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Fatal Haemorrhage and Neoplastic Thrombosis in a Captive African Lion

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Fatal Haemorrhage and Neoplastic Thrombosis in a Captive African Lion Gonzales‑Viera et al. Acta Vet Scand (2017) 59:69 DOI 10.1186/s13028-017-0337-5 Acta Veterinaria Scandinavica CASE REPORT Open Access Fatal haemorrhage and neoplastic thrombosis in a captive African lion (Panthera leo) with metastatic testicular sex cord–stromal tumour Omar Antonio Gonzales‑Viera1,2, Angélica María Sánchez‑Sarmiento1* , Natália Coelho Couto de Azevedo Fernandes3, Juliana Mariotti Guerra3, Rodrigo Albergaria Ressio3 and José Luiz Catão‑Dias1 Abstract Background: The study of neoplasia in wildlife species contributes to the understanding of cancer biology, manage‑ ment practices, and comparative pathology. Higher frequencies of neoplasms among captive non-domestic felids have been reported most commonly in aging individuals. However, testicular tumours have rarely been reported. This report describes a metastatic testicular sex cord–stromal tumour leading to fatal haemorrhage and thrombosis in a captive African lion (Panthera leo). Case presentation: During necropsy of a 16-year-old male African lion, the left testicle and spermatic cord were found to be intra-abdominal (cryptorchid), semi-hard and grossly enlarged with multiple pale-yellow masses. Encap‑ sulated haemorrhage was present in the retroperitoneum around the kidneys. Neoplastic thrombosis was found at the renal veins opening into the caudal vena cava. Metastases were observed in the lungs and mediastinal lymph nodes. Histology revealed a poorly diferentiated pleomorphic neoplasm comprised of round to polygonal cells and scattered spindle cells with eosinophilic cytoplasm. An immunohistochemistry panel of inhibin-α, Ki-67, human placental alkaline phosphatase, cytokeratin AE1/AE3, cKit, vimentin and S100 was conducted. Positive cytoplasmic immunolabeling was obtained for vimentin and S100. Conclusions: The gross, microscopic and immunohistochemical fndings of the neoplasm were compatible with a poorly diferentiated pleomorphic sex cord–stromal tumour. Cause of death was hypovolemic shock from extensive retroperitoneal haemorrhage and neoplastic thrombosis may have contributed to the fatal outcome. To our knowl‑ edge, this is the frst report of sex cord–stromal tumour in non-domestic felids. Keywords: Immunohistochemistry, Panthera leo, Sex cord–stromal gonadal tumour Background techniques such as immunohistochemistry in non- Te study of neoplasia in wildlife species contributes to domestic species. Studies of tumour prevalence in cap- the understanding of cancer biology, species manage- tive felids are scarce and originate from zoo collections, ment [1] and comparative pathology due to the diverse but suggest high frequencies of neoplasia, up to 51% cancer presentations and complementary diagnostic [2–4]. Nevertheless, testicular tumours have rarely been reported. Tose previously reported include: Sertoli cell *Correspondence: [email protected] tumour in a snow leopard (Panthera uncia) [5], a clouded 1 Laboratório de Patologia Comparada de Animais Selvagens, leopard (Neofelis nebulosa) [6], an Amur tiger (Panthera Departamento de Patologia, Faculdade de Medicina Veterinária e tigris altaica) [7], and a jungle cat (Felis chaus) with mul- Zootecnia, Universidade de São Paulo, São Paulo, SP 05508270, Brazil Full list of author information is available at the end of the article tiple neoplasms [8]; and seminoma in a clouded leopard © The Author(s) 2017. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Gonzales‑Viera et al. Acta Vet Scand (2017) 59:69 Page 2 of 6 [9], snow leopards and a tiger [3, 10]. Studies indicate that at 4 °C. For amplifcation and detection, the horserad- older non-domestic felids are more likely to develop tes- ish peroxidase polymer system (Hidef detection®, Cell ticular neoplasms than juveniles as is recognized in other Marque, Rocklin, CA, USA) and the avidin–biotin com- species. Although, testicular neoplasms are rarely seen in plex (Vectastain®, Vector Laboratories, Burlingame, CA, domestic cats, seminoma, Sertoli cell and interstitial cell USA; for PLAP) were employed with 3,3′-diaminoben- tumours have been reported [11]. Testicular neoplasms zidine as the chromogen and Harris’s Haematoxylin for are most commonly found in dogs, with interstitial cell counterstaining. Antibodies were tested with an internal tumours occurring mainly in mature and old animals control (cells expected to display positivity in lion tis- [11]. In dogs, the three main testicular neoplasms are the sues), as well as human and/or another felid (tiger) tis- two types of sex cord–stromal tumours: the Sertoli cell sues as positive controls (Table 1). tumour (sustentacular) and interstitial (endocrine) Ley- Histologically, a highly cellular poorly diferentiated dig cell tumour, and the germ cell tumour: seminoma. pleomorphic neoplasm was present at the left testicle, Te next most common type is the mixed germ cell- composed predominantly of round to polygonal cells sex cord stromal neoplasm (gonadoblastoma) [11]. Tis with scattered spindle cells (Fig. 2a) and “signet ring” study describes a case of metastatic testicular sex cord– cells (Fig. 2b). Neoplastic cells had moderate to abun- stromal tumour with fatal haemorrhage and neoplastic dant eosinophilic cytoplasm, were poorly delineated thrombosis in an African lion (Panthera leo). with round nuclei, fne chromatin and prominent nucle- oli. Marked anisocytosis, anisokaryosis, karyomegaly Case presentation (Fig. 2c), and a mitotic rate of 5 mitotic fgures/high- A 16-year-old male African lion was presented for nec- power feld (40 ×) was observed (Microscope Olympus, ropsy to the School of Veterinary Medicine and Animal Model BX40). Multiple foci of mononuclear cell infltra- Sciences, University of São Paulo, Brazil. Te animal had tion and mineralization were seen in the mass. Metasta- lived for 13 years in a circus and was then transferred ses had similar histologic features to the primary tumour. to an exotic felid sanctuary. According to the sanctuary At the openings of the renal veins into the caudal vena veterinarian, the day before death the animal appeared cava, the thrombus showed multiple clusters of neoplas- depressed, regurgitated, and was ataxic, falling multi- tic cells attached to the luminal surface, surrounded by ple times. An unknown dose of morphine was admin- fbrin, erythrocytes and leukocytes (Fig. 2d). Te right istered and the animal died 5 h later. At necropsy, both testicle was atrophied with no evidence of active sper- kidneys were surrounded by clotted blood in the retrop- matogenesis. Other diagnoses included multiple peri- eritoneum (Fig. 1a). Te left testicle and spermatic cord biliary cysts and proliferative glomerulonephritis with were found intra-abdominal (cryptorchid) and grossly focally extensive erosive pyelitis. Neoplastic cells were enlarged (30 × 9 cm) (Fig. 1a, b) compared to the right PAS-negative, and presented strong positive cytoplasmic testicle (10 × 1.5 cm) (Fig. 1c), which was found in the immunolabeling for vimentin (Fig. 2e) and S100 (Fig. 2f) scrotum. Te enlarged left testicle was semi-hard with immunohistochemistry. Antibody specifcity, dilution, multiple yellow nodules from 0.5 to 6 cm in diameter positive controls and immunohistochemistry results are involving the epididymis, pampiniform plexus, and defer- displayed in Table 1. ent duct (Fig. 1b). On section, the masses were white to grey heterogeneous and vascular. Furthermore, a throm- Discussion and conclusions bus of 5 × 1.5 cm was found at the opening of the renal Considering the gross, microscopic and immunohis- veins into the caudal vena cava (Fig. 1d). Te lungs and tochemical fndings, the neoplasm was diagnosed as mediastinal lymph nodes exhibited multiple semi-soft a poorly diferentiated pleomorphic sex cord–stromal white nodules from 1 to 5 cm in diameter, consistent with tumour [12]. Tis classifcation has only been used in metastases. human medicine with support from immunohistochem- Samples were fxed in 10% neutral bufered formalin, istry with regard to diferential diagnoses [13]. PLAP is a processed by routine methods, embedded in parafn widely used antibody for seminoma diagnosis in humans wax, sectioned at 4 µm and stained with haematoxylin and in domestic dogs. Classical seminoma is the predom- and eosin (HE) and periodic acid Shif reaction (PAS). inant form in humans, expresses the germ cell markers Immunohistochemistry against inhibin-α, Ki-67, human PLAP and cKit, and is PAS-positive. Te spermatocytic placental alkaline phosphatase (PLAP), cytokeratin seminoma is derived from more diferentiated cells and is AE1 + AE3, cKit, vimentin and S100 was carried out. the predominant form of seminoma in dogs [14–16]. Te Heat induced epitope retrieval was performed at 120 °C spermatocytic seminoma is PAS and vimentin negative (pressure cooker) for 3 min in 10 mmol/L citrate bufer, and does not, or only focally, express PLAP and cKit in pH 6.0. All primary antibodies were incubated overnight humans [17, 18]. cKit also has shown marked positivity in Gonzales‑Viera et al.
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