Mycobacterium tuberculosis var. tuberculosis infection in two captive black capuchins (Sapajus nigritus) in Southern Brazil

Abstract

Tuberculosis is a common zooanthroponosis in humans with a high incidence in Brazil, but it may also affect non-human primates (NHPs), of which Old World primates are most commonly involved. Nonetheless, its occurrence in New World primates is unknown, and therefore, this study aimed to describe the infection by Mycobacterium tuberculosis variant tuberculosis in two captive black capuchin monkeys (Sapajus nigritus) in Southern Brazil. The primates were housed in the same enclosure, wherein close contact with humans frequently occurred, and presented apathy, anorexia, and death in a clinical course of 15 days to 2 months. At the necropsy, the tracheobronchial lymph nodes were markedly enlarged and firm to hard and on the cut surface had a caseous aspect. The lungs exhibited two injury patterns: multifocal and disseminated. Microscopically, the lungs exhibited multifocal to coalescing necrotic granulomas and non-necrotic granulomas, with multiple acid-fast bacilli within the cytoplasm of epithelioid macrophages and multinucleated giant cells. Bacilli were also labeled upon immunohistochemistry (IHC) for Mycobacterium tuberculosis. Microbiological culture of lung samples from both cases yielded colonies compatible with M. tuberculosis. The isolates were identified as M. tuberculosis var. tuberculosis through polymerase chain reaction (PCR). Although tuberculosis is poorly described in New World primates, M. tuberculosis var. tuberculosis may cause a highly contagious and progressive disease with high mortality in black capuchin monkeys (S. nigritus).

Keywords: Granulomatous pneumonia; Mycobacterium tuberculosis; New World primates; Zooanthroponosis.

Fig. 1

Gross features of Mycobacterium tuberculosis var. tuberculosis infection in Sapajus nigritus in Southern Brazil. a Unilateral, yellow, catarrhal, nasal discharge in monkey 1. b Monkey 1 lung parenchyma, multifocal yellow nodules measuring 0.5 to 2 cm in diameter (arrow), with mildly enlarged lungs. c Monkey 2 lungs are markedly enlarged, non-collapsed, with almost total parenchyma replacement by multifocal to coalescing yellow nodules measuring 0.3 to 3 cm in diameter, in addition to multifocal areas of pleural adhesion. d Monkey 1 mesenteric lymph nodes, severely enlarged, yellow, and measuring 1 cm in diameter

Fig. 2

Microscopic features of Mycobacterium tuberculosis var. tuberculosis infection in Sapajus nigritus in Southern Brazil. a Lung, caseous granuloma, severe caseous necrosis surrounded by an inflammatory infiltrate of epithelioid macrophages, degenerate neutrophils, and rare multinucleated giant cells. Hematoxylin and eosin (HE), × 100. b Lung, noncaseous granuloma, severe inflammatory infiltrate of epithelioid macrophages, lymphocytes, plasma cells, and neutrophils. HE, × 200. c Large amounts of acid-fast bacilli within the cytoplasm of macrophages and Langhans multinucleated giant cells. Ziehl–Neelsen staining, × 1000. d Marked immunolabeling is observed within the cytoplasm of epithelioid macrophages upon immunohistochemistry anti–M. tuberculosis. 3-amino-9-ethylcarbazole chromogen (AEC), × 1000