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Besnoitiosis of the reproductive tract of a blue Duiker (Cephalophus monticola)
Veterinary Parasitology, 36 (1990) 157-163 Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands
157
Short C o m m u n i c a t i o n
B e s n o i t i o s i s of the R e p r o d u c t i v e T r a c t of a B l u e D u i k e r (Cephalophus monticola) G E O R G E L. FOLEY*, WAYNE I. A N D E R S O N and HOWARD S T E I N B E R G
Department of Veterinary Pathology, New York State College of Veterinary Medicine, Cornell University, Ithaca, New York 14853 (U.S.A.) (Accepted for publication 2 November 1989)
ABSTRACT Foley, G.L., Anderson, W.I. and Steinberg, H., 1990. Besnoitiosis of the reproductive tract of a Blue Duiker ( Cephalophus monticola ) . Vet Parasitol. , 36: 157-163. A mature male Blue Duiker that had been born in the United States was submitted for necropsy examination following a brief illness. On histologic examination of the reproductive tract several Besnoitia cysts were found in the epididymis, prostate and bulbourethral gland. The lack of an inflammatory response or any negative effect on fertility, based on histologic evaluation and breeding history, is in contrast with the severe orchitis, epididymitis and infertility of besnoitiosis in cattle. This is the first report of an autochthonous infection of Besnoitia in the United States as well as the first report of besnoitiosis in a Blue Duiker.
INTRODUCTION
Although the dermal lesions of besnoitiosis are the most well recognized, the reproductive lesions are potentially far more significant. Besnoitia cysts exhibit a genitotropism in a variety of ruminants including domestic cattle (Bigalke, 1967; Basson et al., 1970; Bargai et al., 1980; Kumi-Diaka et al., 1981; Nobel et al., 1981 ), Kudus (McCully et al., 1966), Blue Wildebeest (McCully et al., 1966), and goats (Cheema et al., 1979; Neuman et al., 1981), reindeer (Hadwen, 1922 ) and caribou (Hadwen, 1922; Wobeser, 1976 ). Cysts have been reported to cause small granulomas in the uterine endometrium of domestic cattle (Nobel et al., 1981; Perl et al., 19~ ~ however, their major reproductive significance is infertility in domestic bulls. ~ffected bulls have an orchitis and/ or epididymitis associated with protozoal c~ :ts in the testicle, epididymis, or pampiniform plexus (Pols, 1960). The resulting inflammation and parenchy*Author to whom correspondence should be addressed: 325 Veterinary Research Tower, Department of Pathology, NYSCVM, Cornell University, Ithaca, NY 14853, U.S.A.
0304-4017/90/$03.50
© 1990 Elsevier Science Publishers B.V.
158
G.L. FOLEY ET AL.
real destruction causes abnormal sperm morphology as well as decreased fertility. The Blue Duiker (Cephalophus monticola) is a small ruminant originating from South Africa. A male Duiker from a New York state zoo was submitted for necropsy following a brief period of illness prior to his death. Incidental histologic findings were several Besnoitia cysts within the genital tract and tongue musculature without any inflammatory or degenerative changes. This report is believed to be the first report of besnoitiosis in Blue Duikers. Histologic description of cysts, their reproductive significance and the possible origins of the infection will be discussed. MATERIALS AND METHODS The male Duiker was born in Pennsylvania in a herd of Blue Duikers kept for research purposes. The Duiker was one of a breeding pair sent to The Burnet Park Zoo (Syracuse, N Y ) and housed separately from other ruminants. He had sired three offspring during the 3 years at the zoo. Following a brief illness the Duiker died and was necropsied at the New York State College of Veterinary Medicine. All major organs were examined and representative samples, except the reproductive tract, were fixed in 10% buffered formalin. The entire reproductive tract was collected and fixed in Bouin's fixative. Tissues were paraffin embedded, sectioned at 4 gm and stained with hematoxylin and eosin. In a retrospective study of Blue Duikers, histologic sections of 37 animals necropsied at the Pennsylvania breeding colony were reviewed. Both sexes were represented as well as adults and neonates. Tissues per case varied widely and reproductive tissues were included in only three animals. RESULTS On gross examination, there was a fibrinous peritonitis, multiple hepatic abscesses and a small transmural ulcer in the reticulum. Corynebacterium pyogenes and Fusobacterium necrophorum were cultured from the liver lesions. The reproductive tract was grossly normal. On histologic examination of the reproductive tract, several large protozoal cysts were found within the parenchyma of the epididymis (Fig. 1 ), prostate and bulbourethral gland (Fig. 2). The cysts were round to oval with a thick (10-20/lm) eosinophilic outer capsule. Within the capsule, there were multiple, large host cell nuclei and a thin inner membrane containing the merozoites. The average size of the cysts was 1 2 0 × 1 2 8 / l m (range 80-170/~m). Parenchyma adjacent to the cysts was normal with no inflammatory cell infiltrate in any of the reproductive tissues examined. Epididymal ducts contained abundant spermatozoa with no morphologic lesions even when cysts were im-
BESNOITIOSISOF THE REPRODUCTIVETRACT
159
l Fig. 1. Besnoitia cyst in connective tissue adjacent to epididymal epithelium (E) with spermatozoa (S) in the lumen. Note the lack of inflammatory response to the cyst and multiple host nuclei (arrow). Bar = 30/tm. Hematoxylin and eosin.
Fig. 2. Section of bulbourethral gland and capsule with two Besnoitia cysts in the gland parenchyma without any host response. Bar--30/lm. Hematoxylin and eosin.
160
G.I,. FOLEYET AL.
Fig. 3. A single Besnoitia cyst distorting the overlying epididymal epithelium (E) without reaction or morphologic effect on the spermatozoa (S) within the lumen. Bar--30 ~m. Hematoxylin and eosin.
mediately adjacent to the epididymal epithelium (Fig. 3). While several cysts were located within the epididymis and accessory sex glands, no cysts were found in any of the multiple sections of testicular parenchyma examined. Seminiferous tubules were normal with adequate spermatogenesis. Two Besnoitia cysts were also seen within myofibers of the tongue with no evidence of inflammatory response. No other cysts were found in any of the other organs examined. Only a small section of skin was examined histologically without any evidence of protozoan cysts. Electron microscopy of cyst-containing tissue was considered, however individual cysts were too randomly scattered to justify further examination. Histologic sections of tissues were examined from the 37 Blue Duikers necropsied over the last 5 years from the Pennsylvania breeding facility. No Besnoitia cysts were found in any of the tissues examined. DISCUSSION
Besnoitia besnoiti infection is widespread in a variety of ruminants of South Africa (Levine et al., 1981) and is reported to have a cattle strain and an an-
B E S N O I T I O S I S OF T H E R E P R O D U C T I V E T R A C T
161
telope strain which are morphologically similar. The cattle strain causes more severe dermal and reproductive lesions in domestic ruminants (Bigalke et al., 1967; Basson et al., 1970), while the antelope strain has a tendency to form cysts in visceral organs such as the lung and abomasum (Basson et al., 1970; Cheema et al., 1979). The parasite has been experimentally transmitted through insect vectors and blood (Bigalke, 1967) but the natural life cycle probably requires a definitive host, which for some Besnoitia species is the domestic cat (Fayer, 1980; Levine et al., 1981). The most easily recognized clinical manifestation of besnoitiosis is the dermal lesions which can lead to a sclerodermalike condition (Pols, 1960; Levine, 1985). There are numerous reports on the reproductive effects of infertility and genitotropism of Besnoitia in a variety of species (McCully et al., 1966; Basson et al., 1970; Cheema et al., 1979; Bargai et al., 1980; Kumi-Diaka et al., 1981; Neuman et al., 1981; Nobel et al., 1981; Perl et al., 1981 ). This is believed to be the first report of besnoitiosis in a Blue Duiker, and specifically one born in the United States. The benign presence of Besnoitia cysts in the reproductive tract is in contrast with the lesions of orchitis and epididymitis seen in other ruminants such as domestic bulls (Bargai et al., 1980), kudus (McCully et al., 1966), and goats (Cheema et al., 1979). Three mechanisms of decreased fertility in bulls have been proposed and include a direct inflammatory effect, a vascular blockage effect and an indirect effect via elaboration of a toxic factor (Basson et al., 1970; Cheema et al., 1979; Kumi-Diaka et al., 1981 ). Some have proposed that the inflammatory response in domestic cattle occurs following degeneration of the cysts, others report finding viable, intact cysts with marked inflammation prior to any signs of degeneration (Basson et al., 1970). All the cysts in the Blue Duiker appeared intact and viable. The fertility of the Blue Duiker, based on reproductive history and histologic examination, was unaffected by the Besnoitia cysts. The size of Besnoitia cysts varies in different species: cattle (394 zm), wildebeests ( 567/~m ) and impalas (472/~m ) (Bigalke et al., 1967 ). Besnoitia cysts within the epididymis of goats averaged 132 X 185 ]tm (Cheema et al., 1979) while in the reindeer cysts sizes ranged from 100 to 450/~m (Hadwen, 1922). Basson et al. (1970) reported that the stage of infection also is a factor in cyst size. During acute bovine infections (Days 1-25 ), cysts achieve a size up to 100 /~m in diameter, in subacute infections (Days 26-71 ) cysts can be 100-300/~m in size and with chronicity ( > 71 days) cysts can get larger than 300/lm (Basson et al., 1970). Levine (1981) reports mature cysts in cattle range from 100300/~m in size. Cysts in the current infection ranged in size from the smallest 80 X 100 ~m to the largest of 170 X 140 #m. The smaller size of the cysts in the Blue Duiker may represent a smaller maximal size of the parasite in this particular host or conversely it may represent a subacute infection (Days 26-71 ). Reproductive lesions in domestic cattle are reported to begin prior to the stage of chronic
162
G.L. FOLEY ET AL.
infection (Basson et al., 1970; N e u m a n et al., 1981). Regardless as to whether this infection represents a chronic carrier state or an early infection, there was no evidence of an adverse effect on reproductive function or morphology. Another significant aspect of this case of besnoitiosis is that the animal was born in Pennsylvania and so must have acquired the infection either from other Blue Duikers in the breeding colony or from another animal at the zoo. Besnoitiosis is reported to be widespread in ruminants of South Africa, however the exact mode of transmission of the parasite is still not clear. The original Blue Duikers, imported from South Africa, are in permanent residence at the Pennsylvania breeding facility. Parasite transmission from one of the original imported Duikers is possible, however in reviewing histologic sections of tissues from 37 Duikers necropsied at the Pennsylvania facility over the last 5 years, no additional cases of besnoitiosis were found. This is not conclusive evidence that the infection did not originate from the Pennsylvania herd since only two cases contained reproductive tissues (testicle and epididymis) for retrospective examination. Species of Besnoitia found in the United States include Besnoitiajellisoni in kangaroo rats (Ernst et al., 1968), B. darlingi in opossums and lizards (Levine et al., 1981), and B. tarandi in caribou and reindeer from Alaska (Hadwen, 1922). No reports of besnoitiosis in Pennsylvania or New York were found. Infection of a ruminant with the n o n r u m i n a n t species of Besnoitia is unlikely since the various Besnoitia sp. are reported to be fairly species specific (Bigalke, 1968). The possibility that the Besnoitia infection originated from another zoo animal, such as caribou or another ruminant is feasible but cannot be confirmed. In summary, this is the first report of autochthonous besnoitiosis in a Blue Duiker in the United States. Besnoitia cysts were found in the epididymis, bulbourethral gland and prostate as well as within myofibers of the tongue. The cysts appeared viable and lacked any inflammatory host response. Based on reproductive history and histologic examination, Besnoitia cysts had no effect on reproduction of this animal. The potential for transmission of the parasite from infected ruminant carriers into domestic cattle in the United States would only be significant if bulls became infected and a pathogenic strain (B. besnoiti, cattle strain) was involved.
ACKNOWLEDGMENTS
The authors acknowledge Dr. M. Georgi for her generous help in parasite identification and review of the manuscript, and Dr. C. Wallace for submission of case material.
BESNOITIOSIS OF T H E REPRODUCTIVE TRACT
163
REFERENCES Bargai, U. and Nobel, T., 1980. Besnoitia besnoitii in bulls - Clinical, pathological and radiological observations. Refuah Vet., 37: 52. Basson, P.A., McCully, R.M. and Bigalke, R.D., 1970. Observations on the pathogenesis of bovine and antelope strains of Besnoitia besnoiti (Marotel, 1912) infections in cattle and rabbits. Onderstepoort J. Vet. Res., 37: 105-126. Bigalke, R.D., 1967. The artificial transmission ofBesnoitia besnoiti (Marotel, 1912) from chronically infected to susceptible cattle and rabbits. Onderstepoort J. Vet. Res., 34:303-316. Bigalke, R.D., 1968. New concepts on the epidemiological features of bovine besnoitiosis as determined by laboratory and field investigations. Onderstepoort J. Vet. Res., 35: 3-138. Bigalke, R.D., van Niekerk, J.W., Basson, P.A. and McCully, R.M., 1967. Studies on the relationship between Besnoitia of Blue Wildebeest and Impala, and Besnoitia besnoiti of cattle. Onderstepoort J. Vet. Res., 34: 7-28. Cheema, A.H. and Toofanian, F., 1979. Besnoitiosis in wild and domestic goats in Iran. Cornell Vet., 69: 159-168. Ernst, J.V., Chobotar, B., Oaks, E.C. and Hammond, D.M., 1968. Besnoitia jellisoni (Sporozoa: Toxoplasmea) in rodents from Utah and California. J. Parasitol, 54: 545-549. Fayer, R., 1980. Epidemiology of protozoan infections: The coccidia. Vet. Parasitol., 6: 75-103. Hadwen, S., 1922. Cyst-forming protozoa in reindeer and caribou, and a sarcosporidian parasite of the seal (Phoca richardi). J. Am. Vet. Med. Assoc., 61: 374-382. Kumi-Diaka, J., Wilson, S., Sanusi, A., Njoku, C.E. and Osori, D.I.K., 1981. Bovine besnoitiosis and its effect on the male reproductive system. Therio, 16: 523-530. Levine, N.D., 1985. Veterinary Protozoology. Iowa State University Press, Ames, pp. 256 260. Levine, N.D. and Ivens, V., 1981. The Coccidian Parasites (Protozoa, Apicomplexa) of Carnivores. Illinois Biology Monograph No. 51, University of Illinois Press, Urbana, pp. 142-154. McCully, R.M., Basson, P.A., van Niekerk, J.W. and Bigalke, R.D., 1966. Observations on Besnoitia cysts in the cardiovascular system of some wild antelopes and domestic cattle. Onderstepoort J. Vet. Res., 33: 245-276. Neuman, M. and Nobel, T.A., 1981. Observations on the pathology of Besnoitiosis in experimental animals. Zbl. Vet. Med. B, 28: 345-354. Nobel, T.A., Klopfer, U., Perl, S., Nyska, A., Neuman, M. and Brenner, G., 1981. Histopathology of genital Besnoitiosis of cows in Israel. Vet. Parasitol., 8: 271-276. Perl, S., Klopfer, U., Jacobson, B. and Brener, G., 1981. Besnoitia cysts in the adrenal gland of a cow. Vet. Quart. 3: 148-149. Pols, J.W., 1960. Studies on bovine besnoitiosis with special reference to the aetiology. Onderstepoort J. Vet. Res., 28: 265-355. Wobeser, G., 1976. Besnoitiosis in a Woodland Caribou. J. Wildl. Dis., 12: 566-571.
157
Short C o m m u n i c a t i o n
B e s n o i t i o s i s of the R e p r o d u c t i v e T r a c t of a B l u e D u i k e r (Cephalophus monticola) G E O R G E L. FOLEY*, WAYNE I. A N D E R S O N and HOWARD S T E I N B E R G
Department of Veterinary Pathology, New York State College of Veterinary Medicine, Cornell University, Ithaca, New York 14853 (U.S.A.) (Accepted for publication 2 November 1989)
ABSTRACT Foley, G.L., Anderson, W.I. and Steinberg, H., 1990. Besnoitiosis of the reproductive tract of a Blue Duiker ( Cephalophus monticola ) . Vet Parasitol. , 36: 157-163. A mature male Blue Duiker that had been born in the United States was submitted for necropsy examination following a brief illness. On histologic examination of the reproductive tract several Besnoitia cysts were found in the epididymis, prostate and bulbourethral gland. The lack of an inflammatory response or any negative effect on fertility, based on histologic evaluation and breeding history, is in contrast with the severe orchitis, epididymitis and infertility of besnoitiosis in cattle. This is the first report of an autochthonous infection of Besnoitia in the United States as well as the first report of besnoitiosis in a Blue Duiker.
INTRODUCTION
Although the dermal lesions of besnoitiosis are the most well recognized, the reproductive lesions are potentially far more significant. Besnoitia cysts exhibit a genitotropism in a variety of ruminants including domestic cattle (Bigalke, 1967; Basson et al., 1970; Bargai et al., 1980; Kumi-Diaka et al., 1981; Nobel et al., 1981 ), Kudus (McCully et al., 1966), Blue Wildebeest (McCully et al., 1966), and goats (Cheema et al., 1979; Neuman et al., 1981), reindeer (Hadwen, 1922 ) and caribou (Hadwen, 1922; Wobeser, 1976 ). Cysts have been reported to cause small granulomas in the uterine endometrium of domestic cattle (Nobel et al., 1981; Perl et al., 19~ ~ however, their major reproductive significance is infertility in domestic bulls. ~ffected bulls have an orchitis and/ or epididymitis associated with protozoal c~ :ts in the testicle, epididymis, or pampiniform plexus (Pols, 1960). The resulting inflammation and parenchy*Author to whom correspondence should be addressed: 325 Veterinary Research Tower, Department of Pathology, NYSCVM, Cornell University, Ithaca, NY 14853, U.S.A.
0304-4017/90/$03.50
© 1990 Elsevier Science Publishers B.V.
158
G.L. FOLEY ET AL.
real destruction causes abnormal sperm morphology as well as decreased fertility. The Blue Duiker (Cephalophus monticola) is a small ruminant originating from South Africa. A male Duiker from a New York state zoo was submitted for necropsy following a brief period of illness prior to his death. Incidental histologic findings were several Besnoitia cysts within the genital tract and tongue musculature without any inflammatory or degenerative changes. This report is believed to be the first report of besnoitiosis in Blue Duikers. Histologic description of cysts, their reproductive significance and the possible origins of the infection will be discussed. MATERIALS AND METHODS The male Duiker was born in Pennsylvania in a herd of Blue Duikers kept for research purposes. The Duiker was one of a breeding pair sent to The Burnet Park Zoo (Syracuse, N Y ) and housed separately from other ruminants. He had sired three offspring during the 3 years at the zoo. Following a brief illness the Duiker died and was necropsied at the New York State College of Veterinary Medicine. All major organs were examined and representative samples, except the reproductive tract, were fixed in 10% buffered formalin. The entire reproductive tract was collected and fixed in Bouin's fixative. Tissues were paraffin embedded, sectioned at 4 gm and stained with hematoxylin and eosin. In a retrospective study of Blue Duikers, histologic sections of 37 animals necropsied at the Pennsylvania breeding colony were reviewed. Both sexes were represented as well as adults and neonates. Tissues per case varied widely and reproductive tissues were included in only three animals. RESULTS On gross examination, there was a fibrinous peritonitis, multiple hepatic abscesses and a small transmural ulcer in the reticulum. Corynebacterium pyogenes and Fusobacterium necrophorum were cultured from the liver lesions. The reproductive tract was grossly normal. On histologic examination of the reproductive tract, several large protozoal cysts were found within the parenchyma of the epididymis (Fig. 1 ), prostate and bulbourethral gland (Fig. 2). The cysts were round to oval with a thick (10-20/lm) eosinophilic outer capsule. Within the capsule, there were multiple, large host cell nuclei and a thin inner membrane containing the merozoites. The average size of the cysts was 1 2 0 × 1 2 8 / l m (range 80-170/~m). Parenchyma adjacent to the cysts was normal with no inflammatory cell infiltrate in any of the reproductive tissues examined. Epididymal ducts contained abundant spermatozoa with no morphologic lesions even when cysts were im-
BESNOITIOSISOF THE REPRODUCTIVETRACT
159
l Fig. 1. Besnoitia cyst in connective tissue adjacent to epididymal epithelium (E) with spermatozoa (S) in the lumen. Note the lack of inflammatory response to the cyst and multiple host nuclei (arrow). Bar = 30/tm. Hematoxylin and eosin.
Fig. 2. Section of bulbourethral gland and capsule with two Besnoitia cysts in the gland parenchyma without any host response. Bar--30/lm. Hematoxylin and eosin.
160
G.I,. FOLEYET AL.
Fig. 3. A single Besnoitia cyst distorting the overlying epididymal epithelium (E) without reaction or morphologic effect on the spermatozoa (S) within the lumen. Bar--30 ~m. Hematoxylin and eosin.
mediately adjacent to the epididymal epithelium (Fig. 3). While several cysts were located within the epididymis and accessory sex glands, no cysts were found in any of the multiple sections of testicular parenchyma examined. Seminiferous tubules were normal with adequate spermatogenesis. Two Besnoitia cysts were also seen within myofibers of the tongue with no evidence of inflammatory response. No other cysts were found in any of the other organs examined. Only a small section of skin was examined histologically without any evidence of protozoan cysts. Electron microscopy of cyst-containing tissue was considered, however individual cysts were too randomly scattered to justify further examination. Histologic sections of tissues were examined from the 37 Blue Duikers necropsied over the last 5 years from the Pennsylvania breeding facility. No Besnoitia cysts were found in any of the tissues examined. DISCUSSION
Besnoitia besnoiti infection is widespread in a variety of ruminants of South Africa (Levine et al., 1981) and is reported to have a cattle strain and an an-
B E S N O I T I O S I S OF T H E R E P R O D U C T I V E T R A C T
161
telope strain which are morphologically similar. The cattle strain causes more severe dermal and reproductive lesions in domestic ruminants (Bigalke et al., 1967; Basson et al., 1970), while the antelope strain has a tendency to form cysts in visceral organs such as the lung and abomasum (Basson et al., 1970; Cheema et al., 1979). The parasite has been experimentally transmitted through insect vectors and blood (Bigalke, 1967) but the natural life cycle probably requires a definitive host, which for some Besnoitia species is the domestic cat (Fayer, 1980; Levine et al., 1981). The most easily recognized clinical manifestation of besnoitiosis is the dermal lesions which can lead to a sclerodermalike condition (Pols, 1960; Levine, 1985). There are numerous reports on the reproductive effects of infertility and genitotropism of Besnoitia in a variety of species (McCully et al., 1966; Basson et al., 1970; Cheema et al., 1979; Bargai et al., 1980; Kumi-Diaka et al., 1981; Neuman et al., 1981; Nobel et al., 1981; Perl et al., 1981 ). This is believed to be the first report of besnoitiosis in a Blue Duiker, and specifically one born in the United States. The benign presence of Besnoitia cysts in the reproductive tract is in contrast with the lesions of orchitis and epididymitis seen in other ruminants such as domestic bulls (Bargai et al., 1980), kudus (McCully et al., 1966), and goats (Cheema et al., 1979). Three mechanisms of decreased fertility in bulls have been proposed and include a direct inflammatory effect, a vascular blockage effect and an indirect effect via elaboration of a toxic factor (Basson et al., 1970; Cheema et al., 1979; Kumi-Diaka et al., 1981 ). Some have proposed that the inflammatory response in domestic cattle occurs following degeneration of the cysts, others report finding viable, intact cysts with marked inflammation prior to any signs of degeneration (Basson et al., 1970). All the cysts in the Blue Duiker appeared intact and viable. The fertility of the Blue Duiker, based on reproductive history and histologic examination, was unaffected by the Besnoitia cysts. The size of Besnoitia cysts varies in different species: cattle (394 zm), wildebeests ( 567/~m ) and impalas (472/~m ) (Bigalke et al., 1967 ). Besnoitia cysts within the epididymis of goats averaged 132 X 185 ]tm (Cheema et al., 1979) while in the reindeer cysts sizes ranged from 100 to 450/~m (Hadwen, 1922). Basson et al. (1970) reported that the stage of infection also is a factor in cyst size. During acute bovine infections (Days 1-25 ), cysts achieve a size up to 100 /~m in diameter, in subacute infections (Days 26-71 ) cysts can be 100-300/~m in size and with chronicity ( > 71 days) cysts can get larger than 300/lm (Basson et al., 1970). Levine (1981) reports mature cysts in cattle range from 100300/~m in size. Cysts in the current infection ranged in size from the smallest 80 X 100 ~m to the largest of 170 X 140 #m. The smaller size of the cysts in the Blue Duiker may represent a smaller maximal size of the parasite in this particular host or conversely it may represent a subacute infection (Days 26-71 ). Reproductive lesions in domestic cattle are reported to begin prior to the stage of chronic
162
G.L. FOLEY ET AL.
infection (Basson et al., 1970; N e u m a n et al., 1981). Regardless as to whether this infection represents a chronic carrier state or an early infection, there was no evidence of an adverse effect on reproductive function or morphology. Another significant aspect of this case of besnoitiosis is that the animal was born in Pennsylvania and so must have acquired the infection either from other Blue Duikers in the breeding colony or from another animal at the zoo. Besnoitiosis is reported to be widespread in ruminants of South Africa, however the exact mode of transmission of the parasite is still not clear. The original Blue Duikers, imported from South Africa, are in permanent residence at the Pennsylvania breeding facility. Parasite transmission from one of the original imported Duikers is possible, however in reviewing histologic sections of tissues from 37 Duikers necropsied at the Pennsylvania facility over the last 5 years, no additional cases of besnoitiosis were found. This is not conclusive evidence that the infection did not originate from the Pennsylvania herd since only two cases contained reproductive tissues (testicle and epididymis) for retrospective examination. Species of Besnoitia found in the United States include Besnoitiajellisoni in kangaroo rats (Ernst et al., 1968), B. darlingi in opossums and lizards (Levine et al., 1981), and B. tarandi in caribou and reindeer from Alaska (Hadwen, 1922). No reports of besnoitiosis in Pennsylvania or New York were found. Infection of a ruminant with the n o n r u m i n a n t species of Besnoitia is unlikely since the various Besnoitia sp. are reported to be fairly species specific (Bigalke, 1968). The possibility that the Besnoitia infection originated from another zoo animal, such as caribou or another ruminant is feasible but cannot be confirmed. In summary, this is the first report of autochthonous besnoitiosis in a Blue Duiker in the United States. Besnoitia cysts were found in the epididymis, bulbourethral gland and prostate as well as within myofibers of the tongue. The cysts appeared viable and lacked any inflammatory host response. Based on reproductive history and histologic examination, Besnoitia cysts had no effect on reproduction of this animal. The potential for transmission of the parasite from infected ruminant carriers into domestic cattle in the United States would only be significant if bulls became infected and a pathogenic strain (B. besnoiti, cattle strain) was involved.
ACKNOWLEDGMENTS
The authors acknowledge Dr. M. Georgi for her generous help in parasite identification and review of the manuscript, and Dr. C. Wallace for submission of case material.
BESNOITIOSIS OF T H E REPRODUCTIVE TRACT
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REFERENCES Bargai, U. and Nobel, T., 1980. Besnoitia besnoitii in bulls - Clinical, pathological and radiological observations. Refuah Vet., 37: 52. Basson, P.A., McCully, R.M. and Bigalke, R.D., 1970. Observations on the pathogenesis of bovine and antelope strains of Besnoitia besnoiti (Marotel, 1912) infections in cattle and rabbits. Onderstepoort J. Vet. Res., 37: 105-126. Bigalke, R.D., 1967. The artificial transmission ofBesnoitia besnoiti (Marotel, 1912) from chronically infected to susceptible cattle and rabbits. Onderstepoort J. Vet. Res., 34:303-316. Bigalke, R.D., 1968. New concepts on the epidemiological features of bovine besnoitiosis as determined by laboratory and field investigations. Onderstepoort J. Vet. Res., 35: 3-138. Bigalke, R.D., van Niekerk, J.W., Basson, P.A. and McCully, R.M., 1967. Studies on the relationship between Besnoitia of Blue Wildebeest and Impala, and Besnoitia besnoiti of cattle. Onderstepoort J. Vet. Res., 34: 7-28. Cheema, A.H. and Toofanian, F., 1979. Besnoitiosis in wild and domestic goats in Iran. Cornell Vet., 69: 159-168. Ernst, J.V., Chobotar, B., Oaks, E.C. and Hammond, D.M., 1968. Besnoitia jellisoni (Sporozoa: Toxoplasmea) in rodents from Utah and California. J. Parasitol, 54: 545-549. Fayer, R., 1980. Epidemiology of protozoan infections: The coccidia. Vet. Parasitol., 6: 75-103. Hadwen, S., 1922. Cyst-forming protozoa in reindeer and caribou, and a sarcosporidian parasite of the seal (Phoca richardi). J. Am. Vet. Med. Assoc., 61: 374-382. Kumi-Diaka, J., Wilson, S., Sanusi, A., Njoku, C.E. and Osori, D.I.K., 1981. Bovine besnoitiosis and its effect on the male reproductive system. Therio, 16: 523-530. Levine, N.D., 1985. Veterinary Protozoology. Iowa State University Press, Ames, pp. 256 260. Levine, N.D. and Ivens, V., 1981. The Coccidian Parasites (Protozoa, Apicomplexa) of Carnivores. Illinois Biology Monograph No. 51, University of Illinois Press, Urbana, pp. 142-154. McCully, R.M., Basson, P.A., van Niekerk, J.W. and Bigalke, R.D., 1966. Observations on Besnoitia cysts in the cardiovascular system of some wild antelopes and domestic cattle. Onderstepoort J. Vet. Res., 33: 245-276. Neuman, M. and Nobel, T.A., 1981. Observations on the pathology of Besnoitiosis in experimental animals. Zbl. Vet. Med. B, 28: 345-354. Nobel, T.A., Klopfer, U., Perl, S., Nyska, A., Neuman, M. and Brenner, G., 1981. Histopathology of genital Besnoitiosis of cows in Israel. Vet. Parasitol., 8: 271-276. Perl, S., Klopfer, U., Jacobson, B. and Brener, G., 1981. Besnoitia cysts in the adrenal gland of a cow. Vet. Quart. 3: 148-149. Pols, J.W., 1960. Studies on bovine besnoitiosis with special reference to the aetiology. Onderstepoort J. Vet. Res., 28: 265-355. Wobeser, G., 1976. Besnoitiosis in a Woodland Caribou. J. Wildl. Dis., 12: 566-571.