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Bilateral Malignant Ovarian Teratoma With Peritoneal Metastasis in a Captive African Pygmy Hedgehog (Atelerix albiventris)
AEMV FORUM BILATERAL MALIGNANT OVARIAN TERATOMA WITH PERITONEAL METASTASIS IN A CAPTIVE AFRICAN PYGMY HEDGEHOG (ATELERIX ALBIVENTRIS) Sun-Hye Song, DVM, Noh-Won Park, DVM, Soo-Kyo Jung, DVM, Jae-Hoon Kim, DVM, PhD, and Ki-Dong Eom, DVM, PhD
Abstract A 675-g, 1.4-year-old, female African pygmy hedgehog (Atelerix albiventris) was evaluated for progressive abdominal distension of 2 months duration. A large mass within the abdominal cavity was detected by radiography, ultrasonography, and computed tomography. The irregular, multilobulated mass, containing calcified, necrotic, and fatty areas was consistent with fused bilateral ovaries. Cytology of the mass suggested an ovarian adenoma or adenocarcinoma. The hedgehog died approximately 3 months after the initial presentation. Postmortem computed tomography and necropsy examination revealed a large bilaterally fused ovarian mass with peritoneal metastases. Histologically, the masses were composed of a variety of tissues from all 3 germ layers, including immature (embryonic) cells and neoplastic cells in the lymphatic system, which was consistent with malignant ovarian teratomas. This is the first report to describe malignant ovarian teratomas in a hedgehog. Copyright 2014 Elsevier Inc. All rights reserved. Key words: computed tomography; hedgehog; malignant; ovary; teratoma; tumor
A
1.4-year-old, intact, female African pygmy hedgehog (Atelerix albiventris) was evaluated for abdominal distension. The owner reported that the abdominal distension was first noted 2 months before presentation and had become progressively worse over that time. No other overt clinical disease signs had been observed except for an awkward gait due to a distended abdomen. The animal had a normal appetite, activity level, and urination/defecation. The hedgehog was housed alone in a plastic cage containing a commercial sawdust substrate and was fed a commercial hedgehog diet and mealworms. On physical examination, the hedgehog weighed 675 g and had a firmly distended abdomen and reddened, thickened abdominal skin presumably due to irritation from contact with the cage bottom. Radiographic images were obtained with the hedgehog under anesthesia and maintained with 3.5% isoflurane (Ifran; Hana Pharmaceutical Co., Seoul, South Korea) in oxygen (2 L/min) via a facemask. Radiographic images revealed a large soft tissue opacity occupying the entire abdominal cavity, craniolaterally displacing
the stomach and small intestines. Multiple irregular, radiopaque mineralized areas were dispersed within the mass. There was loss of abdominal serosal detail (Fig. 1). Ultrasonography and computed tomography (CT) were performed under general anesthesia as described earlier to evaluate the anatomic details of the affected area, origin of the mass, and affected organs. Subsequently, an ultrasound-guided fine-needle aspiration was performed to collect diagnostic samples for cytologic examination.
From the Department of Veterinary Radiology and Diagnostic Imaging, College of Veterinary Medicine, Konkuk University, Seoul, Korea; and the Department of Veterinary Pathology, College of Veterinary Medicine, Jeju National University, Jeju-do, Korea. Address correspondence to: Ki-Dong Eom, DVM, PhD, #427, Department of Veterinary Radiology and Diagnostic Imaging, College of Veterinary Medicine, Konkuk University, 120 Neungdong-ro, Gwangjin-gu, Seoul, Korea. E-mail: [email protected]. Ó 2014 Elsevier Inc. All rights reserved. 1557-5063/14/2101-$30.00 http://dx.doi.org/10.1053/j.jepm.2014.07.009
Journal of Exotic Pet Medicine 23 (2014), pp 403–408
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FIGURE 1. Dorsoventral (A) and right lateral (B) abdominal radiographs of a hedgehog show a large mass occupying the entire abdomen, displacing the gastrointestinal tract. There is multifocal mineralization of the mass with loss of serosal detail.
Ultrasound examination identified a massive, multilobulated, heterogeneous echogenic mass containing multiple hyperechogenic foci as well as hypoechogenic to anechogenic cystic/necrotic-like structures. The mass had peripheral vascular responses on color Doppler images (Fig. 2). The displaced abdominal organs, including the liver, both kidneys, and urinary bladder, were unaffected and there was peritoneal effusion. CT images demonstrated an irregular multilobulated mass (7.9 cm 9 cm 5.5 cm) that occupied most of the abdominal cavity. The mass had a heterogeneous soft tissue density with multiple coarse calcifications and a number of hypodense areas, which were suspected to be necrosis and fat. Tubular structures of soft tissue density that originated from the pelvic cavity, thought to be the uterine horns, extended from the mass (Fig. 3A and B). Dissemination of the abdominal mass to other organs was not identified, and there was peritoneal effusion, which was consistent with the ultrasonographic findings. The large abdominal mass was presumed to be a neoplasm of epithelial origin because of the presence of clusters of cohesive glandular epithelial cells in papillomatous arrangement with rare squamous cells and amorphous background material revealed on cytology. There was moderated to marked anisocytosis and anisokaryosis of the neoplastic glandular epithelial cells. Based on the cytology and imaging results, the neoplasm was tentatively identified as an ovarian adenoma or adenocarcinoma. Surgery was declined because of the potential risks and complications. Meloxicam (0.1 mg/kg, orally, every 12 hours for 7 days; Medicox capsule, Myungmoon Pharmaceutical, Co., Seoul, South 4 0 4
Korea) was prescribed to control any pain associated with the mass. The hedgehog was found dead 100 days after discharge from the hospital, and the owner reported that the animal had exhibited decreased appetite and lethargy for 3 to 4 days before death. Postmortem CT was performed to evaluate the status of the mass at the time of death. The abdominal mass was slightly larger (9.8 cm 9.2 cm 6 cm) and contained more calcifications when compared with the initial CT images. In addition, a small peritoneal mass (2.5 cm 1.2 cm 2.7 cm) with an irregular, calcified margin was present. Abnormalities identified on the gross necropsy examination included a firm, multilobulated, variegated, tan-red abdominal mass (10 cm 9.8 cm 8 cm) with normal-appearing uterine horns. One uterine horn was attached to the mass and the other one was separated from the mass. A similar-appearing smaller mass was found on the right parietal peritoneum (Fig. 4). On cut-section, the large mass was solid with multifocal mineralized areas and cavitated spaces containing dark red viscous fluid. Other organs within the abdominal cavity, including the liver, spleen, and kidneys, were grossly unremarkable. Samples were collected from the masses, liver, spleen, kidneys, and uterus, fixed in 10% neutral-buttered formalin, and routinely processed for histologic examination. Histologically, the large mass was composed of tissues derived from the 3 germ cell layers (ectoderm, endoderm, and mesoderm) arranged in a haphazard manner. Numerous glandular structures of various sizes were embedded in the matrix of connective tissue. Some of the glandular structures were lined by a single layer of columnar
Song et al./Journal of Exotic Pet Medicine 23 (2014), pp 403–408
FIGURE 2. Transabdominal ultrasound images of a hedgehog. (A) Note the large mass with heterogeneous echogenicity, which contains hyperechoic mineralization and is hypoechogenic to anechogenic. There is free peritoneal fluid surrounding the mass. (B) Color Doppler image shows peripheral vascularization within the mass. F, free fluid; M, mass; SP, spleen.
mucin-secreting, goblet-type epithelial cells with basal round nuclei, resembling gastrointestinal mucosa (Fig. 5A). Glandular structures lined by a single layer of cuboidal to ciliated columnar epithelial cells, resembling respiratory epithelium, were also present (Fig. 5C). There were numerous cysts lined by stratified squamous epithelium adjacent to hair follicles (Fig. 5B). Cords of immature or mature hyaline cartilage were embedded within the connective tissue matrix (Fig. 5A). Apart from these well-differentiated tissues, the mass contained sheets of primitive mesenchyme characterized by scant cytoplasm and round hyperchromatic nuclei. There was multifocal lymphatic invasion (Fig. 5D and E). The mass was a malignant teratoma based on the
histologic appearance and lymphatic invasion. The histologic features of the peritoneal mass were similar to those of the previously described mass. Incidental findings included hepatic extramedullary hematopoiesis, vacuolar hepatic degeneration, and renal tubular degeneration. A fused bilateral malignant ovarian teratoma with peritoneal metastasis was confirmed based on the anatomic location and the histopathologic findings. DISCUSSION _________________________________ Previous retrospective studies of neoplastic lesions in hedgehogs revealed a high incidence of tumors (53%), including integumentary, hemolymphatic, digestive, endocrine, genital, musculoskeletal, and
FIGURE 3. Dorsal reconstructed computed tomography images. (A and B) Images at different levels on the initial scan. An irregular, lobulated large mass is apparent with heterogeneous density, mineralization, and hypodense areas (white arrows). The tubular soft tissue density structures attached to the mass from the pelvic cavity were considered to be bilateral uterine horns (open arrows). (C) The postmortem image shows a small peritoneal mass with a mineralized margin, suggesting peritoneal metastasis (arrowhead). LIV, liver; SP, spleen; ST, stomach; UB, urinary bladder. Song et al./Journal of Exotic Pet Medicine 23 (2014), pp 403–408
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FIGURE 4. Ovarian teratoma and peritoneal metastasis in the African hedgehog. (A) A large bilaterally fused ovarian teratoma (M) and peritoneal metastasis (asterisk) in situ. The gross and histologic features of the peritoneal mass are similar to the ovarian mass. A uterine horn (white arrow) is attached to the surface of the mass. (B) An irregular multilobulated, firm ovarian mass is overlain by a perforated capsule. The uterine horns (arrows) are identified.
nervous system tumors, in decreasing order of frequency.1,2 In the genital system of captive African hedgehogs, tumors were most frequently found in the uterus and were identified as adenosarcoma, endometrial stromal sarcoma, adenoleiomyosarcoma, and adenoleiomyoma.3 Ovarian granular cell tumor and testicular neurofibrosarcoma have also been reported in hedgehogs.4,5 Teratomas are germ cell tumors that develop from pluripotent germ cells and differentiate into different tissues from 2 or 3 embryonic layers.6 Most teratomas described in the
veterinary literature have been intragonadal and ovarian teratomas; they have been reported in a variety of animals, including dogs,7-9 cats,7,10 pigs,6 horses,11 cattle,7 and rodents.7,12 However, ovarian teratomas have not been previously reported in hedgehogs. Similar to other animals, geriatric hedgehogs have an increased incidence of neoplasia when compared with their younger counterparts. The median age at the time of diagnosis of hedgehog neoplasms is 3.5 years, although the age of reproductive system neoplasia in these animals
FIGURE 5. Photomicrographs of the ovarian teratomas in the African hedgehog. (A) Chondrocytes within lacunae embedded in a cartilaginous matrix (C) and glandular structures (G) with mucin-secreting goblet-type epithelial cells. (B) Stratified squamous epithelium with central keratinization (S) and hair follicles (H). (C) Glandular structure (R) lined by a single layer of cuboidal to ciliated columnar epithelial cells. (D) Primitive mesenchymal cells with scant cytoplasm and round hyperchromatic nuclei are embedded in connective tissue. (E) Neoplastic cells in lymphatics. H&E stain; bar ¼ 50 mm. H&E, hematoxylin and eosin.
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Song et al./Journal of Exotic Pet Medicine 23 (2014), pp 403–408
ranges between 2 and 5 years.1,2 In human medicine, malignant teratomas occur more commonly in younger individuals than benign teratomas or other genital tumors.13 The hedgehog described in this report was younger than the average age at which neoplasia occurs, which is consistent with the finding of malignant teratomas in humans. The clinical presentation of teratomas in humans is nonspecific and mostly asymptomatic, as was observed in this case.13 The abdominal mass was suspected to be an adenoma or adenocarcinoma following fine-needle aspiration and cytologic examination. Cytologically, teratomas are characterized by a necrotic background, keratin debris or keratinocytes, inflammatory cells including neutrophils or macrophages, and clusters of differentiated epithelial cells.14 This case lacked the consistent cytologic features of teratomas except for amorphous background materials. Pleomorphic glandular epithelial cells were presumed to be extracted from glandular elements within the teratoma. Depending on the presence of undifferentiated elements or metastasis, teratomas can be classified as benign (mature) or malignant (immature). Malignant teratomas contain embryonic elements in addition to well-differentiated tissues and may show metastatic features.15 Malignant teratomas are rare, whereas benign cystic teratomas are the most common ovarian neoplasm in humans, accounting for 25% or more of all ovarian tumors.16,17 In this case, the teratoma was found to be malignant because of the presence of immature elements and lymphatic invasion. Furthermore, the malignant nature was confirmed by peritoneal metastasis. In humans, malignant ovarian teratomas can metastasize to the pelvis, abdominal peritoneum, and omentum by implantation, whereas hematogenous metastasis to other organs is rare. Bilateral malignant ovarian teratomas are very rare, whereas benign teratomas are bilateral in 10% to 15% of human patients. Contralateral metastasis can occur in ovarian malignant teratomas in advanced stages.13 In this case, both ovaries were affected and there was fusion of the ovarian masses. Histopathologic examination of other organs showed no metastasis; however, several nonspecific abnormal findings were observed. Splenic extramedullary hematopoiesis is a common finding and is a normal feature in this species.18 Although imaging of ovarian tumors is not specific, and these tumors can range from cystic to
solid masses, the key imaging features for each type of ovarian tumor have been described in human studies and may be helpful in narrowing the differential disease diagnosis.19,20 When compared with the imaging features of ovarian tumors in previous studies, the CT findings in this case were consistent with those of malignant ovarian teratomas characterized by a large, irregular, and predominantly solid component with scattered mineralization, small cystic or necrotic foci, and fat. Benign teratomas, which are mostly cystic mature teratomas, present as rather small cystic structures containing fat, with or without calcification.21 The history, clinical presentation, and diagnostic imaging findings of this African hedgehog were consistent with malignant bilateral ovarian teratomas, and a definitive diagnosis was confirmed by histopathologic examination. Ovarian teratomas should be included in the differential diagnosis of intra-abdominal tumors in female hedgehogs. Furthermore, imaging features of a large, predominantly solid ovarian mass with mineralization, necrosis, or fatty areas are strongly suggestive of a malignant ovarian teratoma. REFERENCES 1. Heatley JJ, Mauldin GE, Cho DY: A review of neoplasia in the captive African hedgehog (Atelerix albiventris). Semin Avian Exot Pet Med 14:182-192, 2005 2. Raymond JT, Garner MM: Spontaneous tumours in captive African hedgehogs (Atelerix albiventris): a retrospective study. J Comp Pathol 124:128-133, 2001 3. Mikaelian I, Reavill DR: Spontaneous proliferative lesions and tumors of the uterus of captive African hedgehogs (Atelerix albiventris). J Zoo Wildl Med 35:216-220, 2004 4. Wellehan JFX, Southorn E, Smith DA, et al: Surgical removal of a mammary adenocarcinoma and a granulosa cell tumor in an African pygmy hedgehog. Can Vet J 44: 235-237, 2003 5. Ramos-Vara JA: Soft tissue sarcomas in the African hedgehog (Atelerix albiventris): microscopic and immunohistologic study of three cases. J Vet Diagn Invest 13:442-445, 2001 6. Schlafer DH, Miller RB: Female genital system, in Maxie M (ed): Jubb, Kennedy and Palmer’s Pathology of Domestic Animals (ed 2), pp 429-564, 2007 7. Dehner LP, Norris HJ, Garner FM, et al: Comparative pathology of ovarian neoplasms: III. Germ cell tumours of canine, bovine, feline, rodent, and human species. J Comp Pathol 80:299-306, 1970 8. Greenlee PG, Patnaik AK: Canine ovarian tumors of germ cell origin. Vet Pathol 22:117-122, 1985 9. Patnaik AK, Schaer M, Parks J, et al: Metastasizing ovarian teratocarcinoma in dogs: a report of two cases and review of literature. J Small Anim Pract 17:235-246, 1976 10. Basaraba RJ, Kraft SL, Andrews GA, et al: An ovarian teratoma in a cat. Vet Pathol 35:141-144, 1998 11. Frazer GS, Robertson JT, Boyce RW: Teratocarcinoma of the ovary in a mare. J Am Vet Med Assoc 193:953-955, 1988
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12. Frisk CS, Wagner JE, Doyle RE: An ovarian teratoma in a guinea pig. Lab Anim Sci 28:199-201, 1978 13. Charles FZ: Tumors of the female genital tract, in Fletcher CD (ed): Diagnostic Histopathology of Tumors (ed 3). London, UK, Churchill Livingstone/Elsevier, pp 567-651, 2007 14. Bertazzolo W, Dell’Orco M, Bonfanti U, et al: Cytological features of canine ovarian tumours: a retrospective study of 19 cases. J Small Anim Pract 45:539-545, 2004 15. MacLachlan NJ, Kennedy PC: Tumors of the genital systems, in Meuten DJ (ed): Tumors in Domestic Animals (ed 4). Ames, IA, Iowa State University Press, pp 547-573, 2002 16. Koonings PP, Campbell K, Mishell Jr DR, et al: Relative frequency of primary ovarian neoplasms: a 10-year review. Obstet Gynecol 74:921-926, 1989 17. Katsube Y, Berg JW, Silverberg SG: Epidemiologic pathology of ovarian tumors: a histopathologic review of
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18.
19.
20.
21.
primary ovarian neoplasms diagnosed in the Denver Standard Metropolitan Statistical Area, 1 July-31 December 1969 and 1 July-31 December 1979. Int J Gynecol Pathol 1:3-16, 1982 Raymond JT, White MR: Necropsy and histopathologic findings in 14 African hedgehogs (Atelerix albiventris): a retrospective study. J Zoo Wildl Med 30:273-277, 1999 Jung SE, Lee JM, Rha SE, et al: CT and MR imaging of ovarian tumors with emphasis on differential diagnosis. Radiograph 22:1305-1325, 2002 Outwater EK, Siegelman ES, Hunt JL: Ovarian teratomas: tumor types and imaging characteristics. Radiograph 21: 475-490, 2001 Saba L, Guerriero S, Sulcis R, et al: Mature and immature ovarian teratomas: CT, US and MR imaging characteristics. Eur J Radiol 72:454-463, 2009
Song et al./Journal of Exotic Pet Medicine 23 (2014), pp 403–408
Abstract A 675-g, 1.4-year-old, female African pygmy hedgehog (Atelerix albiventris) was evaluated for progressive abdominal distension of 2 months duration. A large mass within the abdominal cavity was detected by radiography, ultrasonography, and computed tomography. The irregular, multilobulated mass, containing calcified, necrotic, and fatty areas was consistent with fused bilateral ovaries. Cytology of the mass suggested an ovarian adenoma or adenocarcinoma. The hedgehog died approximately 3 months after the initial presentation. Postmortem computed tomography and necropsy examination revealed a large bilaterally fused ovarian mass with peritoneal metastases. Histologically, the masses were composed of a variety of tissues from all 3 germ layers, including immature (embryonic) cells and neoplastic cells in the lymphatic system, which was consistent with malignant ovarian teratomas. This is the first report to describe malignant ovarian teratomas in a hedgehog. Copyright 2014 Elsevier Inc. All rights reserved. Key words: computed tomography; hedgehog; malignant; ovary; teratoma; tumor
A
1.4-year-old, intact, female African pygmy hedgehog (Atelerix albiventris) was evaluated for abdominal distension. The owner reported that the abdominal distension was first noted 2 months before presentation and had become progressively worse over that time. No other overt clinical disease signs had been observed except for an awkward gait due to a distended abdomen. The animal had a normal appetite, activity level, and urination/defecation. The hedgehog was housed alone in a plastic cage containing a commercial sawdust substrate and was fed a commercial hedgehog diet and mealworms. On physical examination, the hedgehog weighed 675 g and had a firmly distended abdomen and reddened, thickened abdominal skin presumably due to irritation from contact with the cage bottom. Radiographic images were obtained with the hedgehog under anesthesia and maintained with 3.5% isoflurane (Ifran; Hana Pharmaceutical Co., Seoul, South Korea) in oxygen (2 L/min) via a facemask. Radiographic images revealed a large soft tissue opacity occupying the entire abdominal cavity, craniolaterally displacing
the stomach and small intestines. Multiple irregular, radiopaque mineralized areas were dispersed within the mass. There was loss of abdominal serosal detail (Fig. 1). Ultrasonography and computed tomography (CT) were performed under general anesthesia as described earlier to evaluate the anatomic details of the affected area, origin of the mass, and affected organs. Subsequently, an ultrasound-guided fine-needle aspiration was performed to collect diagnostic samples for cytologic examination.
From the Department of Veterinary Radiology and Diagnostic Imaging, College of Veterinary Medicine, Konkuk University, Seoul, Korea; and the Department of Veterinary Pathology, College of Veterinary Medicine, Jeju National University, Jeju-do, Korea. Address correspondence to: Ki-Dong Eom, DVM, PhD, #427, Department of Veterinary Radiology and Diagnostic Imaging, College of Veterinary Medicine, Konkuk University, 120 Neungdong-ro, Gwangjin-gu, Seoul, Korea. E-mail: [email protected]. Ó 2014 Elsevier Inc. All rights reserved. 1557-5063/14/2101-$30.00 http://dx.doi.org/10.1053/j.jepm.2014.07.009
Journal of Exotic Pet Medicine 23 (2014), pp 403–408
4 0 3
FIGURE 1. Dorsoventral (A) and right lateral (B) abdominal radiographs of a hedgehog show a large mass occupying the entire abdomen, displacing the gastrointestinal tract. There is multifocal mineralization of the mass with loss of serosal detail.
Ultrasound examination identified a massive, multilobulated, heterogeneous echogenic mass containing multiple hyperechogenic foci as well as hypoechogenic to anechogenic cystic/necrotic-like structures. The mass had peripheral vascular responses on color Doppler images (Fig. 2). The displaced abdominal organs, including the liver, both kidneys, and urinary bladder, were unaffected and there was peritoneal effusion. CT images demonstrated an irregular multilobulated mass (7.9 cm 9 cm 5.5 cm) that occupied most of the abdominal cavity. The mass had a heterogeneous soft tissue density with multiple coarse calcifications and a number of hypodense areas, which were suspected to be necrosis and fat. Tubular structures of soft tissue density that originated from the pelvic cavity, thought to be the uterine horns, extended from the mass (Fig. 3A and B). Dissemination of the abdominal mass to other organs was not identified, and there was peritoneal effusion, which was consistent with the ultrasonographic findings. The large abdominal mass was presumed to be a neoplasm of epithelial origin because of the presence of clusters of cohesive glandular epithelial cells in papillomatous arrangement with rare squamous cells and amorphous background material revealed on cytology. There was moderated to marked anisocytosis and anisokaryosis of the neoplastic glandular epithelial cells. Based on the cytology and imaging results, the neoplasm was tentatively identified as an ovarian adenoma or adenocarcinoma. Surgery was declined because of the potential risks and complications. Meloxicam (0.1 mg/kg, orally, every 12 hours for 7 days; Medicox capsule, Myungmoon Pharmaceutical, Co., Seoul, South 4 0 4
Korea) was prescribed to control any pain associated with the mass. The hedgehog was found dead 100 days after discharge from the hospital, and the owner reported that the animal had exhibited decreased appetite and lethargy for 3 to 4 days before death. Postmortem CT was performed to evaluate the status of the mass at the time of death. The abdominal mass was slightly larger (9.8 cm 9.2 cm 6 cm) and contained more calcifications when compared with the initial CT images. In addition, a small peritoneal mass (2.5 cm 1.2 cm 2.7 cm) with an irregular, calcified margin was present. Abnormalities identified on the gross necropsy examination included a firm, multilobulated, variegated, tan-red abdominal mass (10 cm 9.8 cm 8 cm) with normal-appearing uterine horns. One uterine horn was attached to the mass and the other one was separated from the mass. A similar-appearing smaller mass was found on the right parietal peritoneum (Fig. 4). On cut-section, the large mass was solid with multifocal mineralized areas and cavitated spaces containing dark red viscous fluid. Other organs within the abdominal cavity, including the liver, spleen, and kidneys, were grossly unremarkable. Samples were collected from the masses, liver, spleen, kidneys, and uterus, fixed in 10% neutral-buttered formalin, and routinely processed for histologic examination. Histologically, the large mass was composed of tissues derived from the 3 germ cell layers (ectoderm, endoderm, and mesoderm) arranged in a haphazard manner. Numerous glandular structures of various sizes were embedded in the matrix of connective tissue. Some of the glandular structures were lined by a single layer of columnar
Song et al./Journal of Exotic Pet Medicine 23 (2014), pp 403–408
FIGURE 2. Transabdominal ultrasound images of a hedgehog. (A) Note the large mass with heterogeneous echogenicity, which contains hyperechoic mineralization and is hypoechogenic to anechogenic. There is free peritoneal fluid surrounding the mass. (B) Color Doppler image shows peripheral vascularization within the mass. F, free fluid; M, mass; SP, spleen.
mucin-secreting, goblet-type epithelial cells with basal round nuclei, resembling gastrointestinal mucosa (Fig. 5A). Glandular structures lined by a single layer of cuboidal to ciliated columnar epithelial cells, resembling respiratory epithelium, were also present (Fig. 5C). There were numerous cysts lined by stratified squamous epithelium adjacent to hair follicles (Fig. 5B). Cords of immature or mature hyaline cartilage were embedded within the connective tissue matrix (Fig. 5A). Apart from these well-differentiated tissues, the mass contained sheets of primitive mesenchyme characterized by scant cytoplasm and round hyperchromatic nuclei. There was multifocal lymphatic invasion (Fig. 5D and E). The mass was a malignant teratoma based on the
histologic appearance and lymphatic invasion. The histologic features of the peritoneal mass were similar to those of the previously described mass. Incidental findings included hepatic extramedullary hematopoiesis, vacuolar hepatic degeneration, and renal tubular degeneration. A fused bilateral malignant ovarian teratoma with peritoneal metastasis was confirmed based on the anatomic location and the histopathologic findings. DISCUSSION _________________________________ Previous retrospective studies of neoplastic lesions in hedgehogs revealed a high incidence of tumors (53%), including integumentary, hemolymphatic, digestive, endocrine, genital, musculoskeletal, and
FIGURE 3. Dorsal reconstructed computed tomography images. (A and B) Images at different levels on the initial scan. An irregular, lobulated large mass is apparent with heterogeneous density, mineralization, and hypodense areas (white arrows). The tubular soft tissue density structures attached to the mass from the pelvic cavity were considered to be bilateral uterine horns (open arrows). (C) The postmortem image shows a small peritoneal mass with a mineralized margin, suggesting peritoneal metastasis (arrowhead). LIV, liver; SP, spleen; ST, stomach; UB, urinary bladder. Song et al./Journal of Exotic Pet Medicine 23 (2014), pp 403–408
4 0 5
FIGURE 4. Ovarian teratoma and peritoneal metastasis in the African hedgehog. (A) A large bilaterally fused ovarian teratoma (M) and peritoneal metastasis (asterisk) in situ. The gross and histologic features of the peritoneal mass are similar to the ovarian mass. A uterine horn (white arrow) is attached to the surface of the mass. (B) An irregular multilobulated, firm ovarian mass is overlain by a perforated capsule. The uterine horns (arrows) are identified.
nervous system tumors, in decreasing order of frequency.1,2 In the genital system of captive African hedgehogs, tumors were most frequently found in the uterus and were identified as adenosarcoma, endometrial stromal sarcoma, adenoleiomyosarcoma, and adenoleiomyoma.3 Ovarian granular cell tumor and testicular neurofibrosarcoma have also been reported in hedgehogs.4,5 Teratomas are germ cell tumors that develop from pluripotent germ cells and differentiate into different tissues from 2 or 3 embryonic layers.6 Most teratomas described in the
veterinary literature have been intragonadal and ovarian teratomas; they have been reported in a variety of animals, including dogs,7-9 cats,7,10 pigs,6 horses,11 cattle,7 and rodents.7,12 However, ovarian teratomas have not been previously reported in hedgehogs. Similar to other animals, geriatric hedgehogs have an increased incidence of neoplasia when compared with their younger counterparts. The median age at the time of diagnosis of hedgehog neoplasms is 3.5 years, although the age of reproductive system neoplasia in these animals
FIGURE 5. Photomicrographs of the ovarian teratomas in the African hedgehog. (A) Chondrocytes within lacunae embedded in a cartilaginous matrix (C) and glandular structures (G) with mucin-secreting goblet-type epithelial cells. (B) Stratified squamous epithelium with central keratinization (S) and hair follicles (H). (C) Glandular structure (R) lined by a single layer of cuboidal to ciliated columnar epithelial cells. (D) Primitive mesenchymal cells with scant cytoplasm and round hyperchromatic nuclei are embedded in connective tissue. (E) Neoplastic cells in lymphatics. H&E stain; bar ¼ 50 mm. H&E, hematoxylin and eosin.
4 0 6
Song et al./Journal of Exotic Pet Medicine 23 (2014), pp 403–408
ranges between 2 and 5 years.1,2 In human medicine, malignant teratomas occur more commonly in younger individuals than benign teratomas or other genital tumors.13 The hedgehog described in this report was younger than the average age at which neoplasia occurs, which is consistent with the finding of malignant teratomas in humans. The clinical presentation of teratomas in humans is nonspecific and mostly asymptomatic, as was observed in this case.13 The abdominal mass was suspected to be an adenoma or adenocarcinoma following fine-needle aspiration and cytologic examination. Cytologically, teratomas are characterized by a necrotic background, keratin debris or keratinocytes, inflammatory cells including neutrophils or macrophages, and clusters of differentiated epithelial cells.14 This case lacked the consistent cytologic features of teratomas except for amorphous background materials. Pleomorphic glandular epithelial cells were presumed to be extracted from glandular elements within the teratoma. Depending on the presence of undifferentiated elements or metastasis, teratomas can be classified as benign (mature) or malignant (immature). Malignant teratomas contain embryonic elements in addition to well-differentiated tissues and may show metastatic features.15 Malignant teratomas are rare, whereas benign cystic teratomas are the most common ovarian neoplasm in humans, accounting for 25% or more of all ovarian tumors.16,17 In this case, the teratoma was found to be malignant because of the presence of immature elements and lymphatic invasion. Furthermore, the malignant nature was confirmed by peritoneal metastasis. In humans, malignant ovarian teratomas can metastasize to the pelvis, abdominal peritoneum, and omentum by implantation, whereas hematogenous metastasis to other organs is rare. Bilateral malignant ovarian teratomas are very rare, whereas benign teratomas are bilateral in 10% to 15% of human patients. Contralateral metastasis can occur in ovarian malignant teratomas in advanced stages.13 In this case, both ovaries were affected and there was fusion of the ovarian masses. Histopathologic examination of other organs showed no metastasis; however, several nonspecific abnormal findings were observed. Splenic extramedullary hematopoiesis is a common finding and is a normal feature in this species.18 Although imaging of ovarian tumors is not specific, and these tumors can range from cystic to
solid masses, the key imaging features for each type of ovarian tumor have been described in human studies and may be helpful in narrowing the differential disease diagnosis.19,20 When compared with the imaging features of ovarian tumors in previous studies, the CT findings in this case were consistent with those of malignant ovarian teratomas characterized by a large, irregular, and predominantly solid component with scattered mineralization, small cystic or necrotic foci, and fat. Benign teratomas, which are mostly cystic mature teratomas, present as rather small cystic structures containing fat, with or without calcification.21 The history, clinical presentation, and diagnostic imaging findings of this African hedgehog were consistent with malignant bilateral ovarian teratomas, and a definitive diagnosis was confirmed by histopathologic examination. Ovarian teratomas should be included in the differential diagnosis of intra-abdominal tumors in female hedgehogs. Furthermore, imaging features of a large, predominantly solid ovarian mass with mineralization, necrosis, or fatty areas are strongly suggestive of a malignant ovarian teratoma. REFERENCES 1. Heatley JJ, Mauldin GE, Cho DY: A review of neoplasia in the captive African hedgehog (Atelerix albiventris). Semin Avian Exot Pet Med 14:182-192, 2005 2. Raymond JT, Garner MM: Spontaneous tumours in captive African hedgehogs (Atelerix albiventris): a retrospective study. J Comp Pathol 124:128-133, 2001 3. Mikaelian I, Reavill DR: Spontaneous proliferative lesions and tumors of the uterus of captive African hedgehogs (Atelerix albiventris). J Zoo Wildl Med 35:216-220, 2004 4. Wellehan JFX, Southorn E, Smith DA, et al: Surgical removal of a mammary adenocarcinoma and a granulosa cell tumor in an African pygmy hedgehog. Can Vet J 44: 235-237, 2003 5. Ramos-Vara JA: Soft tissue sarcomas in the African hedgehog (Atelerix albiventris): microscopic and immunohistologic study of three cases. J Vet Diagn Invest 13:442-445, 2001 6. Schlafer DH, Miller RB: Female genital system, in Maxie M (ed): Jubb, Kennedy and Palmer’s Pathology of Domestic Animals (ed 2), pp 429-564, 2007 7. Dehner LP, Norris HJ, Garner FM, et al: Comparative pathology of ovarian neoplasms: III. Germ cell tumours of canine, bovine, feline, rodent, and human species. J Comp Pathol 80:299-306, 1970 8. Greenlee PG, Patnaik AK: Canine ovarian tumors of germ cell origin. Vet Pathol 22:117-122, 1985 9. Patnaik AK, Schaer M, Parks J, et al: Metastasizing ovarian teratocarcinoma in dogs: a report of two cases and review of literature. J Small Anim Pract 17:235-246, 1976 10. Basaraba RJ, Kraft SL, Andrews GA, et al: An ovarian teratoma in a cat. Vet Pathol 35:141-144, 1998 11. Frazer GS, Robertson JT, Boyce RW: Teratocarcinoma of the ovary in a mare. J Am Vet Med Assoc 193:953-955, 1988
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primary ovarian neoplasms diagnosed in the Denver Standard Metropolitan Statistical Area, 1 July-31 December 1969 and 1 July-31 December 1979. Int J Gynecol Pathol 1:3-16, 1982 Raymond JT, White MR: Necropsy and histopathologic findings in 14 African hedgehogs (Atelerix albiventris): a retrospective study. J Zoo Wildl Med 30:273-277, 1999 Jung SE, Lee JM, Rha SE, et al: CT and MR imaging of ovarian tumors with emphasis on differential diagnosis. Radiograph 22:1305-1325, 2002 Outwater EK, Siegelman ES, Hunt JL: Ovarian teratomas: tumor types and imaging characteristics. Radiograph 21: 475-490, 2001 Saba L, Guerriero S, Sulcis R, et al: Mature and immature ovarian teratomas: CT, US and MR imaging characteristics. Eur J Radiol 72:454-463, 2009
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