5.3 Maintenance Hosts of Mycobacterium bovis

5.3.1 African Buffalo (Syncerus caffer)

African buffaloes are probably the most important known wildlife maintenance host of BTB in Africa (Michel et al. 2006; Woodford 1982a, b).

Aerosol transmission of M. bovis because of the close contact between buffaloes within herds is the primary route of transmission of the infection in this species (Fitzgerald and Kaneene 2013). Herd sizes in the KNP vary substantially from as few as 50 to more than a 1000 buffaloes. These varying herd sizes are partly a function of seasonal fission and fusion events caused by environmental factors. These events ensure genetic exchange between herds, but they also facilitate the spread of BTB between herds (Cross et al. 2005). Normal dispersal behavior of single or small groups of buffalo heifers and bulls over considerable distances and fusion with new herds similarly cause gene flow and the spatial spread of BTB (de Vos et al. 2001; Michel et al. 2006; Caron 2014).

Once infected, the development of tubercles in buffaloes broadly follows the same stages of development and immunopathogenesis as has been described for domestic cattle. They appear to remain persistently infected, and are then, depending on the locality of the lesions, potential shedders of M. bovis.

In buffaloes, tuberculous lesions are more commonly found in the lymph nodes of the head and neck, tonsils, and in the lungs and associated lymph nodes. On many occasions, single, small lesions only are present in any one of the sites in which they usually occur. The appearance of the lesions in buffaloes varies substantially between animals, and when there is a florid reaction the lesions are poorly encapsu­lated and have a lardaceous appearance.

The long-term impact of BTB on the buffalo population is currently unknown as the disease is still spreading in a northerly direction following its entry in the south of the KNP. From the time of the estimated first infection of buffaloes in the south, it took about 50 years for the disease to reach the northern border of the Park, over a distance of about 500 km. Limited data about the effect of the disease on the buffalo population in the KNP reflect an increased vulnerability to drought and predation in herds with a high BTB prevalence (Jolles et al. 2005; Cross et al. 2009). These early indications could be a predictor of wider scale BTB-related ecological disruption that may be expected once the disease has developed to its full extent in that ecosystem (Caron et al.

5.3.2 Greater Kudu (Tragelaphus strepsiceros)

Greater kudus, one of the two subspecies of kudus, are large, gregarious antelopes that live in small groups in woodlands and bush lands where they browse on leaves of thorn trees of the genera Acacia and Ziziphus. Free-ranging greater kudus were among the first wild animals to be diagnosed with BTB in South Africa in the 1920s (Paine and Martinaglia 1929). Kudus are believed to contract the disease by different routes. One is the aerosol route in which case they develop multifocal tuberculous lesions in the lungs and associated lymph nodes with a distribution very similar to that seen in buffaloes and cattle. Generalization of the infection with hematogenous spread to organs, such as the spleen, liver, and kidneys, and to the serosal surfaces, has been observed. More frequently, and probably more importantly, M. bovis can be contracted percutaneously. In this instance, infection occurs at the site of lacer­ations in the oral and esophageal epithelium, and the thin skin of the inside of the ears by M. bovis-contaminated thorny twigs. Following infection of the parotid and retropharyngeal lymph nodes, typical pyogranulomas containing large numbers of mycobacteria develop. These lesions contain an abundant purulent exudate, and cause large irregular parotid and submandibular swellings. The pressure exerted by these lesions causes them often to rupture and to form draining sinuses from which bacilli-laden pus is shed into the environment including onto the browse.

The infection persists in localized kudu populations, at least for a considerable period of time (Michel et al. 2015), and for these reasons kudus are considered to be maintenance hosts, and they may become supershedders with the ability to effectively disseminate M.

5.3.3 Lion (Panthera leo)

Bovine tuberculosis in free-ranging lions was first diagnosed in 1995 in the south of the KNP where, at that time, the prevalence of BTB in buffalo herds was the highest in the Park (Keet et al. 1996). Subsequent surveys showed that the prevalence of the disease in lions had the same south to north gradient as for the infection in buffalo herds, reflecting the spread of BTB in a northerly direction (Keet et al. 2000b; Rodwell et al. 2001). From 1993 to 2008, the prevalence of BTB in lions in the northern part of the KNP (low buffalo BTB prevalence zone) increased from 0 to 41% (Maas et al. 2012). In a study in 2017, the prevalence of BTB in the lion population was 33% in the central region, and 54% in the southern region where the infection appeared to have entered in the Park (Sylvester et al. 2017). Mycobacte­rium bovis infection in lions has also been reported in Tanzania where, compared to seronegative lions, serological data correlated with the presence of clinical signs and reduced survival times indicating the presence of the infection in lions, and its impact on M. bovis-infected prides (Cleaveland et al. 2005).

Lions are the only social felids, and they are the top predator in African ecosys­tems. Their status is listed as vulnerable by the International Union for Conservation of Nature (http://www.iucnredlist.org/apps/redlist/details/15951/0). Their sociality, communal cub rearing, communal hunting, their predilection to hunting buffaloes (a major prey species), and intraspecific aggression predispose them to becoming infected and to sustain the infection in prides once they become infected. Their preference for buffaloes as a prey species is greater during periods of drought when buffaloes are an easier prey due to their deteriorating body condition, weakness, and fission into smaller herds that make them more vulnerable to predation by lions (Mills 1995; Ferreira and Funston 2010; Tambling et al.

Tuberculosis is most frequently a subclinical but ultimately fatal disease in infected lions (Keet et al. 2000a), but there are currently insufficient data to calculate the mortality rate, the duration of the infection before death, or the average age at which they become infected, and how long after infection the onset of clinical signs is most likely to occur.

Lions may become infected by different routes, as reflected by the variable and inconsistent distribution of lesions in infected animals. During a kill and while feeding on infected buffalo carcasses, transmission of the infection may occur by the alimentary route, by aerogenous transmission of M. bovis while suffocating the prey, and during intraspecific aggressive behavior while feeding. Aggression while feeding also facilitates percutaneous transmission through bite wounds. The isola­tion of M. bovis from the mammary lymph nodes of some lionesses is not proof but an indication of a possible pseudo-vertical route of infection for suckling cubs. Similarly, the presence of a tuberculous endometritis in some females suggests that intrauterine transmission is also possible.

Dissemination of the infection followed by spread via the hematogenous and/or lymphatic route results in a generalized infection with the presence of miliary lesions mostly in the lungs but also in other organs (Keet et al. 2000a, b). Progression of an M. bovis infection in lions, similar to other affected species, is generally slow, and body condition scoring during the early stages of the diseases is not useful to clinically detect lions with BTB (Maas et al. 2012). Exposure to consecutive high dose of M. bovis via different pathways may possibly contribute to a more rapid progression of the disease, with an earlier onset of the progressive emaciation and lethargy typically seen in advanced cases of the infection in lions. Bovine TB in lions is further characterized by the presence, in variable combinations in some animals, of swollen elbow joints caused by a tuberculous osteoarthritis, hygromas, lameness, corneal opacity, tuberculous panophthalmitis, a dull coat, and large, poorly healing skin lesions caused by the presence of subcutaneous tuberculous granulomas (Michel et al.

Visible lesions at necropsy in lions are limited to the lungs, skin, joints, and subcutaneous granulomas, and resemble those seen in domestic cats. The lesions are different from those seen in cattle and most other species. The lesions in the lungs are characterized by localized but poorly circumscribed areas of infection resembling an interstitial inflammatory reaction. Macroscopically the lesions in the lungs often contain cavities caused by bronchiectasis, and they contain a mucopurulent exudate containing large numbers of acid-fast bacilli. Histologically the lesions in the various tissues are characterized by a multifocal to confluent granulomatous inflammatory reaction seen as aggregates of predominantly macrophages lacking necrosis and the presence of Langhans giant cells typical of the tuberculous reaction in most other species (Keet et al. 1996). Tuberculous lesions in the lymph nodes of lions cannot be seen macroscopically, and the apparent absence of lesions there is thus not an indication of the absence of an M. bovis infection. When BTB is suspected in lions, it is mandatory to confirm the diagnosis by culture of a collection of specimens from the lungs, superficial and deep lymph nodes, the exudate from hygromas and affected joints, and from subcutaneous granulomatous lesions (Keet et al. 2000b).

The mounting evidence of the role of respiratory transmission of M. bovis infection in prides is currently the subject of an intense debate as to whether lions can be maintenance hosts under certain conditions. It is argued that once the infection has established itself in a critical mass of the population thus ensuring continuous pathogen circulation, that it could probably persist in lion prides in the absence of contact with buffaloes as the ongoing source of the infection. The likelihood that lions may become maintenance hosts is also dependent on their population size, and the long-term effects of BTB on the composition of the pride, and population dynamics.

Debilitating diseases, such as BTB, affect social species like lions in multiple ways. Apart from the direct effect on the health of individual animals, there is also an impact on the size of prides and their structure. Dominant male coalitions with BTB are probably evicted earlier because of the debilitating effects of the disease and the consequent increasing bouts of infanticide have an adverse effect on numbers and the composition of prides. The practice of communal hunting too provides support to lions with BTB allowing extended survival times and shedding of the pathogen over a longer period of time (Michel et al. 2006).

Lions are often translocated between conservation areas in Africa, and the risk of introducing lions subclinically infected with BTB into uninfected areas should always be considered.

5.3.4 Warthog (Phacochoerus africanus)

Bovine TB in warthogs was first diagnosed in the Queen Elizabeth National Park in Uganda by Woodford in 1982 who concluded that it was a spillover infection from African buffaloes (Woodford 1982a, b). It appears to have persisted both in buffa­loes and warthogs in the Park since then, as BTB was still present in both populations when surveyed in 1997 (Kalema-Zikusoka et al. 2005). Warthogs with BTB were also found in several reserves and on private game farms in South Africa where they shared M. bovis strains carried by African buffaloes (Hlokwe et al. 2014). Lesions due to M. bovis are present both in the respiratory and gastrointestinal tracts. Warthogs are omnivores, and they opportunistically feed on carrion potentially containing M. bovis in addition to being exposed to environmental contamination with the pathogen. Once infected, close contact between members of family groups inside the confines of their burrows is thought to effectively facilitate aerosol transmission and the persistence of the infection within the family group. When warthog densities are low, BTB occurs as a sporadic spillover infection in them as their numbers are then too low to sustain the infection within the species. However, in the absence of predators, and when food is readily available and in abundance, the number of warthogs within an ecosystem can reach a threshold number at which they can sustain the infection within the population. Under these circumstances, the prevalence of the disease may vary from 5 to 30%, and they may then act as maintenance hosts (Michel et al. 2015).

5.3.5 Kafue Iechwe (Kobus leche kafuensis)

Tuberculosis in Kafue lechwe was first diagnosed in 1946 (Munyeme et al. 2010). They are the dominant wildlife species in the Kafue Basin and live in very large herds. During the drier months of the year, cattle and lechwe intermingle on the dwindling pastures in the Basin, and congregate at watering points. The consistent high prevalence of BTB in lechwe (ranging from 20 to 36%) led to their classifica­tion as maintenance hosts of BTB (Gallagher et al. 1972; Clancey 1977). They have furthermore been identified as a risk factor for BTB in cattle (Munyeme et al. 2008), and they appear to be a source of spillback infection to cattle (Pandey 1998). The majority of tuberculous lesions is found in the lungs and associated lymph nodes, suggesting aerosol transmission. Generalization of the disease, following hematog­enous spread, occurs in about 10% of diseased animals (Munyeme et al. 2010). The annual mortality rate ascribed to tuberculosis in a study conducted by Gallagher in 1972 was at least 20% (Gallagher et al. 1972), compared to the 10% in African buffaloes in the KNP (de Vos et al. 2001). (Refer to Chap. 23 for further information about tuberculosis in Kafue lechwe.)

5.4