AEMV Forum
Management of an Extraskeletal Osteosarcoma in an African Hedgehog (Atelerix albiventris) Kristen Phair, DVM, James W. Carpenter, DVM, MS, Dip. ACZM, Judilee Marrow, DVM, Gordon Andrews, DVM, PhD, Dip. ACVP, and Bhupinder Bawa, DVM, PhD
Abstract A 5-year-old female African hedgehog (Atelerix albiventris) was presented with a mass on its left caudodorsal flank and progressive lethargy. A fine-needle aspirate of the mass was suggestive of a malignant spindle cell tumor. After the diagnostic test results were obtained, the mass was surgically removed. Histopathological examination of tissue sections from the mass revealed incomplete excision of an extraskeletal osteosarcoma. Approximately 2 months after surgery, the patient suddenly died. Gross examination at necropsy revealed multifocal nodules within the spleen, liver, and lungs. Histopathology of the tissues that contained the multifocal nodules was consistent with metastatic osteosarcoma, originating from the original extraskeletal soft tissue osteosarcoma on the flank. Incidental uterine leiomyoma was also discovered at necropsy. To the authors’ knowledge, this is the first reported attempt at surgical treatment of the rarely documented extraskeletal osteosarcoma in a hedgehog. Copyright 2011 Elsevier Inc. All rights reserved. Key words: Atelerix albiventris; extraskeletal osteosarcoma; hedgehog; leiomyoma; neoplasia; spindle cell tumor
A
5-year-old intact, 374-g female African hedgehog (Atelerix albiventris) was presented to the Kansas State University Veterinary Medical Teaching Hospital for lethargy of 1 week’s duration and progressive swelling of the left caudolateral flank (Fig 1). The hedgehog’s husbandry and behavior were otherwise unremarkable with normal appetite, urination, and bowel movements. The patient was manually restrained and anesthetized with isoflurane gas administered via face mask. On physical examination, a 3.8 ⫻ 5.1 cm ulcerated mass on the left caudolateral dorsum was observed. Mild gingivitis and tartar were also present when the oral cavity was evaluated. While anesthetized, a fine-needle aspirate of the mass was obtained. Cytology of the aspirate showed both individual and aggregate spindle cells with round,
oval, to elongated nuclei, coarsely granular chromatin patterns, prominent nucleoli, and moderate amounts of light blue cytoplasm (Wright’s stain). Binucleation
From the Zoological Medicine Service, Veterinary Medical Teaching Hospital, Kansas State University College of Veterinary Medicine, Manhattan, KS USA; Department of Diagnostic Medicine/Pathobiology, Veterinary Medical Teaching Hospital, Kansas State University College of Veterinary Medicine, Manhattan, KS USA. Address correspondence to: Kristen Phair, DVM, Sacramento Zoo, 3930 West Land Park Drive, Sacramento, CA 95822. E-mail:
[email protected]. © 2011 Elsevier Inc. All rights reserved. 1557-5063/11/2002-$30.00 doi:10.1053/j.jepm.2011.02.011
Journal of Exotic Pet Medicine, Vol 20, No 2 (April), 2011: pp 151–155
151
152
Figure 1. Caudolateral mass (arrows) on the left flank of a 5-yearold African hedgehog.
and multinucleation were common along with moderate anisocytosis and anisokaryosis (Fig 2). A malignant spindle cell tumor was suspected and excisional biopsy was recommended to the owner. Twenty-one days after the initial presentation the hedgehog re-presented for surgical removal of the mass. While at home the hedgehog’s activity level had continued to decrease, its body weight was reduced by 30 g, and the mass had grown to 4.0 ⫻ 6.1 cm and appeared to have necrotic areas. Preoperative radiographs (Fig 3) revealed a large superficial, caudal abdominal, dorsal, soft tissue mass with amorphous regions of mineral opacity. The mass measured approximately 5.2 ⫻ 6.3 ⫻ 4.4 cm on the radiographs and there was concurrent dorsal subluxation of the sacrocaudal intervertebral disc space and mineralization of the larynx and trachea. No obvious metastatic lesions were identified. The pa-
Figure 2. Fine-needle aspirate of the African hedgehog mass: spindle cells (arrows) at 1000⫻ magnification. Wright’s stain.
Phair et al
Figure 3. Right lateral whole body radiograph demonstrating the large soft tissue mass (arrows) associated with amorphous regions of mineral opacity.
tient was premedicated with buprenorphine (0.01 mg/kg subcutaneously, Buprenex; Reckitt Benckiser Pharmaceuticals Inc., Richmond, VA USA), ceftiofur (22 mg/kg subcutaneously, Naxcel; Pfizer Animal Health, New York, NY USA), and warm lactated Ringer’s solution (12 mL subcutaneously). Preanesthetic bloodwork was not performed because of the inherent difficulty in obtaining a blood sample from a conscious hedgehog. Anesthesia was induced via masking with isoflurane gas (5%) and oxygen (2 L/min) and maintained with isoflurane (range, 2%-5%) by means of intubation with an 18-gauge catheter. The patient was manually ventilated intermittently throughout the procedure. A 50-g, malodorous mass was surgically removed (Figs 4 and 5) via an elliptical skin incision and careful dissection from the surrounding tissue layers, and submitted for histopathological examination. The subcutaneous tissues were closed with absorbable suture and the skin was closed with nonabsorbable nylon cruciate sutures. The patient recovered from
Figure 4. Excised soft tissue mass with areas of necrosis.
Extraskeletal Osteosarcoma in an African Hedgehog
anesthesia uneventfully and was administered postoperative medication consisting of buprenorphine (0.01 mg/kg, every 6 hours, subcutaneously), amoxicillin/clavulanate (12 mg/kg, every 12 hours, orally, Clavamox; Pfizer Animal Health), and meloxicam (0.1 mg/kg, every 24 hours, orally, Metacam; Boehringer Ingelheim Vetmedica Inc., St. Joseph, MO USA). Also after the surgery, 10 mL of warm lactated Ringer’s solution was subcutaneously administered to the patient. One day after the surgical procedure the patient was eating well and the surgical site was clean and intact. A warm compress was applied to the surgical site for 10 minutes. The patient was discharged with instructions to apply a cold compress to the surgery site 2 to 3 times daily for 3 to 5 days, and to continue the administration of meloxicam for 3 days and amoxicillin/clavulanate for 10 days. Histopathology of the excised tissue revealed a moderately well-delineated, densely cellular neoplasm contained within the dermis and subcutis. The neoplasm consisted of a highly pleomorphic population of cells including spindyloid cells arranged in bundles and sheets, binucleate and multinucleated osteoclastic-type cells, tumor osteoid, and mineralized neoplastic bone (Figs 6 and 7). The center of the neoplasm was mostly necrotic and the necrosis extended to the ulcerated skin surface. Neoplastic cells also extended to the surgical margins. Based on these findings, a diagnosis of an extraskeletal osteosarcoma with incomplete excision was made. The patient returned 19 days later for suture removal, and based on the owner’s observation at that time the patient was determined to be recovering well from the surgical procedure. During the recheck physical examination, the healed surgical site appeared to have firm margins. The owner was
Figure 5. Closed surgical site (arrows) after mass removal.
153
Figure 6. Photomicrograph of an extraskeletal osteosarcoma. A pleomorphic population of spindyloid to stellate neoplastic osteoblasts surrounds and are embedded within tumor osteoid (asterisk). Part of the osteoid is mineralized (arrow). Hematoxylin and eosin. Bar ⫽ 50 m.
warned of the high risk of recurrence given the tumor type and the incomplete excision. Approximately 2 months after the surgical procedure, the patient was found dead in its cage and was presented for a pathological examination of the body. Gross findings of the hedgehog’s body revealed: multifocal, raised, round, tan, 3 to 4 mm nodules on the lung surface and throughout the parenchyma; multifocal, raised, round, yellow-tan nodules on the liver surface and throughout the parenchyma (Fig 8); multifocal, raised, round, small, light tan opacities on the serosal surface of the kidneys; a very firm distended uterus containing mucoid material within the lumen; and a single spine
Figure 7. Extraskeletal osteosarcoma. Note the multinucleated osteoclastic cells mixed with neoplastic osteoblasts. Hematoxylin and eosin. Bar ⫽ 50 m.
154
Figure 8. Multifocal nodules on the surface of the liver (arrows). These lesions contained osteoid-producing neoplastic cells that had metastasized from the original tumor site.
associated with normal ingesta contained within the stomach. Histopathologic examination of the liver revealed multifocal areas of spindyloid cells arranged in interlacing bundles and streams, marked anisocytosis and anisokaryosis, and osteoid-producing neoplastic cells and associated mineralization within the parenchyma (Fig 9). The spleen contained a focal mass composed of spindyloid neoplastic cells (similar in morphology to those found in the liver), a focal area of necrosis with an adjacent thrombosed blood vessel, and diffuse extramedullary hematopoeisis. Within the lung parenchyma and wall of the bronchi were multifocal nodules composed of spindyloid neoplastic cells. The alveoli contained hemorrhage, proteinaceous fluid, fibrin, and moderate numbers of foamy macrophages. The uterine wall contained a focal polypoid mass composed of welldifferentiated neoplastic smooth cells. Other histopathologic findings included a multifocal, lymphoplasmacytic gastritis within the stomach wall, and multifocal glomerular basement membrane thickening within the kidneys. Given the patient’s history and the similar histopathologic characteristics of the surgically excised mass, the lesions within the liver, lung, and spleen represented metastasis of the original flank osteosarcoma. The mass within the uterus was consistent with a uterine leiomyoma and was considered an incidental finding.
Phair et al
mal) tumors are the third most common type of tumor documented in African hedgehogs, with an incidence of approximately 4% on necropsy.1 Examples of mesenchymal tumors found in African hedgehogs include histiocytic sarcoma, fibrous histiocytoma, neurofibrosarcomas, osteosarcomas, hemangiomas, fibrosarcomas, uterine leiomyomas, and undifferentiated sarcomas.1-4 There have been 7 documented cases, including this case, of osteosarcoma reported in the hedgehog.1-5 Two of the documented cases had multicentric skeletal sarcomas and may have been associated with a retrovirus infection.2 There are even fewer reports of extraskeletal osteosarcomas in hedgehogs. To the authors’ knowledge, there is only one other report of a soft tissue osteosarcoma without an apparent skeletal origin in hedgehogs.1,6 All other previous reports of osteosarcoma in the African hedgehog have originated from a specific skeletal structure.1-4 Regardless of the various origins of osteosarcomas reported in hedgehogs, surgical treatment of the tumors is not mentioned in the literature. In the aforementioned cases of osteosarcoma, the patients were either euthanized because of suspicion of an aggressive neoplastic process with a diagnosis confirmed at necropsy, or the tumors were identified at necropsy as an incidental finding.1-4 This case report represents the first published attempt at surgical management of a confirmed osteosarcoma in the hedgehog. Although the exact mechanism of acute death in this patient is unknown, the degree of metastases present and presumably resulting multi-organ dysfunction may have contributed to the death. The uterine leiomyoma was an incidental finding and most likely did not contribute to the patient’s death,
Discussion Neoplasia is an exceedingly common antemortem and postmortem finding in African hedgehogs. After epithelial and round cell tumors, spindle cell (mesenchy-
Figure 9. Metastatic tumor in the liver. Note the same microscopic features as the primary extraskeletal osteosarcoma in Figure 6. Hematoxylin and eosin. Bar ⫽ 50 m.
155
Extraskeletal Osteosarcoma in an African Hedgehog
although it does demonstrate the concurrent presence of 2 distinct mesenchymal tumor types, osteosarcoma and uterine leiomyoma. Less than 10% of hedgehogs diagnosed with neoplasia have more than 1 tumor type.1-6 The extramedullary hematopoiesis found within the spleen is a common necropsy finding based on previously published case reports.4,5,7,8 The metastatic lesions found during necropsy in this case suggest that osteosarcoma in the African hedgehog is similar to osteosarcoma in other species. Therefore, in all probability hedgehog osteosarcomas are highly aggressive and likely to metastasize.1 A fine-needle aspirate of the tissue mass may be suggestive for tumor type, but ultimately biopsy and histopathology are needed to determine a definitive diagnosis.1,9 Ideally, staging of the disease using diagnostic test results (e.g., blood work, radiographs, abdominal ultrasound, computed tomography) should be performed before surgical therapy to provide prognostic information. However, not all of the diagnostic procedures mentioned above may be practical to perform, and even if performed may not indicate the degree of metastases present. In this case, full body radiographs obtained at the time of surgery did not indicate the presence of lung metastases that were found 2 months later at necropsy. Although surgical management of osteosarcoma is unlikely to prolong survival times and even less likely to be curative (based on our knowledge of osteosarcoma behavior in domestic species), it may play a palliative role and enhance quality of life as perceived by the owner. Until further attempts are made at surgical treatment of osteosarcoma in general and extraskeletal osteosarcoma in particular, the possible benefits of this form of treatment are unknown. If owners are considering surgical treatment, they should be adequately warned of the possibility of concurrent diseases and the effects these diseases may have on patient survival during and after surgery.
Acknowledgments The author wishes to thank Don Peterson, VMD, Steven L. Stockham, DVM, MS, Dip. ACVP, and Jennifer L. Johnson-Neitman, DVM, for assistance with this case.
References 1.
2.
3.
4.
5.
6.
7.
8.
9.
Heatley JJ, Mauldin GE, Cho DY: A review of neoplasia in the captive African hedgehog (Atelerix albiventris). Semin Avian Exotic Pet Med 14:182-192, 2005 Peauroi JR, Lowenstein LJ, Munn RJ, et al: Multicentric skeletal sarcomas associated with probable retrovirus particles in two African hedgehogs (Atelerix albiventris). Vet Pathol 31:481-484, 1994 Rhody JL, Schiller CA: Spinal osteosarcoma in a hedgehog with pedal self-mutilation. Vet Clin Exotic Anim 9:625-631, 2006 Benoit-Biancamano M, d’Anjou M, Girard C, et al: Rib osteoblastic osteosarcoma in an African hedgehog (Atelerix albiventris). J Vet Diagn Invest 18:415-418, 2006 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 Raymond JT, Garner MM: Spontaneous tumors in captive African hedgehogs (Atelerix albiventris): a retrospective study. J Comp Pathol 124:128-133, 2001 Ivey E, Carpenter JW: African hedgehogs, in Quesenberry KE, Carpenter JW (eds): Ferrets, Rabbits, and Rodents: Clinical Medicine and Surgery (ed 2). Philadelphia, PA, W.B. Saunders, pp 339-353, 2004 Ramos-Vara JA: Soft tissue sarcomas in the African hedgehog (Atelerix albiventris): microscopic and immunohistologic study of three cases. J Vet Diagn Invest 13:442-334, 2001 Juan-Salles C, Garner MM: Cytologic diagnosis of diseases of hedgehogs. Vet Clin Exotic Anim 10:51-59, 2001