Review

Veterinary Pathology
1-17
A Review on Chlamydial Diseases in Animals: ª The Author(s) 2018
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Still a Challenge for Pathologists? DOI: 10.1177/0300985817751218
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Nicole Borel1, Adam Polkinghorne2, and Andreas Pospischil1

Abstract
Chlamydiae have a worldwide distribution causing a wide range of diseases in human hosts, livestock, and companion animals as
well as in wildlife and exotic species. Moreover, they can persist in their hosts as asymptomatic infections for extended periods of
time. The introduction of molecular techniques has revolutionized the Chlamydia field by expanding the host range of known
chlamydial species but also by discovering new species and even new families of bacteria in the broader order Chlamydiales. The
wide range of hosts, diseases, and tissues affected by chlamydiae complicate the diagnosis such that standard diagnostic
approaches for these bacteria are rare. Bacteria of the Chlamydiales order are small and their inclusions are difficult to detect by
standard microscopy. With the exception of avian and ovine chlamydiosis, macroscopic and/or histologic changes might not be
pathognomic or indicative for a chlamydial infection or even not present at all. Moreover, detection of chlamydial DNA in
specimens in the absence of other methods or related pathological lesions questions the significance of such findings. The
pathogenic potential of the majority of recently identified Chlamydia-related bacteria remains largely unknown and awaits
investigation through experimental or natural infection models including histomorphological characterization of associated
lesions. This review aims to summarize the historical background and the most important developments in the field of animal
chlamydial research in the past 5 years with a special focus on pathology. It will summarize the current nomenclature, present
critical thoughts about diagnostics, and give an update on chlamydial infections in domesticated animals such as livestock, com-
panion animals and birds, as well as free-ranging and captive wild animals such as reptiles, fish, and marsupials.

Keywords
Chlamydiales, Chlamydiaceae, Chlamydia, Chlamydia-related bacteria, host range, molecular techniques, review, zoonosis

Highlights biphasic developmental cycle while multiplying in eukaryotic

 Chlamydiosis in animals can range from asymptomatic
infection to severe diseases with life-threatening illnesses
 Zoonotic infections due to Chlamydia abortus and Chla-
mydia psittaci are well-known
 Chlamydia-related bacteria might be pathogenic to ani-
mals and pose zoonotic risks
 Chlamydia spp. are either endemic or epidemic in differ-
ent hosts
 Studies of new hosts have uncovered new chlamydial
pathogens or expanded host ranges for existing species
 Virtually all chlamydial species might easily and fre-
quently cross host barriers
 Characteristics of Chlamydia-induced inflammatory
changes depend on the chlamydial species, the infected
host and the tissue affected
hosts. The order is composed, to date, of 9 families of which
members infect humans, wild and domesticated mammals, rep-
tiles, amphibians, and fish. The biphasic developmental cycle
(Fig. 1) begins with the elementary bodies (EBs), the extracel-
lular and infectious form of the bacteria (size of 0.2 mm),
infecting host mucosal epithelial cells. After attachment to and
entry into the host cell, EBs develop within a membrane-bound
endocytic vacuole called an inclusion and inside, differentiate
into larger (0.8 mm), metabolically active but noninfectious
reticulate bodies (RBs). After multiple rounds of division, RBs
redifferentiate into infectious EBs, and mature EBs complete
the developmental cycle, exiting the host cell via lysis or
1
Department of Pathobiology, Institute of Veterinary Pathology, University of
Zurich, Zurich, Switzerland
2
Centre for Animal Health Innovation, Faculty of Science, Health, Education
and Engineering, University of the Sunshine Coast, Sippy Downs, Australia

The Chlamydiales—An Introduction Corresponding Author:

Nicole Borel, Institute of Veterinary Pathology, Vetsuisse Faculty, University of
The members of the Chlamydiales order are fascinating Gram- Zurich, Winterthurerstrasse 268, CH-8057 Zurich, Switzerland.
negative, obligate intracellular bacteria sharing a unique Email: N.Borel@access.uzh.ch
2 Veterinary Pathology XX(X)
Fig. 1. Chlamydia developmental cycle. The elementary body (EB)
attaches to a host cell and differentiates into a reticulate body (RB)
after entry, enclosed in a membrane-bound vacuole. The RB grows by
binary fission and later differentiates into EBs, which are released and
infect a new host cell. The persistence state is characterized by the
formation of the aberrant body (AB) induced by stressful conditions.
extrusion of the inclusion.2 Under adverse environmental con-
ditions, developing chlamydiae may enter a state referred to as
persistence, more recently renamed the chlamydial stress
response or the aberrant RB phenotype.12 Stressed chlamydiae
(termed aberrant bodies [ABs]) remain viable, but do not
develop into EBs and are noninfectious. In vivo, the AB phe-
notype may contribute to prolonged, chronic inflammation,
fibrosis, and scarring through continuing stimulation of the host
immune system, although this concept is still highly controver-
sial.87 Due to their intracellular lifestyle, chlamydiae are
dependent on host metabolites. This has considerable implica-
tions for diagnostics as these bacteria cannot simply grow on
agar plates, requiring cell culture for their isolation. Isolation
procedures require fresh tissue or swab samples immediately
transferred into special transport or preservation media and
proper storage at –80 C, conditions not routinely used or avail-
able in pathology laboratories. Formalin fixation and paraffin
embedding (FFPE) of tissues or autolytic changes of organs
impede any further isolation of chlamydial organisms.
Until recently, members of the Chlamydiaceae family were
considered to be important pathogens of humans and animals
with a well-defined taxonomic diversity and host range. This
paradigm has been challenged with the help of molecular tech-
niques revealing (a) a significantly expanded taxonomic diver-
sity encompassing at least 8 other families of bacteria,
colloquially referred to as Chlamydia-related bacteria (CRB)
or Chlamydia-like organisms (CLO), within the order Chlamy-
diales; and (b) an expanded host range for certain chlamydial
species, for example, C. psittaci and C. pneumoniae, that has
posed new questions about the role of cross-host transmission in
the epidemiology of these pathogens. Furthermore, these studies
of new hosts have not only uncovered expanded host ranges for
existing species but also identified new chlamydial species, for
example, in reptilian and avian hosts.170 Together, the animal
host range of bacteria in the Chlamydiales order is significantly
broader than thought before with over 400 host species docu-
mented globally, the majority of these being wild animals.27
Infections of the latter including birds, reptiles, amphibians, fish
and eutherians focusing on wild ungulates and marsupials have
been recently reviewed27 and are only discussed in this review
in the view of related histomorphological findings.
Chlamydiosis in animals can range from asymptomatic
infection to severe diseases with life-threatening illnesses
depending on the host species affected and chlamydial species
involved. Disease manifestations in chlamydial infections
include conjunctivitis ranging from mild signs to corneal opa-
city, rhinitis, pneumonia, mastitis, arthritis/polyarthritis, peri-
carditis, polyserositis, encephalomyelitis, placentitis leading to
abortion, stillbirth or weak neonates, endometritis/metritis,
orchitis/epididymitis/urethritis, infertility, enteritis, and more.
Still they might not be encountered by the pathologist because
the lesions are too mild to cause death of the animal or chla-
mydiae are not considered as differential diagnosis due to the
presence of other more common and well-known pathogens.
Therefore, chlamydial infections, with the exception of chla-
mydial abortion in ruminants and avian chlamydiosis (also
known as psittacosis/ornithosis) may present a diagnostic chal-
lenge for pathologists. Given the diversity of potential host
species, chlamydial species and range of clinical signs, this
review will try to summarize the most important aspects in the
Chlamydia field tailored to the veterinary pathologist but also
to any other interested reader. Human chlamydial infections
due to C. trachomatis and C. pneumoniae as well as C. mur-
idarum, the chlamydial species isolated from laboratory mice
and hamsters and primarily used as infection inoculum in
mouse studies as models for female genital infections, will be
excluded from this review. Recent investigations in Peromys-
cus spp rodents from sylvatic and laboratory sources indicated
that chlamydial infection is enzootic in this mouse species and
that C. muridarum, or a closely related species or strain, is
likely the agent in the tested rodent species.126 Atypical Chla-
mydiaceae closely related to C. muridarum have been also
detected by PCR in roe deer (Capreolus capreolus) in south-
western France.1 Moreover, C. muridarum was identified in
oral and cloacal swabs of chickens, ducks and geese in China.49
The CBR or CLO share phenotypic and genetic similarities
with the Chlamydiaceae but are phylogenetically separated.
Recently, 20 years of research on the CLO, since the detection
of its first member Simkania, has been reviewed in detail.173
Therefore, we will only elucidate the most important patho-
morphological findings related to CLO-infections in the pres-
ent review.
It is far beyond the scope of this review to cover all aspects
and developments of the recent years. Therefore, we have lim-
ited our review to the past 5 years summarizing the most impor-
tant developments in the field of animal chlamydial research.
Borel et al
Table 1. Disease in Humans Caused by Chlamydiae.
Species Serotype Disease
Chlamydia Ocular Inclusion conjunctivitis in
trachomatis (Trachoma)167 newborns; trachoma
Genital111,113 Infantile pneumonia, urethritis in
men; epididymitis; urethral
syndrome in women; cervicitis;
endometritis; salpingitis; tubal
factor infertility; proctitis;
perihepatitis and peritonitis;
endocarditis
LGV157 Lymphogranuloma venereum
Chlamydia Human137 Pharyngitis; bronchitis; pneumonia;
pneumoniae atherosclerosis
Chlamydial Nomenclature
The chlamydial nomenclature has been under constant
change in recent years. Besides the addition of new fami-
lies, it was also proposed to split the genus Chlamydia into
2 genera, Chlamydia and Chlamydophila, based on analysis
of the 16 S and 23 S rRNA genes. 45 This change was
controversial. After significant debate within the chlamydial
research community, a reversion to a single genus, Chlamy-
dia, was proposed and is now accepted.13,141 To date, the
order Chlamydiales consists of 9 families: Chlamydiaceae,
Clavichlamydiaceae, Cribchlamydiaceae, Parachlamydia-
ceae, Parilichlamydiaceae, Piscichlamydiaceae, Rhabdo-
chlamydiaceae, Simkaniaceae, and Waddliaceae. 173 The
family Chlamydiaceae contains a single genus, Chlamydia,
including 11 species:141 C. abortus, C. avium, C. caviae, C.
felis, C. gallinacea, C. muridarum, C. pecorum, C. pneumo-
niae, C. psittaci, C. suis, and C. trachomatis as well as well
as the 3 Candidatus (Ca.) species: Ca. C. ibidis,176 Ca. C.
sanzinia,168 and Ca. C. corallus.172 The Chlamydiaceae
cause several diseases in humans (Table 1) and animals
(Table 2), some of which are zoonotic, and this also refers
to the CRB (Table 3). In humans, different serovars of C.
trachomatis cause eye and urogenital infections responsible
as the leading cause of infectious blindness worldwide
(blinding trachoma)166,167 and the most common bacterial
sexually transmitted infection (STI).111,113,157 Respiratory
infections in humans are caused by C. pneumoniae, a chla-
mydial species also infecting horses, frog, reptiles and mar-
supials.137 Zoonotic infections due to C. psittaci, a common
pathogen of birds, have the best known zoonotic potential of
the human pathogenic chlamydiae and cause relatively rare
respiratory infections in birds but are associated with severe
clinical manifestations in humans.53,81,165 Infection with C.
abortus in pregnant women after contact with aborting/
lambing sheep and goats may also lead to abortion and, if
untreated, to life-threatening illnesses.44 Several other ani-
mal pathogenic chlamydial species, including C. felis, C.
caviae, and C. suis, are known, or suspected, to cause infre-
quent human infections with various clinical presentations.
3
Historical Background
Trachoma, one of the diseases with a chlamydial etiology caus-
ing blindness in humans and one of the earliest known ocular
diseases, has been identified in Egypt as early as 15 BC. Soldiers
returning from Napoleon’s Egyptian campaign (1798–1802) are
thought to have brought the disease to Europe where it spread by
contact due to poor hygienic conditions.166 Similar disease
descriptions have been found in ancient Chinese documents.76
The importance of trachoma as a disease in humans was recog-
nized early, and immigrants to the United States were routinely
screened for trachoma on arrival in New York and sent back to
their country of origin if infected.76 It was only in 1907 when the
etiology of trachoma was first described on an expedition led by
Albert Neisser to Java to experimentally transmit syphilis to
nonhuman primates. Additional experiments were done inocu-
lating orangutans with conjunctival scrapings from trachoma
patients. As a sequel, conjunctival granulomata (trachoma
knots) developed. Histopathologically, the conjunctival epithe-
lial cells contained small dense bodies (Fig. 2). Suspensions of
the trachoma knots were filtered and successfully used for sub-
sequent infections. Von Prowazek called them “chlamydozoa”
comparing them to the Greek term “mantle.”52,122
Remarkably, in 1909 an Austrian veterinarian reported
smears from cows with transmissible vaginitis and healthy ones
from several farms containing comparable forms to the so
called “trachoma-bodies” and named them “Chlamydozoa”
(Fig. 3).16 Although these findings were well documented by
a conclusive figure, the report remained unnoticed.
Psittacosis most probably originated in South America
where psittacine birds were kept as pets, although alternative
hypotheses have been proposed that Australian native parrots
may have been the original source.24 Fra Bartolomeo in 1615
described diseases in human individuals having had contact
with psittacine birds.122 In the second half of the 19th century,
Jacob Ritter, a Swiss physician described an epidemic of psit-
tacosis in his household causing 3 fatalities from 7 affected
patients.131 In his report, Ritter suspected that pet parrots and
finches recently introduced into the house were the source of
the infection and, accordingly, determined the incubation
period while reporting the nontransmissibility of the disease
from human to human.122 The main clinical finding Ritter
reported was an atypical pneumonia, called pneumotyphus at
that time. In 1895, the term psittacosis derived from the Greek
for parrot was first applied for this disease.108 Later in 1893,
Nocard had isolated a gram-negative bacterium from parrots
dying of psittacosis (Bacillus psittacosis).85 This particular
organism subsequently was not regularly isolated from human
or avian patients and later turned out to belong to the genus,
Salmonella.5,117 The inconsistent bacteriological isolations
prompted the suspicion of a viral etiology of psittacosis espe-
cially during the pandemic of 1929–1930.122 In 1930, indepen-
dently but almost simultaneously, Levinthal,89 Coles,33 and
Lillie92 reported small, filterable bodies in infectious material
and named them “Levinthal-Coles-Lillie (L.C.L.) bodies.”102
Samuel P. Bedson first reported the biphasic developmental
4 Veterinary Pathology XX(X)

Table 2. Diseases in Animals Caused by Bacteria Classified and Proposed to be in the Genus Chlamydia.

Zoonotic
Chlamydial species Host Disease potential

Chlamydia abortus Sheep, goats, cattle, swine44,95,96 Abortion, vaginitis, endometritis, seminal vesiculitis, mastitis (latent) Yes
Chlamydia caviae Guinea pigs109 Follicular conjunctivitis, keratitis (Yes)
Chlamydia felis Cats162 Conjunctivitis, rhinitis (Yes)
Chlamydia Mice, hamsters45 Pneumonitis, ileitis No
muridarum
Chlamydia pecorum Sheep, cattle, swine, Encephalitis, polyarthritis, pneumonia, enteritis, vaginitis, endometritis, No
koalas121,150,177,178 in sheep and cattle; polyarthritis, serositis, enteritis, pneumonia, in
swine; keratoconjunctivitis, vaginitis, ovarian cyst, infertility, in koalas
Chlamydia Koalas, other marsupials, Rhinitis, pneumonia, conjunctivitis No
pneumoniae horses121,158
Reptiles, frogs20 Conjunctivitis, enteritis, granulomatous inflammation of internal organs No
Chlamydia psittaci Birds53,81 Conjunctivitis, pneumonia, enteritis, hepatitis Yes
Chlamydia suis Swine150 Conjunctivitis, pneumonia, enteritis, polyarthritis (Yes)
Chlamydia Birds144 No apparent pathology yet described (Yes)
gallinacea
Chlamydia avium Birds144 Enteritis and respiratory disease; link to apparent pathology uncertain No
Ca. Chlamydia Birds176 No apparent pathology yet described No
ibidis
Ca. Chlamydia Snakes168 No apparent pathology yet described No
sanzinia
Ca. Chlamydia Snakes172 No apparent pathology yet described No
corallus

Table 3. Diseases Caused by Chlamydia-Related Bacteria (CRB). of sulfonamide susceptibility and the demonstration of glyco-
gen accumulation within the inclusion by iodine staining.
Zoonotic
Chlamydial taxa Host Disease potential

Waddlia chondrophila Cattle42,187 Abortion (Yes)

Diagnosis of Chlamydial Infections—
Parachlamydia Cattle, sheep, Abortion, No A Pathologist’s Point of View
acanthamoeba goats23,187,189 pneumonia The very first descriptions of human and animal diseases
Simkaniaceae; multiple Fish159 Epitheliocystis No
other species
involving chlamydiae were based on anamnesis, clinical symp-
Ca. Piscichlamydiaceae Fish159 Epitheliocystis No toms, epidemiology and presenting pathology.16,131 Chlamy-
Ca. Clavochlamydiaceae Fish159 Epitheliocystis No dial infections can have an acute or chronic and even
Ca. Piscichlamydiaceae; Fish159 Epitheliocystis No subclinical course of disease depending on the host species
multiple species infected and the chlamydial species involved. The wide range
Ca. Parilichlamydiaceae; Fish159 Epitheliocystis No of diseases and hosts makes a diagnosis difficult and diagnostic
multiple species approaches cannot be standardized. Other than ovine and avian
chlamydiosis, chlamydiae are often considered pathogens of
little significance and, accordingly, detailed diagnostic inves-
cycle of the psittacosis agent in tissues from experimentally tigations are not performed. Moreover, macroscopic and/or
inoculated mice.14 In 1935, Burnet and Rountree28 propagated histologic changes might not be pathognomonic or indicative
the infectious bodies successfully on the chorioallantoic mem- for a chlamydial infection or they are even not present at all.
brane of embryonated chicken eggs. Chronic chlamydial infections in animals, particularly rumi-
Until Pagès proposal of a taxonomy for Chlamydiaceae in nants and pigs, are subclinical and ubiquitous in nature130 and
1966,114 there were at least 7 attempts to define and name what do often not induce any typical morphological lesions. Due to
we now know as chlamydiae. In 1958, the International Code the variety of clinical pictures and animal hosts, and since
of Nomenclature of Bacteria and Viruses was adopted and the Chlamydiaceae are often diagnosed in combination with other
genus Chlamydia replaced Miyagawanella, proposed by infectious agents, a definitive diagnosis typically requires
Brumpt in 1938.25 The genus name “Chlamydia”, proposed laboratory investigations in most cases.
by Jones and colleagues77 had time precedence over Bedso- To detect chlamydiae in smears, several staining methods
nia101 and Rakeia.88 In 1971, Storz and Page proposed the can be used, for example, modified Machiavello, modified
order Chlamydiales, which contained only one genus, Chlamy- Gimenez, Giemsa, Castaneda, or modified Ziehl-Neelsen
dia. In that genus, Chlamydia trachomatis and Chlamydia (MZN) stain (reviewed in Sachse et al).146 Intracellular chla-
psittaci were distinguished as separate species115 on the basis mydial inclusions can be visualized by Giemsa staining on
Borel et al 5

Fig. 2. Chlamydial inclusions in conjunctival epithelial cells of an experimentally infected orangutan. Conjunctival cells contain small dense bodies
in their cytoplasm forming chlamydial inclusions adjacent to basophilic nuclei. Drawing from Halberstaedter and von Prowazek.52 Fig. 3.
Drawing of follicular vaginitis in a spontaneously infected cow reported by Blaha.16 Figs. 4, 5. Ovine enzootic abortion due to infection with
Chlamydia abortus, placenta, sheep. Figure 4. Purulent to necrotizing placentitis. The placenta is edematous and hemorrhagic and the cotyledons
are covered with purulent exudate and show multifocal areas of necrosis. Figure 5. Well-preserved placenta showing intracytoplasmic
basophilic granular chlamydial inclusion bodies in the trophoblastic epithelium. Hematoxylin and eosin. Fig. 6. Chronic keratoconjunctivitis
due to infection with C. pecorum, right eye, koala (Phascolarctos cinereus). The conjunctiva is reddened and swollen (chemosis) and displays
hyperplasia and fibrosis. Fig. 7. Large intestine, corn snake (Pantherophis guttatus). Positive immunolabeling of inclusions in necrotic intestinal
epithelium in which colonies of rod-shaped bacteria were observed. This snake died due to an enteritis caused by Salmonella enterica
subsp. enterica. Novel unclassified Chlamydia species were isolated from choanal and cloacal swabs by PCR. Immunohistochemistry using a
Chlamydiaceae-family-specific mouse monoclonal antibody targeting the chlamydial lipopolysaccharide (LPS, Clone ACI-P, Progen, Heidelberg,
Germany), AEC/peroxidase method, hematoxylin counterstain.
6 Veterinary Pathology XX(X)
tissue sections, but methylene blue staining was demonstrated to
be more reliable compared to Giemsa when detecting C. abortus
in fetal membranes.36 However, these techniques are nonspecific
and can cross-react with other bacterial species; care, therefore,
must be taken with interpretation of results. During the 1960s,
ultrastructural investigations confirmed the bacterial nature of
chlamydiae by transmission electron microscopy (TEM) but,
today, is primarily used for research purposes.123
Nowadays, antigen detection in pathology laboratories is
generally performed on formalin-fixed and paraffin-
embedded (FFPE) tissue samples using different histochemical
and immunohistochemical techniques.146 Immunohistochem-
ical methods using monoclonal antibodies directed against
chlamydial surface antigens, such as LPS or MOMP, are more
sensitive compared to histochemical staining146 and routinely
used for diagnostic purposes.21 Various other approaches have
been developed such as enzyme-linked immunosorbent assays
(ELISAs) and fluorescent antibody tests (FATs). Although
these methods successfully demonstrate the presence of chla-
mydial organisms in the diagnostic specimen, they generally do
not allow the identification of the involved chlamydial species
and/or serotype/genotype because they use either nonspecific
cytochemical stains or monoclonal antibodies based on Chla-
mydiaceae-specific antigens, such as the chlamydial LPS.146
The role of histopathology during the diagnostic process
should not be underestimated, as it is important to ensure that
the infectious agent identified is related to the lesion present
and that it is not a mere contaminant, possibly originating from
the environment.146 This is especially important since nucleic
acid amplification tests are considered the gold standard to
diagnose animal and human chlamydial infections and novel
culture-independent metagenomic approaches enable identifi-
cation of novel chlamydial species, at least at the Candidatus
level. However, the significance of detecting chlamydial DNA
in specimens is questionable as a sole diagnostic approach, in
the absence of other methods or without related pathological
findings. Demonstration of (1) the presence of viable, replicat-
ing bacteria and (2) etiological importance are mandatory to
draw any conclusion on whether chlamydiae are involved in
the disease process or not.
Avian Chlamydiosis (Chlamydia psittaci,
Chlamydia avium, Chlamydia gallinacea)
Traditionally, avian chlamydiosis, also named psittacosis or
ornithosis, was due to infection with C. psittaci (reviewed in
Knittler and Sachse, 81 Sachse et al, 145 and Szymańska-
Czerwińska and Niemczuk165). The latest findings related to
C. psittaci have been extensively reviewed81,125,145 and there-
fore are discussed only briefly.
Chlamydia psittaci is known to occur in more than 465 avian
species, including domestic, companion and wild birds. The
highest percentage of infection is found in pigeons and psitta-
cine birds. The infection can lead to systemic and occasionally
fatal disease in birds, but especially older psittacine birds and
poultry may not show clinical signs but shed the organisms for
extended periods of time. Necropsy of affected birds often
reveals multifocal hepatic necrosis, splenomegaly and fibri-
nous airsacculitis, pericarditis, and peritonitis. In a recent 5-
year retrospective study of avian diseases at the University of
Georgia including 153 captive bird species, bacterial infection
was the most frequently diagnosed cause of death with gram-
negative bacteria and C. psittaci most commonly involved.110
The highest percentage of bacterial infections was reported in
Psittaciformes, followed by Passeriformes, Galliformes,
Columbiformes, and Anseriformes.
Zoonotic infections due to C. psittaci vary from inapparent
to severe systemic disease with pneumonia, myocarditis and
encephalitis (reviewed in Radomski et al 125 and Sachse
et al145). Human psittacosis cases are most common in bird
keepers, poultry workers, veterinarians, and health care work-
ers. Human-to-human transmission can occur but is exception-
ally rare apart from a recent reported outbreak in Sweden.179
Atypical Chlamydiaceae species in European and Asian
chicken flocks49,191 and urban pigeons142 were described in
recent years and resulted in the proposal of 2 new avian chlamy-
dial species and one Candidatus species in the genus Chlamydia:
Chlamydia gallinacea and Chlamydia avium143,144 and Candida-
tus C. ibidis.176 C. gallinacea and C. avium were detected along-
side C. psittaci in the same flock and even in the same bird.
C. gallinacea has been detected in domestic poultry, guinea
fowl, turkeys, and ducks, which did not shown signs of disease.
It is thought that C. gallinacea is an endemic organism in chick-
ens with the ability to persist over time.49 Experimentally
infected chickens remained without overt clinical disease but
showed significant body weight reduction.49 The type strain of
C. gallinacea has been recently sequenced and harbors a plas-
mid, a suspected virulence factor in some but not all chlamydial
species.59 C. gallinacea has been reported in chickens in differ-
ent European countries, Argentina and China.47,49,64 Recently,
C. gallinacea was detected in wild birds (woodcocks, Scolopax
rusticola) from South Korea, but based on phylogenetic analyses
of polymorphic ompA sequences, the Korean C. gallinacea was
a genetic variant different from European and Chinese isolates.74
The zoonotic potential of C. gallinacea has been suggested after
an outbreak of atypical pneumonia in French poultry slaughter-
house workers.84 Interestingly, a recent study in China90
detected DNA of C. psittaci and C. gallinacea from whole-
blood samples, milk, feces and vaginal swabs of clinically
healthy dairy and beef cattle. The serovars found were identical
with those of poultry in the same region suggesting bird to
ruminant transmission. As it stands, C. gallinacea should be
considered an avian pathogen with the potential to infect humans
and other animals. The potential macroscopic or histomorpho-
logical lesions remain to be elucidated.
C. avium has been found in pigeons and psittacines in Eur-
opean countries with limited data linking it to respiratory dis-
ease in parrots and pigeons.143 The zoonotic potential of C.
avium is unknown. Initial isolates of C. avium were obtained
from cloacal swabs, feces or internal organs from psittacine
birds and pigeons which were asymptomatic or had respiratory
signs and/or diarrhea.144
Borel et al
Candidatus Chlamydia ibidis was isolated from cloacal
swabs of a feral African sacred ibis (Threskiornis aethiopi-
cus).176 The isolate was obtained from a healthy ibis shot dur-
ing an official culling operation carried out in Western France
in 2009 and 2010. To date, the virulence characteristics of Ca.
C. ibidis, its geographical origin, its infectivity and pathogeni-
city for poultry and bird wildlife or other animals and its zoo-
notic potential is completely unknown.
The complexity of chlamydial infections in birds is further
manifested by a recent report of polymerase chain reaction
(PCR)–based avian C. abortus strain detection in Polish
wildfowl.164 To date, the pathogenicity of these new avian C.
abortus strains remains unknown and needs further investiga-
tion. Moreover, a new species, intermediary between C. psit-
taci and C. abortus, from a red-tailed hawk was retrieved by
whole-genome sequencing.78 It has been hypothesized that
birds-of-prey or other scavengers and predators might acquire
multiple chlamydial species in their intestinal tracts resulting in
emergence of novel species by recombination events.
Chlamydia psittaci in Horses
Few reports of chlamydial infections in horses are available in
the literature associated with equine pneumonia or abortion
after infection with C. abortus or C. pneumoniae.100,175 Chla-
mydial abortion in mares due to C. psittaci is a known cause of
equine abortion19,55,163 but has recently gained new attention
when an avian-like C. psittaci strain was found in equine pla-
centitis cases associated with subsequent zoonotic human psit-
tacosis in New South Wales, Australia.31,71,120 In 2014, this
outbreak caused 5 cases of human psittacosis in veterinary
students and staff exposed to equine fetal membranes. A mild,
diffuse, interstitial placentitis was present in a mare who deliv-
ered a live but ill foal that died suddenly one week later. Infec-
tion with C. psittaci was diagnosed by PCR and multilocus
sequence typing showed assignment to the highly virulent C.
psittaci 6BC lineage, identical to sequences recently described
in Australian parrots and humans.24 The authors71 postulated
transmission via indirect contact, presumably via fecal envi-
ronmental contamination from C. psittaci-infected parrots as
the infection source. These findings highlight the risk of zoo-
notic transmission originating from C. psittaci-infected equine
placental membranes and depending on the geographical loca-
lization, indicate the need to consider C. psittaci as differential
diagnosis in equine abortion.
Chlamydia abortus in Ruminants and Other
Hosts
Small ruminants can be infected with C. abortus, C. pecorum,
C. psittaci, and more rarely C. suis. C. abortus causes late-term
abortions, stillbirths and birth of weak neonates which fail to
survive beyond 48 hours after birth in sheep and goats and to a
lesser extent in cattle, pigs, horses and wild ruminants
(reviewed in Longbottom and Coulter95). Moreover, C. abortus
was also suggested to play a role in yak abortion in China after
7
its isolation from 9 aborted fetuses.91 Ovine chlamydiosis due
to C. abortus, also known as enzootic abortion of ewes or ovine
enzootic abortion (OEA), is the most common infectious abor-
tigenic agent worldwide, causing significant economic
losses.96 Chlamydiosis of small ruminants due to C. abortus
is a zoonosis with pregnant women being particularly at risk
(reviewed in Essig and Longbottom44). Recently, a case of an
atypical pneumonia due to C. abortus in a laboratory worker
involved in intranasal experimental C. abortus infections in
sheep was reported.112
C. abortus strains within Europe, in contrast to C. suis
strains, have a limited diversity but strong geographical signa-
tures. They do not harbor a plasmid and recombination was not
identified in a recent study.151
The clinical history of abortion in sheep and goats, often in
late pregnancy (ie, the last 2–3 weeks), precedes the investiga-
tion of a macroscopically changed placenta (if available) with
edema, hemorrhage, necrosis, and purulent exudate (Fig. 4).
The histopathology shows a purulent to necrotizing placentitis
with vasculitis and, if well preserved, intratrophoblastic baso-
philic chlamydial inclusions might be observed (Fig. 5)
(reviewed in Borel et al21 and Sachse et al146). If a large num-
ber of organisms are present in infected placental specimens,
the disease can be diagnosed by stained smears, antigen tests,
immunofluorescence, or immunohistochemistry (IHC) labeling
or by molecular methods such as PCR. In the majority of abor-
tion cases (71.6%) where OEA was present in a flock, other
abortigenic agents such as Toxoplasma, Campylobacter, Sal-
monella and Listeria spp. were also diagnosed,96 highlighting
the importance of considering coinfections and mixed infec-
tions during abortion investigations. Interestingly, while a live
temperature-sensitive vaccine strain 1B of C. abortus has been
available to control infections, it was reported that this vaccine
strain can lead to abortions as shown in Europe184 and recently
in New Zealand,148 causing lesions indistinguishable from
naturally induced C. abortus cases.
In sheep, chlamydial placentitis develops late in gestation
and from then on gradually progresses to a diffuse inflamma-
tory response, with thrombotic vasculitis and tissue necrosis
(reviewed in Sammin et al147). The pathogenesis of abortion
might be the result of a combination of impairment of materno-
fetal nutrient and gaseous exchange, disruption of hormonal
regulation of pregnancy, and induced cytokine aggression.44
Fetal pathology can occur after thrombo-embolic infection of
the fetus and results in focal necrosis in liver, lung, spleen, and
less frequently in lymph nodes and brain.29 During experimen-
tal infection, ewes were susceptible to infection from early
gestation onward and infections of the placenta and fetuses
occurred from about 60 days of gestation, but pathological
changes were not detected until after 90 days of gestation.29
This included rapid replication of C. abortus in the trophoblasts
at the limbus of the placentomal hilus and continuous spread of
infection to the intercotyledonary and cotyledonary placenta.
In nonpregnant ewes, relatively low doses of infectious
organisms (EBs) can induce chlamydial latency as shown in
intranasal infection studies.97 During latency, the infection
8 Veterinary Pathology XX(X)
remains inapparent in the nonpregnant animals and only
becomes evident during a subsequent pregnancy. When the
animals become pregnant, the infection proliferates, and initi-
ates placental infection and abortion.44 The route of primary
infection is presumed to be oronasal following ingestion of
organisms and establishing an initial infection in the tonsil
from where it may disseminate by blood or lymph to other
organs (reviewed in Essig and Longbottom44). Chlamydial
latency was recently investigated experimentally in sheep
using 3 different infection doses of C. abortus.97 The high dose
stimulated a protective immunity resulting in a much lower
abortion rate whereas the medium and low doses resulted in
a latent infection with infection of the placenta and abortion in
the subsequent pregnancy, the key feature of latency.97 In this
study, the most consistent histological lesions were found in the
brains of aborted lambs, lambs born dead and those that died
soon after birth, manifesting as focal leucoencephalomalacia
mostly located in the cerebral white matter and being indicative
of anoxic damage. Histological lesions in the fetal liver were
composed of suppurative periportal hepatitis and focal necro-
sis. Lesions in the fetal lung consisted of neutrophil infiltration
in alveoli, suppurative interstitial inflammation and interlobu-
lar edema and hemorrhage. The latter experimental study by
Longbottom et al97 was performed using the C. abortus strain
S26/3, isolated from the placenta of a sheep that aborted due to
OEA in Scotland, while the same authors93 used strains LLG
and POS, which have been isolated in Greece from aborted goat
and sheep fetuses and which are genetically different to S26/3,
in a recent comparative study. In doing so, they showed that the
placental pathology, infectious load and serological response
was clearly less pronounced for the strains LLG and POS than
for the C. abortus strain S26/3.
C. abortus has also been associated with epididymitis, pneu-
monia, arthritis and conjunctivitis in ruminants and has been
isolated from feces of healthy sheep and goats (reviewed in
Rodolakis and Laroucau133). In a recent study, C. abortus was
detected in the oviduct of 25% of cows by PCR but a firm link
with pathology could not be established as a higher percentage
of PCR-positive oviducts were collected from macroscopically
normal reproductive tracts (37.5%), than from those with
lesions (18.1%).4 Histological lesions in cows with PCR-
positive oviducts comprised ovarian cysts, mucometra, ovarian
adhesions, fibroproliferative lesions of the oviducts, and uter-
ine abscess.
C. abortus has been recently detected by PCR and sequen-
cing in cases of ovine, caprine and bovine infectious kerato-
conjunctivitis in India including mixed infections with C.
psittaci and Mycoplasma spp.50
Chlamydia pecorum in Ruminants
Chlamydia pecorum can infect a wide host range that includes
production animals such as sheep, goats, pigs and cattle, but
also wild ruminants and wild boars, as well as the koala. The
infection is thought to be endemic in cattle and sheep and the
majority of infections are reported as clinically inapparent,
mostly localized in the gastrointestinal tract. However, the sig-
nificance and economic impact of these subclinical infections
in livestock remains uncertain.90,130 More recently, chlamydial
infections due to C. pecorum in sheep and cattle have been
associated with important clinical manifestations such as infec-
tious arthritis, conjunctivitis, encephalomyelitis, infertility,
enteritis, reduced growth rates, mastitis, and pneumonia as
reviewed in detail.177 Recent and new knowledge has been
mostly accumulated from studies in sheep and cattle from Aus-
tralia and New Zealand. Initial reports date back to 1940 and
1960 and described encephalomyelitis cases in cattle and poly-
arthritis in feeder lambs in the USA.177 Polyarthritis and kera-
toconjunctivitis due to C. pecorum infections are commonly
seen in young lambs and calves. Arthritis is characterized by
an inflammatory and proliferative response in synovial mem-
branes possibly progressing to chronic changes with articular
erosions and fibrotic thickening. These changes can result in
weight loss of the animal, animal welfare issues and economic
losses for the farmer. Ovine arthritis cases in Australian
weaned lambs showing joint stiffness and depression were
described recently.178 The majority of animals also suffered
from concurrent conjunctivitis. Histopathology in 2 lambs
revealed chronic, multifocal lymphoplasmacytic synovitis and
mild, multifocal hyperplasia of synoviocytes.
C. pecorum-induced keratoconjunctivitis in ruminants can
lead to prominent conjunctival follicular formation and corneal
neovascularization.177 However, other studies119 could not find
an association between the presence of chlamydial DNA in
sheep conjunctival samples and the onset of clinical ocular
disease. These authors119 also detected C. abortus, C. suis, and
CLO in conjunctival swab samples by PCR and sequencing.
Infection with C. pecorum in young cattle can cause fatal
sporadic encephalomyelitis with encephalomyelitis, systemic
infection and fibrinous polyserositis including pericarditis,
pleuritis, peritonitis and arthritis. Brain lesions consist of a
severe meningoencephalitis with vasculitis, thrombosis and
malacia most severe in the brainstem and cerebellum.72 Histo-
logical brain lesions might overlap with those of Histophilus
somni.65 By IHC, chlamydial antigen can be demonstrated in
the cytoplasm of the endothelium and macrophages of brain,
spleen and lung and in the mesothelium.72 Typing of C. pecorum
strains revealed differences between strains detected in brain,
heart, lung, liver and the intestine, suggesting that different
strains may have different pathogenic potential, an observation
that was previously also suggested from studies of sheep.73
Associations between C. pecorum infection and enteritis or
reproductive diseases such as placentitis and abortion, vagini-
tis, endometritis, mastitis, and orchitis have been reported with
shedding of the organism through the fecal or vaginal route. C.
pecorum has been also implicated in cases of pneumonia in
sheep and cattle, inducing a fibrinous and broncho-interstitial
pneumonia in older reports (reviewed in Walker et al177). A
recent report identified C. pecorum in 8 out of 98 cases of
bovine pneumonia in Scotland, while other common respira-
tory pathogens such as BHV-1, BRSV, and PI-3 were
excluded.189 However, the pathologic findings in the lungs
Borel et al
were not further specified in this case report. Experimental
chronic but subclinical C. pecorum infections in calves led to
follicular bronchiolitis with marked BALT hyperplasia in the
lungs (reviewed in Reinhold et al130).
C. pecorum is abortigenic in small ruminants although to a
much lesser extent than C. abortus. Histological lesions in goat
abortions consisted of a suppurative and necrotizing placentitis
with vasculitis and thrombosis, lymphohistiocytic and neutro-
philic hepatitis and fibrinosuppurative enteritis in fetal liver
and intestine.48 Lesions in the placenta and fetal liver were
similar to C. abortus-induced abortion whereas the intestinal
lesions have not been described before and might represent a
unique pathological feature for infection with C. pecorum.
Moreover, subclinical C. pecorum infections might have a
significant impact on herd performance leading to reduced
growth rates in calves.124 Asymptomatic endemic C. pecorum
infections reduced growth rates in calves by up to 48%, indi-
cating a potential for C. pecorum-induced growth depression
due to chronic low-level systemic inflammation. This study124
also confirmed that infection takes places early in life and
repeatedly by multiple strains circulating ubiquitously in herds
with mixed infections or simultaneous infection with 2 or more
strains at different mucosal sites.
In summary, clinical disease due to C. pecorum infection
might be triggered by other factors such as stress and coin-
fections from the host side and on the pathogen side, depend-
ing on the virulence of the strain resulting in a multifactorial
pathogenesis.
Chlamydia pecorum in Koalas
Chlamydial infections in the koala (Phascolarctos cinereus),
the iconic Australian marsupial, have been associated with
keratoconjunctivitis (Fig. 6), rhinitis/pneumonia, and urogen-
ital tract disease with C. pecorum and C. pneumoniae as
involved chlamydial species (reviewed by Polkinghorne
et al).121 Chlamydiosis in the koala has a prevalence of up to
100% in some populations in the eastern states of Australia.121
C. pecorum, initially named C. psittaci, is more virulent in the
koala than C. pneumoniae and infection can lead to serious
complications such as blindness after ocular infection and
infertility after genital infection.66 The urogenital infection is
sexually transmitted but also mothers are thought to infect their
joeys through close contact. The inflammation of the urinary
tract is called “wet bottom” or “dirty tail” due to brown urine
staining and wetness of the fur in this region caused by cystitis
with subsequent incontinence and urine drippling. Chlamydial
infection in the koala can be considered in 3 categories: sub-
clinical infection (no signs of disease), overt disease (presence
of obvious external clinical signs such as conjunctivitis and
“wet tail”) or inapparent overt disease (lesions are not clinically
obvious but can be only detected using ultrasound, postmortem
examination or histopathology).180 Animals with active clini-
cal disease shed the highest level of C. pecorum organisms/
DNA and might therefore be the most important source of
transmission.121 For many years, anecdotal evidence suggested
9
that chlamydial disease was primarily limited to koalas in
northern populations.121 A more recent study has revealed that
chlamydiosis is indeed evident in South Australian koala popu-
lations, although at a much lower level than in their northern
counterparts.156
Histologically, inflammatory infiltrates consist of lympho-
cytes and plasma cells including follicle formation and to a
lesser extent, macrophages and neutrophils and accompanying
fibrosis. Such inflammatory processes mainly involve the eye
(conjunctivitis with conjunctival hyperplasia and fibrosis, cor-
neal edema and opacity due to ulceration, vascularization and
pigmentation) and the female urogenital tract (uterus, uterine
tubes, cervix, ovarian bursa, vagina, urinary bladder) resulting
in endometritis, metritis, salpingitis, vaginitis and cystitis.54
Cystic lesions of the ovarian bursa are considered a sequela
of previous inflammation and fibrosis with concomitant hydro-
salpinx. However, other organs (kidney, prostate, cloaca, lung)
can be also affected resulting in chronic interstitial, pyogranu-
lomatous nephritis or pyelonephritis, prostatitis, proctitis, and
interstitial pneumonia.57 A case of pyogranulomatous bronch-
opneumonia, proliferation of the bronchiolar and alveolar
epithelium and interstitial fibrosis with chlamydial inclusions
in bronchiolar epithelium was recently reported in a juvenile
male koala that died after an episode of respiratory disease.99
Chlamydial organisms were demonstrated by IHC and TEM
and C. pecorum DNA was detected by PCR.
In general, chlamydial antigen can otherwise be typically
detected by IHC in epithelial cells and macrophages includ-
ing alveolar, hepatic and splenic macrophages of affected
organs.26,54,57
While C. pecorum-induced urethritis and prostatitis in the
male koala is well known, chronic-active granulomatous orchi-
tis and epididymitis with interstitial fibrosis and resulting
aspermia has been described recently in koalas with history
of cystitis.75 Chlamydial inclusions were demonstrated in Ser-
toli cells of the testis by IHC and TEM and chlamydial DNA
was detected by PCR.
Chlamydia suis
Chlamydial species known to infect pigs are C. suis, C. abortus,
C. pecorum, and C. psittaci. Such infections have been associ-
ated with a wider range of lesions such as conjunctivitis,
pneumonia, pericarditis, polyarthritis, polyserositis, pseudo-
membranous or necrotizing enteritis, periparturient dysgalactiae
syndrome, vaginal discharge, return to estrus, abortion, delivery
of weak piglets, increased perinatal and neonatal mortality and
inferior semen quality, orchitis, epididymitis, and urethritis in
boars (reviewed in Schautteet and Vanrompay150). Before 1999,
C. suis strains were referred to as C. trachomatis, and the type
strain of C. suis, S45, was isolated in Europe in the late 1960s
from feces of an asymptomatic pig in Austria by Kölbl.150
Infection with C. suis is mostly associated with conjunctivitis,
respiratory infections, reproductive disorders and enteritis. C.
suis caused enteritis when inoculated in gnotobiotic piglets51,134
or induced histological intestinal lesions in asymptomatic
10
young weanling pigs.135 However, under field conditions, chla-
mydiae are commonly found in the intestine of pigs and are
mostly associated with endemic subclinical infections.58 Recent
studies mostly focused on the tetracycline-resistant C. suis
strains which have been initially detected in the USA86 and later
in Italy, Switzerland, Belgium, Israel and Cyprus (reviewed in
Borel et al22). C. suis is the only chlamydial species known to
have naturally acquired genes encoding for tetracycline resis-
tance and it has been shown recently, that selective pressure
appears to further promote resistance in fattening pig herds.181
By PCR and microarray, C. suis DNA has been detected in
conjunctival swabs of Nepalese trachoma patients 37 and
Belgian slaughterhouse workers.39,40 Recently, isolation of C.
suis from nasal, pharyngeal and stool samples taken from
Belgian farmers was reported, demonstrating the presence of
live organisms.38 These findings indicate the potential zoonotic
transmission of C. suis from pigs to humans. Taken together,
infection with C. suis might be opportunistic in nature and
ocular, respiratory and intestinal virulence variation of C. suis
infection might be influenced by the age and immune status of
the host, possible coinfections and genetic variations of C. suis
strains including high recombination rates.154
Chlamydia felis and Chlamydia caviae
C. felis and C. caviae are agents of infectious conjunctivitis in
cats and guinea pigs, respectively, but their DNA has also been
detected in swab samples of dogs (C. felis, C. caviae), horses
(C. caviae) and rabbits (C. caviae).116
C. felis was initially named Bedsonia sp. (psittacosis/
lymphogranuloma-venereum trachoma group), the agent of
feline pneumonitis causing conjunctivitis, rhinitis and pneumo-
nitis in cats.6,7 Later, it was grouped into C. psittaci and finally
named C. felis.141 Although the original isolate was derived from
the lung of a cat with pneumonia,6 conjunctivitis is now known
to be the most common clinical sign of infection and the term
“feline pneumonitis agent” seems misleading.11 C. felis is ende-
mic among pet cats worldwide with reports of zoonotic infec-
tion.149,161 The first report of a zoonotic infection presented as an
acute follicular keratoconjunctivitis in a cat owner, whose cat
had a recent history of rhinitis and conjunctivitis.149 In cats, C.
felis primarily targets the conjunctival epithelium and causes
acute to chronic or recurrent conjunctivitis, particularly in young
cats (2 to 12 months of age). Infected cats have mucoid/muco-
purulent to follicular conjunctivitis and rhinitis (reviewed in
Sykes162). Chlamydial inclusions can be demonstrated in
Giemsa-stained smears prepared from conjunctival scrapings but
PCR-based methods are more sensitive and specific. During the
acute neutrophilic conjunctivitis phase, high levels of C. felis are
excreted, peaking approximately 1–2 weeks postinfection.
Thereafter, in the chronic conjunctivitis phase, lower levels of
C. felis are excreted persisting up to 2 months postinfection prior
to resolution of clinical signs and cessation of chlamydial shed-
ding. Cats can also remain persistently infected for longer time
periods and may maintain an asymptomatic carrier status. C.
Veterinary Pathology XX(X)
felis infections have been also linked to reproductive tract dis-
ease and lameness but etiological evidence remains weak.16
During experimental infection, signs of conjunctivitis
appeared 5–10 days post infection and lasted for 22–45 days.
In some cats, mild rhinitis but no clinical signs of lower respira-
tory tract disease were present. By histology, small foci of
broncho-interstitial pneumonia were detected in 3 out of 6 cats.
Chlamydial inclusions were present from day 7 to day 14 in the
cytoplasm of conjunctival smears.61 Experimental infection of
kittens not only induced conjunctivitis but also resulted in
fever, lethargy, lameness and reduction of weight gain.174 In
addition, vaginal excretion of C. felis was observed in cats
infected at an age of 4–6 months. Prolonged vaginal and rectal
shedding in cats with conjunctivitis has been reported indicat-
ing that the genital and intestinal tracts might be a reservoir for
persistent infection.162 C. felis has also been found in the lung,
spleen, liver, kidney, and peritoneum of cats, however, the
significance of these findings has to be elucidated.162
The species, C. caviae, was taxonomically separated from C.
psittaci in 1999 along with several other species formerly con-
sidered to be biovars of the latter species.45 C. caviae is a
chlamydial pathogen that has been exclusively isolated from
guinea pigs namely from the conjunctiva (GPIC, guinea pig
inclusion conjunctivitis)109 but is extensively used as an animal
model of human C. trachomatis ocular128 and genital infec-
tions.127 C. caviae is one of the most common infectious causes
of conjunctivitis in guinea pigs, but can also induce rhinitis,
lower respiratory tract disease and abortion. Guinea pigs with
conjunctivitis can be evaluated by preparing cytological smears
from conjunctival swabs stained with Giemsa.160 Intracytoplas-
mic chlamydial inclusion bodies can be observed in conjuncti-
val epithelial cells, enabling the initial diagnosis of GPIC which
can be confirmed by PCR demonstrating C. caviae as the
involved chlamydial species. In a larger case study,98 59 out
of 123 guinea pigs were positive for C. caviae, 48 out of 59
presented ocular signs (ocular discharge, conjunctivitis, chemo-
sis, keratitis), nasal discharge and other respiratory signs and
vaginal discharge whereas 11 PCR-positive guinea pigs
remained asymptomatic. PCR-positive symptomatic guinea
pigs suffered most often from a neutrophilic conjunctivitis with
visible chlamydial inclusion bodies in cytological smears. DNA
of C. caviae was also detected in a rabbit (mild seromucous
discharge and conjunctivitis), a cat (no clinical signs) and the
owner (mild serous ocular discharge) of one guinea pig collec-
tion suggesting interspecies transmission and zoonotic potential.
During experimental ocular infection studies, conjunctival
inflammation in infected guinea pigs is seen for about 30 to
40 days, chlamydial inclusions and PMNs are present for up to
21 days and mononuclear cells (lymphocytes, fewer plasma
cells, and macrophages) are found on days 7 to 25 in conjunc-
tival scrapings.106 Sporadically, a mild, diffuse epithelial and
subepithelial keratitis of the upper half of the cornea occurred.
Repeated ocular infection with C. caviae resulted in severe
conjunctival chronic inflammation lasting for months followed
by pannus and follicle formation in the palpebral conjunctivae,
scarring of the lower conjunctivae and deformities of the lower
Borel et al
lid. The inflammation was dominated by mononuclear cells
and rarely by small numbers of PMNs or chlamydial inclu-
sions.107 The pathological picture during repeated ocular C.
caviae infection closely resembled trachoma disease in human
patients, mediated most likely through a delayed-type
hypersensitivity.
After vaginal experimental infection, C. caviae ascends to
the upper genital tract leading to inflammation and fibrosis of
the oviducts. This ascension results in tubal obstruction, hydro-
salpinx and infertility as observed in C. trachomatis-infected
women,127 making this animal an extensively used model for
studying the pathogenesis of female infertility.
Chlamydia pneumoniae
In humans, C. pneumoniae, an agent of respiratory infection, is
nearly ubiquitous in humans, with seropositivity rates of
70–80% in older populations, suggesting most people experi-
ence infection during their lifetime.32 In animals, infection with
C. pneumoniae has been reported in horses, koalas and other
Australian marsupials, frogs and reptiles.136,137 Moreover,
DNA of C. pneumoniae was recently detected in whole-blood
samples and vaginal swabs of cows from China.90 The horse
strain, N16, was isolated from the respiratory tract of a horse
and contains a plasmid,158 however, proof of associated pathol-
ogy is weak. Previous case studies linked the presence of
C. pneumoniae with disease in free-ranging or captive frog
species15,17,129 but recent data are missing.
The initial description of C. pneumoniae infection in koalas
was in the late 1990s by Wardrop.182 Clinical signs reported in
koalas included respiratory distress, sneezing, coughing, chest
congestion, difficulty in breathing, rhinitis and nasal dis-
charge.182 However, C. pneumoniae infections in koalas are
usually low grade compared to C. pecorum infections in this
host. Unfortunately, detailed information on pathologic
changes in the upper and lower respiratory tract due to C.
pneumoniae is missing as recent studies mostly focused on
genomic and in vitro phenotypic comparisons between the C.
pneumoniae koala type strain LPCoLN and human strains of C.
pneumoniae.103–105 On the other hand, comparisons of strain-
specific differences between C. pneumoniae isolates from both
human and animal origin might help to understand the zoonotic
potential and evolutionary history of this pathogen. Such data
showed that animal isolates were more diverse than the isolates
of human origin with a number of genes in animal isolates
observed to be intact while their human homologues were
decayed.103,104 This observation has led to the suggestion that
animal strains are ancestral to human strains and that cross-host
transmission to humans from animals may have occurred sev-
eral times in the evolutionary history of this pathogen.103,104,137
C. pneumoniae and unidentified Chlamydiales were
detected by PCR in western barred bandicoots (Perameles bou-
gainville) with ocular signs such as corneal opacity, conjuncti-
vitis, ocular discharge, and blepharitis.183 Further studies
confirmed C. pneumoniae as cause of conjunctivitis, cataract
and corneal scarring, as well as possible pneumonia in
11
bandicoots.83 The C. pneumoniae strain B21 isolated from a
western barred bandicoot also harbors a plasmid like the koala
LPCoLN strain and the horse N16 strain and is, as expected,
most closely related to the koala strain.136
Chlamydial Infections in Reptiles
Chlamydial infections have been reported in both free-ranging
and captive reptilian hosts including puff adders, boas, chame-
leons, crocodiles, turtles and tortoises. Initial reports described
C. psittaci as the causative agent of chlamydiosis in rep-
tiles62,132 but nowadays, C. pneumoniae is considered the most
widespread. The infection manifests as granulomatous inflam-
mation in inner organs such as heart, liver, spleen and lung. In a
retrospective study of captive (private, zoo) reptiles (n ¼
90),155 9 snakes and chelonians were positive for C. pneumo-
niae in granulomas of the lung, pericardium, heart, liver and
kidney. Of these, 3 cases had mixed infections with myco-
bacteria. Other previous reports describe cases of histiocytic
granulomas (puff adders),68 granulomatous inflammation
(flap-necked chameleon),70 necrotizing enteritis (green igua-
nas),20 necrotizing myocarditis (green turtles),60 proliferative
pneumonia (Burmese python and other snakes),20,46 multiple
granulomas and lympho-plasmacytic gastroenteritis in emerald
tree boas,67,69 and acute hepatitis and conjunctivitis in croco-
diles.62,63 An unusual case of C. pneumoniae infection was
recently described in a royal python showing neurological
signs.34 Histology revealed lymphocytic enteritis with histio-
cytic granulomas, granulomatous splenitis and meningitis.
Chlamydial IHC was positive in splenic granulomas and PCR
identified C. pneumoniae in pooled visceral tissues.
More recently, it has become clear that chlamydiae might
more often be present as opportunistic pathogens in reptiles. By
PCR, C. pneumoniae was commonly detected in routinely
sampled reptiles from Japanese zoos including snakes, turtles,
lizards, and chameleons79 and in cloacal swab samples of
snakes from an Argentinian recreational area.46 During a long-
itudinal case study in a collection of 58 snakes,138 C. pneumo-
niae infections were not necessarily lethal for snakes but were
common in clinically inconspicuous carriers.
A follow-up study171 investigated and characterized C.
pneumoniae and potential other novel chlamydial infections
in the choana and cloaca samples of 137 clinically healthy
captive snakes from 6 private collections resulting in the
description of novel chlamydial genotypes. In summary,
unique 16S genotypes were designated from 21 choanal or
cloacal swab samples, with closest sequence identity to uncul-
tured Chlamydia sequences, C. pneumoniae strains or a chla-
mydial sequence isolated from a tortoise, indicating the
presence of potentially novel Chlamydia species. Such novel
chlamydial species might be either present as asymptomatic
choanal/cloacal infections or may be able to cause disease in
coinfection with other pathogens (Fig. 7). Culture-independent
full genome sequencing of genomic DNA obtained from the
choana of a captive, clinically inapparent Madagascar tree boa
(Sanzinia madagascariensis volontany) revealed the novel
12
Candidatus species Chlamydia sanzinia,168 which contains a
plasmid and falls in a phylogenetic clade with C. pneumoniae
and C. pecorum. As a follow-up to this investigation, the same
methods were applied to a larger selection of chlamydial PCR-
positive specimens from the collection previously screened by
Taylor-Brown et al.171 While this method was less successful
than the initial study, the genome of another novel chlamydial
species, Candidatus Chlamydia corallus, was retrieved from
the choana of an asymptomatic captive Amazon Basin emerald
tree boa (Corallus batesii).172 Notably, while chlamydial chro-
mosomal sequences could not be resolved for the remaining
samples, plasmid sequences could be, suggesting additional
and untapped Chlamydia genus diversity in the remainder of
the samples. In summary, all these recent findings indicate that
snakes may still harbor a significant and largely uncharacter-
ized level of diverse and novel chlamydial species requiring
further investigation.
CRB, CLO with Proven Pathogenic Potential
At least 13 new Candidatus species of CRB have been reported
in reptilian, amphibian, avian, piscine and protozoan hosts in
the last 4 years.170 Of these, CRB seem to play a pathogenic
role in ruminant abortion and human miscarriage (family Wad-
dliaceae and Parachlamydiaceae) as well as in epitheliocystis
in fish, the common gill disease (families Simkaniaceae, Ca.
Parilichlamydiaceae, Ca. Piscichlamydiaceae, and Ca.
Clavochlamydiaceae).
CRB-related diseases in ruminants have been recently
reviewed in detail.187 Waddlia chondrophila and Parachlamy-
dia acanthamoebae have been demonstrated in placentas of
women with adverse pregnancy outcomes such as miscarriage
(reviewed in Ammerdorffer et al).3
Waddlia chondrophila was initially isolated from a case of
bovine abortion in the United States in 1986 and initially clas-
sified as Rickettsia.42 However, pathological observations
associated with this finding were not reported. A subsequent
study from Germany detected W. chondrophila in a septic still-
born calf in a coinfection with Neospora caninum.56 Patholo-
gical findings included lymphohistocytic meningoencephalitis
with fibrinous exudate and a focal leukoencephalomalacia in
the fetal brain, acute suppurative pneumonia and bronchiolitis
and a multifocal suppurative necrotizing placentitis with vas-
culitis but it remained unclear if these lesions were caused by
W. chondrophila, N. caninum, or both. In a Swiss study inves-
tigating 343 placental samples from late-term bovine abortion
cases, 3 were positive by Waddlia-specific real-time PCR, and
of these, 2 were confirmed by IHC.18 All 3 cases showed a
purulent to necrotizing placentitis and additional vasculitis as
well as the presence of Parachlamydia in 2 cases. Again, it
remained unclear if both or only one agent caused bovine abor-
tion. Most recently, W. chondrophila DNA has been detected in
vaginal swabs and placental tissues taken from Tunisian cows
that had aborted and were also coinfected with Listeria mono-
cytogenes.8–10 However, a recent experimental infection study
failed to demonstrate a clear link between W. chondrophila
Veterinary Pathology XX(X)
infection and abortion in cattle.185 Only 1 out of 9 heifers
intravenously infected with W. chondrophila on day 105 to day
110 of pregnancy had inflammatory lesions of the chorioallan-
tois but this did not result in abortion. Although this study185
could confirm the third and fourth of Koch’s postulates, it was
concluded that W. chondrophila might represent an opportu-
nistic pathogen and that its role in abortion remains to be
confirmed.185
Parachlamydia has been related to bovine abortion
cases and to a lesser extent caprine and ovine abortion in
Switzerland, England, Scotland, Ireland, Hungary, and
Tunisia. 9,18,23,41,82,139,140,186,188,190 Parachlamydial cases
revealed necrotizing or purulent to necrotizing placentitis
sometimes with vasculitis in common. The presence of a non-
suppurative interstitial pneumonia in fetal lungs was also
reported in relation to parachlamydial infection but IHC
remained negative.186 Parachlamydia was demonstrated in
placental lesions by PCR, IHC, or TEM. Positive immunola-
beling for Parachlamydia in the placenta was present within
the cytoplasm of trophoblasts primarily associated with areas
of intense infiltration of polymorphonuclear neutrophils.186
Mixed infections with other abortigenic agents such as Neos-
pora caninum, Coxiella burnetii, C. abortus, Brucella abor-
tus, Campylobacter, bovine herpesvirus type 1 and with
mycotic placentitis are reported but interaction with Para-
chlamydia remains unclear.9,18,140,186 To confirm an etiologi-
cal role for Parachlamydia in bovine abortion, its isolation
from abortion material and subsequent fulfilment of Koch’s
postulates awaits confirmation.
CLO were associated with cattle pneumonia in Scotland,
namely P. acanthamoebae, uncultured Chlamydiales and Rhab-
dochlamydia,189 and Parachlamydia caused mild respiratory
signs in calves when experimentally infected by direct inocula-
tion into the lungs.94 These signs were dose-dependent and
accompanied by macroscopic foci of pneumonic lung lesions
corresponding to intrabronchial inoculation sites. Histologically,
purulent to fibrinous bronchopneumonia was present at 2 dpi
followed by subacute bronchopneumonia at 4 dpi and bronchio-
litis obliterans and perivascular cuffing between 10 and 14 dpi.94
During an intranasal and intratracheal experimental infection
mouse model, P. acanthamoebae induced severe interstitial
pneumonia which was purulent in the early phase (2–4 days after
infection, dpi) and mononuclear at 7–21 dpi.30,118
Transmission modes of CRB are unknown but aquatic
sources might play a role (reviewed in Wheelhouse and Long-
bottom187). A zoonotic potential has to be considered as CRB
have been indirectly linked to recurrent pregnancy failure and
miscarriage in women as well as pneumonia and bronchiolitis in
children and patients with community-acquired pneumonia.187
The common abortion diagnostics do not include testing for
CRB. Correlation of histological changes such as purulent to
necrotizing or necrotizing placentitis with or without vasculitis,
detection of the antigen by IHC within lesions and its DNA by
PCR is recommended to unambiguously establish a diagnosis
of CRB-related abortion. In well-preserved placental speci-
mens, intracellular bacteria and inclusions might be already
Borel et al
observed in H&E-stained sections.21,187 However, more data
are needed to learn more about the pathogenicity, associated
lesions, significance and transmission routes of CRB-related
abortions in ruminants.
Chlamydial Agents of Epitheliocystis in Fish
Epitheliocystis is a disease primarily of the gills of marine and
freshwater fish species and is so named due to the presence of
cyst-like inclusions within the epithelial cells of the fish gills
(reviewed in Stride et al159). More commonly observed in
juvenile fish than in adults, clinical signs are sometimes
observed in fish with epitheliocystis and may include respira-
tory distress and lethargy, among other signs. Mortalities are
thought to be uncommon but have been reported at rates of up
to 100% in juvenile aquaculture production systems for var-
ious species.159
Histology remains the diagnostic method of choice for
detecting epitheliocystis. Histopathologically, epitheliocystis
infections are often benign without any proliferative host
response observable. Where host responses are observed these
can appear as local to multifocal epithelial hyperplasia with
interlamellar filling that can lead to fusion of the lamellae and
cellular hypertrophy. The most severe morphological changes
are associated with mortalities in juvenile fish.159
Prior to the introduction of molecular methods, a chlamydial
etiology was long suspected due to the visualization of
chlamydial-like cell forms in epitheliocysts by TEM. 35
PCR-based methods utilizing Chlamydiales broad-range PCR
primers were subsequently able to confirm a chlamydial origin
for these inclusions.43 Since this confirmation, an increasingly
diverse range of novel CRB in the phylum Chlamydiae have
been described in >20 fish species, including uncultured agents
in a previously described chlamydial family, Simkaniaceae,
and 3 entirely newly described families composed exclusively
of epitheliocystis agents, Ca. Parilichlamydiaceae, Ca. Pisci-
chlamydiaceae, and Ca. Clavochlamydiaceae. 159 In the
absence of a culture system for these pathogens, little is still
known about the biology of these novel CRB, although the
continued identification of new chlamydial epitheliocystis
agents in each fish species examined has led to the suggestion
that (a) a significant unrecognized diversity of CRB may be
present in fish and (b) each CRB may have coevolved with
their respective host.159 A recent culture-independent genome
study of the epitheliocystis agent of orange-spotted grouper
(Epinephelus coioides), Candidatus Similichlamydia epinephi-
lii, revealed that while phylogenetically distant from the family
Chlamydiacaceae, the genomes of these bacteria are quite sim-
ilar in size and virulence gene content.169
Complicating the differential diagnosis of epitheliocystis for
pathologists is the recent realization that other bacteria from
completely different bacterial phyla including beta- and
gamma-proteobacteria80,152 may cause similar diseases as
CRB. Many of these alternative agents may have subtle differ-
ences in their morphology compared to chlamydial agents so
microscopic differentiation may be possible,153 however, this
13
will need to be supported by PCR and in situ hybridization for
confirmatory diagnosis at this stage.
Conclusions
Zoonotic diseases like chlamydial abortion in ruminants due to
C. abortus and psittacosis/ornithosis in birds due to C. psittaci,
both presenting with characteristic pathomorphological
lesions, have been well known for decades. With the advent
of molecular techniques, emerging novel chlamydial species
have been detected in a variety of host species and host barriers
for known chlamydial species may be less stringent than pre-
viously thought. At present, nucleic acid amplification tests are
considered the state-of-the-art methods to diagnose chlamydial
infections in animals and humans due to their sensitivity and
specificity. This might implicate that the pathologist is of
minor importance and his or her role might be underestimated
in chlamydial diagnostics. However, the behavior of well-
characterized chlamydial veterinary pathogens in new hosts
is understudied and reports mostly rely on molecular findings
only. Moreover, many of the emerging CRB are thought to
have the potential to cause disease in their respective hosts, but
pathogenesis and associated pathological changes are awaiting
proof of this. In the future of chlamydial research, as such, the
pathologist is an important player when investigating associ-
ated pathology due to natural infection with novel chlamydial
species or known chlamydial species in novel hosts or when
evaluating the pathogenesis of novel chlamydial species in
experimental animal models.
Acknowledgements
Figure 6 image courtesy of the Australia Zoo Wildlife Hospital.
Declaration of Conflicting Interests
The author(s) declared no potential conflicts of interest with respect to
the research, authorship, and/or publication of this article.
Funding
The author(s) received no financial support for the research, author-
ship, and/or publication of this article.
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