Abstract

During 1995 and 1996, a total of 16 (eight male and eight female) wild-caught Pallas’ cats (Otocolobus manul) were imported into the U.S. and Canada from Russia, providing a rare opportunity to re-establish a small felid population using known founder animals. Captive propagation of these wild-caught cats remains a high priority. However, anecdotal reports from several zoological institutions suggested the occurrence of excessive neonatal deaths in the offspring of these paired Pallas’ cats, presumably caused by infection with Toxoplasma gondii. In February 1999, a detailed questionnaire was sent to the five North American institutions (Birmingham Zoo, Cincinnati Zoo & Botanical Garden, Denver Zoological Gardens, Mountain View Farms Conservation & Breeding Center, Oklahoma City Zoological Park) that currently held breeding pairs of Pallas’ cats to investigate these reports. All five institutions responded within 2 months of survey distribution and the survey findings were compiled.

Between 1996 and 1998, these five institutions reported the birth of nine Pallas’ cat litters, comprising a total of 32 kittens (Table 1). Of these kittens, 23 (72%) were either stillborn or died within the first 16 weeks after birth. Of the stillbirths or neonatal deaths, 16 (70%) kittens were subjected to necropsy, six (26%) were eaten by the dam and one (4%) was not evaluated (Table 2). For the 16 necropsied kittens, 13 (81%) died due to toxoplasmosis, 1 (6%) due to sepsis, 1 (6%) due to disseminated intravascular coagulation and 1 (6%) to unknown causes. Kitten deaths attributed to confirmed toxoplasmosis were biphasic, with many deaths (38%) occurring at or near birth (one stillbirth, four neonatal deaths within 23 days of birth) and the remaining deaths (62%) occurring after 60 days (eight neonatal deaths between 62 and 112 days of birth).

Table 1. Breeding success and neonatal losses in
Pallas’ cats in North American institutions (1996–1998)

^aSB = stillbirth; NN = neonatal (birth to 16 weeks of age)

Table 2. Causes of neonatal deaths in Pallas’ cats in North American institutions (1996–1998)

^aSB = stillbirth; NN = neonatal (birth to 16 weeks of age)

Antibody titers against T. gondii were evaluated in 14 of the original wild-caught Pallas’ cats shortly after their importation into North America (Table 3). Of these cats, 11 (79%) tested positive for antibodies against T. gondii within 6 weeks of arrival from Russia. For some cats (pairings 2, 3, 6 and 7), an IgG-specific ELISA was used for testing, demonstrating high IgG titers (≥1:512 dilution) in seven of eight cats within 3 weeks of their arrival from Russia. Four of five institutions also reported the presence of anti-T. gondii antibodies in other cat species in their collection. However, none have observed any cases of confirmed toxoplasmosis as causes of stillbirths or neonatal death in any of these other species. At all five institutions, Pallas’ cats have access to dietary items potentially containing T. gondii tissue cysts. These potential dietary sources include whole prey items, such as baby/adult mice, chicks, and quail (five institutions), commercially available raw horse meat (four institutions), wild rodents and/or birds in outdoor exhibits (four institutions) and raw organ meat from chickens or cattle (one institution).

At four institutions, newborn kittens were treated with clindamycin (25–50 mg/kg BW, SID or BID PO) for suspected toxoplasmosis (Table 4). However, clindamycin treatment appeared to be ineffective in kittens showing any symptoms of toxoplasmosis before the initiation of therapy. All surviving kittens were generally asymptomatic for toxoplasmosis and were treated with clindamycin based on deaths or symptoms observed in siblings. It is possible that these surviving kittens never had active T. gondii infections.

Table 3. Anti-Toxoplasma antibody status of wild-caught Pallas’ cats

^aPeriod of time between arrival of Pallas’ cats at the North American institution (from Russia) and collection of blood samples for anti-T. gondii antibody testing

Table 4. Treatment of T. gondii-infected kittens

The findings from this survey indicate that Pallas’ cats are experiencing very high losses of newborn kittens due to toxoplasmosis, with two peaks in deaths: at or near birth (i.e., within 24 days) and near weaning (i.e., between 60 and 120 days of age). The early deaths are most likely due to in utero infection of fetuses with T. gondii. Most wild-caught Pallas’ cats have persistent antibody titers against T. gondii, reflecting previous exposure either in the wild or in captivity in Russia, and presumably indicating encysted T. gondii within their tissues. In contrast to domestic cats and all other nondomestic cats, maternal immune responses apparently are not protective during pregnancy in Pallas’ cats, allowing cyst reactivation and in utero infection to occur. Chronic captive stress in these wild-caught cats also may be a factor.

The later deaths (near weaning) may reflect delayed proliferation of T. gondii acquired in utero from the dam or newly acquired infection from tissue cysts ingested in the diet, both potentiated by decline of anti-T. gondii colostral antibodies and reduced access to any milk-derived antibodies. It is difficult to eliminate all potential exposure to T. gondii, especially if cats are maintained outdoors on relatively natural diets (raw meat, whole prey). Treatment of Pallas’ cat kittens with clindamycin after observation of clinical signs has a very poor prognosis.

At this time, options are limited for addressing in utero transmission and early deaths caused by toxoplasmosis. Hand-raising healthy kittens (either from shortly after birth or beginning at approximately 6–8 weeks of age) in a tightly controlled environment (no access to wild prey, T. gondii-free whole prey, cooked meat and/or processed diet) and/or prophylactic treatment with clindamycin beginning approximately 8–12 weeks of age are possible alternatives for reducing T. gondii-related mortality at later time points. However, diarrhea can be a problem with clindamycin treatment, and hydration must be monitored closely. Maturation of the kitten’s immune system after 4 months of age hopefully will provide improved immunologic responsiveness to subsequent T. gondii exposure (as in domestic cat kittens). Studies are being initiated to investigate immune responses of Pallas’ cats against T. gondii to gain a better understanding of the unusual etiology of toxoplasmosis in this species.

Acknowledgments

The assistance of the following individuals and institutions with this survey are very much appreciated: Dr. Mel Shaw, Birmingham Zoo; Dr. Mark Campbell, Cincinnati Zoo & Botanical Garden; Dr. David Kenny, Denver Zoological Gardens; Mr. Gordon Blankstein, Mountain View Farms Conservation & Breeding Center; and Dr. Michael Barrie, Oklahoma City Zoological Park.