Abstract
Disseminated toxoplasmosis is a primary, highly fatal disease in some zoo species, mainly New World monkeys, prosimians, and Australian marsupials. High-risk situations are the practice of feeding raw meat to susceptible species and the presence of stray cats within the zoo grounds. During the period of 1992–1995, disseminated toxoplasmosis was a considerable problem at the Barcelona Zoo, with epizootic episodes affecting golden lion tamarins (Leontopithecus rosalia) and slender-tailed meerkats (Suricata suricatta). A high case-fatality ratio (apparently 100%) was observed. Unexpected death with no premonitory signs was a common outcome, so a rapid diagnosis at necropsy is often required to initiate an appropriate therapy.
Introduction
Toxoplasma gondii is a ubiquitous intestinal coccidian parasite both of domestic and wild cats; congenital and neonatal toxoplasmosis can be sporadically seen in zoo cats. The list of intermediate host species is wide, but their susceptibility to T. gondii varies considerably. Some of the most susceptible species can be commonly found in zoos throughout the world.
The purpose of this communication is to discuss some conflictive aspects about the occurrence of disseminated toxoplasmosis (DT) in susceptible zoo species, based mainly upon the literature and the authors’ experience originated from epizootic DT episodes in golden lion tamarins (Leontopithecus rosalia) (Juan-Sallés et al., submitted) and slender-tailed meerkats (Suricata suricatta)12 at the Barcelona Zoo (Spain) during the period of 1992–1995. Spontaneous DT has been rarely reported in callitrichids,15 and meerkats were recently added to the list of susceptible zoo species.12
Epizootiology
During the last years, DT at the Barcelona Zoo has frequently been a highly fatal epizootic condition in small breeding groups, although isolated cases also occurred.12 When we compared the number of cases of DT and avian tuberculosis (ATB), a disease with a high incidence at the Barcelona Zoo during the period of 1990–1994,11 it was fairly evident that DT can become a serious problem.
High-risk situations for DT in zoos seem to be mainly the practice of feeding raw meat to susceptible species and the presence of stray cats within the zoo. It is easy to avoid the first high-risk situation; however, many reports of epizootic DT in zoo species have been thought to be the result of feeding raw meat. It may be an inappropriate food item for some zoo species, because it can be a source not only of T. gondii, but also of other pathogens, such as Streptococcus zooepidemicus.17 Moreover, feeding raw meat to zoo felines contributes to the presence of T. gondii in zoos.7
If stray cats are a problem, then prevention is not always easy. For example, in our case, trapping cats was an unpopular procedure, and there was always an ongoing release of cats within the park where the zoo is located. Therefore, it becomes a problem difficult to eradicate for the veterinarian. Stray cats had easy access to the enclosure of a group of meerkats with DT.12 Most reports on epizootic DT in herbivorous marsupials provided evidence of stray cat involvement in the transmission of T. gondii.6,13,14
In the absence of these high-risk situations, other sources of infection (e.g., ingestion of mice or birds, transport hosts of oocysts)7 will most likely account, in our opinion, for enzootic DT. These other sources of infection seem to be sporadic or not major pathways for DT to occur, and, anyway, they are mostly the reflection of the presence of stray cats within a zoo. Ingestion of feral mice could be the source of infection in three golden lion tamarins (Leontopithecus rosalia) that died of DT at the Barcelona Zoo (Juan-Sallés et al., submitted).
Latency and reactivation of T. gondii in highly susceptible zoo species do not seem to be common. However, evidence has accumulated about the ability of even highly susceptible species to survive the acute phase of toxoplasmosis;2,6,8 therefore, latency and reactivation of T. gondii could account for some DT cases. For example, reactivation of T. gondii has been reported in an experimentally infected owl monkey (Aotus lemurinus)8 and apparently in a Barbary macaque (Macaca sylvanus) with previous experimental inoculation of simian immunodeficiency virus.16 Although we could not confirm it, a litter of newborn meerkats could die of DT between two DT episodes;12 in such case, transplacentary or transmammary transmission from a latently infected dam would have been a likely source of infection. The possibility of T. gondii latency in highly susceptible zoo species makes this parasite an undesirable candidate to be introduced in wild populations of endangered species that are being reintroduced in their natural habitats, such as the golden lion tamarin.
The susceptibility to T. gondii varies between different species, perhaps depending on their ecology in the wild and the characteristics of their natural habitat:
1. The absence of felines in the habitats where lemurs and Australian marsupials evolved seems to be responsible for their high susceptibility to T. gondii.2,7
2. The arboreal habits, and therefore the lack of contact with cat-contaminated food, of most New World primates have been incriminated as factors contributing to their high susceptibility to T. gondii.
3. The feeding ecology of some susceptible species in the wild (the absence or sporadic presence of meat in their diet) seems to be a major contributing factor for their susceptibility to T. gondii. For example, the feeding ecology together with the arboreal habits of callitrichids would account for their extreme susceptibility. Surprisingly, there are very few reports on DT in callitrichids.15 Our experience both with zoo and pet callitrichids shows that DT can become a serious problem if high-risk situations occur.
4. The temperature and humidity influence the survival of T. gondii oocysts; some species living in dry, desert regions—such as the gondi (Ctenodactylus gondi)—have proven to be highly susceptible to T. gondii.4
The feeding ecology of the slender-tailed meerkat, as well as the characteristics of its habitat, are perhaps good reasons for its apparently high susceptibility to T. gondii.12 Other mammals belonging to the order Carnivora seem to have a better-balanced parasite–host relationship; for example, DT in bears and mustelines is mainly reported in neonatal or young specimens, whereas sporadic toxoplasmosis cases in foxes, raccoons, and red pandas are often associated with canine distemper.12
Pathology
DT can be tentatively diagnosed at necropsy if smears or touch imprints of organs with lesions are taken.2,12,13 This simple procedure is of great value to rapidly initiate a T. gondii-specific therapy before DT kills most animals in a group. Major gross findings that can be seen in DT cases are:
1. Lymphadenopathy and/or necrotizing [sic] are common findings at least in New World primates, prosimians, and meerkats (Juan-Sallés et al., submitted).4,5,12
2. Pulmonary edema and/or reddened, non-collapsed lungs (sometimes with pale foci), suggestive of interstitial pneumonia (Juan-Sallés et al., submitted).1,2,9,12,14
3. Hemorrhages, pale streaks or foci, and/or mineralization can be frequently seen in marsupials.1,13 Occasionally, severe myocarditis may be present.12
4. Gastrointestinal ulceration and hemorrhagic enteritis have been described in marsupials and callitrichids (Juan-Sallés et al., submitted),1 but they do not seem to be very common. However, intestinal lesions can become prominent microscopic findings (Juan-Sallés et al., submitted).1,5,14
5. Splenomegaly, multifocal necrotizing hepatitis, hydrothorax, ascites, and hydropericardium are sometimes present.1,5,9,12,13
Microscopically, DT affects most tissues; kidneys are rarely damaged. Lesions are often necrotizing with varying degrees of mixed inflammatory response, but some tissues have characteristic lesions. For example, acute to subacute interstitial pneumonia and/or pulmonary edema are frequent in meerkats, marsupials, and New World monkeys (Juan-Sallés et al., submitted).1,2,12,14 The occurrences of syncytial cells in the lungs of zoo animals with DT and interstitial pneumonia are not described, but we did find them in meerkats and callitrichids (Juan-Sallés et al., submitted).12
Toxoplasma gondii-like organisms become widely distributed through the tissues of animals with DT and can be readily seen in H&E sections of most DT cases. However, especially in peracute and acute cases, tachyzoites can be overlooked; this is also true for some severe lesions containing few T. gondii organisms.
DT is often consistent with a primary infection with T. gondii, whereas localized toxoplasmosis (fairly uncommon in susceptible zoo species) is more consistent with the reactivation of a latent T. gondii infection, at least in the mouse and man.3 The distribution of lesions in localized toxoplasmosis may reflect the common distribution of T. gondii tissue cysts in the muscular tissues and brain of latently infected hosts.
Therapy
DT is rarely suspected antemortem since short clinical courses with nonspecific signs or unexpected deaths are common in highly susceptible species. Therefore, getting a rapid diagnosis at necropsy during epizootic episodes is the key to initiate an appropriate therapy. Harper and coworkers used five drug regimens in experimentally infected squirrel monkeys (Saimiri sciureus); although the treatment began 48 hours after intragastric inoculation, two animals became parasitemic and recovered.9 Sulfamethoxazole alone or combinations of sulfonamides with trimethoprim or pyrimethamine were the most effective drugs in preventing clinical disease and death.9 The clinical course of DT in meerkats seemed to lengthen when animals were treated with clindamycin, but it did not prevent death.12 Trimethoprim-sulfadiazine therapy was successful in clinical cases of suspected toxoplasmosis in Australian macropods, as well as in a binturong.10,13
Prevention
Depopulating stray cats and discontinuing the practice of feeding raw meat to susceptible zoo species and large cats are major pathways to prevent DT from devastating valuable breeding groups of zoo species. Control of rodents and birds, often difficult, would be a minor pathway since they have to be preyed upon to become infectious, and, therefore, they would only account for sporadic DT cases.
Literature Cited
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