A fatal infection in a bengal tiger resembling cytauxzoonosis in domestic cats

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<ul><li><p>J. Comp. Path. 1996 Vol. 114, 439-444 </p><p>SHORT PAPER </p><p>A Fatal Infection in a Bengal Tiger Resembling Cytauxzoonosis in Domestic Cats </p><p>W. Jakob and H.-H. Wesemeier </p><p>Institute for Zoo Biology and 14qldlife Research, Alfred-Kowalke-Str. 17, 10315 Berlin, Germany </p><p>Summary A young Bengal tiger born and kept in a German zoo had died of an unknown protozoal infection in 1984. Retrospective histological and electron microscopical examination of the organs showed the changes to be identical with those of cytauxzoonosis in domestic cats. This is the first report of fatal cytauxzoonosis in a tiger. 9 1996 W.B. Saunders Company Limited </p><p>Cytauxzoonosis is a fatal disease in domestic cats caused by a protozoan parasite, Cytauxzoonfelis (subphylum Apicomplexa, order Piroplasmida, family Theileriidae). Species of the family Theileriidae are characterized by a schizo- gonous tissue phase and an intraerythrocytic stage of development. Theileria spp. are known to form schizonts within lymphocytes and lymph9 The genus Cytauxzoon was established for those species which have the schizogonous tissue phase within cells of the monocyte-phagocyte system. Cytauxzoonosis was first described by Neitz and Thomas (1948) in the African grey duiker (Sylvicapra grimmia). Cytauxzoon spp. have since been identified in other African ungulates such as the kudu (Neitz, 1957), eland (Brocklesby, 1962), giraffe (McCully et al., 1970), roan and sable antelope (Wilson et al., 1974) and tsessebe (Jardine, 1992). </p><p>The first report of a cytauxzoonosis-like disease in the domestic cat came from the state of Missouri in the United States (Wagner, 1976). Since then, further sporadic cases of fatal cytauxzoonosis in cats have been recognized in several Midwestern and Southern states (Wightman et al., 1977; Hauck, 1982; Glenn and Stair, 1984; Hoover et al., 1994). In addition, Glenn et al. (1982, 1983), Kier et al. (1982a,b) and Blouin et al. (1984) demonstrated a Cytauxzoon- like organism in the erythrocytes of apparently healthy bobcats (Lynx rufus); the organism could be transmitted to cats. Free-living bobcats are now believed to be the definitive host and natural reservoir for this parasite, domestic cats being an accidental or dead-end host (Kier and Wagner, 1987). The Florida panther (Felix concolor coryi) may be another natural host for C. felis (Butt et al., 1991). </p><p>To the best of our knowledge, fatal cases of feline cytauxzoonosis have only been reported in domestic cats (naturally or experimentally infected) and in one Florida bobcat after experimental infection (Kier el al., 1982b). This paper </p><p>0021-9975/96/040439 + 06 $12.00/0 9 1996 W.B. Saunders Company Limited </p></li><li><p>440 W. Jakob and H . -H . Wesemeier </p><p>Fig. 1. </p><p>Fig. 2. </p><p>Numerous mononuclear macrophages with schizonts comparable with those of Cytauxzoonfelis m a venous blood vessel of a lymph node. HE. x 300. </p><p>Schizont-laden macrophages at higher magnification. The macrophages adhering to the inner surface of the blood vessel contain immature developmental stages of the parasite. The cytoplasm of the centrally located dark cell is filled with numerous merozoites. HE. x 750. </p><p>reports a fatal case of a cytauxzoonosis-like disease in a Bengal tiger. It is the first report of this protozoal infection in a tiger. </p><p>A female Bengal tiger (Panthera tigris) born in a German zoo in 1984 suddenly fell ill at the age of 18 weeks, the main clinical symptoms being anorexia, lethargy and dyspnoea. Auscultation and radiography indicated acute pneu- monia, and the animal died a few hours after the commencement of antibiotic treatment. A twin brother of this animal, which had lived in the same enclosure, remained unaffected and grew normally to adulthood. </p><p>Post-mortem examination showed that the tiger was in good nutritional condition. The lungs were oedematous and heavily congested, with diffuse petechial haemorrhages on the serosal surfaces and within the interstitium. The pleural cavity contained a yellowish fluid. All visible lymph nodes of the body were enlarged, congested and haemorrhagic. The spleen was also enlarged and congested, and the liver showed slightly rounded edges and a mottled appearance. </p><p>Tissue samples from several organs, fixed in 10% formalin and embedded in paraffin wax, as well as tissue sections stained with haematoxylin and eosin (HE), were still available. For electron microscopy, tissue samples of liver, </p></li><li><p>Cytauxzoonosis in a T iger 441 </p><p>Fig. 3. A macrophage with a large multilobular schizont (S). The host cell nucleus (N) has been displaced to the ceil periphery. EM. x 3000. </p><p>Fig. 4. A macrophage in a liver vein containing many mature merozoites characterized by a distinct nucleus. The host cell nucleus (N) is damaged. EM. x 1395. Inset: Two merozoites at higher magnification. Note the distinct osmiophilic nucleus and the paler vacuolated cytoplasm, EM. x 13 200. </p><p>lymph node and small intestine embedded in paraffin wax were dewaxed, post-fixed or precontrasted in 2 % OsO4 solution, and embedded in Epon 812. Semithin and ultrathin sections were cut. The ultrathin sections were examined with a Zeiss EM 902 A electron microscope. </p><p>Histologically, the most characteristic lesion was the accumulation of varying numbers of mononuclear phagocytes in the blood vessels of all organs ex- amined. These enlarged cells were roundish or irregular in shape and showed a large pale nucleus with a prominent nucleolus. The cytoplasm contained the parasite in various stages of development. In HE-stained tissue sections, the majority of the cells showed early stages in the form of granular, reticulated or finely vacuolated structures within the cytoplasm (Fig. 1). At higher mag- nification, many round vesicular structures containing one or more distinct basophilic dots were seen (Fig. 2). Other macrophages contained more ad- vanced stages in the form of clearly nucleated macroschizonts. A small proportion of the macrophages displayed numerous round basophilic granular bodies, probably merozoites, which occupied the whole cytoplasm around the nucleus (Fig. 2). The largest numbers of these parasitized mononuclear macrophages were found in the vessels of lymph nodes and spleen, where they also occurred in the sinusoids and in the germinal centres of the lymphoid nodules. Protozoa-laden macrophages were also present in the lumina of veins, venules and capillaries of the lung, liver, kidney, heart, intestines, brain, leptomeninx and bone marrow. The cells partly adhered to the inner surface of the large and medium-sized blood vessels or floated freely in the blood </p></li><li><p>442 W. Jakob and H.-H. Wesemeier </p><p>Fig. 5. </p><p>Fig. 6. </p><p>r ..... ' ! </p><p>6 </p><p>An intraerythrocytic form with resemblance to a merozoite in a submucosal vein of the small intestine. The unipolar nucleus (N), vacuoles and free ribosomes are visible. EM. x 23 100. </p><p>A parasitic form in another erythrocyte indistinctly showing ribosomes, vacuoles and chromatin masses. EM. x 19 200. </p><p>plasma. In some veins or venules of the lymph nodes, spleen and lung these macrophages were so numerous and tightly packed that they seemed to occlude the vascular lumina. In association with these vascular changes, scattered focal haemorrhages were observed, mainly in the brain and lung. In the latter organ a severe oedema was also found. </p><p>Electron microscopical examination showed various parasitic stages in the cytoplasm of the intravascular mononuclear macrophages and in some erythrocytes of all organs examined. In the cytoplasm of the large macrophages attached to the endothelium of veins and venules, multilobular schizonts occurred, each surrounded by a distinct single membrane. The internal constituents of these immature schizonts were not clearly discernible (Fig. 3). In cells filled with large schizonts, the host cell nucleus was often displaced to the cell periphery. Later stages of schizogony were characterized by the development of merozoites. These structures accumulated in high numbers in the host cell cytoplasm (Fig. 4). The merozoites were round to ovoid in shape, about 1 1"6 gm in diameter, and showed a distinct nucleus. The cytoplasm was vacuolated and surrounded by a double membrane (Fig. 4; inset). Protozoan parasites were also found in some erythrocytes, which usually contained one (occasionally two or three) round to oval organisms. These </p></li><li><p>Cytauxzoonosis in a Tiger 443 </p><p>parasites, 1 1.7 gm in diameter, usually showed a poorly to well defined, sometimes unipolar nucleus and a more or less distinct pale grey cytoplasm (Figs 5 and 6). </p><p>The gross and histological findings in the Bengal tiger were consistent with those reported in cases of spontaneous cytauxzoonosis in domestic cats. Post- mortem findings such as congestion and oedema of the lungs, splenomegaly and enlarged and haemorrhagic lymph nodes are also common lesions of naturally occurring (Kier and Wagner, 1987) and experimentally induced (Kier et al., 1987) cytauxzoonosis in the domestic cat. Ultrastructurally, the protozoal tissue stages within the cytoplasm of large mononuclear phagocytes and the piroplasm-like organisms within erythrocytes were identical with those reported in experimentally infected domestic cats (Simpson et al., 1985a,b; Kier et al., 1987; Butt et al., 1991). From all these changes we conclude that the Bengal tiger died of acute cytauxzoonosis. </p><p>To our knowledge, cytauxzoonosis has not been reported in domestic cats in Europe, and no fatal case has previously been reported in any feline species in zoological collections. </p><p>The question now arises as to the source of this infection and the mode of transmission. It has been shown under experimental conditions that C. felis is transmissible from bobcats to domestic cats by the American dog tick, Derma- centor variabilis (Blouin et al., 1984), and arthropods are believed to play an important role in the natural transmission of the parasite from the bobcat (the suggested definitive host) to the domestic cat. No infestation with ticks was noticed in the tiger. It should be noted, however, that about 14 months before the tiger's death three young bobcats directly imported from the United States had been introduced into the zoo. Since it has been shown experimentally (Kier et al., 1982b) that parasitaemia can persist in bobcats for more than 4 years, transmission may have occurred. Unfortunately, however, the blood of the three bobcats was not examined for parasites and the origin of the infection therefore remains unknown. </p><p>References </p><p>Blouin, E. F., Kocan, A. A., Glenn, B. L., Kocan, K. M. and Hair, J. A. (1984). Transmission of Cytauxzoon felis Kier, 1979 from bobcats, Fells rufus (Schreber), to domestic cats by Dermacentor variabilis (Say). Journal of Wildlife Diseases, 20, 241-242. </p><p>Brocklesby, D. M. (1962). Cytauxzoon taurotragi, Martin and Brocklesby, 1960, a piroplasm of the eland (Taurotragus oryx pattersonianus Lydekker, 1906). Research in Veterinary Science, 3, 334-344. </p><p>Butt, M. T., Bowman, D., Barr, M. C. and Roelke, M. E. (1991). Iatrogenic transmission of Cytauxzoon fells from a Florida panther (Felis concolor coryi) to a domestic cat. Journal of Wildlife Diseases, 27, 342 347. </p><p>Glenn, B. L., Kocan, A. A. and Blouin, E. F. (1983). Cytauxzoonosis in bobcats. Journal of the American Veterinary Medical Association, 183, 1155 1158. </p><p>Glenn, B. L., Rolley, R. E. and Kocan, A. A. (1982). Cytauxzoon-like piroplasms in erythrocytes of wild-trapped bobcats in Oklahoma. Journal of the American Veterinary Medical Association, 181, 1251 1253. </p><p>Glenn, B. L. and Stair, E. L. (1984). Cytauxzoonosis in domestic cats: report of two </p></li><li><p>444 W. Jakob and H.-H. Wesemeier </p><p>cases in Oklahoma, with a review and discussion of the disease. Journal of the American Veterinary Medical Association, 184, 822-825. </p><p>Hauck, W. N. (1982). Cytauxzoonosis in a native Louisiana cat. Journal of the American Veterinary Medical Association, 180, 1472 1474. </p><p>Hoover, J. P., Walker, D. B. and Hedges, J. D. (1994). Cytauxzoonosis in cats: eight cases (1985 1992). Journal of the American Veterinary Medical Association, 205, 455 460. </p><p>Jardine, J. E. (1992). The pathology of cytauxzoonosis in a tsessebe (Damaliscus lunatus). journal of the South African Veterinary Association, 63, 49-5 l. </p><p>Kier, A. B. and Wagner,J. E. (1987). Cytauxzoonosis. In: Diseases of the Cat: Medicine and Surgery, J. Holzworth, Ed., W. B. Saunders Company, Philadelphia, pp. 391 393. </p><p>Kier, A. B., Wagner, J. E. and Kinden, D. A. (1987). The pathology of experimental cytauxzoonosis. Journal of Comparative Pathology, 97, 415-432. </p><p>Kier, A. B., Wagner, J. E. and Morehouse, L. G. (1982a). Experimental transmission of Cytauxzoon felis from bobcats (Lynx rufus) to domestic cats (Felis domesticus). American Journal of Veterinary Research, 43, 97 101. </p><p>Kier, A. B., Wightman, S. R. and Wagner, J. E. (1982b). Interspecies transmission of Cytauxzoon felis. American Journal of Veterinary Research, 43, 102 105. </p><p>McCully, R. M., Keep, M. E. and Basson, P. A. (1970). Cytauxzoonosis in a giraffe, Giraffa cameleopardalis (Linnaeus, 1758) in Zululand. Onderstepoort Journal of Veterinary Research, 37, 7 10. </p><p>Neitz, W. O. (1957). Theileriosis, gonderiosis and cytauxzoonosis. A review. Onder- stepoort Journal of Veterinary Research, 27, 275 430. </p><p>Neitz, W. O. and Thomas, A. D. (1948). Cytauxzoon sylvicaprae gen. nov., spec. nov., a protozoan responsible for a hitherto undescribed disease in the duiker Sylvicapra grimmia (Linn@ Onderstepoort Journal of Veterinary Science and Animal Industry, 23, 63-76. </p><p>Simpson, C. F., Harvey, J. W. and Carlisle, J. W. (1985a). Ultrastructure of the intraerythrocytic stage of Cytauxzoon felis. American Journal of Veterinary Research, 46, 1178 1180. </p><p>Simpson, C. F., Harvey, J. W., Lawman, M. J. P., Murray, J., Kocan, A. A. and Carlisle, J. W. (1985b). Ultrastructure of schizonts in the liver of cats with experimentally induced cytauxzoonosis. American Journal of Veterinary Research, 46, 384-390. </p><p>Wagner, J. E. (1976). A fatal cytauxzoonosis-like disease in cats. Journal of the American Veterinary Medical Association, 168, 585-588. </p><p>Wightman, S. R., Kier, A. B. and Wagner, J. E. (1977). Feline cytauxzoonosis: clinical features of a newly described blood parasite disease. Feline Practice, 7, 23-26. </p><p>Wilson, D. E., Bartsch, R. C., Bigalke, R. D. and Thomas, S. E. (1974). Observations on mortality rates and disease in roan and sable antelope on nature reserves in the Transvaal. Journal of the South African W~ldl~ Management Association, 4, 203 206. </p><p>f Received, October 9th, 1995 1 Accepted, December 4th, 1995J </p></li></ul>

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