparum: implications for malaria control and elimi-
nation worldwide. PLoS Med. 5, e38.
Hammouda, N.A., Lebshtein, A.K., Abdel Fattah, M.M., Wasfi, A.S., Omar, E.A., Higazi,
N.A., 1986. Parasitic infections and nutritional status of school children in the western
region of Saudi Arabia. J. Egypt. Soc. Parasitol. 16, 675–688.
Hamza, A.A., Al Musawi, M., Fernandes, E.L., 2006. Epidemics in Bahrain from 1925 to
1965: an historical perspective Parts II of 3. J. Bahrain Med. Soc. 18, 151–152.
Harrison, P.W., 1924. The Arab at Home. Thomas Y. Cromwell & Co, New York, p. 345.
Hira, P.R., Behbehani, K., Al-Kandari, S., 1985. Imported malaria in Kuwait. Trans. R. Soc.
Trop. Med. Hyg. 79, 291–296.
Horton, M.C., 1987. The Swahili Corridor and the Southern African Iron Age. Department
of History, University of Nairobi, Nairobi.
Ismaeel, A.Y., Senok, A.C., Al Khaja, K.A.J., Botta, G.A., 2004. Status of malaria in the King-
dom of Bahrain: a 10 year review. J. Travel Med. 11, 97–101.
Jalal, H., Lin, N.H., 1972. Evaluation of Anti-Malarial Activities in Eastern Province, Saudi
Arabia, 1972. World Health Organization, Eastern Mediterranean Regional Office
archive, Cairo.
Khalifa, M.A., September 1999. The Malaria Eradication Programme in the Sultanate of
Oman: Situation Analysis. Department of Environmental Health and Malaria Eradica-
tion, Ministry of Health.
Kinsara, A.J., Abdelaal, M.A., Jeje, O.M., Osoba, A.O., 1997. Chloroquine-resistant Plasmo-
dium falciparum malaria: report of two locally acquired infections in Saudi Arabia. Am. J.
Trop. Med. Hyg. 56, 573–575.
Kondrachine, A.V., 2001. Malaria Control and Prevention in the United Arab Emirates.
Assignment report 6–16 April 2001.World Health Organization, Eastern Mediterranean
Regional Office report; EM/MAL/268/E/R/05.01/28.
Kondrachine, A.V., 2002. Aspects of Malaria Prevention and Control in Qatar, Report of
Visit 5–15 February 2002.World Health Organization, Eastern Mediterranean Regional
Office report; EM/MAL/278/E/R/04.02/21.
Kondrachine, A.V., 2004. Strategy for malaria elimination in the Kingdom of Saudi Arabia
(2004–2007). Malaria Elimination Strategy in Saudi Arabia. National Malaria Control
Programme in Saudi Arabia, Ministry of Health, p. 63.
Kondrachine, A.V, 2006. Review on the Implementation Strategy for Malaria Elimination
of the National Malaria Control Programme, Saudi Arabia. 15 January–14 February
2006. World Health Organization, Eastern Mediterranean Regional Office report; EM/
Kondrachine, A.V., 2009. Assessment of Malaria Elimination Activities in Socotra Island,
Republic of Yemen. World Health Organization, Eastern Mediterranean Regional
Office archive, Cairo.
Kouznetzov, R.L., 1976. Distribution of Anophelines in the Yemen Arab Republic and Its
Relation to Malaria. World Health Organization, WHO/MAL/76.879.
Kravchenko, V.K., 1978. Some aspects of malaria epidemiology in the Peoples Democratic
Republic of Yemen.Yemeni Med. J. 3, 35–37.
Lehman, H., Maranjian, G., Mourant, A.E., 1963.The distribution of sickle cell haemoglobin
in Saudi Arabia. Nature 198, 492.
Lysenko, A.J., Semashko, I.N., 1968. Geography of malaria. A medico-geographic profile of
an ancient disease. In: Lebedew, A.W. (Ed.), Itogi Nauki, Medicinskaja Geografija, USSR:
Academy of Sciences, Moscow, pp. 25–146.
Magzoub, M., 1980. Plasmodium falciparum and Plasmodium vivax infections in Saudi Ara-
bia, with a note on the distribution of anopheline vectors. J. Trop. Med. Hyg. 83,
Malaria Transition in the Arabian Peninsula 249

Mahmood, R.A., 1992. History of eradication of malaria in Bahrain. J. Bahrain Med. Soc.
4, 118–119.
Malaria Control Service Ministry of Health, June 1980. A Brief Report on the Malaria Con-
trol Programme in the Kingdom of Saudi Arabia in 1979. Ministry of Malaria Control
Service, Ministry of Health.
Malaria Control Service Ministry of Health, March 1986. Annual Report on Malaria Con-
trol Programme in the Kingdom of Saudi Arabia, 1985. Malaria Control Service, Min-
istry of Health.
Malik, G., Khan, A., Abdulla, S., 1997. No response to chloroquine therapy in a case of Saudi
falciparum malaria. Saudi Med. J. 18, 99–100.
Mamser, A.A., 1984. Report on a Mission to Kuwait from: 1–6 April 1984. World Health
Organization, Eastern Mediterranean Regional Office archive, Cairo.
Mashaal, H.A.H., 1998. Report on the Assessment of the Malaria Eradication Programme
in the Sultanate of Oman. 10 October–26 December 1997.World Health Organization,
Eastern Mediterranean Regional Office archive, Cairo.
Mashaal, H.A.H., 2000. Progress in Malaria Eradication Programme in North Batinah: the
Danger of Expatriates Who Enter Illegally. World Health Organization, Eastern Medi-
terranean Regional Office archive, Cairo.
Mashaal, H.A.H., 2005. Letter to Dr Hussein Gezairy, EMRO, Dated 25,May 2005. World
Health Organization, Eastern Mediterranean Regional Office archive, Cairo.
Mashaal, H.A.H., 2006. A Story of Success: Eradication of Malaria from Oman 1991–
2006. World Health Organization, Eastern Mediterranean Regional Office archive,
Mashaal, H.A.H.H., Khalida, M.A.M., Mohammad Ali, O.A., Ahmad, M.I., 1998. Malaria
Situation in Hodeidah Governorate, Republic of Yemen. Based on epidemiological
surveys and evaluation of health services suggested plans for malaria control Ministry of
Matta, S.E., 1984. Assignment Report: Malaria Control Programme, Oman, January
1975–December 1984. World Health Organization, Eastern Mediterranean Regional
Office archive, Cairo.
Meleigy, M., 2007. Arabian Peninsula states launch plan to eradicate malaria. BMJ 334, 117.
Ministry of Health Kingdom of Saudi Arabia, 1963. Sketch Map Showing Operational
Zones in 1962. World Health Organization, Eastern Mediterranean Regional Office
archive, Cairo.
Ministry of Health – UAE, 2002. Background Document for Requesting the Certification
of Malaria-free Status by the World Health Organization. Ministry of Health, United
Arab Emirates.
Ministry of Health – UAE, 2007. Ongoing Efforts towards Maintaining Malaria Free Status.
Ministry of Health, United Arab Emirates.
Ministry of Health, Sultanate of Oman, 2003. Annual Report for the Year 2003. Accessed:
03-05-2012. (accessed
Ministry of Health, Sultanate of Oman, 2009. Annual Report for the Year 2009. http:// (accessed 04.05.12.).
Ministry of Health, Sultanate of Oman, 2011a. Communicable Diseases Control in Sultanate
of Oman. (accessed
Ministry of Health, Sultanate of Oman, 2011b. The Malaria Eradication Programme in
Oman – A Success Story.
malariaeread.htm (accessed 30.07.12.).
Ministry of Health Yemen, 1989. Annual Descriptive Report for 1989. Malaria Control Pro-
gramme,Yemen Arab Republic.
250 Robert W. Snow et al.

Ministry of Public Health and Population, 2011. Yemen's National Malaria Control and
Elimination Strategic Plan 2011–2015. Ministry of Public Health and Population, Pri-
mary Health Care Sector, National Malaria Control Program.
Ministry of Public Health, 1981. Malaria Control Project: Draft Plan of Action for 1981.
Ministry of Public Health, Peoples Democratic Republic of Yemen.
Mount, R.A., 1953. Medical mission to Yemen, Southwest Arabia, 1951 I. Geomedical
observations. Am. J. Trop. Med. Hyg. 2, 1–12.
Muiz, D., 1989. Report on an Assignment for Dhofar, Sultanate of Oman. World Health
Organization, Eastern Mediterranean Regional Office archive, Cairo.
National Malaria Control Programme Yemen, 2001.The National Strategic Plan for Roll Back
Malaria in the Republic of Yemen 2001–2005. Prepared by Noman, Y.A.W., Al Mawri,
S., Khalifa, M.A., for the Ministry of Public Health and Population, Republic of Yemen.
National Malaria Control Programme Yemen, 2003. The National Malaria Control Pro-
gramme in Yemen. Progress Report April 2003. Ministry of Health Report, 2003.
National Malaria Control Programme Yemen, 2006. The Strategic Plan of the National
Malaria Control Programme in the Republic of Yemen: 2006–2010. Developed by
Khalifa, M.A., Amran, J.G., Ali, O.M.A., Al Henami, M., National Malaria Control Pro-
gramme, Ministry of Health, Sana'a, Republic of Yemen.
National Malaria Control Programme Yemen, 2009. Report on the Final Results of the
National Malaria Indicators Survey 2009. National Malaria Control Programme, Pri-
mary Health Care Sector, Ministry of Public Health and Population, Republic of Yemen.
Oddo, F.L., Payne, D., 1982. Report on an Assessment on the Status of Malaria Eradication
in the Bahrain Emirate. 27 October–7 November 1982. World Health Organization,
Eastern Mediterranean Regional Office archive, Cairo.
Petrie, P.W.R., Seal, K.S., 1943. A Medical Survey of the Western Aden Protectorate, 1939–
1940. British Colonial Office, Aden.
Phipson, E.S., 1933. Medical Survey of Aden in 1933. Cowasjee Dinshaw & Bros. Press,
Public Health Department Ministry of Health, 1979. Malaria Control Programme in Sultan-
ate of Oman. Malaria Control Project, Public Health Department, Ministry of Health,
Sultanate of Oman.
RBM, August 2008. The Global Malaria Action Plan For a Free Malaria World. Roll Back
Malaria Partnership. World Health Organization, Geneva (accessed 07.07.12.) http://
Rogan, E.L., 2011. The Arabs – a History. Penguin Books, pp. 701.
Salem, K.I., September, 1999. Malaria Control in the State of Kuwait. Report prepared by
Chief Epidemiologist Public Health Services Bureau, Muscat.
Saudi Arabian Monetary Agency, 2011. Forty Sixth Annual Report. The Latest Economic
Developments 1431H (2010G). Research and Statistics Department. http://www.
EN_2010_11_14.pdf (accessed 30.01.12.).
Sebai, Z.A., 1988. Malaria in Saudi Arabia. Trop. Doc. 18, 183–188.
Sher, A., Mohammad, A.G.H., Al-Owaish, R., 2004. Infectious diseases detected among
immigrants in Kuwait. Kuwait Med. J. 36, 124–127.
Shidrawi, G.R., 1976. Report of a Visit to Qatar, October 1975. World Health Organization,
Eastern Mediterranean Regional Office archive, Cairo.
Shidrawi, G.R., 1980a. Report on a Visit to the Yemen Arab Republic 27 November–10
December 1980. World Health Organization, Eastern Mediterranean Regional Office
report; EM/MAL/180.
Shidrawi, G.R., 1980b. Report on a Third Visit to the Sultanate of Oman, 12–26 October
1979.World Health Organization, Eastern Mediterranean Regional Office report; EM/
Malaria Transition in the Arabian Peninsula 251

Shidrawi, G.R., 1982. Report on a Visit to the Sultanate of Oman, 28 April–16 May
1982. World Health Organization, Eastern Mediterranean Regional Office report;
Shililu, J.I., Grueber, W.B., Mbogo, C.M., Githure, J.I., Riddiford, L.M., Beier, J.C., 2004.
Development and survival of Anopheles gambiae eggs in drying soil: influence of the rate
of drying, egg age, and soil type. J. Am. Mosq. Control Assoc. 20, 243–247.
Shweiki, H.M., Al-Harbi, M., Sethi, S.K., West, P.W.J., Hira, P.R., 2002. Status of imported
malaria in Kuwait: experience from Al-Jahra hospital. Kuwait Med. J. 34, 201–204.
Sinka, M.E., Bangs, M.J., Manguin, S., Coetzee, M., Mbogo, C.M., Hemingway, J., et al.,
2010.The dominant Anopheles vectors of human malaria in Africa, Europe and the Mid-
dle East: occurrence data, distribution maps and bionomic précis. Parasites and Vectors
3, e117.
Souleimanov, G.D., 1999. Assignment Report on a Mission to Yemen 11 April–10 June 1999.
World Health Organization, Eastern Mediterranean Regional Office archives, Cairo.
State of Bahrain Central Statistics Organization, 2002. Basic Results Population, Housing,
Buildings and Establishments Census Part One. 2001 Census. State of Bahrain, Ministry
of Cabinet Affairs.
Sultanate of Oman Ministry of National Economy, 2012. Oman Census Overview, Popula-
tion 1993–-2010.
on&selectedWafers=0&selectedColumns=0 (accessed 30.07.12.).
Thuriaux, M.C., 1971. Notes on the epidemiology of malaria in Yemen Arab Republic. Ann.
Soc. Belge. Med. Trop. 51, 229–238.
UAE National Bureau of Statistics, 2006. Population by Emirates 1975–2005. http://www.
D=104&MenuId=1 (accessed 30.07.12.).
UNDP, 1987. Terminal Report Malaria Control Project, Oman. United Nations Develop-
ment Programme report; OMA/81/010/A/01/14.
UN Population Projections, 2011.
htm (accessed 04.05.12.).
Wernsdorfer, W.H., 2004. Report on a Visit to the United Arab Emirates. 5–29 March 2004.
World Health Organization, Eastern Mediterranean Regional Office archives, Cairo.
WHO, 1989. Weekly Epidemiological Record, August 1989.
(accessed 04.05.12.).
WHO-Aden, 1956. Information on the Malaria Control Programme in Aden (Colony).
World Health Organization report; WHO/MAL/163.17.
WHO-Yemen, 1956. Information on the Malaria Control Programme in the Yemen. World
Health Organization report; WHO/MAL/163.15.
Yemen Central Statistics Organization, 2010. Yemen Central Statistics Organization and
World Bank, Statistical Master Plan, Yemen, 2006–2010.
publication/smp/english.pdf (accessed 04.05.12.).
Zahar, A.R., 1969. Report on a Malaria Survey in the Northern Trucial States 22 March–11
April 1969. World Health Organization report; EM/MAL/83.
Zahar, A.R., 1974. Review of the ecology of malaria vectors in the WHO Eastern Mediter-
ranean Region. Bull. World Health Organ. 50, 427–440.
Zahar, A.R., Delfini, L.F., Ruebush, R.K., 1982. Report on Assessment on the Malaria Con-
trol Programme Sultanate of Oman.World Health Organization, Eastern Mediterranean
Regional Office archives, Cairo.

Microsporidia and ‘The Art of

Living Together’
Jiří Vávra*,†,1, Julius Lukeš*,
*Biology Centre, Institute of Parasitology, Czech Academy of Sciences, and Faculty of Science,
University of South Bohemia, České Budějovice, Czech Republic
†Faculty of Science, Charles University in Prague, Prague, Czech Republic
1Corresponding author: E-mail:

1. Defining Microsporidia 254
1.1. Basic Characteristics 254
1.2. What Is in a Name? 255
1.3. The Fungi that Do Not Look like Fungi, or Sisters of Fungi? 257
1.3.1. Gene Sequences and Microsporidia Phylogeny 259
1.3.2. Gene Order Analysis and Microsporidia Phylogeny 260
1.3.3. Gene Products and Microsporidia Phylogeny 261
1.3.4. Are Microsporidia Sisters of Fungi? 262
2. The ‘Art of Living Inside the Cell’ 263
2.1. Microsporidia Are Not Only Intracellular, but Truly Intracytoplasmic Parasites 263
2.2. Structural and Genomic Reduction 264
2.2.1. Extensive Structural Reduction 264
2.2.2. Reduced Genomes 266
2.2.3. Reduced Ribosomes 269
2.3. Full Dependence on the Host Cell 270
2.3.1. Gene Transfer from the Host 271
2.4. Influence on the Host Cell 272
3. The ‘Art of Dissemination’ 275
3.1. Spore Is a Gun Cell Powering the Missile Projection 275
3.1.1. Microsporidian Spore: a Masterpiece of Compaction 275
3.1.2. Single Species but Different Spores 280
3.1.3. Spore Germination and Its Evolutionary Significance 281
4. The ‘Art of Living in the Host’ 287
4.1. Well-Adapted Pathogens 287
4.2. Host-Specific Parasites 289
4.3. Ubiquitous Parasites 291
4.4. Cryptic Existence Masks Wide Occurrence 293
4.5. Strong Adaptation to Host Life Cycles and Biology 294
5. Envoi – the ‘Master Parasites’ 297
6. Conclusion 298
Advances in Parasitology, Volume 82 © 2013 Elsevier Ltd.
ISSN 0065-308X, All rights reserved. 253
254 Jiří Vávra and Julius Lukeš

Parasitism, aptly defined as one of the ‘living-together’ strategies (Trager, 1986), presents
a dynamic system in which the parasite and its host are under evolutionary pressure
to evolve new and specific adaptations, thus enabling the coexistence of the two
closely interacting partners. Microsporidia are very frequently encountered obligatory
intracellular protistan parasites that can infect both animals and some protists and are a
consummate example of various aspects of the ‘living-together’ strategy. Microsporidia,
relatives of fungi in the superkingdom Opisthokonta, belong to the relatively small
group of parasites for which the host cell cytoplasm is the site of both reproduction
and maturation. The structural and physiological reduction of their vegetative stage,
together with the manipulation of host cell physiology, enables microsporidia to live
in the cytosolic environment for most of their life cycle in a way resembling endocyto-
bionts. The ability to form structurally complex spores and the invention and assembly
of a unique injection mechanism enable microsporidia to disperse within host tissues
and between host organisms, resulting in long-lasting infections. Microsporidia have
adapted their genomes to the intracellular way of life, evolved strategies how to obtain
nutrients directly from the host and how to manipulate not only the infected cells, but
also the hosts themselves. The enormous variability of host organisms and their tissues
provide microsporidian parasites a virtually limitless terrain for diversification and eco-
logical expansion. This review attempts to present a general overview of microsporidia,
emphasising some less known and/or more recently discovered facets of their biology.

1.1. Basic Characteristics
Microsporidia are protistan (=single cell eukaryotes) parasites of animals
and, less frequently, of protists belonging to the ‘Sar’ kingdom as defined by
Adl et al. (2012). Microsporidia have been known to science for about 150
years, and 1300 to 1500 species in 187 genera have been described. These
unique organisms are strictly intracellular parasites with relatively uniform
life cycle (Cali and Takvorian, 1999).The germinating spore injects the spore
contents in the form of a small cell, the ‘sporoplasm’, into the cytoplasm of
a host cell by means of an explosively evaginable ‘injection tube’ (usually
referred to as a polar tube, polar filament or invasion tube) (Delbac and
Polonais, 2008; Franzen, 2004, 2005; Weidner, 1972; Xu and Weiss, 2005)
(see Section 3.1, p. 275). The sporoplasm grows into cells called meronts,
which divide by ‘merogony’ into daughter meronts. The meronts progres-
sively fill the cytoplasm of the host cell. Then, after an unknown signal, the
synthesis of proteins that will constitute the spore wall is activated and the
cell wall material consisting of chitin and microsporidia-specific proteins is
progressively deposited on the plasma membrane of stages called sporonts
Microsporidia and ‘the Art of Living Together’ 255

(Bohne et al., 2000; Brosson et al., 2005; Hayman et al., 2001; Li et al., 2009;
Peuvel-Fanget et al., 2006; Southern et al., 2007; Wu et al., 2008, 2009; Xu
et al., 2006). Sporonts, depending on the species, may continue to divide
and produce daughter sporonts but, finally, each sporont cell matures by a
process termed sporogony into a complex infective spore equipped with an
injection apparatus (see Section 3.1, p. 275). The spore is thus the product
of internal differentiation of a single cell (Vávra and Larsson, 1999). It is
the only stage that can survive in the environment and is responsible for the
dissemination of the parasite. The presence of the injection apparatus in
the spore is an autapomorphic character that sharply delineates microsporidia
as a monophyletic taxon presently classified as the phylum Microsporidia.

1.2. What Is in a Name?

The taxonomy of the phylum Microsporidia is, by tradition, considered
under the Code of Zoological Nomenclature (ICZN). It has been pro-
posed that this tradition continues (Redhead et al., 2009) despite the
fact that Microsporidia are now believed to be related to Fungi, the tax-
onomy of which is formally subjected to the Botanical Code [ICBN].
Practical reasons favour this solution; the Zoological and Botanical Codes
are technically incompatible and the nature of microsporidia–fungi rela-
tionship is unresolved (see Section 1.3, p. 257 and 1.3.4, p. 262) (Note
that in this paper ‘Fungi’ and ‘Microsporidia’ are used when meaning the
respective taxons, otherwise the vernacular names ‘fungi’ and ‘microspo-
ridia’ are used).
Although microsporidia represent a well-defined monophyletic group
of organisms, it is paradoxically the phylum name that is problematic. The
French embryologist Edouard-Gerard Balbiani was the first to use the name
‘microsporidies’ (Balbiani, 1882), but did not specify their taxonomic level.
This led to a taxonomic confusion and a discussion concerning the proper
name for the phylum representing these unicells. Most authors presently
use the name-author-date combination for the phylum Microsporidia
Balbiani 1882 (the name used in this paper); some authors, however, prefer
Microspora Sprague 1977 as the proper name (see discussion in Sprague
and Becnel, 1998). For more details on microsporidia early taxonomy and
its revisions, see Corradi and Keeling 2009.
Classification of microsporidia is primarily based on structural char-
acters observed under light and electron microscopy (Issi, 1986; Sprague,
1977; Sprague et al., 1992; Weiser, 1977); however, rRNA gene sequences
are now currently used as a supporting and sometimes even the principal
256 Jiří Vávra and Julius Lukeš

tool in defining taxa (see Section 2.2.3, p. 269). Consequently, some new
taxons are insufficiently characterised because the procedures for
protist taxa description, recently summarised by Lynn and Simpson (2009),
were ignored. As far as higher taxonomic categories are concerned, host
ecology has been proposed as a means to categorise microsporidian classes
(Vossbrinck and Debrunner-Vossbrinck, 2005) (see Section 4.2, p. 289).
The most recent summary of microsporidia identification is that of Larsson
(1986, 1988, 1999). The latest census of genera dates from 1999 to 2000
(Canning and Vávra, 2000; Larsson, 1999; Sprague and Becnel, 1999). It is
inevitably incomplete and subject to change because at least 43 genera have
been added since 1999, increasing the total number of existing genera to
187 (as of February 2013).
A consistent problem for classifying microsporidia is that many struc-
tural characters either do not bear a phylogenetic signal or the potential as
a signal has not been recognised. Thus, the formal classification of micro-
sporidia based on morphology and host range is in many cases incongru-
ent with phylogenetic relationships revealed by molecular methods. On
the other hand, the use of these methods facilitated the recognition that
some structural characters are phylogenetically informative and prompted
the reclassification and renaming of a number of microsporidian species.
The correct names of several species frequently used in current investiga-
tions of microsporidian biology are presented in Table 4.1. Other examples

Table 4.1  Taxonomically valid names of some microsporidia frequently used in

contemporary research that have been recently reclassified
Present valid name Older synonym(s)
Anncaliia algerae Franzen et al., 2006 Nosema algerae Vávra & Undeen, 1970
Brachiola algerae Lowman, Takvorian &
Cali, 2000
Paranosema locustae Sokolova et al., 2003 Nosema locustae Canning, 1953
Antonospora locustae Slamovits,
­Williams & Keeling, 2004
Hamiltosporidium tvaerminnensis Octosporea bayeri Jírovec, 1936*
Haag et al., 2011*
Tubulinosema kingi Nosema kingi Kramer, 1964
Franzen et al., 2005
Tubulinosema acridophagus Nosema acridophagus Henry, 1967
Franzen et al., 2005
*These two microsporidia are not identical; however, all molecular and population biology data on O. bayeri
reported to the year 2011 actually concern H. tvaerminnensis.
Microsporidia and ‘the Art of Living Together’ 257

of microsporidia reclassified to new genera could be cited here but these

transfers were made sufficiently long ago that the new correct names are
now in common usage.

1.3. The Fungi that Do Not Look like Fungi,

or Sisters of Fungi?
The structure and biology of microsporidia is so unique that their phylo-
genetic relationship with other organisms is not obvious. Historically, the
taxon Microsporidia appeared as an isolated group of organisms (Vávra,
1966). Due to their protistan nature, microsporidia were considered to
be parasitic protozoans and at a certain time, they were considered to
represent eukaryotic organisms lacking mitochondria, the Archezoa
of Cavalier-Smith (1983) (Corradi and Keeling, 2009; Keeling, 2009).
Presently, microsporidia are firmly anchored within the superkingdom
Opisthokonta (Adl et al., 2005, 2012). The evidence supporting phy-
logenetic position of microsporidia within the opisthokonts is based
exclusively on molecular biology characters because microsporidia lack
flagella, a hallmark of opisthokonts (though secondarily lost in a number
of their representatives). Like other opisthokonts, microsporidia have a
unique 11 amino acid-long insertion in the EF-1α gene and their THS-
DHFR genes are separated (Stechmann and Cavalier-Smith, 2003;
Steenkamp et al., 2006; Vivares et al., 1996).
While several molecular characters indicate that microsporidia are
related to fungi (Section 1.3.4. p. 262), microsporidia do not resemble fungi
morphologically, and no extant ‘missing link’ between these two groups of
organisms is known. Meaningful structural similarity between microspo-
ridia and fungi is limited to the deposit of cell wall material on the cell
membranes of certain developmental stages and the structure of spindle
pole bodies from which spindle microtubules emerge. The latter character
resembles the spindle plaque of yeast and ascomycetous fungi (Desportes,
1976; Desportes and Theodorides, 1979; Vávra and Larsson, 1999). Other
characters shared by microsporidia and fungi, and claimed to reflect their
relationship, include the formation of spores, presence of chitin in spores,
cryptomitosis, presence (in some species) of a formation of two adjacent
nuclei called diplokaryon, some features of meiosis and the presence of
trehalose (Cavalier-Smith, 2001; Thomarat et al., 2004). These characters,
however, are not exclusive for fungi and occur in a number of protist groups
(Flegel and Pasharawipas, 1995; Hine et al., 2007; Iturriaga et al., 2009;
Mulisch, 1993; Raikov, 1982).
258 Jiří Vávra and Julius Lukeš

Because microsporidia are structurally so dissimilar to other protists,

molecular phylogenies seemed to be the useful tool for revealing their
evolutionary relationships. However, the first sequences of ribosomal
genes (Vossbrinck et al., 1987) demonstrated the limitations of using gene
sequencing for the inference of evolutionary relationships of microsporidia.
Due to their extremely accelerated evolutionary rates (Katinka et al., 2001;
Slamovits et al., 2004a; Thomarat et al., 2004), the trees based on micro-
sporidian genes are prone to the artefact of ‘long-branch attraction’ (LBA),
in which divergent lineages (i.e. those having long evolutionary branches)
are invariably drawn to the base of the tree. This prompted Vossbrinck et al.
(1987) to suggest that microsporidia are extremely ancient eukaryotes, and
Cavalier-Smith (1983) to propose the now obsolete taxon Archezoa.
That the deep position of microsporidia in trees based on amino acid
sequences is an artefact was first convincingly shown by Hirt et al. (1999),
and it serves as one of the most striking examples of LBA in eukaryotic
trees (Brinkmann et al., 2005; Philippe and Adoutte, 1998). Today, we know
that microsporidia are relatively modern organisms (Keeling, 2009). Their
branches may be up to 8–10 times longer than those of most other fungal
organisms (Cavalier-Smith, 2001). The problem associated with the LBA
has been to some extent alleviated by the use of protein-coding genes with
relatively low evolutionary rates, or by the implementation of computa-
tional methods, which restrict the LBA artefact. However, as described
below, a degree of uncertainty concerning microsporidian phylogeny per-
sists in nearly all studies, in which protein sequences have been used.
Although microsporidia do not resemble fungi in terms of structure,
the molecular evidence supporting their relationship is overwhelming.
Sequences of many of their protein-coding genes (e.g. α, β tubulin; hsp-70;
EF-1α; valyl, glutamyl and seryl synthases; RPB1; vacuolar ATPase; TATA
box binding protein;TF-II; mitochondrial pyruvate dehydrogenase subunits
α, β) and the rRNA gene are related to those of fungi (Arisue et al. 2002;
Brown and Doolittle, 1999; Edlind et al., 1996; Fast et al., 1999; Germot
et al., 1997; Fischer and Palmer, 2005; Hirt et al., 1997, 1999; Katinka et al.,
2001;Van de Peer et al., 2000;Williams et al. 2002). Furthermore, microspo-
ridia possess a three-component mRNA-capping system similar to that of
fungi (Hausmann et al., 2002; Texier et al., 2005) and, like fungi, the micro-
sporidian SSU rRNA gene lacks a paromomycin-binding site (Katiyar
et al., 1995). Recently, the battery of molecular features supporting the
microsporidia–fungi relationship was strengthened by a synteny of ribo-
somal protein genes RPS9 and RPL21 unique to fungi and microsporidia
Microsporidia and ‘the Art of Living Together’ 259

and by the absence in microsporidia of gene fusion between glutamyl-pro-

lyl tRNA synthetase and the ubiqutin–ribosomal subunit S30 present in
fungi, but absent in other opisthokonts (Lee et al., 2010). In addition, the
types of microsporidia septins, GTPases involved in organising the sites of
cell division, vesicle trafficking, apoptosis and cell movement support fungal
affiliation to microsporidia. Interestingly, however, microsporidia septins are
closely related to septins of yeast but not of other fungi (Pan et al., 2007)
(The reader is further referred to Fast and Keeling (2005),Van de Peer et al.
(2000) and Vossbrinck et al. (2004) for a more detailed account of the rela-
tionship between microsporidia and fungi).
Although the concept that microsporidia are related to fungi is pres-
ently generally accepted, some authors have denied that such a relationship
exists. Microsporidial origin was sought near the Animal-Fungi divergence
because microsporidia lack a two amino acid fungi-specific indel present in
the EF-1α gene (Tanabe et al., 2002, 2005). Ebersberger et al. (2009) nested
microsporidia between Mycetozoa and Amoebozoa, a rather improbable
placement. Voigt and Kirk (2011) published a tree based on 1262 aligned
amino acids comprising actin, β-tubulin and translation elongation fac-
tor 1-α from 80 eukaryotic taxa, including numerous fungi. In this tree,
the microsporidia branch off close to the root of the tree with no specific
relationship to fungi, although the length of the microsporidian branch is
indicative of the LBA involvement.
Although the view that microsporidia are related to fungi seems to be
generally accepted, it is the exact nature of the relationship that is uncertain.
Are microsporidia nested within the fungi, derived from a specific fungal
group or do they represent their sister group? Three different approaches,
based respectively on the phylogenetic signal of gene sequences, the genome
architecture involving gene synteny, and the presence of specific gene prod-
ucts, can be used to address this question.

1.3.1. Gene Sequences and Microsporidia Phylogeny

Although numerous genes mentioned above show that microsporidia
are affiliated to fungi, some gene trees seemed to pinpoint the position
of microsporidia within fungi with more precision. Tubulin phylogenies
indicated the emergence of microsporidia after the chytrid fungi (Keeling
et al., 2000) or from within Zygomycetes (Keeling, 2003). An eight-
protein-concatenated tree showed that microsporidia are related to the com-
bined ascomycetes/basidiomycetes clade, the Dikarya (Gill and Fast, 2006).
Other phylogenies, however, suggest that microsporidia emerged close to
260 Jiří Vávra and Julius Lukeš

the origin of fungi.Thomarat et al. (2004) could not decide if microsporidia

branched off right after the basal chytrid fungi or represent a sister group
outside the fungi. Similarly other fungal trees show microsporidia as either
a sister group to fungi (Liu et al., 2006) or interpret them as their earliest
diverging branch (Wang et al., 2009). McLaughlin et al. (2009) present fun-
gal classification in which microsporidia are a part of a basal fungal lineage
including non-monophyletic group of ‘chytrids and zygomycetes’. Alterna-
tively, microsporidia were proposed to be derived from a basal endoparasitic
chytrid ancestor similar to Rozella allomycis ( James et al., 2006) (see Section
1.3, p. 259). Recently, the position of microsporidia as branching close to
the origin of fungi has been further strengthened by a study exploiting the
available 121 sequenced ‘fungal genomes’ (six of them microsporidian), by
large sampling and the use of specific methods overcoming the limitations
of other phylogenies, possibly affected by the LBA (Capella-Gutierrez et al.,
2012). Ensuing analysis of the phylomes (assemblage of gene phylogenies
of an organism) and of 53 concatenated genes of six microsporidian spe-
cies, showed topology with microsporidia constituting either the earliest
diverging branch of fungi or their sister group. The authors believe that
these two positions cannot be resolved on a factual basis. Due to ‘the exis-
tence of a number of synapomorphies between microsporidia and fungi’,
Capella-Gutierrez et al., 2012, favour the former placement. Authors of
another extensive phylogenomic study that compared the Nematocida parisii
genome to seven other microsporidian and 13 fungal genomes arrived to
the same conclusion (Cuomo et al., 2012). Finally, another study claims that
together with R. allomycis and an algal intracellular parasite Amoeboapheli-
dium protococcarum, microsporidia form a monophyletic sister clade (ARM
or Cryptomycota) to Fungi (Letcher et al., 2013; Karpov et al., 2013). It
should be pointed here, however, that none of the four above-mentioned
publications provides any evidence that microsporidia are fungi as opposed
to being related to fungi (see Section 1.3.4, p. 262).

1.3.2. Gene Order Analysis and Microsporidia Phylogeny

Gene order has been used as a method for overcoming the limitations
imposed on phylogeny studies by the LBA. Gene order (synteny) in micro-
sporidia seems relatively stable and allows informative comparison with
other organisms (Cornman et al., 2009; Corradi et al., 2007; Peyretaillade
et al., 2012; Slamovits et al., 2004a). This approach indicated a significant
similarity between microsporidia and zygomycete fungi (Dyer, 2008; Lee
et al., 2008), as they share a synteny of genes encoding a triose-phosphate
Microsporidia and ‘the Art of Living Together’ 261

transporter, transcription factor high mobility group (involved in sexuality of

zygomycetes) and an RNA helicase. This seemed to confirm previous indi-
cations that microsporidia are related to zygomycetes based on the analysis
of tubulin genes (Keeling, 2003). However, this synteny-based evidence has
been challenged on the basis of the evolutionary history of genes involved.
First, it was suggested that the genes in microsporidia/zygomycetes syntenic
clusters may not be orthologous but paralogous and hence allow no con-
clusion about the evolutionary relationship of the two taxa (Ebersberger
and Koestler, 2009; Lee et al., 2010). Further, it was shown that the
shared synteny of the respective clusters represents at best a shared ances-
tral character (plesiomorphy), and is not phylogenetically informative.
Similarity in gene order between microsporidia and zygomycetes does
not exceed that between microsporidia and other fungi and even some
animals (Koestler and Ebersberger, 2011). That a reliable phylogeny of
microsporidia cannot be inferred from the gene neighbourhood analysis
has recently been confirmed by additional authors. Heinz et al. (2012)
reported a lack of synteny or orthology among the relevant genes of two
microsporidia (Trachipleistophora hominis and Nosema ceranae) and zygo-
mycetes. Capella-Gutierrez et al. (2012) found that there is a similarly
low level of gene neighbourhood conservation between fungal groups
and microsporidia. Such observation makes the gene order conservation
not sufficiently informative.

1.3.3. Gene Products and Microsporidia Phylogeny

While both the gene sequences and genome architecture failed to provide
convincing evidence regarding the evolutionary history of microsporidia,
the presence/absence of certain gene products may serve as possible phy-
logenetic markers and indicate more precisely if microsporidia are early
fungi or their sister group. Cell wall components could possibly serve in
this context because cell wall chemistry and structure have some impor-
tance in fungal taxonomy. Indeed cell wall polysaccharides were used for
delimitation of high level taxa and their role in fungal evolution (Bartnicki-
Garcia, 1970; Ruiz-Herrera et al., 2002). In addition to some specific
proteins, α-chitin is the major component of the microsporidian spore
wall (Vávra, 1976; Wu et al., 2008). While there is a single type of chitin
synthase gene per species in a typical animal genome, in fungi the chitin
synthesis is based on the regulation of distinct chitin synthase (CHS) iso-
enzymes with one to five classes in filamentous fungi (Ruiz-Herrera et al.,
2002). Individual isoenzymes are involved in respective morphogenetic
262 Jiří Vávra and Julius Lukeš

events of fungal life cycles (Roncero, 2002). Recent analyses of the evolu-
tion of structural elements of the fungal cell wall and of genes involved in
their synthesis indicate that there is an evolutionary signal in the way how
the fungal cell wall is built (Xie and Lipke, 2010). In particular, it is the
evolution of CHSs, which accompanied fungal evolution (Ruiz-Herrera
and Ortiz-Castellanos, 2010). In addition to chitin deacetylases (Brosson
et al., 2005), microsporidia possess a gene for a single type of CHS (class
IV CHS-1), which is believed to represent an ancestral form of CHS, that
existed prior to the split of fungi from other opisthokonts (Ruiz-Herrera
and Ortiz-Castellanos, 2010) and is a member of CHS supergroup 2 to
which CHS of animals belong (Latge, 2007; Ruiz-Herrera et al., 2002). So
far this ancestral type of CHS has been found in Encephalitozoon cuniculi,
Encephalitozoon intestinalis, Hamiltosporidium tvaerminnensis, N. ceranae and
Spraguea lophii (Cornman et al., 2009; Corradi et al., 2009, 2010; Hinkle
et al., 1997; Katinka et al., 2001) thus suggesting that microsporidia seem
to have branched off close to the origin of fungi. Moreover, microsporidia
lack β-1,3, β-1,6 glucans and mannans, common matrix components asso-
ciated with chitin in cell walls of fungi (Ruiz-Herrera and Ortiz-Castel-
lanos, 2010). Rather in the microsporidian cell wall, chitin is complexed
with glycoproteins, as it is in many organisms other than fungi (Xie and
Lipke, 2010). Further research is needed to ascertain if the presence of the
single ancestral type of CHS-1 class IV truly reflects an early-branching
position of microsporidia near the animal-fungi divergence, and is not the
result of the loss of other CHS types, which has occurred (although very
rarely) in some fungi (Bowen et al., 1992).

1.3.4. Are Microsporidia Sisters of Fungi?

In summary, the origin of microsporidia and the nature of their relationship
to fungi remain unresolved. It is almost certain that microsporidia are not
derived from within a certain group of existing fungi, e.g. Zygomycetes or
the Dikarya, while deep-branching of microsporidia in relation to fungi
is now firmly supported. The view that microsporidia are a sister group
to fungi (lastly pronounced by Heinz et al., 2012), and indicated also by
the nature of their cell wall material and its corresponding genes discussed
above, seems to be the best current hypothesis worthy of further investiga-
tion, especially in situations where newly found organisms affiliated with
fungi (‘cryptomycota’) ( James and Berbee, 2011; Jones et al., 2011) promise
to contribute to our understanding of the origin of fungi. According to
the view postulating that microsporidia are sisters to fungi, it is suggested
Microsporidia and ‘the Art of Living Together’ 263

here that in articles dealing with these parasites, the systematic affilia-
tion ‘(Opisthokonta: Microsporidia)’ is used, instead of the usual ‘(Fungi:


2.1. Microsporidia Are Not Only Intracellular, but Truly
Intracytoplasmic Parasites
As described below in more detail (see Section 3.1, p. 275), the first step of
the microsporidian life cycle is the injection of the germplasm contained
in the spore into the cytoplasm of the host cell. This is a highly unusual
mechanism of cell infection among eukaryotic pathogens. Somewhat simi-
lar infection mechanisms are used by some basal oomycetes for injection
of the germplasm into the body cavity of nematodes, tardigrades and roti-
fers (Glockling and Beakes, 2002; Hakariya et al., 2002; Robb and Barron,
1982) and by rhizarian plasmodiophorids for injection into plant roots (Aist
and Williams, 1971). These respective injection mechanisms evidently arose
independently during the course of evolution, since microsporidia, oomy-
cetes and rhizarians belong to different kingdoms (Adl et al., 2005). Direct
introduction of the sporoplasm into the host cell means that, in contrast to
intracellular parasites that live in vacuoles (a kind of “growth chamber”)
derived from host-cell plasmalemma (e.g. the parasitophorous vacuole of
Apicomplexa, phagosome-like vacuoles of some kinetoplastid flagellates or
the symbiontophoric vacuoles of many intracellular prokaryotic or eukary-
otic symbionts), microsporidia are not only intracelullar but are genuinely
intracytoplasmic (cytosolic) parasites.
The sole interface between the injected sporoplasm and the host-cell
cytoplasm is the parasite plasma membrane often covered with glycocalyx.
This glycocalyx is highly developed in some microsporidia, forming struc-
tures deeply intruding into the host cytoplasm, suggesting that the glycoca-
lyx plays a role in the transport of nutrients into the microsporidian parasite
(Koudela et al., 2001). Different interfacial relationships of microsporidia
with host cells were categorised by Cali and Takvorian (1999), however,
the basic fact is that the parasite resides among host-cell organelles, often
surrounded by accumulated mitochondria and by lamella of the endoplas-
mic reticulum. A sole exception to this rule seems to be the intracellular
location of Encephalitozoon spp. (and possibly also of Endoreticulatus spp.) in
what resembles a parasitophorous vacuole (i.e. vacuole formed by the host
cell). At present its origin is far from resolved (Bohne et al., 2011; Fasshauer
264 Jiří Vávra and Julius Lukeš

et al., 2005; Rönnebäumer et al., 2008), and is beyond the scope of this
review. The intimate relationship between the parasite and the host cell is
maintained throughout merogony, during which the parasite does not cause
visible harm to the host cell except for some loosening and disintegration
of myofibrils in muscle infections. During merogonial growth and division,
microsporidia thus resemble an intracytoplasmic symbiont rather than a
typical parasite. The integrity of the host-cell cytoplasm in proximity to
the parasite cells is altered only when the microsporidium begins to form
a cell wall and enters the sporulation phase. The entire life cycle takes place
within the host cell into which the sporoplasm has been injected; there is no
evidence of vegetative stages actively moving among the host cells (see also
discussion below). It is a unique character of microsporidia that they remain
hidden within host cells and their vegetative stages remain sheltered from
extracellular milieu, thus limiting their recognition by the host immune

2.2. Structural and Genomic Reduction

2.2.1. Extensive Structural Reduction
The injected microsporidian sporoplasm, which is the beginning of the life
cycle in the host cell, consists of the contents of the infective spore, which,
although being forcibly passed through a long (up to several hundreds µm)
and very narrow (0.1–0.2 µm) injection tube, has maintained its integrity.
The sporoplasm, a few micrometres in diameter, is surrounded by a plasma
membrane of a peculiar origin – it was originally folded within the mature
spore as an accordion-like membranous stack known as the polaroplast
(see Section 3.1.1, p. 275). During germination, the polaroplast membranes
are drawn into the injection tube together with the spore cytoplasm and
nucleus, and are in part ejected from the end of the injection tube as a
germplasm-containing vesicle (see Section 3.1.3, p. 281). The origin of the
sporoplasm cell membrane is thus quite unusual, as it would involve a rever-
sal of membrane polarity (the former cytoplasmic side of the membrane
is now exposed to the environment). It was reported that the cytoplasmic
proteins tubulin and dynactin appear at the outer surface of the sporoplasm
plasma membrane and, consequently, its outer leaf lacks cholesterol and
lectin-binding molecules (Weidner, 2000, 2001;Weidner and Findley, 1999),
yet these data need to be verified.
The freshly injected sporoplasm can be considered as a kind of ‘minimal
eukaryotic cell’. Its cytoplasm is dense with ribosomes and contains
an inconspicuous nucleus (or two adhering nuclei forming a diplokaryon
Microsporidia and ‘the Art of Living Together’ 265

in some species – see Section 2.4, p. 272), non-specific vesicles, and some
membrane whorls and fragments that are not yet organised into cellu-
lar compartments. There is no visible Golgi apparatus and no struc-
tures reminiscent of cristae bearing mitochondria or other organelles
(Takvorian et al., 2005; Weidner, 1972). Cell membranes and organelles
appear progressively in later stages but structural reduction remains the
general feature of vegetative cells. Microsporidia have lost peroxisomes,
their mitochondria are reduced to mitosomes (see below) and their
membrane trafficking machinery is highly reduced (Dacks and Field,
2007; Mironov et al., 2006). The Golgi apparatus of microsporidia is
unstacked (Vávra, 1965; Mowbrey and Dacks, 2009), reduced to a clump of
varicose tubules embedded in an electron opaque material (Beznoussenko
et al., 2007; Dolgikh et al., 2010; Vávra and Larsson, 1999). Although it is
rather inconspicuous in vegetative stages, the Golgi apparatus plays a central
role in elaborating components of the extrusion apparatus during sporogen-
esis (Vávra, 1976) (see Section 3.1.1, p. 275).
The highly reduced mitochondria, called mitosomes, appear as small,
double-membrane vesicles distributed close to the terminus of the
microtubular division spindle and also scattered in the cytoplasm of veg-
etative stages (Vávra, 2005; Willwswiams et al., 2002, 2008a). Mitosomes
are minimalistic organelles with fewer than 20 mitosomal proteins iden-
tified, as compared to yeast mitochondria with well over 1000 proteins
(Paldi et al., 2010). Mitosomes lack a genome, oxidative phosphorylation
and Krebs cycle proteins and their protein import machinery is much
reduced (Waller et al., 2009). The Fe–S cluster assembly machinery seems
to be the only presently known function of microsporidian mitosomes
(Goldberg et al., 2008; Heinz et al., 2012; Williams, 2009; Williams et al.,
2002). In contrast, however, the gene for alternative oxidase (AOX) was
found in genomes of several other microsporidia (Heinz et al., 2012;
Williams et al., 2010), and the respective protein and glycerol-phosphate
dehydrogenase were localised to the mitosomes, indicating that these
organelles are involved in reoxidising the reducing equivalents produced
by glycolysis (Dolgikh et al., 2011). Structures corresponding to lyso-
somes and peroxisomes, which are components of a typical eukaryotic
cell, are missing in the vegetative stages of microsporidia (Vávra and
Larsson, 1999); however, the posterior vacuole, which plays an important
role in spore germination, may be a primitive or extremely specialised
peroxisomal organelle (Findley et al., 2005; Weidner and Findley, 2002)
(see Section 3.1.3, p. 281).
266 Jiří Vávra and Julius Lukeš

2.2.2. Reduced Genomes

Interestingly, the general structural simplification of microsporidian cell
is reflected in reduction and compaction at the molecular level, which is
most obvious in the organisation of their genomes (Corradi and Selman,
2013). Microsporidian genomes are characterised by gene loss (mostly of
metabolic genes, the products of which can be obtained from the host –
see below), reduction of gene length and by genome compaction, with
these events varying in different lineages (Corradi and Slamovits, 2011;
Heinz et al., 2012; Keeling et al., 2005; Keeling and Slamovits, 2004, 2005; 
Texier et al., 2005;   Vivares and Metenier, 2000). Initial data on micro-
sporidian genomics have been obtained from the analysis of the small,
2.9 Mbp genome of E. cuniculi (Katinka et al., 2001;  Vivares et al., 2002).
The recently sequenced genomes of other Encephalitozoon spp. are even
smaller (E.intestinalis, 2.3 Mbp – Corradi et al., 2010; Encephalitozoon hel-
lem and Encephalitozoon romaleae, 2.5 Mbp – Pombert et al., 2012; Selman
et al., 2011). Additionally, several surveys based on low coverage assemblies
of microsporidia with larger genomes are now available (Gill et al., 2008;
Hinkle et al., 1997; Mittleider et al., 2002; Slamovits et al., 2004a; Williams
et al., 2008b) as well as the following draft quality genomes: (Enterocytozoon
bieneusi <6.0 Mbp [Akiyoshi et al., 2009]; N. ceranae <7.86 Mbp [Cornman
et al., 2009]; Hamiltosporidium tvaerminnensis <24.2 Mbp [Corradi et al.,
2010]; N. parisii <4.1 Mbp [Cuomo et al., 2012]).These have been comple-
mented recently by an in-depth coverage of 8.5 Mbp from the T. hominis
genome which is about 11.6 Mbp in size (Heinz et al., 2012) and by
high-quality annotation of a large (23 Mbp) genome of Anncaliia algerae
(Peyretaillade et al., 2012). If the smallest genomes of Encephalitozoon spp.
are disregarded, the mean genome size calculated from the available data
exceeds 12 Mbp. Thus, the typical microsporidia genome is much larger
(up to tenfold) than the extremely small genomes of Encephalitozoon spp.,
which represent rather an exception. The size differences of microspo-
ridia genomes are, however, not reflected in the number of their genes.
The smallest (2.9–2.3 Mbp) genomes of E. cuniculi and E. intestinalis con-
tain 2094 and 1907 genes, respectively, while the so far largest (23 Mbp)
genome of A. algerae contains 2075 genes (this number has been estab-
lished by annotation using transcriptional signals – see Peyretaillade et al.,
2012). Currently the highest number of genes in sequenced microsporidia
is represented by the 3266 ORFs in the 11.6 Mbp genome of T. hominis
(Heinz et al., 2012). This number is still quite low when compared to the
Microsporidia and ‘the Art of Living Together’ 267

genome of Saccharomyces cerevisiae, which contains ∼6000 genes (Corradi

and Slamovits, 2011).
The size of microsporidia genes is generally smaller than of their eukary-
otic counterparts (see below), but again there is no rule that small micro-
sporidia genomes have smaller genes than the larger ones; for example, the
A. algerae genes are generally shorter than those found in E. cuniculi and E.
intestinalis (Peyretaillade et al., 2012). Hence, the tenfold variation in genome
sizes cannot be attributed to the size and number of genes, but to highly
variable gene density, ranging from 119 bp in E. cuniculi to 1.18 Kbp in T.
hominis (Heinz et al., 2012). The gene density depends on the length varia-
tion of intergenic regions, the number of sequence repeats and transposable
elements and the size of telomeric regions (Cuomo et al., 2012; Peyretaillade
et al., 2012).The difference between large genomes and the streamlined ones
can to some extent also be attributed to the presence of overlapping genes in
the latter genomes (Corradi and Slamovits, 2010; Heinz et al., 2012).
The genome compaction is evidently a product of the parasitic life style.
Many widespread and conserved eukaryotic genes, whose functions can be
provided by the host cell, such as the genes for biosynthesis of nucleotides,
genes of the tricarboxylic acid cycle, and electron-transport respiratory
chain, are missing (Katinka et al., 2001). In the extreme case, the 1833 and
1750 protein-coding genes identified in the respective E. intestinalis and
E. bieneusi genomes could represent the lower limits of a functional eukaryotic
genome (Corradi et al., 2010; Peyretaillade et al., 2012).
Moreover, microsporidian protein-coding genes are about 20% shorter
than their yeast orthologues. Intergenic regions are truncated and gene
transcription is modified as demonstrated by overlapping mRNAs between
contiguous genes in some microsporidia (Corradi et al., 2008, 2009, 2010;
Williams et al. 2005). In comparison with meronts, this ‘multi-gene tran-
scription’, in which mRNA transcripts of neigbouring genes partially and
in different degree overlap, occurs at a higher rate during the spore stage
of the life cycle, suggesting that it might play a role in accelerating and
streamlining proteosynthesis right after host infection (Corradi and Slamo-
vits, 2011; Gill et al., 2010; Grisdale and Fast, 2011) (see Section 2.4, p. 272).
Regardless of their size, even evolutionary distant microsporidian genomes
retain a high degree of gene order (synteny) (Slamovits et al., 2004a).
Thus, despite the rapid evolution of the coding sequences (Thomarat
et al., 2004), the genome architecture seems to be rather stable and conserved in
some microsporidia up to the point that homologous, yet divergent genes can
268 Jiří Vávra and Julius Lukeš

be identified due to their location in the genome (Polonais et al., 2005). Gene
compaction and overlapping transcription may contribute to this maintenance
of gene order (Corradi et al., 2007). From the evolutionary point of view, it is
probable that the gene loss responsible for the relative paucity of microsporidian
genomes may have been an ancestral feature that emerged as a consequence of
intracellular parasitism (Heinz et al., 2012;Williams et al., 2008b). However, due
to evolutionary pressures concurrent with intracellular parasitism, the evolution
of microsporidian genomes has not been marked only by losses and reduc-
tions, as some new genes and protein families have been gained, which enabled
microsporidia to become successful intracellular parasites (Heinz et al., 2012).
Microsporidia perfected the strategy of acquiring metabolites and nutrients
from host cells, amplified the number of transport proteins in their genome and
acquired some essential genes (ATP transporters, one class of nucleoside trans-
porters and some genes with their products involved in metabolism) by HGT
from prokaryotes or in rare cases from animal hosts (Cuomo et al., 2012; Lee
et al., 2009; Pombert et al., 2012; Tsaousis et al. 2008) (see Section 2.3, p. 270).
All this resulted in a massive loss of dispensable genes and the retention of an
assemblage of the ‘core of further irreducible sets of genes preserved through-
out microsporidian evolution’ (Corradi and Slamovits, 2011). Establishing this
‘core’ will require a broad sampling of genomes across microsporidia diversity.
Additional specific differences in individual genomes may be due to
their adaptation to different hosts and to different genomic environments
(Texier et al., 2010). One such example is the genome of E. bieneusi, the
most frequently recovered mammalian microsporidium. In contrast to other
species, which contain a full complement of genes for carbon metabolic
pathways (glycolysis, trehalose metabolism and pentose-phosphate path-
way), it appears that E. bieneusi has lost nearly all these genes and has no
known mechanism to produce energy on its own (Keeling et al., 2010);
however, since the E.bieneusi genome remains currently incomplete, this
view has to be considered preliminary.The loss of genes for energy produc-
tion makes Enterocytozoon extremely dependent on the host cell and possi-
bly explains why this species has so far resisted in vitro cultivation (Corradi
and Slamovits, 2011). In addition to the ability to generate energy from
sugars, E. bieneusi has also lost introns and the spliceosome (Keeling et al.,
2010). Surprisingly, despite all these losses, the E. bieneusi genome seemed to
contain a relatively large set of novel protein-coding genes as compared to
other microsporidia (Akiyoshi et al., 2009). Following comparative analysis,
however, pointed to the absence of typical microsporidian promoters for
a total of 387 these genes (Peyretaillade et al., 2012). While microsporidia
Microsporidia and ‘the Art of Living Together’ 269

were proved to acquire genes from their hosts as well as from other organ-
isms (see Section 2.3.1), conclusions about large-scale acquisitions seem to
be premature. Thus, it is most probable that the existing E. bieneusi assem-
bly has been contaminated with bacterial sequences (Heinz et al., 2012).
Actually, as shown above, the genome of E. bieneusi with its 1750 genes
(after re-annotation by Peyretaillade et al., 2012) is one of the smallest of
Microsporidia genomes (if not the smallest one). One can speculate that the
extreme streamlining of the E. bieneusi genome may allow the parasite to
accelerate its life cycle, a necessity if enterocytes with a life span of mere 3–5
days are parasitised (see Section 2.4, p. 272).
Numerous whole-genome sequencing initiatives that are currently
under way are bringing more data of individual microsporidian species.
Indeed, it is expected that as more microsporidia genomes are analysed
(Corradi and Slamovits, 2011; Texier et al., 2010), more genomic differ-
ences reflecting individual life histories of respective microsporidia will be
discovered. The loss of splicing machinery that happened independently in
several microsporidian lineages is one of such results (Cuomo et al., 2012).

2.2.3. Reduced Ribosomes

Considering the highly reduced nature of microsporidian genomes, it is not
surprising that the respective ribosomal RNA genes are highly truncated, with
the sedimentation coefficient of microsporidian ribosomes resembling that
of the prokaryotic 70S ribosomes (Curgy et al., 1980; Ishihara and Hayashi,
1968). Microsporidian large subunit (LSU) rRNA is reduced to the universal
core (De Rijk et al., 1998), ITS-2 is missing altogether and the 5.8S rRNA is
covalently linked either to LSU or, less frequently, to the small subunit (SSU)
rRNA (Peyretaillade et al., 1998;  Vossbrinck and Woese, 1986). In the first
case, the rRNA unit has the typical eukaryotic organisation (SSU-ITS-LSU),
while for Nosema spp. and a few other microsporidia an alternative and very
unusual reverse organisation (LSU-ITS-LSU) is characteristic (Huang et al.,
2004; Refardt and Mouton, 2007). Microsporidia are the only eukaryotes
known to lack an individual 5.8S rRNA molecule; however, the relevance of
this fact is unknown (Torres-Machorro et al., 2010). It is of interest that not
all ribosomes inside one cell are necessarily the same. The rRNA genes are
multicopy and distributed on different chromosomes (Katinka et al., 2001),
and are either identical (E. cuniculi), or exist in multiple variants, mostly dif-
fering in the ITS region (Tay et al., 2005). In Nosema bombi, a bumblebee
parasite, two such rRNA variants were found to co-exist in almost equal
proportions in the same cell (spore), and it was hypothesised that they are
270 Jiří Vávra and Julius Lukeš

restricted to separate nuclei of the diplokaryon (O’Mahony et al., 2007). Sig-

nificance of such variability is not known and its occurrence implies that the
concerted evolution of microsporidian rRNA genes is uniquely relaxed.The
co-occurrence of rRNA variants has, however, two important implications.
First, the occurrence and distribution of variants suggests that recombination
among them is taking place (Ironside, 2013), implying that a sexual haplo–
diploid cycle producing new haplotypes occurs in species such as N. ceranae
(Sagastume et al., 2011). Second, care has to be taken when multicopy rRNA
genes are used for population genetics and ­phylogenetic analyses (O’Mahony
et al., 2007) or in barcoding (Ironside, 2013).

2.3. Full Dependence on the Host Cell

The structural and genomic reduction mentioned above is only possible
because in terms of the metabolic and energy needs, microsporidia fully
rely on the host cell (Williams, 2009). Besides the partial or total loss of
energy-producing pathways mentioned above, the absolute dependence
on the host-cell metabolism is documented by the so far unprecedented
total loss of all components of the Tor pathway, a nutrient-sensing signalling
cascade that is otherwise universally present in eukaryotes. Microsporidia
probably relaxed their control of nutrient sensing and lost the Tor genes
while modifying their cellular machinery to adjust to intracellular growth
in a nutrient-rich environment (Shertz et al., 2010).
Once inside the host cell, microsporidia can proliferate very quickly
because the sporoplasm and the early meronts are loaded with ribosomes
that are needed for rapid proteosynthesis. Indeed, about 14% of proteins
encoded by the E. cuniculi genome are involved in proteosynthesis (Vivares
et al., 2002). The cell cycle of microsporidia is possibly accelerated by the
loss in microsporidia of the tumour suppressor gene Retinoblastoma, and
in this respect, microsporidia resemble some cancer cells (Cuomo et al.,
2012). Some species are able to complete their entire life cycle and form
mature spores within 3–4 days (Leitch and Ceballos, 2008; Wasson and
Barry, 2003) and, in accordance, time course analysis of selected transcripts
of N. parisii indicated a doubling time of 3.3 h, comparable to the doubling
time of yeasts in a rich culture medium (Cuomo et al., 2012). Consider-
able amounts of nutrients and energy are needed for such rapid intracel-
lular growth. Although microsporidia have lost in various degrees the genes
required for key energy-generating reactions, and their ATP production
is only possible by substrate level phosphorylation (Katinka et al. 2001;
Weidner et al., 1999b; ), microsporidia have developed a unique capacity to
Microsporidia and ‘the Art of Living Together’ 271

appropriate ATP from the host cell, and became ‘energy parasites’ (Vivares
et al., 2002). For this purpose, they use a series of recently discovered ATP
transporters, which were acquired from intracellular bacteria such as Rick-
ettsia or Chlamydia (Tsaousis et al., 2008).
An additional cunning mechanism that might help microsporidia to cope
with energy and nutrient demands has recently been proposed by Cuomo
et al. (2012). These authors found that microsporidian hexokinases gained
a microsporidia-specific secretion signal sequence, possibly allowing these
enzymes to be exported into host cells and reprogram them towards bio-
synthesis. Microsporidia thus could stimulate the energy balance of infected
tissues. Indeed, in the fat body of crickets infected by Paranosema grylli, the
ATP content and the ATP/ADP concentrations are increased about four
times, while at the same time, the infection causes depletion of glycogen in
the host (Dolgikh et al., 2002). Sugar metabolism is upregulated in midgut
cells of bees infected by N. ceranae (Dussaubat et al., 2012). The metabolic
needs of microsporidia are evidently the basis of the tendency for these
parasites to infect diverse metabolically active tissues including muscles,
fat bodies, ovaries, and salivary and silk glands. The capacity to ‘steal’ ATP
mentioned above likely explains the frequently observed accumulation of
host-cell mitochondria around the vegetative stages of the parasite (Scanlon
et al., 2004), as well as the propensity of a few species of microsporidia to
live in host-cell nuclei, a rich source of ATP and of nucleoside triphos-
phates (Metenier and Vivares, 2001; see Section 2.4, p. 272). To facilitate
nucleoside uptake, microsporidia acquired nucleoside transporters, one new
class of them probably hijacked from bacteria (Cuomo et al., 2012). The
high demand for energy also explains why these protists survive in a kind
of dormancy within cells that are temporarily metabolically inactive, such
as the germ-line cells, before initiation of embryonic development (Weiser,
1961). Regulation of gene expression is clearly needed in order for such an
adaptation to the metabolic state of the host cell to occur. RNA interfer-
ence, recently shown to be functional in N. ceranae (Paldi et al., 2010) and
likely present also in T. hominis (Heinz et al., 2012), yet absent from
E. cuniculi (Katinka et al., 2001), might be one example of a gene expres-
sion-regulating mechanisms.

2.3.1. Gene Transfer from the Host

Although microsporidia live in an extremely intimate relationship with the
host-cell cytoplasm or, as mentioned above in host-cell nucleus, the transfer
of genetic material between the animal host and the parasite is evidently
272 Jiří Vávra and Julius Lukeš

a rare event. Only two cases of a horizontal gene transfer (HGT) from a
host have been fully documented. In one case, two sister microsporidia,
E. romaleae and E. hellem from insects and vertebrates, respectively, contain a
gene for purine nucleotide phosphorylase (PNP), evidently acquired from
an unknown insect host in the E. hellem – E. romaleae ancestor (other known
members of the genus Encephalitozoon lack the PNP gene – Selman et al.,
2011). However, further investigations are needed to establish the extent of
the HGT from animal hosts. It will certainly be worth analysing the evolu-
tionary history of genes involved in folate and purine metabolism specific
for E. hellem and E. romaleae, which were evidently acquired by their ances-
tor in several HGT events, involving different organismal donors, some of
them probably eukaryotic (Pombert et al., 2012). In a highly unusual HGT
event, a transposable element in the genome of T. hominis was evidently
obtained from an ant or a close relative (Heinz et al., 2012).

2.4. Influence on the Host Cell

Microsporidia have mastered both the entry into host cell and the exploita-
tion of its metabolism, and have developed a number of physiological adap-
tations enabling them to subvert host-cellular machinery to their benefit
(see Section 2.3, p. 270). Another peculiar feature is the capacity of micro-
sporidia to synchronise their life cycle with that of the host cell, and even
modify its cytoskeleton and organelle arrangement (Scanlon et al., 2000,
2004; Weidner et al., 1999b). Specifically, the normal cell cycle of infected
host cells is blocked at multiple points, their division is often arrested and
their susceptibility to apoptosis is reduced (Scanlon et al., 1999, 2000)
because the parasite inhibits activation of the p53 apoptotic pathway (del
Aguila et al., 2006). Delayed apoptosis allows the parasite to increase its
numbers and complete its development to the mature spore stage.
Very little is known about the interaction between microsporidia and
the host-cell cytoskeleton, which is presumed to play a role in the enlarge-
ment of infected cells and in the intracellular positioning of the parasite
(see below). Because the microsporidian tubulin and dynactin appear at the
surface of the freshly discharged sporoplasm, it was hypothetised that the
latter protein may be responsible for the positioning of the parasite within
the host cell (Weidner, 2000). Some species occupy a specific location in
the host cell, e.g. E. bieneusi is usually abutted to the enterocyte nucleus
and is often situated inside the concavity of the invaginated nuclear mem-
brane (Desportes-Livage et al., 1996; Chalifoux et al., 1998). Members of
the genera Nucleospora and Enterospora are nucleotropic (Lom and Dyková,
Microsporidia and ‘the Art of Living Together’ 273

2002; Stentiford and Bateman, 2007; Stentiford et al., 2007), but how they
reach their destination remains unknown. The interaction with the host
cytoskeleton was described for N. parisii, which destroys the spectrin–yosin
terminal web of infected gut enterocytes of its host, the model nematode
Caenorhabditis elegans (Troemel et al., 2008).
The enlargement of the host cells post-invasion reflects the ability of
microsporidia to subvert the host-cell cytoskeleton and volume control in
order to secure a sufficiently spatial and protected niche. Hypertrophy of
infected host cells is characteristic of microsporidian infections in general
(Lom and Dyková, 2005) and is accompanied by several secondary effects;
individual infected cells may dedifferentiate into a syncytium, undergo
nuclear hypertrophy and fragmentation, increase RNA synthesis, and some-
times produce an increased number of cell nuclei (Canning and Hazard,
1982; Leitch et al., 2005a; Martins and Perondini, 1977). Another notable
effect is the enlargement and increase in the degree of polyteny of giant
chromosomes in Diptera, signalling the generalised hyperfunction of the
cell genome under the influence of microsporidian infection (Pavan et al.,
1969) and the inactivation of cell-type-specific Balbiani rings and puffs sig-
nalling a change in the cell-type-specific genetic program (Staiber, 1994).
Infected lymphocytes of annelids form multiple microvilli on their surface,
which probably serve to increase the absorptive capacity of the cell (Janisze-
wska et al., 1978).
The most spectacular host-parasite interaction as far as the increase
of cell volume is concerned is represented by giant, usually macroscopic,
spore-filled formations termed xenoma, characteristic for numerous micro-
sporidian species infecting fish. Xenoma are not limited to fish; giant cells
induced by microsporidia occur in number of other hosts including oligo-
chaetes, crustaceans and insects (Lom and Dyková, 2005). Xenomas in fish
may reach several millimetres in size but remain a single cell with one, albeit
significantly modified, nucleus, cytoplasm containing developmental stages
of the parasite and, finally, mature spores. The host cell and the parasite are
morphologically and physiologically integrated in the xenoma and it is sup-
posed that this alliance shelters the parasite from the host’s immune system.
Indeed, the inflammatory reaction in host tissues occurs when the xenoma
reaches maturity, looses its integrity and the spores are released (Kent and
Speare, 2005). The xenomas in fish supposedly originate in many cases in
infected leukocytes and they occur in many forms, differing mostly in the
nature and thickness of the wall surrounding the xenoma cell (Lom and
Dyková, 2005). So far, it is not known how the cell volume of infected cells
274 Jiří Vávra and Julius Lukeš

is controlled, how the parasite regulates the metabolism of its host cell, and
how it recognises the critical mass of its life stages inside the cell. As the
host cell has a limited parasite-carrying capacity, signals must exist to induce
the parasite to complete merogony and initiate sporogony in order to form
mature spores before cell death. No data on such signalling exist. Regretta-
bly, the macroscopic xenomas have so far been ignored by molecular biolo-
gists despite their relative amenability for molecular analyses, the lack of
their availability in culture being the probable reason.
In some cases, the key factor that determines if a microsporidium is able
to infect a certain tissue is the rate of its development related to the host-cell
cycle and cellular turnover. This is best demonstrated in species infecting
enterocytes of digestive systems. The turnover time for enterocytes is in the
range of 3–5 days (and there is no data suggesting that the infected enterocyte
lives longer), into which the microsporidium has to complete several multi-
plication cycles along with the formation of spores. As mentioned in Section
2.3 (p. 270) some microsporidia develop in their host cells with astonishing
speed. E. intestinalis and E. hellem are able to form spores within 3 days (Leitch
and Ceballos, 2008), a fact confirmed by real-time quantitative PCR showing
that E. intestinalis DNA is detectable in colonic enterocytes in tissue culture at
4 h post-inoculation, replication is completed by 36 h and spores are released
from host cells at 72 h post-inoculation (Wasson and Barry, 2003). Spore-
specific mRNAs of N. parisii are detectable already at 40 h post-infection
(Cuomo et al., 2012), while in E. cuniculi mRNAs involved in spore chitin
synthesis are induced 20–48 h post-infection (Rönnebäumer et al., 2006).
The same high rate of development must exist in E. bieneusi, in which the
precocious formation of the extrusion apparatus begins already during the
plasmodial stage (Desportes-Livage et al., 1991).Within the short life span of
a gut enterocyte, this microsporidium will produce about 60 spores from a
single sporoplasm (Vávra and Larsson, 1999).
As mentioned in the Section 2.3 (p. 270), physiological factors in micro-
sporidia are set up to promote rapid growth of the parasite. It is how-
ever possible that also other, less obvious factors allow microsporidia to
develop quickly in order to exploit the limited viability of host cells. One
might speculate that specific features such as the size of ribosomes (Curgy
et al., 1980; Ishihara and Hayashi, 1968), truncated genes (Katinka et al.,
2001) and peculiarities in genomic expression (Gill et al., 2010; Grisdale
and Fast, 2011) may contribute to the rapid rate at which microsporidia
develop. There are two structural characters that provide evidence to support
the potential for rapid cell cycling. One, previously mentioned, is the high
Microsporidia and ‘the Art of Living Together’ 275

abundance of ribosomes (isolated ribosomes in meronts, polyribosome aggre-

gates in spores), and the other is the frequent occurrence (either permanent
or transitory) of two adhering haploid nuclei that form the so-called diplo-
karyon (Canning, 1988;Vávra and Larsson, 1999). Although the physiological
reason for the presence of two nuclei in a cell remains to be established (and
in the much-reduced microsporidian cell is somewhat surprising), one may
speculate that having two nuclei facilitates the nucleus/cytoplasm transport
and makes the mRNA ‘ratcheting’ (Stewart, 2007) out of the nucleus more
efficient. The presence of two nuclei in a cell also increases its ploidy and
confers advantage to the organism as the ploidy-levels regulate gene expres-
sion (Galitski et al., 1999; Hieter and Griffiths, 1999) and influence rates of
evolution (Otto, 2007). It should be mentioned here that the presence of
two nuclei in cells of some microsporidia raises the question of how the
genetic complementarity in both nuclei is maintained and its putative associa-
tion with sexual processes. This is a contentious subject that would require a
detailed treatment that is beyond of the scope of this review.


3.1. Spore Is a Gun Cell Powering the Missile Projection
Because of their obligate intracellular life stages and lack of motility, microspo-
ridia became adapted to solving the problem of how to disperse among hosts
and how to disseminate within their host. To that end they evolved a form of
dispersal, which might be appropriately called the ‘missile projection’.The ger-
minating spore functions as a ‘gun cell’, which by means of an evaginable ‘injec-
tion tube’ (conventionally called the polar tube) nearly instantly propels the
sporoplasm to a distance from several to hundreds of µm from the germinating
spore. This tube, first described by the French protistologist Thélohan (1892),
has a tremendous penetration power. It pierces host tissues with ease and injects
the microsporidian sporoplasm directly into the host cells as documented by
early TEM observations (Ishihara, 1968). This missile form of infection is used
for new host invasions as well as for dissemination within the host tissues. For
this dual purpose, a single microsporidian species produces either spores that
look similar but differ in germination readiness, or in some cases spores that dif-
fer both physiologically and morphologically (see Section 3.1.2, p. 280).

3.1.1. Microsporidian Spore: a Masterpiece of Compaction

The microsporidian spore is a highly compact product of a single cell
differentiation. Spore cytoplasm, one or two nuclei and a three-part
276 Jiří Vávra and Julius Lukeš

injection apparatus, which consists of the injection tube, the polaroplast

(an accordion-like membrane storage organelle) and a posterior vacu-
ole (a pressure-building organelle), fill a body of only several microns in
length and diameter; the smallest spores are similar in size to a bacterium
(1.2 × 0.9 µm in E. bieneusi, 4 × 2.5 µm in a typical Nosema). All parts of
the injection apparatus and the spore case are secretory products processed
through the classical endoplasmic reticulum-Golgi synthetic pathway and
are fully formed in the mature spore (Delbac et al., 2001). Spore structure
and function has been the subject of several exhaustive reviews (Delbac and
Polonais, 2008; Franzen, 2004, 2005; Keohane and Weiss, 1999; Vávra, 1976;
Vávra and Larsson, 1999; Xu and Weiss, 2005).
The spore is essentially a miniature pressure vessel with a thick and
complex cell wall that consists of two layers: the internal endospore layer,
which is composed of a complex of proteins and α-chitin, and the exter-
nal proteinaceous exospore (Vávra, 1976). The shapes of spores (e.g. oval,
round, pyriform, rod-like) are ideal for withstanding the high internal
pressure (>7.0 Mpa) that is generated inside the spore during germination
(Lom and Vávra, 1963) The endospore is the pressure-resistant layer of the
spore envelope, while the exospore is believed to mediate contact with
environmental stimuli. This is most evident in species from aquatic hosts,
which often bear spines, tubules, fibrils or mucous layers on their exospores
(Vávra and Larsson, 1999) (see Section 4.5, p. 294).The spore wall proteins
have no homologues in protein databases outside of microsporidia. Some
of them bear a heparin-binding motif, indicating a possible interaction
of spores with glycosoaminoglycans, that occurs on the surface of host
cells and which may influence spore infectivity (Bohne et al., 2000; Bros-
son et al., 2005; Hayman et al., 2001; Li et al., 2009; Peuvel-Fanget et al.,
2006; Southern et al., 2007; Wu et al., 2008, 2009; Xu et al. 2006). Proteins
associated with the spore wall are typically found in either the exo- or
endospore layer of the spore envelope but curiously, in one instance, the
protein SWP5 of Nosema bombycis was found not only in the exospore, but
also inside the spore in association with the coils of the injection tube.This
protein is thought to interact with injection tube proteins PTP 2 and 3
and can be detected immunologically in the extruded injection tubes (Li
et al., 2012). Considerable inter- and intraspecific variability of the spore
wall proteins exists, and it has been suggested that these proteins might
be used in diagnostics and in molecular epidemiology s­tudies (Xiao et al.,
Microsporidia and ‘the Art of Living Together’ 277

The injection tube, which is ejected from the spore during germination
and serves to make the missile projection possible, is the most characteristic
structure within the spore. It is also the only component of the injection
apparatus that is universally present in microsporidian spores, while other
structures such as the polaroplast and the posterior vacuole are occasionally
lacking (or exist in an unusual, as yet unrecognised form?), which is the case
of some putatively primitive microsporidia of the order Metchnikovellida
(Desportes and Theodorides, 1979; Larsson, 2000; Larsson and Koie, 2006).
The tube has been referred to as ‘polar filament’, ‘polar tube’ and ‘invasion
tube’; however, the term ‘injection tube’ expresses best its function and is our
preferred use for the structure. It has to be stressed here that the injection tube,
while inside the spore, does not resemble a hollow tube, as it looks rather like
a solid structure (hence ‘polar filament’ in older descriptions) (see below).
However, its tubular nature is revealed during spore germination.
The tube is usually coiled into one or multiple coils to fit within the
spore volume and is quite long in some species. The bacterium-sized spore
of E. bieneusi contains an injection tube that, according to only rough calcu-
lations, should be between 10 and 20 µm in length when extruded (no data
have been published concerning its actual length). The spore of the well-
known honey bee-infecting Nosema apis is approximately 5 µm in length
and extrudes an injection tube that exceeds 300 µm in length (Olsen et al.,
1986). However, about 20% of microsporidian genera have spores that con-
tain straight, uncoiled, rod-like tubes, which in the unextruded state just
fit within the length of the spore (Canning and Vávra, 2000). The tube is
anchored to the inner apex of the spore by a mushroom-like structure called
the polar cap, consisting of filament mushroom-like terminal (anchoring
disc), enveloped by a membraneous bag-like structure called the polar sac.
The polar cap area (sometimes called polar sac – anchoring disc complex)
is the major site for mannose-rich glycoproteins (Taupin et al., 2006; Vávra,
1972; Vávra and Larsson, 1999) and is present in all microsporidia. It rep-
resents an autapomorphic character that can be elucidated by staining and
can be used in light microscopic diagnostics to differentiate microsporidian
spores from other spore-forming organisms (Vávra and Maddox, 1976). The
polar cap anchors the injection tube to the spore apex during eversion (Lom,
1972) and it is speculated that the abundance of hydrophilic sugars associ-
ated with the polar cap facilitates exit of the tube from the spore ­(Taupin
et al., 2006).The polar cap region is also rich in the spore wall protein EnP1,
which might assist in adherence of spores to host cells (Southern et al., 2007).
278 Jiří Vávra and Julius Lukeš

From the spore apex, the injection tube descends in a straight path through-
out the apical volume of the spore and is eventually coiled in the posterior
region. The PTP proteins, best characterised in E. cuniculi, E. intestinalis and
E. hellem (Delbac et al., 2001), constitute a novel protein family (Delbac and
Polonais, 2008).Three proteins labelled PTP1, PTP2 and PTP3 represent the
major and, so far, the only defined components of the injection tube ­(Delbac
et al., 1998; Keohane and Weiss, 1998; Peuvel et al., 2002; Xu and Weiss,
2005) and their structural interaction in injection tube assembly remains
to be elucidated (Bouzahzah et al., 2010). The major component (70%) of
the injection tube is PTP1, a proline-cysteine-rich O-mannosylated protein.
O-mannosylation may protect the injection tube from degradation in the
gastrointestinal tract of the hosts, and may mediate its interaction with man-
nose receptors of the host-cell membrane, and thus facilitate the adherence
of the tube to the host cells (Bouzahzah and Weiss, 2010; Xu et al., 2004).
PTP1 is a highly immunogenic; it induces a strong immune response
in vaccinated animals and was sufficient for inducing protective immunity
against E. cuniculi (Moretto et al., 2010). Moreover, this protein is claimed to
be responsible for the relatively frequent occurrence of antibodies to micro-
sporidia in healthy humans (Furuya et al., 2008; Peek et al., 2005).The high
cysteine content of PTP1 and PTP2, which is also rich in lysine, suggests
that disulphide bridges play an essential role in the injection tube assembly
and are responsible for its high tensile strength. Finally, the PTP3 protein
lacks cysteine residues and its role in tube construction is not clear.The PTP
proteins are conserved and the respective genes of their homologues have
been identified in a number of microsporidian species (Akiyoshi et al., 2009;
Cornman et al., 2009; Corradi et al. 2009). Their general presence is likely
due to the unique character of the microsporidian injection mechanism.
The PTP proteins 1 and 2 are suitable for phylogenetic inference within
Microsporidia. For example, PTPs from N. ceranae share only ∼20% iden-
tity with orthologues from the distantly related E. cuniculi (Cornman et al.,
2009), whereas they display 67% and 85% identity with PTPs from more
closely related Paranosema locustae and P. grylli, respectively (Polonais et al.,
2005). Interestingly, the high variability of the PTP locus corresponds with
the existence of three epidemiological genotypes of E. cuniculi, namely those
of  “rabbit”, ‘mouse’ and ‘dog’, which are known to differ in other molecular
biology markers as well (Didier et al., 1995; Peuvel et al., 2000; Xiao et al.,
2001). Extensive PTP polymorphism was recorded in N. ceranae (Hatjina
et al., 2011) and among different isolates of E. hellem (Haro et al., 2003;
Peuvel et al., 2000). This polymorphism may be the cause of differential
Microsporidia and ‘the Art of Living Together’ 279

infectivity of various isolates of E. hellem (Haro et al., 2006). As a practical

outcome, the PTP polymorphism may be used as a suitable marker for trac-
ing sources of infection of some microsporidia (Peuvel et al., 2000). It is of
interest that despite a careful search for proteins with structural organisation
reminiscent of PTP1, Heinz et al. (2012) failed to identify its homologue in
the T. hominis genome. Further research is needed to prove that the exten-
sive polymorphism of PTP proteins is not responsible for this ‘absence’.
Even though the fine structure of the injection tube is well known
and its main proteins have been characterised, many aspects of its struc-
ture and function remain to be elucidated. The fine structure of the tube,
when coiled in the resting spore, typically consists of 3–20 concentric layers
(Vávra and Larsson, 1999; Xu and Weiss, 2005) of materials of different elec-
tron density. One of the layers is glycoprotein-rich. As already stated above,
the tube-like nature of the injection tube is not evident from ultrastructural
studies of non-germinated spores (Cali et al., 2002; Lom, 1972; Vávra, 1976;
Vávra and Larsson, 1999), yet the structure functions during germination
as an actual tube (see Section, p. 281). The fine structure of the
tube markedly differs among individual species and the above-mentioned
variability of PTPs is probably a basis for these differences. Moreover, the
injection tube structure may also vary among different spore morphs of
the same species. Vairimorpha disparis forms three types of spores, each with
a specific length and polar tube structure (5, 12 and 30 filament coils in
respective spore types) (Vávra et al., 2006) (see Section 3.1.2, p. 280). The
structure of the individual tube also varies along the length of the unex-
truded tube, being uniformly thick along the entire length (isofilar tubes),
or being thicker at its proximal part (anisofilar tubes). If the proximal part
is very thick, it is called manubrium (Lom, 1972; Vávra and Larsson, 1999).
There is no explanation for these differences in the injection tube structure.
It is worth mentioning that the extruded tube is usually longer than
estimated from TEM photomicrographs of spore coils in the dormant spore.
It remains to be determined whether the tube is fully preformed in the
dormant spore (this is most probable) and is extruded as such, or if it is
actually partly assembled during eversion from the spore. Lom and Corliss
(1967) calculated the length of the tube from ultrathin sections of a fish
microsporidium to be in the range of 100–120 µm, while, after extru-
sion, the tube was estimated to be 300–500 µm long. Such an expansion
of length suggested that the tube may actually grow during eversion by
the addition, and polymerisation on its growing tip, of material deposited
in the interior of the unextruded tube (Keohane and Weiss, 1999;
280 Jiří Vávra and Julius Lukeš

Weidner, 1982). However, elongation of the tube might be simply due to its
extensive elasticity, witnessed as it momentarily thickens during sporoplasm
passage (up to several µm – Olsen et al., 1986), and its recoiling by 5–10% of
length when germination pressure ceases. The elasticity might reside in the
tube substructure since extruded tubes have a complex substructure (Cali
et al., 2002), and negatively stained extruded tubes (after tryptic digestions)
appear to possess a fibrillar ultrastructure reminiscent of the ­meshwork
structure of a firefighter’s hose (Vávra, 1976).
The evolutionary origin of the injection tube is not known. Due to the
‘fungal connection’ of microsporidia, attempts were made to interpret the
injection tube as homologous to fungal structures involved in host inva-
sion, such as the polar bodies of the ‘holdfast’ appressoria of trichomycete
harpellaelan fungi (Cavalier-Smith, 1998), spore appressorium and pen-
etration tube-like peg of the “chytridiomycete” R. allomycis ( James et al.,
2006) ­(similar penetration tube-like formation exists in Amoeboaphelidium,
see Karpov et al., 2013; Letcher et al., 2013), and the sporangiophore of
zygomycetous fungi (Lee et al. 2008). These fungal structures, however, are
basically modified hyphae formed by the cell wall expansion and are likely
to have a completely different chemical composition than that of the injec-
tion tube. Hence, they cannot be easily compared with the injection tube
preformed inside the spore by cytoplasmic differentiation that does not
involve the cell wall of the spore (Williams, 2009). Kugrens et al. (1994)
and Vivares and Metenier (2001) remarked that the microsporidian injec-
tion apparatus resembles extrusomes, which are membrane-bound ejectable
organelles common in some protists, especially ciliates and dinoflagellates,
and capable of discharging their contents under certain conditions to the
outside of the cell (Hausmann, 1978). The fundamentally unique feature of
the microsporidian injection tube resides in the fact that it serves for emp-
tying the entire spore contents and not only the specific extrusome mate-
rial as occurs in protist extrusomes. It can be concluded that the origin of
microsporidian injection apparatus remains to be unknown and appears to
be a specific evolutionary apomorphy of these parasites.

3.1.2. Single Species but Different Spores

The extreme adaptation of microsporidia to their host physiology and
life cycle is reflected in the facts that even within a single-host species,
spores may be formed that are different both physiologically and struc-
turally. When two or more different spore types are produced, the given
species is termed to be dimorphic or polymorphic respectively. Distinct
Microsporidia and ‘the Art of Living Together’ 281

spore types are formed either in different hosts through which the organism
completes its life cycle, or as an outcome of different life cycle paths occur-
ring in the same host. For example, V. disparis, a parasite of the gypsy moth
­(Lymantria dispar L.), forms three spore types: one for quick dissemination
within the host, and two other types that serve for interhost transmission
(Vávra et al., 2006). Some species parasitising mosquitoes form different
spores either in the same or in different hosts (Becnel et al., 2005; Lukeš
and Vávra, 1990). The life cycle of Amblyospora spp., involves three hosts:
a copepod, a male mosquito larva and a female mosquito adult. A differ-
ent spore type is formed in each host (Andreadis, 2007). The individual
types differ to the extent that they would be assigned to different genera in
conventional classification. Kneallhazia solenopsae forms four distinct spore
types in various life cycle stages and tissues of its host, the fire ant ­Solenopsis
invicta (Sokolova and Fuxa, 2008). An interesting example is that of the
human microsporidian opportunist Trachipleistophora anthropophthera, which
forms two structurally very distinct spore types that are probably involved
in intra- and interhost dissemination, respectively. Both types are formed in
the same brain tissue and sometimes within a single cell (Vávra et al., 1998).
It is perhaps of e­ volutionary importance that the capacity to form several
distinct spore types occurs in the putatively primitive microsporidia, class
Metchnikovellidea (Weiser, 1977), hyperparasites of gregarines and some
insects (Desportes and Theodorides, 1979; Larsson, 2000; Larsson and Koie,
2006; Purrini and Weiser, 1985). However, even in monomorphic species,
not all spores produced are identical. As discussed below, spore variability
expressed as a differential response to germination stimuli probably plays an
important role in microsporidia evolution.

3.1.3. Spore Germination and Its Evolutionary Significance The Germination Event
Although spore germination has been well documented (Frixione et al.,
1992; Lom and Vávra, 1963), several aspects of the process are only par-
tially understood. What initiates spore germination under natural condi-
tions is unknown, although several experimental stimuli such as shifts in pH
and ionic concentration have been identified (Keohane and Weiss, 1999).
­Germination can be triggered in some species by simply wetting dried
spores (Olsen et al., 1986). It is generally accepted that germination is an
osmotic event and it was proposed that the first step of the signalling cas-
cade that triggers germination is calcium/calmodulin binding at the spore
surface (Weidner and Byrd, 1982;Williams, 2009). It was postulated that the
282 Jiří Vávra and Julius Lukeš

next step in spore germination is the influx of water into the spore, possibly
due to the activity of ionophore molecules (Dall, 1983) or aquaporins in
the spore membrane (Frixione et al., 1997). Indeed, aquaporin-like genes
were identified in genomes of several microsporidia (Akiyoshi et al., 2009;
Corradi et al., 2009; Ghosh et al., 2006).
Germination begins by swelling of the polaroplast area during which
the polaroplast membranous stacks dissociate. The pressure inside the spore
rises to a point where the thinner apex of the spore case ruptures and
the injection tube is expelled explosively while turning inside out during
the process (‘finger of a glove’ model). While the tube everts, the posterior
vacuole in the spore expands and forces the cytoplasm and the nucleus of
the spore through the tube. The small cell appearing at the tip of the fully
everted tube is enveloped by plasma membrane that is derived from the
folded membrane system of the polaroplast and which was forced into the
tube along with the cytoplasm and the nucleus (Weidner et al., 1984). After
germinating, the spore case remains essentially empty but is lined inside by
the former plasma membrane. During germination, the tip of the evagi-
nating injection tube advances through the environment and penetrates
any obstacle in its way, including other microsporidian spores (Weidner,
1972), and, injects the sporoplasm like a hypodermic needle, into the cyto-
plasm of an encountered host cell (Ishihara, 1968). The penetration power
of the injection tube is enormous, e.g. spores of Pleistophora hyphessobryconis
ingested by the ciliate Paramecium germinate in its food vacuoles, shoot
the tubes throughout the ciliate cytoplasm and cell pellicle and deliver the
sporoplasms to the ciliate surroundings (J. Vávra and J. Lom, unpublished
observations). The penetration power resides in the fact that it is only the
tip of the evaginating tube that advances through the environment while
the entire length of the tube behind the tip is immobile (Franzen, 2004,
2005; Lom and Vávra, 1963; Weidner, 1972). The process of germination is
so rapid that it takes approximately 2 s for the tip of the tube to advance
through environment at a ‘rocket speed’ estimated to be more than 100 µm
per second (Frixione et al., 1992).
Spore germination requires energy; however, the source of this energy
remains unknown. Rapid breakdown of trehalose into glucose and the con-
commitant increase of osmotic pressure within the spore had been pro-
posed as a source of the energy required for germination (Undeen, 1990).
Both trehalose and the enzyme trehalase occur in microsporidia (Dolgikh
and Semenov 2003; Metenier and Vivares, 2001), and trehalose is known to
accumulate at the final stage of spore maturation (Undeen and Solter, 1996).
Microsporidia and ‘the Art of Living Together’ 283

However, it is unlikely that trehalose powers the germination process

because Undeen and Van der Meer (1999) reported that the level of tre-
halose decreases during in vitro spore germination in microsporidia from
aquatic hosts but not in those from terrestrial hosts. It is quite counterin-
tuitive that different microsporidia would use several osmolytes for ger-
mination instead of a single and universal source. It is also questionable to
distinguish aquatic and terrestrial microsporidia because there are species
that have different spore morphs in both types of hosts. Thus, it seems more
reasonable to suppose that, in microsporidian spores, trehalose serves as an
energy source for spore survival and as an anti-desiccation agent (Metenier
and Vivares, 2001). The depletion of trehalose that occurs in spores exposed
to stress factors and to long-term storage corroborates this proposed func-
tion (Undeen and Solter, 1996).
A different source of energy for spore germination was suggested to be
located in the posterior vacuole. Findley et al. (2005) suggested that the pos-
terior vacuole is a giant peroxisome in which hydrogen peroxide produced
by the decomposition of long-chain fatty acids is converted by catalase
into water and oxygen. This causes the posterior vacuole to swell and eject
the spore contents from the spore. Although catalase was histochemically
detected in spores of Spraguea lophii (Weidner and Findley, 2002, 2003),
the general presence of catalase in microsporidia remains questionable; the
gene for catalase seems to be missing from the E. cuniculi genome but, in
contrast, P. locustae possesses a catalase gene of prokaryotic origin (Fast et al.,
2003).The uncertainty concerning the presence of catalase in microsporidia
requires further investigation as one could reasonably expect that all micro-
sporidia should utilise the same germination mechanism. In summary, the
source of energy for spore germination has yet to be determined.
Microsporidia spread via spore germination either within cells of an
individual host (intrahost dissemination) or by invading another host usu-
ally when spores are ingested and germinate within digestive tract (inter-
host dissemination). Some microsporidian species form special spore types
for intrahost dissemination but it seems that, in most microsporidian spe-
cies, spores are essentially similar but differ in their readiness to germinate.
Spores that could be called ‘precocious germinators’ germinate as soon as
they are formed inside the host cells or released from bursting cells. For
example, many E. cuniculi spores, freshly liberated from bursting infected
cells into a cultivation medium, immediately germinate while other spores
remain unchanged (Vávra et al., 1972). When this occurs in infected tis-
sue, the sporoplasms are introduced into surrounding host tissues and
284 Jiří Vávra and Julius Lukeš

thus parasite disseminates within the host. Systematic data addressing this
scenario in vivo are not available because inside-the-host germination is
usually not recorded; empty spores are quickly degraded by the host and/
or spore remains are reported as artefacts. The stimuli that promote intra-
cellular germination are currently unknown; however, ionic changes that
accompany cell death are suspect as a candidate. In general, the formation
of precociously germinating spores is a very little known phenomenon,
despite that it is probably of common occurrence.
As mentioned previously, some microsporidia that infect Diptera,
­Hymenoptera and Lepidoptera form special generation(s) of precociously ger-
minating spores, which are structurally distinct and which are produced at
an early stage of infection. Such ‘early’ or ‘primary’ spores have thin spore
walls, large posterior vacuoles and relatively short injection tubes. They
­germinate spontaneously, immediately after formation, and inject their spo-
roplasms into distant target tissues of the host where another generation(s)
of ‘secondary’ or ‘environmental’ spores is formed. A microsporidium that
infects the gypsy moth L. dispar represents an example of this strategy.
Ingested ‘secondary’ spores are acquired from the environment by larvae
and germinate in their midgut tissues. The first generation of spores is pro-
duced very quickly (30 h post-infection) in muscle cells surrounding the
gut. These early spores germinate spontaneously upon maturation and their
sporoplasms are injected into fat body, salivary and silk glands, and other
tissues where environmental spores destined for interhost transmission are
produced.These secondarily formed spores have a smaller posterior vacuole,
thicker spore walls and a long injection tube (Solter and Maddox, 1998b;
Vávra et al., 2006). It seems that the production of primary spores is con-
trolled genetically rather than by the host, because they are produced also in
microsporidia that are grown in tissue cultures (Iwano and Ishihara, 1991;
Iwano and Kurtti, 1995). Evolutionary Aspects of Spore Germination

We can only speculate about the potential evolutionary aspects of spores
that are formed in the same host but endowed with a different sensitivity
to germination stimuli. Spores with a capacity for delayed germination may
pass through (even numerous) non-specific hosts before they eventually
release their sporoplasms in a host that provides the most favourable condi-
tions. Kramer (1973) noted that most spores of Octosporea muscae-domesticae,
which parasitise the gut epithelium of the house fly, germinate during the
first passage through the alimentary tract; some spores, however, germinate
Microsporidia and ‘the Art of Living Together’ 285

only after they have undergone two to four passages. The combination of
delayed germination and a lack of specific germination stimuli (meaning
that germination would occur only in the most favourable and specific
host) may thus be a powerful factor inherent to microsporidian evolution.
Human infections caused by opportunistic microsporidia of probable insect
or fish origin (see Section 4.3, p. 291, for the list and references) and the
present expansion of the Asian honeybee, Apis cerana, parasite N. ceranae
among populations of the European honey bee Apis mellifera (Fries, 2010)
provide a cogent testimony that potential incidents of host-switching and
of host range expansions continuously occur. The peculiar germination
mechanism that microsporidia possess also allows them to successfully infect
parasitic organisms that do not possess a functional digestive tube. Members
of the supposedly primitive order Metchnikovellida are examples of such
a strategy, as they live as hyperparasites in gregarines that inhabit the ali-
mentary tract of polychaetes, sipunculids and echiurids (Canning and Vávra,
2000; Larsson, 2000; Larsson and Koie, 2006). One microsporidian lives
as a hyperparasite in the protist Marteilia, parasite of oysters (Comps et al.,
1979). Several microsporidian species are known to be hyperparasites of
parasitic platyhelminths, tapeworms and trematodes (Canning, 1975; Sene
et al., 1997). In each of these hosts, the sporoplasm must be injected into the
host from outside, through the host’s cell membrane complex (­gregarines,
­Marteilia) or tegument (platyhelminths). The stimulus for spores to germi-
nate must be provided in the digestive tract of the host that harbours the
gregarine, tapeworm or trematode. This peculiar germination–injection
mechanism explains why the larvae (rediae) of the fluke Fasciola hepatica
become infected when the snail Lymnea, hosting the trematode, is fed spores
of the mosquito microsporidium A. algerae (Costa and Bradley, 1980). Spore Germination: the Unknowns

Many questions need to be answered in order to satisfactorily understand
the spore germination event and its impact on the distribution of micro-
sporidia and their host and tissue specificity. Even the basic question of how
the injection tube penetrates the cell has been debated. Although direct
mechanical piercing represents the generally accepted explanation, Agaud
et al. (1997) and Rönnebäumer et al. (2008) suggested that the extrusion
of the injection tube of E. cuniculi into an invagination of the host-cell
membrane might be integral in the infection process, meaning that it is
different from that of other microsporidia. This is an improbable conten-
tion, especially if one realises that the penetration power of the tube is such,
286 Jiří Vávra and Julius Lukeš

that a cell membrane does not present any obstacle to the germ injection
(see Section, p. 281). Together with the question of how the para-
sitophorous vacuole in which Encephalitozoon develops is formed, the issue
needs further research at best and is beyond the scope of the present review.
Additional questions include the following: Is the spore somehow oriented
before discharge and do the spores germinate preferentially when adjacent
to the host tissues? In vitro experiments demonstrated that the adherence
of spores to glycosoaminoglycans of target cell is related to the success of
the infection (Hayman et al., 2005; Leitch et al., 2005b; Southern et al.,
2007). However, no contact with host tissue was found to be required in
germination of N. apis and N. ceranae spores (Gisder et al., 2011). There is
also some evidence that intestinal mucus may influence spore orientation
(Leitch and Ceballos, 2008). Spores of E. intestinalis were shown to express
an endospore-targeted protein (EnP1) on their coat with most of this pro-
tein detected in the area of the anchoring disc, which is the apex of the
injection tube. Potentially, EnP1 mediates spore attachment to the host-cell
glycosoaminoglycans (Hayman et al., 2005). Within-Host Dissemination: More Unknowns

Very little data is extant on the within-host dissemination of microsporidia.
As mentioned previously, within-host spore germination is involved in dis-
semination (at least in some species); however, it seems that there should
be another mechanism enabling the parasite to spread among host cells.
A remarkable characteristic common in many microsporidian infections is the
massive invasion of host tissues. This is most obvious in small invertebrate
hosts where the host often becomes a living ‘bag’ of spores. Yet, how the
infection progresses rapidly from cell to cell is not understood and, for some
species, internally germinating spores have never been observed. A typi-
cal case is that of Amblyospora spp. which progressively infects the oocytes
of copepods. The entire host ovary appears to become one large mass of
spores, all of them at the same stage of maturation, yet no germinated spores
are present ( J.Vávra, unpublished observation). This phenomenon certainly
requires further research.
The tissue tropism and specificity of microsporidia also remain largely
obscure. Enterospora canceri and Enterospora sp. are confined to the nuclei of
epithelial cells lining the hepatopancreas of the European edible crab, Cancer
pagurus (Stentiford et al., 2007). These hepatopacreatocytes are not in direct
contact with the food consumed by the host, so it is quite enigmatic as
to how the parasite finds way to its specific location. Similarly, Nucleospora
Microsporidia and ‘the Art of Living Together’ 287

salmonis, Nucleospora secunda and Enterospora sp. specifically infect host cell
nuclei (Chilmonczyk et al., 1991; Lom and Dyková, 2002; Stentiford and
Bateman, 2007). Do these species occur in the nucleus because the injection
tube strikes the nucleus either by chance or due to an unknown targeting
mechanism? Or were they injected first into the cytoplasm and then trans-
located into the nucleus? The notion that microsporidia can be translocated
secondarily into a specific cell compartment seems unlikely, but cannot be
excluded. Most intriguing is the case of several species of the genus Spraguea,
which infect neural tissues of the angler fish Lophius. The parasite evidently
travels from cutaneous mucous gland to medulla oblongata, and then to
various nerves, with spores being finally excreted in urine (Freeman et al.,
2011). How the parasite finds the way to its locations is not known.


4.1. Well-Adapted Pathogens
Microsporidia qualify as parasites, sine qua non as they ‘infect host cells,
exploit what is in there to replicate within them, produce spores and then
transmit themselves to other cells within the same host or to a new host’
(Agnew et al., 2003). However, during the life cycle, each individual micro-
sporidium passes through a less extreme form of symbiotic relationship,
behaving first as a seemingly harmless, intracellular commensal. Infected
host cells are ultimately destroyed during the period when the parasite
forms spores. To what extent the host is harmed during this last phase of
the microsporidian life cycle depends on many factors, several of which
involve the host itself. This makes the host–parasite relationships strongly
context-dependent and subject to variation between deleterious (including
host mortality), more or less neutral, or even positive in some cases (Ryan
and Kohler, 2010). Consequently, the variety of host–microsporidian inter-
actions, categorised for the first time for mosquito microsporidia by Kellen
et al. (1965), is enormous. It depends on the respective parasite and host
species, the degree of their co-adaptation, tissue tropism, genotype or sex of
the host, environmental conditions, means of transmission and other factors
(Agnew et al., 2003; Becnel et al., 2005; Ebert, 1995, 2008; Issi, 2002; Little
and Ebert, 1999; Ryan and Kohler, 2010; Smith, 2009).
In retrospect, microsporidia have mastered the means to maximise repro-
duction and transmission by producing large numbers of infectious spores
and/or by efficient transmission mechanisms that maintain the pathogens in
host populations. This is demonstrated by some infections in insects. Many
288 Jiří Vávra and Julius Lukeš

insect microsporidia cause infections that initially do not appear to injure

the host in obvious ways, even when massive multiplication of the parasite
in host organs takes place. For example, some species that infect lepidopteran
larvae progressively destroy the fat bodies of their hosts as the cells become
filled with spores. Infected larvae still feed and behave in a more or less nor-
mal way; however, they usually die during molt or pupation, when energy
reserves of the host’s fat body tissues needed for molting and metamor-
phosis are unavailable (Agnew et al., 2003; Goertz and Hoch, 2008a; Siegel
et al., 1986;Weiser, 1961). Delaying the death of the host until the late stage
molt or pupation allows the parasite to maximise the production of spores;
this reservoir of spores released by the cadavers provides the inoculum to
infect new hosts (Goertz and Hoch, 2008a,b). In some Lepidopteran species
that produce silk, microsporidian spores may be transmitted along the silk
secreted by larvae from infected silk glands ( Jeffords et al., 1987).
The maximum production of spores and their dissemination into the
environment is also the strategy employed when the microsporidian patho-
gen targets a tissue that has high regenerative capacity (gut or excretory
epithelia), thus allowing the continuous production of spores. In such
case, even a massive infection leaves the host apparently unaffected, at least
temporarily. This occurs in midgut infections of gypsy moth larvae by
­Endoreticulatus schubergi (Hoch et al., 2009) or in the nematode C
­ aenorhabditis
infected with N. parisii (‘the nematode-killer from Paris’). The nematode
host can carry a large parasite burden in its gut epithelial cells and still feed
and behave relatively normally, at least for some time. Ultimately, however,
its life span is shortened (Troemel, 2011).
In mammals (and probably true for many vertebrates), microsporidian
infections have a chronic character, provided that the host is immunocom-
petent and the infection remains localised (Ghosh and Weiss, 2012). On the
contrary, immunocompromised hosts may develop a lethal disease (Texier
et al., 2010). The apparent benign nature of chronic infections is, however,
relative. This is best demonstrated in rabbit encephalitozoonosis, a very fre-
quent microsporidiosis caused by E. cuniculi in farm-bred rabbits worldwide.
The spores of the pathogen are excreted in the urine and the infection is
easily transmitted from cage to cage by contamination in intensive breeding
situations (Vávra et al., 1986, 1987). Rabbit encephalitozoonosis usually fol-
lows a subclinical course (no preventive or curative measures are applied by
breeders) and infected animals appear healthy (Künzel and Joachim, 2010).
However, a detailed examination of a group of well-fed, clinically healthy
broiler rabbits, with relatively high titres of antibodies against E. cuniculi,
Microsporidia and ‘the Art of Living Together’ 289

showed 11% reduction in the weight of the meat carcass at slaughter com-
pared with serologically negative animals (Vávra et al., 1980).
Extending the life span of the host is beneficial for many pathogens and
microsporidia are a prime example of such a strategy as they usually do not
excessively or prematurely harm the host. However, physiological weaken-
ing of the host’s immune defences may lead to explosive colonisation of the
host by the parasite with ensuing deleterious consequences. In such cases,
microsporidia behave as opportunists that are not only able to excessively
colonise their usual host, but also potentially infect atypical hosts. Micro-
sporidioses are thus included in the Emerging Diseases category (Didier,
2005). Their opportunism is best shown in HIV/AIDS-positive or severely
immunosuppressed humans, in whom a cryptic infection can be exacer-
bated or an infection by a species of unknown source can occur (Anane
and Attouchi, 2010; Didier et al., 2004; Didier and Weiss, 2006, 2011). The
immune status dependency of microsporidian infections is reflected in the
recently improved immune status of HIV-infected humans; due to the avail-
ability of more efficient anti-HIV drug cocktails, a notable decrease has
occurred in the number of publications addressing microsporidia/HIV co-
infections (Heyworth, 2012). The opportunistic character of microsporidia
is also revealed in infections of the eye, an immunoprivileged site. Human
and animal keratoconjuctivitis and uveitis caused by microsporidia are not
a rarity. Exposure to dust and muddy water, minor injuries, hot springs
exposure and warm and wet climates are risk factors for ocular microspo-
ridiosis (Alkatan et al., 2012; Fan et al., 2012; Juarez et al., 2005; Kunzel and
Joachim, 2010; Quek et al., 2011; Sharma et al., 2011). Eye infections are
in principle, dangerous as they can progress to systemic diseases (Koudela
et al., 2001).

4.2. Host-Specific Parasites

Most microsporidia are host-specific parasites which evolved and co-­
speciated with their original hosts. Their specificity is typically restricted to
a single host species or to a group of affiliated species (Baker et al., 1998;
Shafer et al., 2009; Smith, 2009). It is the concensus among traditional tax-
onomists that the host is an important indicator of microsporidian species.
Two good examples of microsporidian co-speciation with their hosts is the
phylogeny of Loma spp., which mirrors the evolutionary course of gaddid
fish in the Pacific Basin (Brown et al., 2010) and the phylogeny of mosquito
microsporidia, which reflects the evolutionary relationships of respective
genera with their hosts (Andreadis et al., 2012).
290 Jiří Vávra and Julius Lukeš

Since microsporidia tend to group by hosts (Brown et al., 2010), and

host phylogeny and ecology are mostly compatible, an attempt was made to
define formal microsporidia taxons according to their host habitat. Hence,
classes ‘Aquasporidia’, ‘Marinosporidia’ and ‘Terresporidia’ were proposed
for species parasitising hosts in the respective freshwater, marine and ter-
restrial habitats (Vossbrinck and Debrunner-Vossbrinck, 2005).These classes
have been occasionally used in actual classification (Stentiford et al., 2010),
despite criticism raised after their creation by those who respect formal
taxonomy rules (Larsson, 2005).
Host ecology also seems to play a role in the maintenance of host spec-
ificity and microsporidian diversity. Some microsporidia that are able to
infect multiple host species under experimental conditions (when the gen-
eral compatibility between the pathogen and the host, termed ­‘physiological
specificity’ is determined) do not infect the same host in nature because
ecological barriers between atypical hosts and the parasite exist. These
barriers determine the ‘ecological specificity’ of the pathogen (Solter and
Maddox, 1998a). Vertically transmitted species parasitising forest Lepidoptera
represent parasites for which the physiological and the ecological specific-
ity are often not congruent (Solter, 2006; Solter et al., 2005). Frequently,
host and tissue specificity are related, e.g. N. apis is confined to the midgut
enterocytes of the honeybee (although it is also able to infect gypsy moth
cells in a tissue culture – Gisder et al., 2011), and S. lophii parasitises the
neural ganglia of the angler fish Lophius sp. (Freeman et al., 2004, 2011).
Other microsporidia, however, parasitise broader groups of hosts, and are
less tissue-specific; mammalian microsporidia are a good example. For the
widespread E. cuniculi, E. hellem and E. intestinalis, low host and practically
no tissue specificity are characteristic, whereas E. bieneusi is mostly but not
totally confined to the enterocytes and occasionally infects epithelial cells
of the respiratory and urinary tracts of its multiple mamalian hosts (Botterel
et al., 2002; Sak et al., 2011b,c).
The physiological basis of host and tissue specificity in individual
microsporidian species is not known, but one possible reason is genome
­reduction leading to the close dependency of the parasite on host metabo-
lism ­(Peyretaillade et al., 2011). Interestingly, investigation of several human-
infective species, including those that parasitise mammals or are simply
opportunists, showed that these microsporidia contain a specific inter-B
gene family, located in the subterminal chromosomal regions. This inter-B
multigene locus is absent in a number of species not implicated in human
infections (Dia et al., 2007). Several members of the inter-B gene family
Microsporidia and ‘the Art of Living Together’ 291

possess predictable transmembrane domains and N-terminal signal peptides,

suggesting that respective proteins are targeted to parasite surface (Williams,
2009), and hence likely have an impact on host–parasite relationships.

4.3. Ubiquitous Parasites

The ability to inject their germplasm (sporoplasm) into the intracellular
milieu of a host opened for microsporidia an ecological niche represented
by a vast variety of hosts and their respective tissues, and allowed them to
rapidly radiate. Microsporidia are recognised as one of the most frequently
observed parasites of both invertebrates and vertebrates, including humans.
While they have been found to occur in representatives of about half of
metazoan phyla, it is without doubt that many, if not most, species still
await discovery, given the low number of experts studying these parasites
and the plethora of prospective animal hosts. True microsporidian diversity
might approach and or surpass the number of animal species (Keeling and
Slamovits, 2004); parasitism of a single-host species by several microsporid-
ian species is not uncommon (Krebes et al., 2010).
Most microsporidian diversity is found in invertebrates, with crustaceans
and insects being the most frequent hosts. In the paper of Vossbrinck and
Debrunner-Vossbrinck (2005) proposing microsporidian classes based on
host ecology, 69% out of the 125 species listed have crustacea and/or insects
as their hosts. Although this number has only a limited value due to low
sampling, it reflects the relative abundance of microsporidia in respective
Insect microsporidia are memorable as the agent of the collapse
of E ­uropean silk industry in the mid-nineteenth century, caused by
N. ­bombycis, the first microsporidian described (Nägeli, 1857).This species is
unquestionably the most important parasite of the silkworm as even today
it is a threat to the silkworm industry (Bhat et al., 2009; Kawarabata, 2003).
Nosema bombi infections of bumblebees and N. apis and N. ceranae infec-
tions of honey bees exemplify widespread pathogens of principal pollinators
(Cameron et al., 2011; Chen et al., 2009; Otti and Schmid-Hempel, 2007).
Nosema ceranae, originally the parasite of the Asian Apis cerana, has progres-
sively invaded on the world-wide scale the colonies of the European honey
bee, A. mellifera (Fries, 2010).This parasite has a significant pathogenic effect
on its new host. It disturbs gut tissue regeneration and homeostasis and
influences a number of physiological functions of the bee gut ­(Dussaubat
et al. 2012). It is of considerable economic importance that even the sub-
lethal levels of pesticide residues, now commonly occurring in agriculture,
292 Jiří Vávra and Julius Lukeš

significantly increase the sensitivity of honey bees to Nosema infections and

contribute to bee colonies mortality (Pettis et al., 2012; Wu et al., 2012).
More than 150 microsporidian species have been described from different
mosquito genera worldwide, and it is believed that most if not all mosquito
species serve as hosts for at least one microsporidian parasite (Andreadis,
2007; Andreadis et al., 2012). Some microsporidia act as regulators and/
or agents of biological control for noxious insects of economic or health
importance (Bargielowski and Koella, 2009; Hajek and Delalibera, 2010;
Lomer et al., 2001). Nosema pyrausta, which infects the European corn borer,
Ostrinia nubilalis, is a classical example of a parasite that effectively helps to
regulate an important agricultural insect pest (Lewis et al., 2009), while
P. locustae (better known to public by its original name Nosema locustae) is
used as a biological pesticide for grasshopper control (Henry and Oma,
1981; Lomer et al., 2001).
The second most numerous group of microsporidia are found in crus-
tacean hosts. Economically significant representatives are Enterocytozoon
­hepatopenaei and Myospora metanephrops from shrimps and lobsters, respec-
tively (Tourtip et al., 2009; Stentiford et al., 2010).
Fish, the most common vertebrate hosts of microsporidia, with more
than 160 described species assigned to more than 17 genera (Canning
and Lom, 1986; Lom, 2002; Lom and Nilsen, 2003), are known to cause
important losses to fisheries, both in natural conditions and in aquaculture
­(Abdel-Ghaffar et al., 2011; Dyková, 2006; ). Loma salmonae has a significant
negative impact on commercial cultures of salmonids (Shaw et al., 2000),
while Pseudoloma neurophilia and P. hyphessobryconis occasionally plague the
research colonies of the laboratory model zebrafish Danio rerio (Matthews
et al., 2001; Sanders et al., 2010). Several microsporidian species are known
to parasitise mammals (Canning and Lom, 1986). Of about 14 microspo-
ridian species found infecting humans, only four (E. cuniculi, E. hellem,
E. ­intestinalis and E. bieneusi) are specific to mammals, while others (e.g.
­Vittaforma corneae, T. hominis, T. anthropophthera, A. algerae, Tubulinosema spp.,
Endoreticulatus-like microsporidium, and several organisms assembled under
the collective genus Microsporidium) are opportunists that have been acquired
by humans from insects or unknown hosts (Anane and Attouchi, 2010; Cali
and Takvorian, 2004; Canning and Lom, 1986; Coyle et al., 2004; Curry
et al., 2005; Didier, 2005; Didier et al., 2004; Didier and Weiss, 2006; Cali
et al., 2010; Choudhary et al., 2011; Fan et al., 2012; Field et al., 2012; Juarez
et al., 2005; Mathis et al., 2005; Meissner et al., 2012; Suankratay et al., 2012;
Vávra et al., 1998), or as in the case of Pleistophora ronneafiei, probably from
Microsporidia and ‘the Art of Living Together’ 293

fish (Cali and Takvorian, 2003). The ability of some mammalian microspo-
ridia to infect insect hosts (and thus possibly be of insect origin) has been
experimentally proved (Vávra et al., 2011; Weidner et al., 1999a).

4.4. Cryptic Existence Masks Wide Occurrence

Because of their cryptic existence in their hosts, only a relatively small
fraction of putatively extant microsporidia has been discovered to date.
Many infections pass unnoticed, either permanently or at least temporarily,
when the infections are mild and spore loads are low. This cryptic exis-
tence of microsporidia is shown most clearly by the use of molecular tech-
niques that allow sensitive diagnosis of low-level infections (Accoceberry
and ­D'Almeida-Fourquet, 2012; Franzen and Müller, 1999; E ­ l-Matbouli
and Soliman, 2006; Hamiduzzaman et al., 2010; Refardt and Ebert, 2006;
Valenčáková et al., 2012; Weiss and Vossbrinck, 1999). Indeed, molecu-
lar techniques have shown microsporidia to be unexpectedly common
parasites. The human intestinal microsporidium E. bieneusi was originally
described as a rare, HIV-associated pathogen (Desportes et al., 1985). Pres-
ently, more than 90 genotypes of this organism, distinguished on the basis
of the hypervariable ITS region of the SSU rRNA gene, have been recog-
nised from a number of mammalian hosts, most of which exhibit no overt
clinical symptoms (Santin and Fayer, 2009a,b; 2011; Thellier and Breton,
2008). E. bieneusi actually may be one of the most common human parasites
with a prevalence attaining 58% in some populations (Nkinin et al., 2007).
Although most infections are inapparent, the association of this parasite with
diarrhoeal disease is well known (Akinbo et al., 2012; Ojuromi et al., 2012),
and recently the capacity of E. bieneusi to cause small food-borne epidem-
ics in immunocompetent subjects has been documented (Decraene et al.,
2012). The number of its genotypes recovered from humans continues to
rise (Sak et al., 2011b,c; Zhang et al., 2011). The widespread prevalence of
E. bieneusi is evidently due to its low host specificity, since no clear-cut asso-
ciation exists between its genotypes and specific hosts. Many genotypes, the
human-ones included, occur in several hosts: out of 12 genotypes identified
in humans in China, nearly one half occur also in animals, strongly indicat-
ing the possibility of zoonotic transmission (Zhang et al., 2011). Overall,
the tendency of genotypes to segregate according to the host species is
weak and is revealed only through the use of quantitative phylogenetic tests
(Widmer and Akiyoshi, 2010).
Another example of a cryptic, yet extensive occurrence is the presence
of the E. bieneusi, E. cuniculi, E. intestinalis and E. hellem DNA in birds.
294 Jiří Vávra and Julius Lukeš

Eleven percent of feral pigeons in Amsterdam excrete spores of these micro-

sporidia in fecal droppings (Bart et al., 2008) and nearly 40% of droppings of
300 healthy pet birds were PCR-positive for the above species (Kašicková
et al., 2009). The actual prevalence of these cryptic infections may be even
higher as shown by PCR-based daily examination of individual droppings
of a group of budgerigars (Mellopsittacus undulatus) (Sak et al., 2010). All
birds excreted DNA of several microsporidian species during the whole
investigation period (one month), but respective parasite species DNAs
were excreted at irregular intervals in individual birds. The birds seemed
healthy and the necropsy search for microsporidia by histopathology was
negative, although various internal organs were PCR-positive (Sak et al.,
2010). Another example of the widespread occurrence of microsporidia is
that of wild mice. Sak et al. (2011c) examined by PCR the intestinal con-
tents of nearly 300 specimens of the wild mouse, Mus musculus trapped in
Central Europe, and found the respective DNA of E. cuniculi, E. hellem and
E. bieneusi in 33% of the sampled individuals. Six percent of infected animals
contained more than one microsporidian species (Sak et al. 2011c).
The cited examples of broad microsporidian occurrence suggest that
humans are exposed to microsporidia to a degree that is not fully appreci-
ated. This is documented in a recent survey for microsporidian DNA in a
healthy human population in the Czech Republic, a country with good
hygienic standards. Among 400 healthy people, 42% excreted microsporid-
ian DNA in their feces, with Encephalitozoon spp. being the most frequently
identified, followed by E. bieneusi (Sak et al., 2011a). In another longitudinal
study, a group of healthy persons with some occupational risk of contact
with animals was followed for three months on a weekly basis using PCR
and immunological methods. The study demonstrated convincingly that
microsporidian infections are widespread and long lasting: out of the 15
monitored individuals, 13 excreted spores in their feces and urine (13 and 7
of Encephalitozoon spp. and E. bieneusi, respectively), yet no clinical symptoms
were observed during the examination period (Sak et al., 2011b).

4.5. Strong Adaptation to Host Life Cycles and Biology

The mechanism for spore germination provides two ways for microsporidia
to infect the host. Most frequently, the host is infected horizontally by spores
that are acquired from the environment. Alternatively, infection occurs ver-
tically by transovarial transmission when sporoplasms are injected into ger-
minal cells of the gonads inside the parental organism. In some cases, mature
spores are found in eggs (Phelps and Goodwin, 2008). Remarkably, however,
Microsporidia and ‘the Art of Living Together’ 295

the sporoplasms injected into the germinal cells usually postpone their
development to the beginning of embryogenesis (Weiser, 1961). Although
horizontal transmission is most common, vertical transmission is apparently
underreported, and in many cases, microsporidia are transmitted both hori-
zontally and vertically (Dunn and Smith, 2001; Solter, 2006).The difference
in virulence of ensuing infections is attributed to these respective trans-
mission ways. Species that rely principally on vertical transmission tend to
produce more cryptic infections and best represent the intimate relationship
between parasite and host. Several microsporidian species that infect gam-
marids (Crustacea: Amphipoda) are primarily transmitted vertically, and cause
feminisation of host males by preventing the development of their andro-
genic gland, thereby abolishing production of the hormone that is essential
for male development (Haine et al., 2004; Rodgers-Gray et al., 2004; Terry
et al., 2004). Feminisation of the host benefits the parasite because it is trans-
ovarially transmitted via the gonadal tissues of females (Bandi et al., 2001).
In developing embryos, microsporidia ensure their distribution in the host
by being segregated to specific daughter embryonal cells (Weedall et al.,
2006). The infection of daughter embryonal cells is secured by positioning
of the parasites along the axis of the nuclear spindle (Terry et al., 1999).
Feminisation not only favours the parasite by augmenting the number of
female individuals bearing infection, but unexpectedly seems to be advanta-
geous for the host because infected females of Gammarus roeseli breed earlier
in the reproductive season.This is the first case in which a positive effect of a
microsporidian infection on the host has been recorded (Haine et al., 2004,
2007). Surprisingly, however, this positive effect is dependent on infection
intensity: female gammarids have higher fecundity and more reproductive
bouts only at intermediate infection intensity. Neither light nor high intes-
nsity infections have the same effect (Ryan and Kohler, 2010).
In addition to the influence on the host sexual orientation mentioned
above, there are multiple additional impacts of microsporidia on hosts, and
consequently only a few examples can be given here. Microsporidia were
reported to influence the host transcriptome (Dussaubat et al., 2012) and
proteome (Biron et al., 2005), alter the courtship and shoaling of infected fish
(Pelabon et al., 2005;Ward et al., 2005) and change the swimming behaviour
of cladoceran crustacea (Makrushin, 2010;  Vávra and Pražáková, 1983).
In insects, infection by microsporidia may extend the developmental period
of the host and lead to host-larval gigantism (Blaser and S­ chmid-Hempel,
2005; Down et al., 2008; Henn and Solter, 2000). The physiological reasons
for such extension are multiple and depend on the specific host, the parasite,
296 Jiří Vávra and Julius Lukeš

the timing of infection and its dose (Henn and Solter, 2000). Analysis of
these factors is beyond the scope of this chapter but it is worth mention-
ing that some infections in insects, leading to extended larval development
and host gigantism, were originally explained by the parasite’s capacity to
physiologically manipulate production of the juvenile hormone in the host.
This may lead to the delay in moulting (Fisher and Sanborn, 1962, 1964).
This issue has been debated extensively and the metabolic stress caused by
the infection was proposed to be the factor that mimics the effect of the
juvenile hormone (Henn and Solter, 2000; Issi and Tokarev, 2002; Seleznev,
2003; Karlhofer et al., 2012). Other reports, however, claim that infected
insect larvae have indeed elevated levels of the juvenile hormone, causing
extension of their pre-moulting time. This may allow the parasite to pro-
duce more spores and increase its reproductive fitness (Down et al., 2008).
Many interesting adaptations of microsporidia to their hosts and to their
life cycles have been described for species inhabiting the freshwater environ-
ment.The aquatic habitat significantly influences the distribution of infective
spores in the environment. Spores of numerous aquatic species are equipped
with mucous layers, sporal hairs, tubules or tails formed as outgrowth of
the exospore layer (Canning and Vávra, 2000;Vávra et al., 2005). The likely
function of these apendages is to serve as aids in buoyancy, thus helping to
retain the spores in the water column and influencing their accessibility and
uptake by the host. There are no experimental data in support of this func-
tion, except for an anecdotal case when microsporidian spores floating in
pond water were originally described as a planktonic alga (Lemmermann,
1900). However, their true identity was revealed only much later (Vávra
et al., 2005). In the aquatic environment, spores can pass from host to host
more easily, thus facilitating the complex life cycles involving several host
species. Such life cycles have been described (with several modifications) for
Amblyospora spp. that complete their life cycle by cycling between mosquito
larvae, copepods and mosquito female adults. Spore morphs, structurally so
distinct that they would be ranked into different genera, are formed in each
host and male killing allows transmission of infection from mosquito larvae
to copepods (Andreadis, 2005, 2007; Lukeš and Vávra, 1990; Sweeney et al.,
1985). Similar life cycles may exist in many other aquatic microsporidia but
have yet to be discovered. For example, in some aquatic microcrustacea, the
spores fed to the original host do not cause infection.This provides circum-
stantial evidence that host exchange is evidently needed to perpetuate the
life cycle (Mangin et al., 1995; Refardt et al., 2002, 2008;Vávra, 1964;Vávra
and Larsson, 1994;Vávra et al., 2005;Wolinska et al., 2009). The examination
Microsporidia and ‘the Art of Living Together’ 297

of life cycles in this context would appear to be a major issue of future

microsporidian research.


Microsporidia, a distinct form of life identified more than 150 years
ago, are an unprecedented resource for the investigating the mechanisms
involved in host-parasite interactions. These organisms developed morpho-
logical characteristics and life-cycle strategies that are totally different from
fungi (probably their sister taxon) and to some extent, are also unique in
the world of protists. Evolution of the injection apparatus and its projectile
movement enabled microsporidia to colonise the intracellular niche of ani-
mal cells, to become intracytoplasmic parasites totally dependent on the host
cell, and resembling, at a certain phase of the life cycle, intracytoplasmic sym-
bionts. Upon entering into the new environment of the intracytoplasmic
space, microsporidia gained an unprecedented ecological opportunity, which
enabled them to quickly radiate. Their intracellular existence also allowed
them to reduce certain elements of their cell structures and genomes, in
some cases to the minimum required for eukaryotic existence.The availabil-
ity of a wide variety of animal and protistan hosts and host tissues provided
microsporidians with a vast opportunity to adapt to individual hosts and
tissues and also to evolve rapidly and readily disseminate from host to host.
We suggest that the accelerated evolution of these ubiquitous parasites was
facilitated by their ability to produce infective spores that vary in their readi-
ness to germinate. Microsporidia are considered to be very specific parasites,
intimately adapted to their host species, specific tissues and even specific
cell compartments. Nevertheless, they are constantly probing the environ-
ment by stochastically germinating spores, thus providing the potential to
infect new hosts and new tissue sites.We speculate that the ability to produce
spores of different germination readiness has been the key factor allowing
microsporidia to radiate and to become one of the most common parasites
of animals.
Microsporidia also provide a rich ground for further research. Having
undergone dramatic reductive evolutionary events, microsporidia represent
a fascinating model to study molecular, genome and cellular evolution.Vast
numbers of microsporidia species remain to be discovered. Despite their
abundance in nature, their relationship to the fungi has not yet been fully
resolved, life cycles of many species remain to be clarified and interactions
with their hosts need to be more precisely analysed using modern methods.
298 Jiří Vávra and Julius Lukeš

Microsporidia are unique organisms that can serve as models for a
more thorough understanding of the, living-together, biological phenomenon.

This review is dedicated to the memory of two outstanding Czech Microsporidia researchers:
Prof. Otto Jírovec (1907–1972), founder of the Czech parasitology school, and Dr Jaroslav
Weiser (1920–2012), ‘the father of modern insect pathology in Europe’. The following col-
leagues provided invaluable assistance to improve this paper: Dr Leellen Solter (Illinois Natural
History Survey, University of Illinois, Urbana, USA), Dr Michael L. McManus (USDA Forest
Service [retired] Hamden, USA), Dr David J. Morris (University of Strathclyde, UK), Prof.
John. Lucocq (University of St Andrews, UK), Prof. T. Martin Embley and Dr Robert Hirt
(Newcastle University, UK), Dr Toni Gabaldon (Centre for Genomic Regulation, Barcelona,
Spain), Prof. Ronny Larsson (University of Lund, Sweden) and Prof. Andreas Linde
(Hochschule für Nachhaltige Entwicklung, Eberswalde, Germany). Their critical comments
and suggestions have been deeply appreciated. J.L. is a Fellow of the Canadian Institute for
Advanced Research and was supported by the Praemium Academiae Award.

Abdel-Ghaffar, F., Bashtar, A.R., Mehlhorn, H., Al-Rasheid, K., Morsy, K., 2011. Micro-
sporidian parasites: a danger facing marine fishes of the Red Sea. Parasitol. Res. 108,
Accoceberry, I., D’Almeida-Fourquet, M., 2012. Diagnosis of intestinal microsporidia.
Revue Francophone des Laboratoires 440, 27–34.
Adl, S.M., Simpson,  A.G., Farmer, M.A.,  Andersen, R.A.,  Anderson,  O.R., Barta, J.R.,
Bowser, S.S., Brugerolle, G., Fensome, R.A., Fredericq, S., James,T.Y., Karpov, S., K
­ ugrens,
P., Krug, J., Lane, C.E., Lewis, L.A., Lodge, J., Lynn, D.H., Mann, D.G., MCCourt,
R.M., Mendoza, L., Moestrup, Ø., Mozley-Standridge, S.E., Nerad, T.A., Shearer, C.A.,
Smirnov, A.V., Spiegel, F.W., Taylor, M.F.J.R., 2005. The new higher level classification
of Eukaryotes with emphasis on the taxonomy of protists. J. Eukaryot. Microbiol. 52,
Adl, S.M., Simpson, A.G., Lane, C.E., Lukeš, J., Bass, D., Bowser, S.E., Brown, M., Burki, F.,
Dunthorn, M., Hampl, V., Heiss, A., Hoppenrath, M., Lara, E., leGall, L., Lynn, D.H.,
McManus, H., Mitchell, E.A.D., Mozley-Standridge, S.E., Wegener Parfrey, L., Paw-
lowski, J., Rueckert, S., Shadwick, L., Schoch, C., Smirnov, A., Spiegel, F.W., 2012. The
revised classification of eukaryotes. J. Eukaryot. Microbiol. 59, 429–493.
Agaud, A.M., Achbarou, A., Desportes-Livage, I., 1997. Cell invasion by the microsporidium
Encephalitozoon intestinalis. J. Eukaryot. Microbiol. 44, 81S.
Agnew, P., Becnel, J.J., Ebert, D., Michalakis,Y., 2003. Symbiosis of microsporidia and insects. In:
Bourtzis, K., Miller,T. (Eds.), Insect Symbiosis, CRC Press LLC, Florida, USA, pp. 145–163.
Aist, J.R., Williams, P.H., 1971. The cytology and kinetics of cabbage root hair penetration
by Plasmodiophora brassicae. Can. J. Bot. 49, 2023–2034.
Akinbo, F.O., Okaka, C.E., Omoregie, R., Dearen, T., Leon, E.T., Xiao, L., 2012. ­Molecular
epidemiologic characterization of Enterocytozoon bieneusi in HIV-infected persons in
Benin City, Nigeria. Am. J. Trop. Med. Hyg. 86, 441–445.
Microsporidia and ‘the Art of Living Together’ 299

Akiyoshi, D.E., Morrison, H.G., Lei, S., Feng, X., Zhang, Q., Corradi, N., Mayanja, H.,
Tumwine, J.K., Keeling, P.J., Weiss, L.M., Tzipori, S., 2009. Genomic survey of the non-
cultivatable opportunistic human pathogen, Enterocytozoon bieneusi. PLoS Pathog. 5,
Alkatan, H.M.,  Al-Zaaidi, S.,  Athmanathan, S., 2012. Microsporidial keratitis: literature
review and report of 2 cases in a tertiary eye care center. Saudi J. Ophthalmol. 26,
Anane, S., Attouchi, H., 2010. Microsporidiosis: epidemiology, clinical data and therapy.
­Gastroenterologie Clinique et Biologique 34, 450–464.
Andreadis, T.G., 2005. Evolutionary strategies and adaptations for survival between
­mosquito-parasitic microsporidia and their intermediate copepod hosts: a compara-
tive examination of Amblyospora connecticut and Hyalinocysta chapmani (Microsporidia:
Amblyosporidae). Folia Parasitol. 52, 23–35.
Andreadis, T.G., 2007. Microsporidian parasites of mosquitoes. J. Am. Mosq. Control Assoc.
23, 3–29.
Andreadis, T.G., Simakova, A.V.,Vossbrinck, C.R., Shepard, J.J.,Yurchenko,Y.A., 2012. Ultra-
structural characterization and comparative phylogenetic analysis of new microsporidia
from Siberian mosquitoes: evidence for coevolution and host switching. J. Invertebr.
Pathol. 109, 59–75.
Arisue, N., Sanchez, L.B., Weiss, L.M., Muller, M., Hashimoto, T., 2002. Mitochondrial-type
hsp70 genes of the amitochondriate protists, Giardia intestinalis, Entamoeba histolytica and
two microsporidians. Parasitol. Int. 51, 9–16.
Baker, M.D., Vossbrinck, C.R., Becnel, J.J., Andreadis, T.G., 1998. Phylogeny of Amblyospora
(Microsporida: Amblyosporidae) and related genera based on small subunit ribosomal
DNA data: a possible example of host parasite cospeciation. J. Invertebr. Pathol. 71,
Balbiani, G., 1882. Sur les microsporidies ou psorospermies des articules. C. R. Acad. Sci.
Paris 95, 1168–1171.
Bandi, C., Dunn, A.M., Hurst, G.D.D., Rigaud, T., 2001. Inherited microorganisms,
­sex-specific virulence and reproductive parasitism. Trends Parasitol. 17, 88–94.
Bargielowski, I., Koella, J.C., 2009. A possible mechanism for the suppression of Plasmodium
berghei development in the mosquito Anopheles gambiae by the microsporidian Vavraia
culicis. PLoS One 4 e4676.
Bart, A., Wentink-Bonnema, E.M., Heddema, E.R., Buijs, J., Van Gool, T., 2008. Frequent
occurrence of human-associated microsporidia in fecal droppings of urban pigeons in
Amsterdam, the Netherlands. Appl. Environ. Microbiol. 74, 7056–7058.
Bartnicki-Garcia, S., 1970. Cell wall composition and other biochemical markers in fungal
phylogeny. In: Harborne, J.B. (Ed.), Phytochemical Phylogeny, Academic Press, London,
pp. 81–103.
Becnel, J.J., White, S.E., Shapiro, A.M., 2005. Review of microsporidia-mosquito relation-
ships: from the simple to the complex. Folia Parasitol. 52, 41–50.
Beznoussenko, G.V., Dolgikh, V.V., Seliverstova, E.V., Semenov, P.B., Tokarev, Y.S., Trucco, A.,
Micaroni, M., Di Giandomenico, D., Auinger, P., Senderskly, I.V., Skarlato, S.O.,
Snigirevskaya, E.S., Komissarchik, Y.Yu., Pavelka, M., De Matteis, M.A., Luini, A.,
Sokolova, Y.Ya., Mironov, A.A., 2007. Analogs of the Golgi complex in microsporidia:
structure and avesicular mechanisms of function. J. Cell Sci. 120, 1288–1298.
Bhat, S.A., Bashir, I., Kamili, A.F., 2009. Microsporidiosis of silkworm, Bombyx mori L.
­(Lepidoptera-Bombycidae): a review. Afr. J. Agric. Res. 4, 1519–1523.
Biron, D.G., Agnew, P., Marché, L., Renault, L., Sidobre, C., Michalakis, Y., 2005. Proteome
of Aedes aegypti larvae in response to infection by the intracellular parasite Vavraia culicis.
Int. J. Parasitol. 35, 1385–1397.
300 Jiří Vávra and Julius Lukeš

Blaser, M., Schmid-Hempel, P., 2005. Determinants of virulence for the parasite Nosema
whitei in its host Tribolium castaneum. J. Invertebr. Pathol. 89, 251–257.
Bohne, W., Ferguson, D.J.P., Kohler, K., Gross, U., 2000. Developmental expression of a
tandemly repeated, glycine- and serine-rich spore wall protein in the microsporidian
pathogen Encephalitozoon cuniculi. Infect. Immun. 68, 2268–2275.
Bohne, W., Böttcher, K., Groß, U., 2011. The parasitophorous vacuole of Encephalitozoon
cuniculi: biogenesis and characteristics of the host cell-pathogen interface. Int. J. Med.
Microbiol. 301, 395–399.
Botterel, F., Minozzi, C.,Vittecoq, D., Bouree, P., 2002. Pulmonary localization of Enterocyto-
zoon bieneusi in an AIDS patient: case report and review. J. Clin. Microbiol. 40, 4800–4801.
Bouzahzah, B., Weiss, L.M., 2010. Glycosylation of the major polar tube protein of Encepha-
litozoon cuniculi. Parasitol. Res. 107, 761–764.
Bouzahzah, B., Nagajyothi, F., Ghosh, K., Takvorian, P.M., Cali, A., Tanowitz, H.B., Weiss,
L.M., 2010. Interactions of Encephalitozoon cuniculi polar t