Non-tuberculous Mycobacteria in South African Wildlife: Neglected Pathogens and Potential Impediments for Bovine Tuberculosis Diagnosis

Abstract

Non-tuberculous mycobacteria (NTM) are not only emerging and opportunistic pathogens of both humans and animals, but from a veterinary point of view some species induce cross-reactive immune responses that hamper the diagnosis of bovine tuberculosis (bTB) in both livestock and wildlife. Little information is available about NTM species circulating in wildlife species of South Africa. In this study, we determined the diversity of NTM isolated from wildlife species from South Africa as well as Botswana. Thirty known NTM species and subspecies, as well as unidentified NTM, and NTM closely related to Mycobacterium goodii/Mycobacterium smegmatis were identified from 102 isolates cultured between the years 1998 and 2010, using a combination of molecular assays viz PCR and sequencing of different Mycobacterial house-keeping genes as well as single nucleotide polymorphism (SNP) analysis. The NTM identified in this study include the following species which were isolated from tissue with tuberculosis- like lesions in the absence of Mycobacterium tuberculosis complex (MTBC) implying their potential role as pathogens of animals: Mycobacterium abscessus subsp. bolletii, Mycobacterium gastri, Mycobacterium species closely related to Mycobacterium goodii/Mycobacterium smegmatis, Mycobacterium brasiliensis, Mycobacterium sinense JMD 601, Mycobacterium avium subsp. avium, Mycobacterium sp. GR-2007, Mycobacterium bouchedurhonense, and Mycobacterium septicum/M. peregrinum. Mycobaterium brasiliensis, Mycobacterium gastri, Mycobacterium sp. GR-2007, and a potential novel Mycobacterium species closely related to Mycobacterium goodii were found for the first time in this study to be potential pathogens of animals. Mycobacterium simiae was isolated from a sample originating from a tuberculin skin test positive reactor, demonstrating its potential to elicit inappropriate immune responses in animals that may interfere with diagnosis of tuberculosis by immunology. Mycobacterium abscessus subsp. bolletti was the most frequently detected NTM identified in 37 of the 102 isolates. Other NTM species were also isolated from animals not showing any pathological changes. Knowledge gained in this study contribute to the understanding of NTM species circulating in wild animals in South Africa and the pathogenic potential of certain species, whose role in disease causation need to be examined, as well as to a certain extent the potential of M. simiae to hamper the diagnosis of bTB.

Tuberculosis serosurveillance and management practices of captive African elephants (Loxodonta africana) in the Kavango-Zambezi Transfrontier Conservation Area

“…Banded mongoose in South Africa were recently found to be hosts of M. bovis (Brüns et al., ), and nearly all of the other wildlife species reportedly seen on the facilities are known natural hosts of M. bovis or other tuberculous mycobacteria (Mukundan, Chambers, Waters, & Larsen, ). A variety of non‐tuberculous mycobacteria have been cultured from tissues of South African wildlife species, including elephants (Botha, Gey van Pittius, & van Helden, ), and non‐tuberculous mycobacteria can induce cross‐reaction to MTBC antigens (Gcebe & Hlokwe, ). Relatively little is known about movement of mycobacteria among humans, wildlife and domestic species, especially in southern Africa.…”

Nocardiosis and mycobacteriosis of bivalves: “Yet‐to‐emerge” zoonoses of public concern?

“…The clinical pictures differ in that is prevalently disseminated, or both pulmonary and disseminated, in HIV-infected patients, whereas it is mainly pulmonary in other patients (van Ingen et al, 2011). The first isolations of this mycobacterium in wild animals were recorded in Africa by Botha, Gey van Pittius, and Helden (2013) and again in Africa in 2017, there was the first isolation from a sick lion with tuberculous-like lesions (Gcebe & Hiokwe, 2017). Finally, very recently, M. sherrisii has been involved in mass mortality events affecting the bivalve Pen shell Pinna nobilis, recorded in two different regions of Italy, Campania and Sicily, in the Mediterranean Sea (Carella et al, 2019).…”

Isolation, identification and associated risk factors of non‐tuberculous mycobacteria infection in humans and dromedary camels in Samburu County, Kenya

“…These NTM species are often found in the environment as biofilm formation, free‐living or in association with amoeba (Nishiuchi et al., 2017). However, information on the zoonotic significance of NTM, diagnostic implications in both humans and animals, as well as the impact on the management of human TB in developing countries is scanty (Gcebe & Hlokwe, 2017; Hoza, Mfinanga, Rodloff, Moser, & Konig, 2016). Some of the important NTM species isolated from animals include M. avium intracellulare complex ( M. avium subspecies avium , M. avium paratuberculosis ), M. marinum , M. shimoidei , M. chelonae , M. septicum , M. porcinum , M. lentiflavum , M. fortuitum , M. peregrinum , M. gordonae , M. neoaurum , M. parafortuitum , M. moriokaense and M. confluentis (Batista et al., 2017; Gcebe et al., 2018; Katale et al., 2014; Nuru et al., 2017).…”

“…The members of this genus that have been isolated from tissue lesions and milk of camelids include M. tuberculosis , M. bovis , M. pinnipedii , M. caprae , and M. microti , as well as, atypical mycobacteria such as M. Kansasii (Beyi, Gezahegne, Mussa, Ameni, & Ali, 2014; García‐Bocanegra et al, 2010; Wernery & Kinne, 2012). Until recently, the focus has been on identifying known zoonotic mycobacteria such as M. bovis ; however, not much is known about the epidemiology and implications of the other potentially zoonotic mycobacteria including M. avium intracellulare complex and other NTM (Gcebe & Hlokwe, 2017). This is despite the growing evidence base of the role of NTM as true human pathogens in NTM pulmonary disease, their resistance to first‐ and second‐line anti‐TB drugs and the implications for the management of human TB cases (Cheng et al., 2017; Fedrizzi et al., 2017; Hoza et al., 2016; Kankya et al., 2011; Monde, Munyeme, Muwonge, Muma, & Malama, 2018; Muwonge et al, 2011; Nishiuchi et al., 2017; Wang et al., 2014).…”

“…This is despite the growing evidence base of the role of NTM as true human pathogens in NTM pulmonary disease, their resistance to first‐ and second‐line anti‐TB drugs and the implications for the management of human TB cases (Cheng et al., 2017; Fedrizzi et al., 2017; Hoza et al., 2016; Kankya et al., 2011; Monde, Munyeme, Muwonge, Muma, & Malama, 2018; Muwonge et al, 2011; Nishiuchi et al., 2017; Wang et al., 2014). In addition to their growing pathogenic significance and drug resistance, environmental NTM compromise accurate diagnosis of TB in both humans and livestock, through the cross‐reactivity and the reduction in sensitivity of common diagnostic tests (Gcebe & Hlokwe, 2017; Jenkins et al., 2018).…”