BILATERAL OVARIAN CYSTADENOMA IN A GERIATRIC AFRICAN ELEPHANT (LOXODONTA AFRICANA) Author(s): Stefan Hoby, Dr. med. vet., Fabio Aloisio, D.V.M., Dipl. A.C.V.P., and Vanessa L. Schumacher, D.V.M., M.S., Dipl. A.C.V.P. Source: Journal of Zoo and Wildlife Medicine, 45(2):406-409. 2014. Published By: American Association of Zoo Veterinarians DOI: http://dx.doi.org/10.1638/2013-0149R.1 URL: http://www.bioone.org/doi/full/10.1638/2013-0149R.1
BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/ terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.
BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.
Journal of Zoo and Wildlife Medicine 45(2): 406–409, 2014 Copyright 2014 by American Association of Zoo Veterinarians
BILATERAL OVARIAN CYSTADENOMA IN A GERIATRIC AFRICAN ELEPHANT (LOXODONTA AFRICANA) Stefan Hoby, Dr. med. vet., Fabio Aloisio, D.V.M., Dipl. A.C.V.P., and Vanessa L. Schumacher, D.V.M., M.S., Dipl. A.C.V.P.
Abstract: A 59-yr-old, captive female African elephant (Loxodonta africana) died of a cardiovascular collapse. Necropsy revealed bilateral replacement of the ovarian tissue by multiple cystic formations of up to 10 cm in diameter. The cysts were thin walled and filled with clear watery fluid. Smaller solid masses with an irregular surface projected from the wall of a few of the cysts. Histologically, the cystic structures were characterized by a single layer of well-differentiated cuboidal epithelial cells resting on a basement membrane. Occasionally the cysts contained nodular proliferations of single-layered, well-differentiated cuboidal epithelial cells forming anastomosing tubules and occasional papillary projections. The ovarian neoplasia was diagnosed as a bilateral multilocular serous ovarian cystadenoma. The nulliparous status and the advanced age may have contributed to the ovarian pathology. Key words: African elephant, aging, cystadenoma, ovary, pathology, reproduction.
BRIEF COMMUNICATION A 59-yr-old female African elephant (Loxodonta africana) was found dead in the outside enclosure at Zoo Basel, Switzerland. According to the European and American studbooks, this was the oldest African elephant in captivity. The elephant was wild born in the Ruaha Plain, Tanzania (7831952S, 34838913E) and arrived in Zoo Basel in 1952 along with four other young African elephants. The female held the position as matriarch in the herd of four other female African elephants (approximately 15, 16, 34, and 39 yr old) that were housed in an exhibit with an outside area of 1,300 m2 and an inside area of 190 m2. A bull (approximately 14 yr old) with limited access to the females was kept separately. The diet consisted of grass hay, oat and wheat straw, branches, low-fiber pellets (3719, Kliba Nafag, Provimi Kliba AG, 4303 Kaiseraugst, Switzerland), and a small amount of seasonally available vegetables and fruits. The elephant’s medical history for the last 10 yr of life was characterized by transient mild colic often associated with sudden changes of the weather, diffuse chronic hyperkeratosis of the skin, and intermittent stiff gait and mild lameness of the forelimbs. Six years before death, the elephant had to be lifted from From Zoo Basel, Postfach, 4011 Basel, Switzerland (Hoby); and the Institute of Animal Pathology, Vetsuisse Faculty, University of Berne, La¨nggassstrasse 122, 3012 Bern, Switzerland (Aloisio, Schumacher). Present addresses (Aloisio): IDEXX Laboratories, via Turati 16/18, 20121 Milano, Italy; (Schumacher): Roche Diagnostics GmbH, Nonnenwald 2, 82377 Penzberg, Germany. Correspondence should be directed to Dr. Hoby ([email protected]).
the fire brigade by means of several hover cushions after it was found in lateral recumbency and unable to get up by itself. The ovarian cycle of the nulliparous female was monitored via urinary 5a-pregnane-3-ol-20-one assessments7 in 2000, 2004, and 2005 and revealed acyclicity. Since then the monitoring of the ovarian cycle was stopped due to the advanced age of the elephant. At necropsy, the elephant was in good body condition. The ovarian tissue was bilaterally completely effaced and replaced by approximately three to five cystic structures per ovary. The cysts varied in size from approximately 4–10 cm in diameter (Fig. 1). On cut surface, the cysts were thin walled and filled with clear watery fluid. Smaller, solid tan firm masses protruded into the lumina. Bilaterally on the surface of the fimbria, multifocal, raised, solid nodular masses with an irregular surface and a diameter of 1–2 cm were distributed in a linear fashion (Fig. 1). Other pathologic findings included severe primary degenerative joint disease of the right proximal carpal joint with chronic synovitis and acute, synovial hemorrhage as well as mild degenerative joint disease of the atlanto–occipital joint, right elbow joint, and right stifle joint. Incidental and age-related findings included focal pulmonary fibrosis, an acute subserosal hematoma in the stomach, marked cholelithiasis in the liver and gallbladder, and focal subintimal fibrosis of the aorta. Representative samples of the lesions were taken for histopathologic examination and fixed in 10% neutral buffered formalin. Samples were processed routinely, sectioned at 2 lm, and stained with hematoxylin and eosin (H&E).
406
HOBY ET AL.—OVARIAN CYSTADENOMA IN AN AFRICAN ELEPHANT
407
Figure 2. Ovary, 59-yr-old African elephant (Loxodonta africana). Complete effacement of the normal ovarian structure and replacement by multiple cystic formations. Hematoxylin and eosin (H&E), 310.
Figure 1. Cranial view of multiple cystic formations (CY) of up to a 10-cm diameter in the right ovary of a 59-yr-old African elephant (Loxodonta africana). FM ¼ fimbrial masses, UT ¼ uterine horn.
On microscopic examination of the ovary, the normal ovarian structure was completely effaced and replaced by multiple cystic formations lined by a single layer of well-differentiated cuboidal epithelial cells that were often attenuated (Fig. 2). Occasionally, cilia were present at the apical portion of these cells. The cystic structures sometimes contained nodular proliferations of single-layered, well-differentiated cuboidal epithelial cells forming anastomosing tubules and occasional papillary projections (Fig. 3). These cells were supported by a moderate amount of fibrovascular stroma. Eosinophilic proteinaceous material was sometimes present in the lacunar and cystic spaces. The mitotic index was, on average, less than one mitosis per high-power field (3400). Based on these features, a diagnosis of multilocular serous ovarian cystadenoma was made. The fimbrial nodules were composed of papilliferous to polypoid proliferations of fibrous connective tissue lined by a single layer of well-
differentiated cuboidal cells, for which two possible differential diagnoses were considered: either extension of the neoplastic process in the ovaries to the fimbria or preexisting hyperplastic changes of the fimbrial epithelium as described earlier.1 The ovarian lesions were unrelated to the ultimate cause of death, which was cardiovascular collapse. The examination of all the other parts of the reproductive tract was without pathologic findings. This is the first description of a bilateral ovarian cystadenoma in an African elephant. To the authors’ knowledge, only one other report of an ovarian neoplasia in an Asian elephant (Elephas
Figure 3. Ovary, 59-yr-old African elephant (Loxodonta africana). Cystic formations lined by a single layer of well-differentiated cuboidal epithelial cells with occasional papillary projections. Arrows indicate the wall of the cysts. H&E, 3100.
408
JOURNAL OF ZOO AND WILDLIFE MEDICINE
maximus) has been published, but a detailed description of the morphology and neoplastic type was not reported.9 Reproductive tract diseases are of major concern for the captive elephant population as they may impede breeding and lead to non–self-sustaining ex situ populations.10 In female African elephants, common pathologies include cyst formations in the vestibule, vagina, cervix, endometrium, oviduct or ovary, and vestibular polyps.11 Three different types of ovarian cysts were characterized by ultrasound with maximal diameters of 25 mm and were observed in approximately 15% of captive African elephants. In contrast, the diameter of the neoplastic cysts exceeded the size of the previously reported nonneoplastic cysts by far, and normal ovarian tissue could not be detected in this case. Ovarian cysts in general can be classified as functional or nonfunctional cysts. Functional cysts are most commonly follicular cysts or luteal cysts. Nonfunctional cystic lesions of the ovary include ovarian cystadenoma, dermoid cysts, and cystic adenofibroma. Ovarian cystadenomas are benign neoplasms that are further classified as serous, as seen in this case, or as mucinous.17 They arise from epithelial structures within the ovary and tend to be infrequently bilateral and rarely malignant. At the time of death, the ovarian cycle of the female was not monitored, but earlier progesterone metabolite measurements, observed behaviors, and the lack of functional ovarian tissue at necropsy clearly indicated acyclicity. Ovarian cysts may be associated with acyclicity.2 Inactive ovaries are a common phenomenon in the captive African elephant population.3 In a recent survey, 30.5% of African elephants in North America showed ovarian inactivity with constant baseline progesterone metabolite concentrations.4 In Europe, a service to monitor the reproductive status revealed acyclicity in 13% of the African elephants (data 2012, n ¼ 136, Oerke, pers. comm., 03 June 2013). Apart from pathologic changes of the ovaries, acyclicity in elephants has been related to various other reasons such as seasonal changes,14 hyperprolactinemia,3 and hierarchy status.6 As opposed to many mammalian species where dominant females remain reproductively active, dominant captive African elephants are prone to develop acyclicity. A main cause for reproductive tract pathologies and acyclicity in captive elephants may be asymmetric reproductive aging due to prolonged nonreproductive periods and, thus, continuous exposure to endogenous sex steroids.8
Hence, apart from the ovarian pathology that led to acyclicity, this animal was at an increased risk to develop acyclity due to its social rank as a group leader and its nulliparous status. This elephant was of advanced age and the oldest African elephant reported in captivity. In the wild, the maximum lifespan is over 65 yr. African elephants may reproduce until the end of their lifespan, but there is a sharp drop in fecundity as they reach their 50s.12 Reproductive senescence has been described in other long-lived mammals such as chimpanzees (Pan troglodytes verus)15 and cetaceans,16 but its relation to pathologic changes needs to be further investigated. Reproductive senescence in African elephants may represent an adaptive trait as shown in killer whales (Orcinus orca)5 and Asian elephants.13 However, in the described case the inactivity of the ovaries was clearly associated with the complete, bilateral destruction of the ovarian tissue caused by a serous cystadenoma. Acknowledgements: The authors thank the elephant keepers, curators, and veterinary staff at Zoo Basel. Thanks are also due to Dr. John Edwards (Texas A&M University) and Dr. Martin Surbeck for consulting on this case and to Beatrice Steck for editorial assistance.
LITERATURE CITED 1. Allen WR, Mathias S, Wooding FBP, van Aarde RJ. Placentation in the African elephant (Loxodonta africana): II. Morphological changes in the uterus and placenta throughout gestation. Placenta. 2003;24:598– 617. 2. Brown JL, Hildebrandt TB, Theison W, Neiffer DL. Endocrine and ultrasound evaluation of a noncycling African elephant: identification of an ovarian follicular cyst. Zoo Biol. 1999;18:223–232. 3. Brown JL, Walker SL, Moeller T. Comparative endocrinology of cycling and noncycling Asian (Elephas maximus) and African (Loxodonta africana) elephants. Gen Comp Endocrinol. 2004;136:360–370. 4. Dow TL, Holaskowa I, Brown JL. Results of the third reproductive assessment survey of North American Asian (Elephas maximus) and African (Loxodonta africana) female elephants. Zoo Biol. 2011;30:699–711. 5. Foster EA, Franks DW, Mazzi S, Darden SK, Balcomb DC, Ford JKB, Croft DP. Adaptive prolonged postreproductive life span in killer whales. Science. 2012;337:1313. 6. Freeman EW, Weiss E, Brown JL. Examination of the interrelationships of behavior, dominance status, and ovarian activity in captive Asian and African elephants. Zoo Biol. 2004;23:431–448. 7. Heistermann M, Trohorsch MB, Hodges JK. Assessment of ovarian function in the African elephant
HOBY ET AL.—OVARIAN CYSTADENOMA IN AN AFRICAN ELEPHANT
(Loxodonta africana) by measurement of 5 a-reduced progesterone metabolites in serum and urine. Zoo Biol. 1997;16:273–284. 8. Hermes R, Hildebrandt TB, Go¨ritz F. Reproductive problems directly attributable to long-term captivity—asymmetric reproductive aging. Animal Reprod Sci. 2004;82/83:49–60. 9. Hildebrandt TB. Reproductive and diagnostic ultrasonography. In: Fowler ME, Mikota SK (eds.). Biology, medicine, and surgery of elephants. Oxford, Victoria: Blackwell; 2006. p. 357–376. 10. Hildebrandt TB, Go¨ritz F, Hermes R, Reid C, Dehnhard M, Brown JL. Aspects of the reproductive biology and breeding management of Asian and African elephants. Int. Zoo Yearb. 2006;40:20–40. 11. Hildebrandt TB, Go¨ritz F, Pratt NC, Brown JL, Montali RJ, Schmitt DL, Fritsch G, Hermes R. Ultrasonography of the urogenital tract in elephants (Loxodonta africana and Elephas maximus): an important tool for assessing female reproductive function. Zoo Biol. 2000;19:321–332. 12. Moss CJ. The demography of an African elephant (Loxodonta africana) population in Amboseli, Kenya. J Zool. 2001;255:145–156. 13. Robinson MR, Mar KU, Lummaa V. Senescence and age-specific trade-offs between reproduction and
409
survival in female Asian elephants. Ecol Lett. 2012;15: 260–266. 14. Schulte BA, Feldman E, Lambert R, Oliver R, Hess DL. Temporary ovarian inactivity in elephants: relationship to status and time outside. Physiol Behav. 2000;71:123–131. 15. Thompson ME, Jones JH, Pusey AE, BrewerMarsden S, Goodall J, Marsden D, Matsuzawa T, Nishida T, Reynolds V, Sugiyama Y, Wrangham RW. Aging and fertility patterns in wild chimpanzees provide insights into evolution of menopause. Curr Biol. 2007;17:2150–2156. 16. Whitehead H, Mann J. Female reproductive strategies of cetaceans. In: Mann J, Connor RC, Tyack PL, Whitehead H (eds.). Cetacean societies—field studies of dolphins and whales. Chicago, Illinois, USA: University of Chicago Press; 2000. p. 219–246. 17. Zaloudek CF. Tumors of the female genital tract, Part A: ovary, fallopian tube and broad and round ligaments. In: Fletcher CDM (ed.). Diagnostic histopathology of tumors. Volume 1, 3rd ed. Boston, Philadelphia: Churchill Livingstone Elsevier; 2007. p. 567–651. Received for publication 1 July 2013
BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/ terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.
BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.
Journal of Zoo and Wildlife Medicine 45(2): 406–409, 2014 Copyright 2014 by American Association of Zoo Veterinarians
BILATERAL OVARIAN CYSTADENOMA IN A GERIATRIC AFRICAN ELEPHANT (LOXODONTA AFRICANA) Stefan Hoby, Dr. med. vet., Fabio Aloisio, D.V.M., Dipl. A.C.V.P., and Vanessa L. Schumacher, D.V.M., M.S., Dipl. A.C.V.P.
Abstract: A 59-yr-old, captive female African elephant (Loxodonta africana) died of a cardiovascular collapse. Necropsy revealed bilateral replacement of the ovarian tissue by multiple cystic formations of up to 10 cm in diameter. The cysts were thin walled and filled with clear watery fluid. Smaller solid masses with an irregular surface projected from the wall of a few of the cysts. Histologically, the cystic structures were characterized by a single layer of well-differentiated cuboidal epithelial cells resting on a basement membrane. Occasionally the cysts contained nodular proliferations of single-layered, well-differentiated cuboidal epithelial cells forming anastomosing tubules and occasional papillary projections. The ovarian neoplasia was diagnosed as a bilateral multilocular serous ovarian cystadenoma. The nulliparous status and the advanced age may have contributed to the ovarian pathology. Key words: African elephant, aging, cystadenoma, ovary, pathology, reproduction.
BRIEF COMMUNICATION A 59-yr-old female African elephant (Loxodonta africana) was found dead in the outside enclosure at Zoo Basel, Switzerland. According to the European and American studbooks, this was the oldest African elephant in captivity. The elephant was wild born in the Ruaha Plain, Tanzania (7831952S, 34838913E) and arrived in Zoo Basel in 1952 along with four other young African elephants. The female held the position as matriarch in the herd of four other female African elephants (approximately 15, 16, 34, and 39 yr old) that were housed in an exhibit with an outside area of 1,300 m2 and an inside area of 190 m2. A bull (approximately 14 yr old) with limited access to the females was kept separately. The diet consisted of grass hay, oat and wheat straw, branches, low-fiber pellets (3719, Kliba Nafag, Provimi Kliba AG, 4303 Kaiseraugst, Switzerland), and a small amount of seasonally available vegetables and fruits. The elephant’s medical history for the last 10 yr of life was characterized by transient mild colic often associated with sudden changes of the weather, diffuse chronic hyperkeratosis of the skin, and intermittent stiff gait and mild lameness of the forelimbs. Six years before death, the elephant had to be lifted from From Zoo Basel, Postfach, 4011 Basel, Switzerland (Hoby); and the Institute of Animal Pathology, Vetsuisse Faculty, University of Berne, La¨nggassstrasse 122, 3012 Bern, Switzerland (Aloisio, Schumacher). Present addresses (Aloisio): IDEXX Laboratories, via Turati 16/18, 20121 Milano, Italy; (Schumacher): Roche Diagnostics GmbH, Nonnenwald 2, 82377 Penzberg, Germany. Correspondence should be directed to Dr. Hoby ([email protected]).
the fire brigade by means of several hover cushions after it was found in lateral recumbency and unable to get up by itself. The ovarian cycle of the nulliparous female was monitored via urinary 5a-pregnane-3-ol-20-one assessments7 in 2000, 2004, and 2005 and revealed acyclicity. Since then the monitoring of the ovarian cycle was stopped due to the advanced age of the elephant. At necropsy, the elephant was in good body condition. The ovarian tissue was bilaterally completely effaced and replaced by approximately three to five cystic structures per ovary. The cysts varied in size from approximately 4–10 cm in diameter (Fig. 1). On cut surface, the cysts were thin walled and filled with clear watery fluid. Smaller, solid tan firm masses protruded into the lumina. Bilaterally on the surface of the fimbria, multifocal, raised, solid nodular masses with an irregular surface and a diameter of 1–2 cm were distributed in a linear fashion (Fig. 1). Other pathologic findings included severe primary degenerative joint disease of the right proximal carpal joint with chronic synovitis and acute, synovial hemorrhage as well as mild degenerative joint disease of the atlanto–occipital joint, right elbow joint, and right stifle joint. Incidental and age-related findings included focal pulmonary fibrosis, an acute subserosal hematoma in the stomach, marked cholelithiasis in the liver and gallbladder, and focal subintimal fibrosis of the aorta. Representative samples of the lesions were taken for histopathologic examination and fixed in 10% neutral buffered formalin. Samples were processed routinely, sectioned at 2 lm, and stained with hematoxylin and eosin (H&E).
406
HOBY ET AL.—OVARIAN CYSTADENOMA IN AN AFRICAN ELEPHANT
407
Figure 2. Ovary, 59-yr-old African elephant (Loxodonta africana). Complete effacement of the normal ovarian structure and replacement by multiple cystic formations. Hematoxylin and eosin (H&E), 310.
Figure 1. Cranial view of multiple cystic formations (CY) of up to a 10-cm diameter in the right ovary of a 59-yr-old African elephant (Loxodonta africana). FM ¼ fimbrial masses, UT ¼ uterine horn.
On microscopic examination of the ovary, the normal ovarian structure was completely effaced and replaced by multiple cystic formations lined by a single layer of well-differentiated cuboidal epithelial cells that were often attenuated (Fig. 2). Occasionally, cilia were present at the apical portion of these cells. The cystic structures sometimes contained nodular proliferations of single-layered, well-differentiated cuboidal epithelial cells forming anastomosing tubules and occasional papillary projections (Fig. 3). These cells were supported by a moderate amount of fibrovascular stroma. Eosinophilic proteinaceous material was sometimes present in the lacunar and cystic spaces. The mitotic index was, on average, less than one mitosis per high-power field (3400). Based on these features, a diagnosis of multilocular serous ovarian cystadenoma was made. The fimbrial nodules were composed of papilliferous to polypoid proliferations of fibrous connective tissue lined by a single layer of well-
differentiated cuboidal cells, for which two possible differential diagnoses were considered: either extension of the neoplastic process in the ovaries to the fimbria or preexisting hyperplastic changes of the fimbrial epithelium as described earlier.1 The ovarian lesions were unrelated to the ultimate cause of death, which was cardiovascular collapse. The examination of all the other parts of the reproductive tract was without pathologic findings. This is the first description of a bilateral ovarian cystadenoma in an African elephant. To the authors’ knowledge, only one other report of an ovarian neoplasia in an Asian elephant (Elephas
Figure 3. Ovary, 59-yr-old African elephant (Loxodonta africana). Cystic formations lined by a single layer of well-differentiated cuboidal epithelial cells with occasional papillary projections. Arrows indicate the wall of the cysts. H&E, 3100.
408
JOURNAL OF ZOO AND WILDLIFE MEDICINE
maximus) has been published, but a detailed description of the morphology and neoplastic type was not reported.9 Reproductive tract diseases are of major concern for the captive elephant population as they may impede breeding and lead to non–self-sustaining ex situ populations.10 In female African elephants, common pathologies include cyst formations in the vestibule, vagina, cervix, endometrium, oviduct or ovary, and vestibular polyps.11 Three different types of ovarian cysts were characterized by ultrasound with maximal diameters of 25 mm and were observed in approximately 15% of captive African elephants. In contrast, the diameter of the neoplastic cysts exceeded the size of the previously reported nonneoplastic cysts by far, and normal ovarian tissue could not be detected in this case. Ovarian cysts in general can be classified as functional or nonfunctional cysts. Functional cysts are most commonly follicular cysts or luteal cysts. Nonfunctional cystic lesions of the ovary include ovarian cystadenoma, dermoid cysts, and cystic adenofibroma. Ovarian cystadenomas are benign neoplasms that are further classified as serous, as seen in this case, or as mucinous.17 They arise from epithelial structures within the ovary and tend to be infrequently bilateral and rarely malignant. At the time of death, the ovarian cycle of the female was not monitored, but earlier progesterone metabolite measurements, observed behaviors, and the lack of functional ovarian tissue at necropsy clearly indicated acyclicity. Ovarian cysts may be associated with acyclicity.2 Inactive ovaries are a common phenomenon in the captive African elephant population.3 In a recent survey, 30.5% of African elephants in North America showed ovarian inactivity with constant baseline progesterone metabolite concentrations.4 In Europe, a service to monitor the reproductive status revealed acyclicity in 13% of the African elephants (data 2012, n ¼ 136, Oerke, pers. comm., 03 June 2013). Apart from pathologic changes of the ovaries, acyclicity in elephants has been related to various other reasons such as seasonal changes,14 hyperprolactinemia,3 and hierarchy status.6 As opposed to many mammalian species where dominant females remain reproductively active, dominant captive African elephants are prone to develop acyclicity. A main cause for reproductive tract pathologies and acyclicity in captive elephants may be asymmetric reproductive aging due to prolonged nonreproductive periods and, thus, continuous exposure to endogenous sex steroids.8
Hence, apart from the ovarian pathology that led to acyclicity, this animal was at an increased risk to develop acyclity due to its social rank as a group leader and its nulliparous status. This elephant was of advanced age and the oldest African elephant reported in captivity. In the wild, the maximum lifespan is over 65 yr. African elephants may reproduce until the end of their lifespan, but there is a sharp drop in fecundity as they reach their 50s.12 Reproductive senescence has been described in other long-lived mammals such as chimpanzees (Pan troglodytes verus)15 and cetaceans,16 but its relation to pathologic changes needs to be further investigated. Reproductive senescence in African elephants may represent an adaptive trait as shown in killer whales (Orcinus orca)5 and Asian elephants.13 However, in the described case the inactivity of the ovaries was clearly associated with the complete, bilateral destruction of the ovarian tissue caused by a serous cystadenoma. Acknowledgements: The authors thank the elephant keepers, curators, and veterinary staff at Zoo Basel. Thanks are also due to Dr. John Edwards (Texas A&M University) and Dr. Martin Surbeck for consulting on this case and to Beatrice Steck for editorial assistance.
LITERATURE CITED 1. Allen WR, Mathias S, Wooding FBP, van Aarde RJ. Placentation in the African elephant (Loxodonta africana): II. Morphological changes in the uterus and placenta throughout gestation. Placenta. 2003;24:598– 617. 2. Brown JL, Hildebrandt TB, Theison W, Neiffer DL. Endocrine and ultrasound evaluation of a noncycling African elephant: identification of an ovarian follicular cyst. Zoo Biol. 1999;18:223–232. 3. Brown JL, Walker SL, Moeller T. Comparative endocrinology of cycling and noncycling Asian (Elephas maximus) and African (Loxodonta africana) elephants. Gen Comp Endocrinol. 2004;136:360–370. 4. Dow TL, Holaskowa I, Brown JL. Results of the third reproductive assessment survey of North American Asian (Elephas maximus) and African (Loxodonta africana) female elephants. Zoo Biol. 2011;30:699–711. 5. Foster EA, Franks DW, Mazzi S, Darden SK, Balcomb DC, Ford JKB, Croft DP. Adaptive prolonged postreproductive life span in killer whales. Science. 2012;337:1313. 6. Freeman EW, Weiss E, Brown JL. Examination of the interrelationships of behavior, dominance status, and ovarian activity in captive Asian and African elephants. Zoo Biol. 2004;23:431–448. 7. Heistermann M, Trohorsch MB, Hodges JK. Assessment of ovarian function in the African elephant
HOBY ET AL.—OVARIAN CYSTADENOMA IN AN AFRICAN ELEPHANT
(Loxodonta africana) by measurement of 5 a-reduced progesterone metabolites in serum and urine. Zoo Biol. 1997;16:273–284. 8. Hermes R, Hildebrandt TB, Go¨ritz F. Reproductive problems directly attributable to long-term captivity—asymmetric reproductive aging. Animal Reprod Sci. 2004;82/83:49–60. 9. Hildebrandt TB. Reproductive and diagnostic ultrasonography. In: Fowler ME, Mikota SK (eds.). Biology, medicine, and surgery of elephants. Oxford, Victoria: Blackwell; 2006. p. 357–376. 10. Hildebrandt TB, Go¨ritz F, Hermes R, Reid C, Dehnhard M, Brown JL. Aspects of the reproductive biology and breeding management of Asian and African elephants. Int. Zoo Yearb. 2006;40:20–40. 11. Hildebrandt TB, Go¨ritz F, Pratt NC, Brown JL, Montali RJ, Schmitt DL, Fritsch G, Hermes R. Ultrasonography of the urogenital tract in elephants (Loxodonta africana and Elephas maximus): an important tool for assessing female reproductive function. Zoo Biol. 2000;19:321–332. 12. Moss CJ. The demography of an African elephant (Loxodonta africana) population in Amboseli, Kenya. J Zool. 2001;255:145–156. 13. Robinson MR, Mar KU, Lummaa V. Senescence and age-specific trade-offs between reproduction and
409
survival in female Asian elephants. Ecol Lett. 2012;15: 260–266. 14. Schulte BA, Feldman E, Lambert R, Oliver R, Hess DL. Temporary ovarian inactivity in elephants: relationship to status and time outside. Physiol Behav. 2000;71:123–131. 15. Thompson ME, Jones JH, Pusey AE, BrewerMarsden S, Goodall J, Marsden D, Matsuzawa T, Nishida T, Reynolds V, Sugiyama Y, Wrangham RW. Aging and fertility patterns in wild chimpanzees provide insights into evolution of menopause. Curr Biol. 2007;17:2150–2156. 16. Whitehead H, Mann J. Female reproductive strategies of cetaceans. In: Mann J, Connor RC, Tyack PL, Whitehead H (eds.). Cetacean societies—field studies of dolphins and whales. Chicago, Illinois, USA: University of Chicago Press; 2000. p. 219–246. 17. Zaloudek CF. Tumors of the female genital tract, Part A: ovary, fallopian tube and broad and round ligaments. In: Fletcher CDM (ed.). Diagnostic histopathology of tumors. Volume 1, 3rd ed. Boston, Philadelphia: Churchill Livingstone Elsevier; 2007. p. 567–651. Received for publication 1 July 2013
