Abstract
Introduction
In the literature there is a lack of information about lemur medicine in captivity. There is scanty information concerning general medical aspects2,7,8 and there are very few reports on specific disease9. Neoplasia in lemurs has been scarcely reported apart from some primary liver tumors4,5,13,22 and pulmonary tumors13,19. We describe the clinical, anatomo-histomorphologic features of two unusual cases of neoplasia in two different lemurs hosted at Parco Natura Viva—Garda Zoological Park, Italy.
Case Report
Case 1: Lymphoma in Lemur catta
Clinical History
Prior to 2005 the 5-year-old female ring-tailed lemur did not show any clinical signs of illness. In March 2005 the animal was evaluated for depression, apathy, inappetence and a few episodes of regurgitation. She was thin (1.7 kg) and showed abdominal pain during palpation. Hematologic tests did not reveal any abnormalities; thus we started a medical treatment with carprofen (2 mg/kg) and joscina N-butilbromuro. Some weeks later, as no clinical improvement was noted, the lemur was anesthetized (medetomidine 0.05 mg/kg + ketamine 5 mg/kg) to perform a more detailed examination. A big firm mass was revealed in the epigastrium by the abdominal palpation and it was confirmed by radiographs: a large radiopaque mass about 3–4 cm in diameter. Two days later we decided to perform surgery: during laparotomy we found that the suspected neoplasm was completely inside the intestinal wall and the mass was removed through intestinal resection and anastomoses. The resected mass was submitted for histopathologic analysis. After ten days the lemur started to eat. However, 1 month later the same clinical signs reappeared: anorexia and several episodes of vomiting. The mass had regrown and was much bigger than before. The lemur was euthanatized due to poor prognosis.
Histopathology
The histologic evaluation of the first sample revealed heavy changes of the intestinal wall in the area of the ring inspissation. The intestinal wall was infiltrated by intense, multiphocal masses of neoplastic lymphocitis. There was also a complete absence of the tonaca propria, a massive degeneration of the submucosal tonaca and a strong and exuberant connectival new growth and a partial destruction of muscolar tonaca. The histologic feature revealed also different areas of multifocal necrosis that was often punctiform.
At the edge of the ring lesion there was an interesting inflammatory feature similar to “gluten-sensitive enteropathy” or “coeliac disease:” plasma cell and lymphocyte infiltration in the lamina propria, impressive villous atrophy and crypt hyperplasia with decreased villous height-to-crypt depth ratio and a pronounced increase in the number of intraepithelial lymphocytes. This complex histologic feature is known as media cells intestinal lymphoma associated with enteritis and is similar to “coeliac disease” of 3b level Marsh-Oberhuber.12 Tissue collected at necropsy revealed similar lesions.
Case 2: Leiomyosarcoma in Eulemur macaco macaco
Clinical History
In January 2005 a 9-year-old female black lemur was evaluated for a swelling in the left lower lip. Despite that, the lemur ate regularly and did not show any other clinical signs.
Twenty days later the neoplasm was so big (about 5 cm of diameter) that the lemur had difficulty eating normally. The animal was anesthetized to remove the neoplasm with a combination of medetomidine and ketamine IM and then intubated and maintained on isoflurane. This surgery was complicated because the neoplasm was so firmly attached to the tissue that it was impossible to remove the tumor entirely. Tissue was submitted for histologic examination. After 15 days the left lower lip had a deviated profile. Over the next 3 months the neoplasm recurred three times and thus in April 2005 the animal was humanely euthanatized.
Histopathology
Histopathology revealed a homogeneous neoplastic proliferation organized in a mass with very irregular edges and different degrees of local invasiveness. This neoplastic proliferation did not look ulcerative even if it deeply penetrated so that it involved abundantly the striate portion of buccinator muscles and labial glands. Some portions of the surface showed epidermic hyperplasia with serious invagination of the epidermis. This aspect is common in neoplasms like histiocytoma of the dog and equine sarcoid. Moreover, the inside part of the mass looked well-vascularized apart from different necrotic centers with hemorrhagic phenomenon. Structural and cytologic characteristics suggest that the mass was a cutaneous leiomyosarcoma originating with the piloerector muscles (pyeloleiomyosarcoma).
Discussion
Case 1
In literature there are few studies about lymphoma in primates and reports of this tumor in lemur are very rare.14 Thus this case is important because it gives information about lymphoma in Lemur catta and it is also interesting because in this case the tumor is associated with a similar “coeliac disease.” Furthermore, different authors underline that there is a higher risk to develop small-bowel non-Hodgkin’s lymphoma in human with coeliac disease.6,9,11,21 This report indicates that perhaps further investigation into the link between these two diseases in lemurs are warranted.
Case 2
Skin tumors of non-striated muscles are unusual both in domestic carnivores10 and in humans3. In particular leiomyosarcoma is rare: it represents about 2–3% of human dermal mesenchymal tumors18 and less of 1% of dermal tumors of domestic carnivores16. This neoplasm occurs more frequently in dogs and ferrets.15 To the authors’ knowledge in non-human primates there is only one previous report of a skin tumor in a Peruvian squirrel monkey. The present paper represents an interesting integration to the existing literature. It is important to underline that the clinical and histologic features of the described neoplasm seem to be more aggressive than those seen in other species. It is also noteworthy that the tumor originated from the piloerector muscle as this is not very often seen.
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