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Spontaneous external endometriosis in a De Brazza's monkey
J. Comp.
Path.
1989 Vol.
101
Spontaneous
External De Brazza’s
A. A. Binhazim*,
Endometriosis Monkey
R. P. Tarara
and
in a
M. A. Sulemant
Institute of Primate Research, National Museums of Kenya, Box 24481, Karen, Kenya
Summary A spontaneous case of external endometriosis in a 22-year-old female De Brazza’s monkey is described. During diagnostic laparotomy, peritoneal adhesions of the uterus to the urinary bladder, ovaries and abdominal wall were seen. A surgical biopsy of soft tissue attached to the ventral surface of the uterus was examined histologically and consisted of endometrial glands and stroma. These findings were compatible with a diagnosis of endometriosis. Iihroduction The De Brazza’s monkey (Cercopithecus neglectus) in Kenya is estimated to number slightly more than 100 and is considered an endangered species by primate conservationists. This forest guenon faces almost certain extinction unless conservation attempts are soon implemented. The pressures now facing the population of this non-human primate include loss of habitat, reproductive isolation and a decline in numbers as the result of being killed as a food source or as agricultural pests (Brennan, 1985). Spontaneous endometriosis has been reported in various non-human primate species (Merrill, 1968; McCann and Myers, 1970; DiGiacomo, Hooks, Sulima, Gibbs and Gajdusek, 1977; Cary, Peter and Schiffer, 1982; Dore and Lagace, 1985). Most reported cases of endometriosis have involved rhesus monkeys (Macaca mulatta). The condition has been induced surgically in rhesus as well as in cynomolgus monkeys (M. fascicularis) (MacKenzie and Casey, 1975; Schenken, Asch, Williams and Hodgen, 1984). Moreover, the disease in rhesus monkeys is reported to be much more severe than in other species of monkeys and often progresses irreversibly to death (McClure, Ridley and Graham, 197 1; MacKenzie, Splitter and Valerio, 1972). In women, the disease is a relatively common occurrence, and histologically proved endometriosis was found in 33 per cent of patients undergoing surgical assessment of infertility (Robbins, Cotran and Kumar, 1984). Therefore, non-human primates have been suggested as animal models of the disease. This paper describes spontaneous endometriosis in a De Brazza’s monkey.
*Present address: The University Athens, Georgia, 30602, U.S.A. 0022-9975/89/08047
of Georgia, College t Requests for reprints
I+ 04 $03.00/O
of Veterinary Medicine, Department should be sent to this address. 0
1989 Academic
of Pathology, Press Limited
472
A. A. Binhazim
et al.
Case Report
A 22-year-old female De Brazza’s monkey was housed in a group cage with a male cage mate and was maintained on a balanced commercial monkey cube diet (Unga Ltd, Nairobi, Kenya) supplemented with fresh fruits and vegetables thrice weekly. Water was provided ad libitum. The animal had a history of four abortions and two live births within a period of six years, the last abortion occurring two months before investigative surgery. She was examined for evidence of reproductive abnormalities and a diagnostic exploratory laparotomy was done. All tissues collected were fixed in 10 per cent neutral buffered formalin, processed by standard procedures and examined histologically. During diagnostic laparotomy, several fibrous adhesions were noted. There were peritoneal adhesions attaching both ovaries to the uterine wall and the ventral surface of the uterus to the urinary bladder, abdominal wall and surrounding mesentery. Soft dark tissue attached to the ventral surface of the uterus and close to the cervix was observed grossly and sampled for light microscopy. Microscopically, two characteristic features of endometriosis, endometrial glands and stroma, were noted on the serosal surface of the uterus. These endometrial glands were lined by columnar epithelial cells. The lumina of some glands contained sloughed epithelial cells with erythrocytes and mononuclear cells. The stroma was very vascular and haemorrhage into the lumina of endometrial glands and surrounding tissue was evident. The stroma had a moderate mononuclear cell infiltration consisting predominantly of lymphocytes. Discussion
Endometriosis externa is described as the presence of endometrial tissue, with both glandular and stromal components, in an abnormal location. Several theories have been suggested for the pathogenesis of endometriosis (McClure, 1979). These include 1. retrograde menstruation and implantation of viable endometrial cells on extrauterine abdominal organs, 2. serosal metaplasia of coelomic epithelium, 3. cell rests of the Wolffian duct system undergoing transformation to endometrial tissue, 4. haematogenous or lymphatic metastasis, and 5. direct myometrial impression. It is probable that more than one mechanism might be necessary to explain the histogenesis of endometriosis. The lesions of endometriosis observed in non-human primates at necropsy have been described in detail (DiGiacomo, 1977; McClure, 1979). In addition, endometriosis in non-human primates may be found incidentally during hysterotomy or laparotomy performed for other reasons and as a sequel to ionizing radiation (Splitter, Kirk, Mackenzie and Rawlings, 1972; MacKenzie and Casey, 1975; McClure, 1979). Lesions found in the De Brazza’s monkey described in this report are consistent with pathological findings in other nonhuman primates and in women with endometriosis (Robbins et al., 1984; Fanton, Hubbard and Wood, 1986). Endometrial cysts frequently form as the result of endometriosis. Haemorrhage from these cysts into surrounding tissues results in the release of free iron, which is intensely fibrogenic and causes the formation of adhesions (Fox and
Endometriosis
in a Monkey
473
Buckley, 1984). In addition, pelvic adhesions in endometriosis can affect fertility by preventing ovum pickup (Schenken et al., 1984). Viability of ectopic endometrial tissue is reliant on endogenous oestrogen. This hormonal dependence is further supported by the fact that lesions regress in women after menopause (Merrill, 1968). To our knowledge, this is the first reported case of spontaneous external endometriosis in a De Brazza’s monkey. Since this non-human primate faces extinction, it is necessary to consider the health problems of the guenon as they relate to the animal’s reproductive performance in captivity. In non-human primates, endometriosis should be considered as a possible cause of infertility whenever the reproductive performance of the monkey is lowered. The condition may be diagnosed antemortem when attention is given to detailed reproductive tract examination.
Acknowledgments
The authors wish to thank MessrsZ. Maheli and R. Korir for technical assistanceand ProfessorW. L. Chapman, Jr for editorial assistance. References
Brennan, E. J. ( 1985). De Brazza’s monkeys (Cercopithecus neglectus)in Kenya: census, distribution, and conservation. American Journal of Primatology, 8, 269-277. Gary, C. J., Peter, A. K. and Schiffer, S. P. (1982). A case report and review of endometriosisin nonhuman primates. Laboratol;y Animal Science, 32, 426. Dore, M. and Lagace, A. (1985). Spontaneous external endometriosis in a gorilla (Gorilla
gorilla).
Canadian
Veterinary Journal,
26, 347-349.
DiGiacomo, R. F. (1977). Gynecologic pathology in the rhesus monkey (Macaca mulatta). II. Findings in laboratory and free-ranging monkeys. Veterinary Pathology, 14,539-546.
DiGiacomo, R. F., Hooks, J. J., Sulima, M. P., Gibbs, C. and Gajdusek, D. C. (1977). Pelvic endometriosis and simian foamy virus infection in a pig-tailed macaque. Journal of American Veterinary Medicine Association, 171, 85S86 1. Fanton, J. W., Hubbard, A. B. and Wood, D. H. (1986). Endometriosis: clinical and pathologic findings in 70 rhesusmonkeys. American Journal of Veterinary Research, 47, 1537-1541. Fox, H. and Buckley, C. H. (1984). Current concepts of endometriosis. Clinical Obstetrics and Gynecology, 11, 279-287.
MacKenzie, W. F. and Casey, H. W. ( 1975). A nimal model: endometriosisin rhesus monkeys. American Journal of Pathology, 80, 341-344. MacKenzie, W. P., Splitter, G. A. and Valerio, M. G. (1972). Endometriosis in primates. Medical Primatology, 1, 288-297. McCann, T. 0. and Myers, R. E. (1970). Endometriosis in rhesusmonkeys. American Journal of Obstetrics and Gynecology, 106, 5 16546. McClure, H. M., Ridley, J. H. and Graham, C. E. (1971). Disseminatedendometriosis in a rhesusmonkey (Macaca mulatta) . Journal of the Medical Association of Georgia, 60, 11-13.
McClure, H. M. (1979). Endometriosis. In Spontaneous Animal Models of Human Disease. Vol. 1. Andrews, E. J., Ward, B. C. and Altman, N. H. Eds, Academic Press,New York, pp. 215-218. Merrill, J. A. (1968). Spontaneousendometriosisin the Kenya baboon (Papio doguera). American Journal of Obstetrics and Gynecology, 101, 569-570. Robbins, S. L., Cotran, R. S. and Kumar, V. (1984). Female Genital Tract. In Pathologic Basis of Disease. 3rd Edit., W. B. Saunders, Philadelphia, pp. 1130-l 137.
474
A. A. Binhazim
et al.
Schenken, R. S., Asch, R. H., Williams, R. F. and Hodgen, A. D. ( 1984). Etiology of infertility in monkeys with endometriosis: luteinized unruptured follicles, luteal phase defects, pelvic adhesions, and spontaneous abortions. Fertility and Sterility, 41, 122-130. Splitter, G. A., Kirk, J. H., MacKenzie, W. F. and Rawlings, C. A. (1972). Endometriosis in four irradiated rhesus monkeys. Veterinary Pathology, 9, 249-262. [Received for publication,
October 3rd, 19881
Path.
1989 Vol.
101
Spontaneous
External De Brazza’s
A. A. Binhazim*,
Endometriosis Monkey
R. P. Tarara
and
in a
M. A. Sulemant
Institute of Primate Research, National Museums of Kenya, Box 24481, Karen, Kenya
Summary A spontaneous case of external endometriosis in a 22-year-old female De Brazza’s monkey is described. During diagnostic laparotomy, peritoneal adhesions of the uterus to the urinary bladder, ovaries and abdominal wall were seen. A surgical biopsy of soft tissue attached to the ventral surface of the uterus was examined histologically and consisted of endometrial glands and stroma. These findings were compatible with a diagnosis of endometriosis. Iihroduction The De Brazza’s monkey (Cercopithecus neglectus) in Kenya is estimated to number slightly more than 100 and is considered an endangered species by primate conservationists. This forest guenon faces almost certain extinction unless conservation attempts are soon implemented. The pressures now facing the population of this non-human primate include loss of habitat, reproductive isolation and a decline in numbers as the result of being killed as a food source or as agricultural pests (Brennan, 1985). Spontaneous endometriosis has been reported in various non-human primate species (Merrill, 1968; McCann and Myers, 1970; DiGiacomo, Hooks, Sulima, Gibbs and Gajdusek, 1977; Cary, Peter and Schiffer, 1982; Dore and Lagace, 1985). Most reported cases of endometriosis have involved rhesus monkeys (Macaca mulatta). The condition has been induced surgically in rhesus as well as in cynomolgus monkeys (M. fascicularis) (MacKenzie and Casey, 1975; Schenken, Asch, Williams and Hodgen, 1984). Moreover, the disease in rhesus monkeys is reported to be much more severe than in other species of monkeys and often progresses irreversibly to death (McClure, Ridley and Graham, 197 1; MacKenzie, Splitter and Valerio, 1972). In women, the disease is a relatively common occurrence, and histologically proved endometriosis was found in 33 per cent of patients undergoing surgical assessment of infertility (Robbins, Cotran and Kumar, 1984). Therefore, non-human primates have been suggested as animal models of the disease. This paper describes spontaneous endometriosis in a De Brazza’s monkey.
*Present address: The University Athens, Georgia, 30602, U.S.A. 0022-9975/89/08047
of Georgia, College t Requests for reprints
I+ 04 $03.00/O
of Veterinary Medicine, Department should be sent to this address. 0
1989 Academic
of Pathology, Press Limited
472
A. A. Binhazim
et al.
Case Report
A 22-year-old female De Brazza’s monkey was housed in a group cage with a male cage mate and was maintained on a balanced commercial monkey cube diet (Unga Ltd, Nairobi, Kenya) supplemented with fresh fruits and vegetables thrice weekly. Water was provided ad libitum. The animal had a history of four abortions and two live births within a period of six years, the last abortion occurring two months before investigative surgery. She was examined for evidence of reproductive abnormalities and a diagnostic exploratory laparotomy was done. All tissues collected were fixed in 10 per cent neutral buffered formalin, processed by standard procedures and examined histologically. During diagnostic laparotomy, several fibrous adhesions were noted. There were peritoneal adhesions attaching both ovaries to the uterine wall and the ventral surface of the uterus to the urinary bladder, abdominal wall and surrounding mesentery. Soft dark tissue attached to the ventral surface of the uterus and close to the cervix was observed grossly and sampled for light microscopy. Microscopically, two characteristic features of endometriosis, endometrial glands and stroma, were noted on the serosal surface of the uterus. These endometrial glands were lined by columnar epithelial cells. The lumina of some glands contained sloughed epithelial cells with erythrocytes and mononuclear cells. The stroma was very vascular and haemorrhage into the lumina of endometrial glands and surrounding tissue was evident. The stroma had a moderate mononuclear cell infiltration consisting predominantly of lymphocytes. Discussion
Endometriosis externa is described as the presence of endometrial tissue, with both glandular and stromal components, in an abnormal location. Several theories have been suggested for the pathogenesis of endometriosis (McClure, 1979). These include 1. retrograde menstruation and implantation of viable endometrial cells on extrauterine abdominal organs, 2. serosal metaplasia of coelomic epithelium, 3. cell rests of the Wolffian duct system undergoing transformation to endometrial tissue, 4. haematogenous or lymphatic metastasis, and 5. direct myometrial impression. It is probable that more than one mechanism might be necessary to explain the histogenesis of endometriosis. The lesions of endometriosis observed in non-human primates at necropsy have been described in detail (DiGiacomo, 1977; McClure, 1979). In addition, endometriosis in non-human primates may be found incidentally during hysterotomy or laparotomy performed for other reasons and as a sequel to ionizing radiation (Splitter, Kirk, Mackenzie and Rawlings, 1972; MacKenzie and Casey, 1975; McClure, 1979). Lesions found in the De Brazza’s monkey described in this report are consistent with pathological findings in other nonhuman primates and in women with endometriosis (Robbins et al., 1984; Fanton, Hubbard and Wood, 1986). Endometrial cysts frequently form as the result of endometriosis. Haemorrhage from these cysts into surrounding tissues results in the release of free iron, which is intensely fibrogenic and causes the formation of adhesions (Fox and
Endometriosis
in a Monkey
473
Buckley, 1984). In addition, pelvic adhesions in endometriosis can affect fertility by preventing ovum pickup (Schenken et al., 1984). Viability of ectopic endometrial tissue is reliant on endogenous oestrogen. This hormonal dependence is further supported by the fact that lesions regress in women after menopause (Merrill, 1968). To our knowledge, this is the first reported case of spontaneous external endometriosis in a De Brazza’s monkey. Since this non-human primate faces extinction, it is necessary to consider the health problems of the guenon as they relate to the animal’s reproductive performance in captivity. In non-human primates, endometriosis should be considered as a possible cause of infertility whenever the reproductive performance of the monkey is lowered. The condition may be diagnosed antemortem when attention is given to detailed reproductive tract examination.
Acknowledgments
The authors wish to thank MessrsZ. Maheli and R. Korir for technical assistanceand ProfessorW. L. Chapman, Jr for editorial assistance. References
Brennan, E. J. ( 1985). De Brazza’s monkeys (Cercopithecus neglectus)in Kenya: census, distribution, and conservation. American Journal of Primatology, 8, 269-277. Gary, C. J., Peter, A. K. and Schiffer, S. P. (1982). A case report and review of endometriosisin nonhuman primates. Laboratol;y Animal Science, 32, 426. Dore, M. and Lagace, A. (1985). Spontaneous external endometriosis in a gorilla (Gorilla
gorilla).
Canadian
Veterinary Journal,
26, 347-349.
DiGiacomo, R. F. (1977). Gynecologic pathology in the rhesus monkey (Macaca mulatta). II. Findings in laboratory and free-ranging monkeys. Veterinary Pathology, 14,539-546.
DiGiacomo, R. F., Hooks, J. J., Sulima, M. P., Gibbs, C. and Gajdusek, D. C. (1977). Pelvic endometriosis and simian foamy virus infection in a pig-tailed macaque. Journal of American Veterinary Medicine Association, 171, 85S86 1. Fanton, J. W., Hubbard, A. B. and Wood, D. H. (1986). Endometriosis: clinical and pathologic findings in 70 rhesusmonkeys. American Journal of Veterinary Research, 47, 1537-1541. Fox, H. and Buckley, C. H. (1984). Current concepts of endometriosis. Clinical Obstetrics and Gynecology, 11, 279-287.
MacKenzie, W. F. and Casey, H. W. ( 1975). A nimal model: endometriosisin rhesus monkeys. American Journal of Pathology, 80, 341-344. MacKenzie, W. P., Splitter, G. A. and Valerio, M. G. (1972). Endometriosis in primates. Medical Primatology, 1, 288-297. McCann, T. 0. and Myers, R. E. (1970). Endometriosis in rhesusmonkeys. American Journal of Obstetrics and Gynecology, 106, 5 16546. McClure, H. M., Ridley, J. H. and Graham, C. E. (1971). Disseminatedendometriosis in a rhesusmonkey (Macaca mulatta) . Journal of the Medical Association of Georgia, 60, 11-13.
McClure, H. M. (1979). Endometriosis. In Spontaneous Animal Models of Human Disease. Vol. 1. Andrews, E. J., Ward, B. C. and Altman, N. H. Eds, Academic Press,New York, pp. 215-218. Merrill, J. A. (1968). Spontaneousendometriosisin the Kenya baboon (Papio doguera). American Journal of Obstetrics and Gynecology, 101, 569-570. Robbins, S. L., Cotran, R. S. and Kumar, V. (1984). Female Genital Tract. In Pathologic Basis of Disease. 3rd Edit., W. B. Saunders, Philadelphia, pp. 1130-l 137.
474
A. A. Binhazim
et al.
Schenken, R. S., Asch, R. H., Williams, R. F. and Hodgen, A. D. ( 1984). Etiology of infertility in monkeys with endometriosis: luteinized unruptured follicles, luteal phase defects, pelvic adhesions, and spontaneous abortions. Fertility and Sterility, 41, 122-130. Splitter, G. A., Kirk, J. H., MacKenzie, W. F. and Rawlings, C. A. (1972). Endometriosis in four irradiated rhesus monkeys. Veterinary Pathology, 9, 249-262. [Received for publication,
October 3rd, 19881