Pathology of the emerging Mycobacterium tuberculosis complex pathogen, Mycobacterium mungi, in the banded mongoose (Mungos mungo)

Authors: ALEXANDER, KATHLEEN - Virginia Polytechnic Institution & State University; LAVER, PETER - Virginia Polytechnic Institution & State University; WILLIAMS, MARK - University Of Pretoria; SANDERSON, CLAIRE - Virginia Polytechnic Institution & State University; KANIPE, CARLY - Iowa State University; Palmer, Mitchell

Submitted to: Veterinary Pathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/12/2017
Publication Date: 12/19/2017
Citation: Alexander, K.A., Laver, P.N., Williams, M.C., Sanderson, C.E., Kanipe, C., Palmer, M.V. 2017. Pathology of the emerging Mycobacterium tuberculosis complex pathogen, Mycobacterium mungi, in the banded mongoose (Mungos mungo). Veterinary Pathology. 55(2):303-309. doi:10.1177/0300985817741730.
DOI: https://doi.org/10.1177/0300985817741730

Interpretive Summary: Wild banded mongooses (Mungos mungo) in northeastern Botswana and Northwest Zimbabwe are infected with a new tuberculosis-causing bacterial species known as Mycobacterium mungi. This bacteria, which is closely related to the bacteria causing human tuberculosis, is transmitted environmentally between mongoose through exposure to infected scent marks (urine and anal gland secretions). We examined a total of 200 banded mongooses, analysing 145 of these microscopically. Signs of tuberculosis were most common in the lung, liver, spleen, lymph nodes, perirectal tissue and kidneys. Lungs showed signs of tuberculosis only in cases of severely advanced disease. These signs are consistent with bacterial shedding occurring through infected scent glands and subsequent invasion through the nasal cavity or breaks in the skin on the bridge of the nose, followed by spread through blood or lymphatic vessels. This method of transmission is novel compared to tuberculosis-causing bacteria in other species. Using scent marking allows the bacteria to be transmitted indirectly to other mongoose without direct contact. This route of transmission should be investigated in other wildlife species where tuberculosis persists, causing risk to humans or livestock.

Technical Abstract: Wild banded mongooses (Mungos mungo) in northeastern Botswana and Northwest Zimbabwe are infected with a novel Mycobacterium tuberculosis complex pathogen (MTC), M. mungi. This pathogen is transmitted environmentally between mongoose hosts through exposure to infected scent marks used in olfactory communication (urine and anal gland secretions). In Northern Botswana, repeated dry season outbreaks (2000 to 2016) threaten persistence of smaller troops with infected individuals dying within three months of clinical presentation. We conducted gross examination of banded mongooses (n=200) and further analysed a subset of these histologically (n=145, 1999-2017). Across tissues, multifocal irregular, lymphohistiocytic infiltrates to multifocal or coalescing non-caseating to caseating granulomas were observed with variable numbers of intralesional acid-fast bacilli (AFB). Tissue involvement varied among affected individuals but was highest in the lung, liver, spleen, and lymph nodes with involvement of the perianal tissue, anal lymph nodes, and kidneys. Pulmonary lesions were present only in cases of advanced disseminated disease. The pathological presentation is consistent with pathogen shedding occurring through infected scent glands and subsequent invasion occurring through percutaneous movement of the pathogen through breaks in the skin, nasal planum, and/or rostrum. Given the character and distribution of lesions and presence of intracellular AFB, we hypothesize that pathogen spread occurs through haematogenous and/or lymphatic spread. Features common in prototypical granulomas such as multinucleated giant cells and peripheral fibrosis were rarely present in affected mongooses. AFB were consistently found intracellularly, even in regions of necrosis. The mongoose genome has a specific deletion (RD1mon), which includes part of the encoding region for PPE68 (Rv3873), a gene co-operonic with PE35. These proteins can influence the host’s cellular immune response to mycobacterial infections and remains an important area of future investigation into the pathophysiology of M. mungi infection in the banded mongoose host.