BTB Control in Wildlife
19.4.1 Background
Mycobacterium bovis is a multi-host pathogen with an extremely broad host range, and although susceptibility varies greatly between species, it is able to infect many mammalian species, whether domesticated, wildlife, or humans.
The potential for causing widespread dissemination of the infection and the development of clinical disease is probably greater in animals in managed, multi-species systems with high population densities, than in natural, free-ranging ecosystems (Renwick et al. 2007).When BTB was first detected in free-ranging wildlife populations in different geographical settings around the globe, including South Africa, it was generally not anticipated that these species would become significant role players in the epidemiology of BTB in cattle. Infected wildlife populations are now known sources of spillback of M. bovis infection for cattle (Musoke et al. 2015), and this situation puts additional pressure on BTB control programs in countries in which BTB-infected wildlife reservoirs are present.
The establishment of wildlife reservoirs that allow the maintenance and spread of BTB independent of cattle is a major problem in BTB-infected developed countries such as the UK and New Zealand attempting to eradicate BTB, and they have great difficulty in dealing with the problem because of the presence of wildlife BTB reservoirs. The implications for South Africa with its large commercial game farming enterprise and extensive conservation areas are unparalleled in the world, and they create extreme challenges when attempting to control the spread of BTB and its eventual eradication.
To date, M. bovis infection has been diagnosed in 21 free- or semi-free-ranging wild mammal species in South Africa (Michel et al. 2015). Here only African buffaloes (Syncerus caffer) are regarded as true and greater kudus (Tragelaphus strepsiceros) as highly likely maintenance hosts of BTB.
The remaining 19 species lack the attributes to sustain a persistent intraspecific infection (De Lisle et al. 2001) and are dead-end, spillover hosts. They should, however, not be ignored as a source of infection as they could still play a role in disease transmission especially during times of drought when animals cluster around water points and exposure to stress factors, such as overstocking. The epidemiology of BTB in wildlife is complex and largely unknown, and unexpected sources of infection should be anticipated. One such example is the recent event of a BTB-free African buffalo population in the Madikwe Game Reserve that became infected with BTB, most probably by infected greater kudus entering the reserve (Hlokwe et al. 2016).Private ownership of wildlife in South Africa was sanctioned by the state in 1991, which led to a boom in activities relating to hunting, breeding, sale, ecotourism, and game meat production. The wildlife industry has become one of the fastest growing economic sectors in South Africa and generated US$ 1,000,000,000 and created 120,000 job opportunities in 2012. During that time, the number of commercial game farms increased from 3500 in 1992 to 5000 in 2014. Additionally, there are over 4000 mixed livestock/game farms. Sixty percent of the country’s game animals are privately owned compared to the 40% (6 million) in protected areas. Over the past 15 years, the financial turnover from game ranching grew at an annual rate of 20%, and it now outstrips that of the dairy sector (Lewis 2015).
In addition to the risk of severe economic losses by the growing game industry when BTB-free animals are infected, the disease is also a potential threat to wildlife conservation, particularly when endangered species such as the African wild dog (Lycaon pictus), black rhinoceros (Diceros bicornis), and others are affected.
It is imperative that future BTB control programs in South Africa, and the other African countries with large wildlife populations, take wildlife maintenance species of BTB into account when designing and executing their national BTB control programs.
Unless this is done, attempts to control and eradicate the disease will be a futile waste of financial and other resources.19.4.2 BTB Control in African Buffaloes
African buffaloes play a major role in the maintenance and transmission of several important livestock diseases including foot-and-mouth disease (FMD), Corridor disease (CD), bovine tuberculosis (BTB), and bovine brucellosis (BR) in South Africa (Michel and Bengis 2012). Buffalo herds in the Kruger National Park (KNP) and the Hluhluwe/iMfolozi Park (HIP) are endemically infected with BTB, and they serve as sources of infection for other wild animal species and as a source of spillback transmission to cattle (Musoke et al. 2015; Michel et al. 2015; Michel 2002; Keet et al. 1996). In some of the larger multi-host conservation areas such as these, it is considered to be virtually impossible to eradicate the disease.
Breeding and the sale of African buffaloes are a particularly lucrative business with increasing numbers of prime animals being sold at auctions, sometimes at exorbitant prices (Anon 2013; Wildlife Ranching 2015). To control BTB, and the other important diseases that they carry, the Directorate of Animal Health of the Department of Agriculture, Forestry and Fisheries maintains strict control over all buffalo movements in the country (Department of Agriculture, Forestry and Fisheries 2014). When contemplating keeping buffaloes, landowners must apply to the National Director of Animal Health for approval, and they must also comply with the fencing regulations as stipulated by in the Buffalo Veterinary Procedural Note (VPN) regulating the keeping of African buffaloes in South Africa. Irrespective of their disease status, buffaloes may under no circumstances be kept on the same land as cattle, and they may only be moved between farms or conservation areas following the issuing of a veterinary red-cross movement permit after having been tested for the presence of specified diseases, and after the results have been communicated to the responsible state veterinarian (Department of Agriculture, Forestry and Fisheries 2014).
The comparative cervical tuberculin skin test (CCT) for the diagnosis of BTB is the required test when moving African buffaloes. The OIE guidelines for interpreting skin reactions in cattle for BTB testing have been adapted for buffaloes, and these guidelines are included in the Buffalo VPN. Although the IFN-γ test has great value as a screening tool in free-ranging buffalo populations (Michel et al. 2011), it is currently not approved by DAFF as a sole test for movement purposes. The IFN-γ test may only be used as an ancillary test at the discretion of the state veterinarian or the provincial Director of Veterinary Services. Because BTB is a controlled disease, the CCT must be carried out under the supervision of a state veterinarian. All the buffaloes presented for testing at any time should be visibly identifiable and microchipped to provide an unambiguous record of the test results.
To facilitate the uniform application of the diagnostic tests and standardized recording of the results, the National Director of Animal Health developed a guideline defining the BTB status of buffaloes and buffalo herds on private buffalo farms.
19.4.2.1 BTB Status of a Buffalo or a Buffalo Herd
BTB-Free Buffalo Herd or BTB-Free Facility This is a herd or a facility in which all animals have undergone three consecutive negative CCT tests if sourced from a herd of unknown status, or five consecutive negative tests if sourced from a known BTB-infected herd.
Unknown Status Herd This is a buffalo herd that has never been tested, or in which a proportion of the herd may have been sampled or examined through either testing or necropsies, and no positive cases have been identified.
Infected Herd This is a herd in which BTB has been detected and confirmed by culture in, at least, one animal.
BTB-Positive Animal This is an animal that has tested positive on the appropriate blood-based or intradermal tuberculin test, or in which the disease has been confirmed by culture.
19.4.2.2 Standard Procedures for the Eradication of BTB from a Buffalo Herd
The Buffalo VPN determines that any suspect or positive BTB test result must be reported to the Provincial Director of Veterinary Services and that the entire portion of land or a farm must then be placed under quarantine until the diagnosis can be either confirmed or dismissed. In such a case, no further movement of buffaloes, or any other susceptible species, will be allowed onto, off, or through the land registered for keeping buffaloes.
Should the diagnosis of BTB be confirmed by culture, the land/farm will remain under quarantine until such time that all the buffaloes on the property have undergone five consecutive negative CCT tests. However, if the population is too big and the testing scheme cannot be applied, then the manager or owner of the land may decide to remain under permanent quarantine with no movement of buffaloes allowed from the land to any BTB-free area. If the owner/manager decides to cull all the positive animals with the intention of regaining BTB disease-free status, a suitable, science-based action plan must be developed in collaboration with the relevant Provincial Director of Veterinary Services. Action plans must always also be submitted to the Directorate of Animal Health for approval before the final approval can be given for the implementation of the plan. A complete, accurate, and digitally accessible record of all test results for each buffalo is required to allow forward and backward tracing of the disease status of all the buffaloes on the property.
19.4.2.3 BTB Control in Other Free-Ranging Wildlife Species
Although the BTB risk posed by the South African buffalo population for the transmission of BTB is very well monitored and controlled, the same is not true for most of the other susceptible wildlife, especially the cloven-hoofed species. Thousands of head of game are captured and translocated annually across the country, yet unless they are clinically ill, none of these animals is ever screened for BTB or any other disease.
A major obstacle to screening the various wildlife species for the presence of BTB is that, with the exception of tests for African buffaloes, the accepted diagnostic tests have been validated for use in only a few wildlife species. The CCT has been validated for use in lions (Keet et al. 2010), and it also holds some promise for use in warthogs (de Klerk pers. comm.). The IFN-γ test and the various serological tests used to detect BTB infection in lions and rhinoceros are also being evaluated (Duncan et al. 2009; Miller et al. 2015; Morar et al. 2013; Maas et al. 2012). The intra-palpebral tuberculin test is the test of choice for the diagnosis of BTB in baboons in Africa (Keet et al. 2000).
An additional impediment to BTB risk management in wildlife is that owners of these species, other than African buffaloes, are not required by law to have any of their animals tested prior to movement from one area to another. It does, however, sometimes so happen that owners might request that an animal be tested to prove freedom from BTB prior to an auction or for specific breeding purposes. This is problematic because no validated tests are available for most antelope species, and there are no validated guidelines for the interpretation of the SIT or CCT in those species. A “positive” or “negative” test result in these cases is unreliable and may create a false sense of security (Maas et al. 2013). This situation emphasizes the need for future research and the development of validated diagnostic assays for the detection of BTB in a range of game species, most of all, those that are in high demand for sale at auctions and in which BTB has been detected, i.e., greater kudu, nyala (Tragelaphus angasii), and other medium-sized and small antelopes. Equally important is the development of suitable and practical, long-term surveillance programs for the early detection of the disease at herd level in wildlife. It is important to understand that the practice of translocating wildlife of which the BTB status is unknown may have serious consequences for other wildlife species in the same environment. Most of these game species easily contract BTB, and they constitute sources of infection that are mostly ignored by owners of BTB-free buffalo herds and their veterinarians.
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