Human-origin Tuberculosis in Southeast Asian Bears: Epidemiological and Diagnostic Insights

Kirsty M Officer

Exploitation of bears via the illegal wildlife trade risks exposing them to pathogens unlikely to be encountered in the wild, through conditions inherent to capture, transit, and ongoing captivity. Tuberculosis (TB), a disease of humans and livestock that requires close contact to spread, is a prime example of this risk, particularly in regions with high human TB endemism alongside the trade in, and rescue of, bears. This thesis aimed to explore the origin/s and epidemiology of an outbreak of TB in a population of sun bears (Helarctos malayanus) and Asiatic black bears (Ursus thibetanus) at a bear rescue centre in Cambodia, and the utility of locally available diagnostic methods for management of such outbreaks. Confirmed TB of human origin had not previously been described in either species. Between 2009 – 2024, Mycobacterium tuberculosis was isolated from 35 cases (31 sun bear, three Asiatic black bear, and one staff member). Using isolates from the first 32 cases (occurring between 2009 and 2019), alignment of antimicrobial susceptibility testing and genotyping of isolates revealed two clusters, which were confirmed and further explored with whole genome sequencing. We combined epidemiolocal data with single nucleotide polymorphism analysis and exploration of mixed base calls to indicate the evolution of each cluster. We established a likely transmission route in one cluster where the human case acted as an intermediatory between bear cases. Results from testing of 344 bears at three regional bear rescue centres were used to build a Bayesian latent class model to explore the accuracy of available tests for diagnosing pulmonary TB in bears. Five tests were included; microscopy, PCR, and culture of respiratory tract samples, thoracic radiography, and a patient-side lateral flow test designed to detect antibodies to key Mycobacterium tuberculosis complex antigens in serum from elephants and cervids. Our model demonstrated the high specificity and suboptimal sensitivity of the microbiological tests, and a need for caution when interpreting the serological test results. Thoracic radiography was the only diagnostic method with both sensitivity and specificity estimated by the Bayesian latent class model to be above 90%. Finally, we explored the use of thoracic radiography as a screening tool for sun bears at risk of TB, using radiographs from a subpopulation of confirmed TB cases and control (apparently healthy) sun bears. Our results supported the high specificity of radiographic changes for TB diagnosis, and highlighted sensitivity challenges when radiographic changes are subtle, extra-pulmonary, or there are concurrent differential diagnoses to explain changes. The results of this thesis drive evidence-based recommendations to support veterinary and husbandry staff managing bears in resource-poor, high human TB settings, where the surveillance for, and response to, TB outbreaks can have significant consequences for animal welfare, public health, and conservation goals.

Human-origin Tuberculosis in Southeast Asian Bears: Epidemiological and Diagnostic Insights

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