From the Mouths of Monkeys: Detection of Mycobacterium tuberculosis Complex DNA From Buccal Swabs of Synanthropic Macaques

Abstract

Although the Mycobacterium tuberculosis complex (MTBC) infects a third of all humans, little is known regarding the prevalence of mycobacterial infection in nonhuman primates (NHP). For more than a century, tuberculosis has been regarded as a serious infectious threat to NHP species. Advances in the detection of MTBC open new possibilities for investigating the effects of this poorly understood pathogen in diverse populations of NHP. Here we report results of a cross-sectional study using well-described molecular methods to detect a nucleic acid sequence (IS6110) unique to the MTBC. Sample collection was focused on the oral cavity, the presumed route of transmission of MTBC. Buccal swabs were collected from 263 macaques representing 11 species in four Asian countries and Gibraltar. Contexts of contact with humans included free ranging, pets, performing monkeys, zoos, and monkey temples. Following DNA isolation from buccal swabs, the PCR amplified IS6110 from 84 (31.9%) of the macaques. In general, prevalence of MTBC DNA was higher among NHP in countries where the World Health Organization reports higher prevalence of humans infected with MTBC. This is the first demonstration of MTBC DNA in the mouths of macaques. Further research is needed to establish the significance of this finding at both the individual and population levels. PCR of buccal samples holds promise as a method to elucidate the mycobacterial landscape among NHP, particularly macaques that thrive in areas of high human MTBC prevalence.

The risk of tuberculosis transmission to free‐ranging great apes

“…Moreover, transmission pathways from humans through other animal hosts whose contact with humans and great apes are high must be closely evaluated. Spillover of MTC infection from domestic animals and possibly humans into free-living monkey populations is well documented and may be an important source of transmission of human or domestic animal tuberculosis infection to great apes [Keet et al, 2000;Sapolsky & Else, 1987;Tarara et al, 1985;Wilbur et al, 2012]. A recent diagnosis of tuberculosis infection in a wild chimpanzee by a novel MTC strain underscores the knowledge gaps on the epidemiology and impact of tuberculosis to primate conservation [Coscolla et al, 2013].…”

“…These statistics as well as the high prevalence of HIV co-infection among humans in this region raises additional concern for transmission risk, as co-infection with HIV generally results in a higher likelihood of active tuberculosis. Furthermore, recent evidence of MTC DNA among populations of free-ranging synanthropic macaques demonstrates that frequent human contact and high tuberculosis prevalence within the human population increases the risk of tuberculosis for non-human primate populations [Wilbur et al, 2012]. Unfortunately, the epidemiology of tuberculosis is not so simple as to be explained by basic SIR models.…”

“…Saliva samples from animals with clinical signs of disease could be utilized for the detection and genotyping of M. tuberculosis through culture and/or commonly employed techniques such as IS6110 PCR-RFLP, spoligotyping, or mycobacterial interspersed repetitive unit-variable number tandem repeat (MIRU-VNTR) genotyping [Sankar et al, 2011;Wilbur et al, 2012]. These techniques are useful in distinguishing M. tuberculosis from infection with other MTC strains.…”

Wildlife Tuberculosis: An Emerging Threat for Conservation in South Asia

“…One study from a zoological collection in India reported TB in spotted deer [50], while a similar study in Pakistan reported TB in spotted deer and two antelopes, namely, chinkara gazella and black buck [62]. A few studies have reported TB from langur in India and rhesus monkey in Nepal [63,64], and these may be associated with M. tuberculosis transmission from contact with humans as in South Asia as there are many feral monkeys residing in communities. However, TB in wildlife in South Asia has not been adequately studied to fully understand the impact.…”

Detection of Mycobacterium tuberculosis Complex in New World Monkeys in Peru

“…Polymerase chain reaction amplification of the IS 6110 repetitive nucleic acid sequence, which is specific to MTBC subspecies has recently been employed to detect the presence of MTBC DNA in buccal swabs from laboratory pig-tailed macaques and free-ranging macaques in Asia (Engel et al 2012; Wilbur et al 2012b). Amplification of the IS 6110 sequence is both sensitive and specific for the detection of MTBC DNA (Wood et al, in review;Eisenach 1994), and buccal swab collection may overcome logistical barriers associated with use and interpretation of TST, radiographs and physical examinations in NHP.…”