Discussion
The main source of parasitic infection in zoo animals is not well known.
At the Ljubljana Zoo, as in other European zoos, feeding carnivores with
raw meat that is potentially infected with T. gondii tissue cysts
is a common practice. Infected felids can spread T. gondiioocysts in their environment and thus contaminate food, bedding, and
water. In some zoo felids (Otocolobus manul ), toxoplasmosis with
a fatal outcome has been reported (Bartova 2014). Carnivores can also be
infected by hunting some small prey species with free access to the zoo,
such as small wild rodents and birds. Another source of infection might
be the presence of feral cats in the zoo, which can spread oocysts in
their feces to zoo enclosures. In our study, T. gondii was
detected by PCR in tissues of four wild rodents and in one laboratory
mouse that died. The laboratory mouse came from a specific pathogen-free
breeding compound; the route of infection of this animal remains
unknown. One possibility is food contaminated with sporulated T.
gondii oocysts due to improper storage of prepared pellets.
Fatal toxoplasmosis was described in six tammar wallabies
(Macropus eugenii ) in the Budapest Zoo and Botanical Garden
between 2006 and 2010 (Sós, 2012). Wallabies are known to be
susceptible to T. gondii infection, and feral cats are suggested
as the main source of the parasite in the zoo environment. In our study,
a high prevalence of T. gondii was found in Camelids and
Diprotodontia, which could be related to contamination of food such as
hay or of substrate material in their enclosures, which is mostly sand.
A high risk of contamination of this substrate with the feces of feral
cats as well as difficulties in keeping stray cats outside the zoo (it
is located in the city) increase the possibility of infection withT. gondii oocysts. New World Primates are highly susceptible to
clinical toxoplasmosis, and the infection is often fatal with various
pathological manifestations (Epiphanio, 2003). High prevalence was
previously recorded in primates such as the red-faced spider monkey
(Ateles paniscus ) and tufted capuchin (Cebus apella ) from
a zoo in Brazil, at 67% (Minervino, 2010), and in a Barbary macaque
(M. sylvanus ), gorilla (Gorilla gorilla ), chimpanzee
(Pan troglodytes ), and orangutan (Pongo pygmaeus ) in the
Czech Republic, at 45% (Sedlák, 2006). In our study, T. gondiiantibodies were found in 25% of primates (chimpanzee, Pan
troglodytes ). Ingestion of sporulated T. gondii oocysts in
contaminated feed is presumed to be the main source of infection.
Carefully washing vegetables and fruits as well as regularly cleaning
the kitchen may reduce the risk of infection in this group of animals.
Toxoplasmosis has been recorded in zoo birds; for example, in canaries
and black-winged lories (Eos cyanogenia ) (Weiss, 2011). In
our study, antibodies to T. gondii were not found in any of the
birds tested; however, two mute swans died and T. gondii was
detected in their tissue by PCR. These samples were genotyped and
characterized as type II, which is known to be highly predominant in
humans and animals in Europe and North America (Costache, 2013; de
Sousa, 2006). Water contaminated with T. gondii oocysts is one
possible source of the infection in this case.
E. cuniculi is a very important parasite of rabbits throughout
Europe (Jordan, 2006). This is in accordance with results from our study
because we found the highest prevalence of E. cuniculi antibodies
in Lagomorpha (83%) in European rabbits (Oryctolagus cuniculus ).
Placentitis, premature birth, and perinatal death has been described in
connection with E. cuniculi infection in an alpaca (Vicugna
pacos ) (Webster, 2008). In our study, a high prevalence of E.
cuniculi antibodies was found in Bovidae (81%) and Camelidae (67%).
Antibodies to E. cuniculi were found in an alpaca (Vicugna
pacos ) and a guanaco (Lama guanicoe ). One E.
cuniculi –seropositive alpaca died, but the parasite was not detected
by PCR in its tissue.
Clinical disease and positive isolation of E. cuniculi was
reported in captive emperor tamarins (Saguinus imperator ) and
cotton-top tamarins (Saguinus oedipus ), which seem to be highly
susceptible to infection (Guscetti 2003; Juan-Sales 2006). In our study,
chimpanzees, lemurs, and gibbons were negative. Herbivores had a higher
chance of being infected compared to carnivores, which could suggest the
presence of E. cuniculi spores in the environment as a main
source of infection. E. cuniculi infection in birds has no
clinical importance, but some avian species could serve as reservoirs
for these microsporidia (Hinney, 2016). In our study, antibodies toE. cuniculi were found in mute swans and helmeted guineafowls
(Numida meleagris ).
Chlamydia abortus and Coxiella burnetii are pathogens that
are well known to cause abortions as well as various health problems in
zoo animals (Lloyd, 2010). The negative results obtained in our study
may be due to limited exposure, good preventive veterinary care, and
suitable disinfection plans.
Zoos are institutions open to the public. A large variety of different
animal species usually with a high density of animals, open enclosures,
the presence of stray cats and wild rodents, and close contact with
people are important factors for transmission of diseases, often with
anthropo-zoonotic potential, which raises public health concerns.
Therefore, monitoring transmissible diseases in zoo animals and
understanding their dynamics is of great importance and is an
inseparable part of preventive health care in zoological collections.
Financial support: The study was supported by internal grant of
VFU Brno (FVHE/Literák/ITA2019).