Reasons for Controlling BTB

The presence of BTB is not only a livestock issue, but it has an, often unquantified, impact on human health, wildlife, income generated by international trade in live­stock and livestock products, tourism and its various related activities, ecosystems, and the national economy.

There are three principal reasons, addressing both animal and human health, for controlling BTB in cattle:

• The financial loss and societal impact caused by the decreased productivity (meat and milk), reproductivity, and replacement costs of BTB-infected animals, in addition to the inability to participate in the lucrative international trade in livestock and dairy products.

• The zoonotic health risk for humans.

• The risk of infecting other livestock and wildlife with the consequent impact on ecosystems and the development of additional maintenance hosts for M. bovis.

Many of these matters are dealt with in other chapters in this book in more detail, and only the highlights of each will be given as background for the rationale of controlling BTB.

10.2.1 Economic Importance of Bovine Tuberculosis

Bovine TB is a chronic debilitating disease, characterized by a progressive loss of body condition, reduced milk production, lower reproductive rates, and losses caused by reduced feed utilization, a decrease in the average productive age, a reduced market value due to poor body condition, condemnation of carcasses or portions of carcasses at abattoirs of BTB-infected cattle, and the additional processing costs following condemnation at abattoirs. The presence of BTB in the national herd also prevents participation in international trade in cattle, milk, and milk-derived products. There is an attempt by the WTO to reduce trade restrictions, such as using certain diseases like BTB as trade barriers, to increase globalization and the integration of markets with decreasing border control, as is the case in Western Africa. All these efforts will put additional strain on countries with limited resources to manage livestock diseases.

There are few publications detailing the actual cost of the consequences of a BTB infection in a country and the benefits that accrue when the disease is dealt with successfully. Some data are available with emphasis on the cost/benefit ratios of eradication programs. A good example of the accrued benefits of an eradication program is in the USA where the control campaign is considered to have been both an economic and animal health success. When the cooperative State-Federal Erad­ication Program was initiated in 1917 in the USA, about 5% of the cattle population was tuberculous, and about 50,000 carcasses were annually condemned in abattoirs because of BTB (Ranney 1960). From its initiation until 1959, the focus was on single animal testing and, from then on, on abattoir surveillance. It takes a long time for the prevalence to decline, and in the USA, it took 40 years for it to decline from 1% of the cattle population to 0.1%. The benefits obtained by this reduction are the costs not experienced because of the reduction in the number of infected animals, the so-called foregone costs.

With respect to a more detailed analysis of the costs, according to some estimates, the overall productive efficiency of BTB-infected cows may be reduced by 10-25% and the milk production by 10-12%; and sterility of tuberculous cows increases by 5-10% due to the involvement of the reproductive organs (DAFF 2016). There is a decrease of the average weight of cattle with detectable BTB-like lesions of 14 kg compared to healthy carcasses in Niger, while in Madagascar, Malagasy zebu carcasses with gross visible lesions weighed 3.1-9.7 kg less than those without lesions (Boukary et al. 2012). In Morocco the annual direct and indirect losses due to BTB were estimated at $44,260,411 (Berrada 1993). Ejeh et al. (2014) estimated the direct economic loss attributable to BTB in cattle slaughtered in Makurdi abattoirs, Nigeria. Out of 61,654 cattle slaughtered from 2008 to 2012, 1172 (1.9%) were positive for BTB.

It is probably impossible to quantify the economic losses attributable to BTB in Africa at this stage, but there is no reason to believe that the nature and extent of the losses will be different to those in other countries across the globe. An additional factor on the continent is that the disease also causes an indirect loss in agricultural productivity because of the reduction in animal traction power caused by the debilitation that is characteristic of cattle suffering from BTB. Some data exist, and in Central Ethiopia it was estimated that the milk yield was reduced by 5-13%, the number of services per conception increased from 1.25 to 2.02, and the number of milking days was reduced from 328 days in BTB-negative to 294 days in BTB-positive cows (Ameni et al. 2010).

A common argument, which may be a gross generalization, against the imple­mentation of BTB eradication schemes in Africa, is that a large proportion of the cattle herd is managed under extensive, free-ranging conditions that limit the spread of the diseases. Consequently, should BTB be present, its prevalence will be low and remain so, and it thus does not have a significant impact on the animals or pose a public health risk. The situation, however, is changing rapidly. Intensive livestock improvement schemes that include the importation of improved European breeds of cattle are being implemented in several African countries. An increasing risk too lies in the rapid urbanization driven by poverty and public neglect across the whole of Africa and the establishment of small-scale dairy farms in peri-urban and urban areas to satisfy the increasing demand for milk.

10.2.2 Public Health Importance of BTB

During the 1900s zoonotic tuberculosis was highly prevalent in some of the coun­tries of the developed world such as in the UK and Germany. It is unlikely that it will ever be known how many people actually died from M. bovis infection during the course of time. It is clear though that it was a major problem at times and that it had a substantial impact on human health. In the early 1900s in Great Britain, the propor­tion of human cases of TB caused by M. bovis varied from 5 to 30% (Cousins 2001), and in 1917, zoonotic M. bovis infections were responsible for 15,000 deaths in the USA (Palmer 2013). Nevertheless, the nationwide BTB eradication programs and the pasteurization of milk successfully decreased the incidence of M. bovis infection in humans in these countries to negligible levels (Palmer and Waters 2011). There is

no doubt though that human TB caused by M. bovis still occurs in developed countries (Collins and Grange 1983; Grange and Collins 1987) but that it is of minor importance.

The protection of consumers from contracting milk-borne zoonotic diseases, such as tuberculosis, brucellosis, and others, is the main reason for the introduction and the general use of pasteurization.

With the exception of South Africa and Namibia where the commercial dairy industry is on par with those in the developed world, and where pasteurized milk is available to almost the entire population, the situation in Africa is unclear and complex. That pasteurized milk is widely available in South Africa and Namibia is the likely reason that in those areas in which TB is rife, no or very few cases of M. bovis infection have been detected in humans (see Chap. 3 for further information).

The information for the rest of the continent is limited and fragmented. In Africa, routine laboratory human TB diagnostics do not differentiate between M. bovis and M. tuberculosis infections, and it is not possible to evaluate the contribution of M. bovis to the current TB epidemic in humans. Where the situation was investi­gated, zoonotic TB occurred, albeit in varying, and in many instances, at a low prevalence. For instance in Tanzania, where BTB is widespread in livestock, M. bovis has been diagnosed in humans (Roug et al. 2014), and in Ethiopia it was isolated from pastoralists (Gumi et al. 2012) and from the consumers and producers of dairy products (Kidane et al. 2002). Generally, researchers, quoting the results of various studies to substantiate this view, conclude that M. bovis, also in Africa, does not contribute significantly to the number of human TB cases. One such example is that only four sputum samples collected from 984 tuberculous patients yielded M. bovis (Firdessa et al. 2013). Similar results were obtained in Ethiopia (Berg et al. 2015), which is globally ranked seventh in respect to its TB burden, with close to 400 TB cases per 100,000 of the population (WHO 2013). Several other African studies, however, confirmed human TB caused by M. bovis (Cleaveland et al. 2005; Kazwala et al. 2001; Kidane et al. 2002; Oloya et al. 2008). In countries such as Ethiopia, where 80% of the population owns livestock (CSA 2011) and 82% of the milk supplied to consumers is unpasteurized (Ameni and Erkihun 2007), it is unlikely that zoonotic TB will not be present. In addition, in central Ethiopia, 83% of farmers keep their shoats inside their house at night (Tschopp et al. 2011), and because of this there is a continuous risk of aerosol exposure to M. bovis even in rural areas due to this close association between humans and their livestock.

To resolve the uncertainties about the prevalence and distribution of the disease, studies on TB due to M. bovis in both cattle and humans should be accorded high priority, particularly in those communities across Africa that live in known BTB hot spots where the occurrence of zoonotic infections can be expected. It is important again to emphasize that in events where BTB establishes itself in dairy herds, the disease poses a serious public health risk, especially for children, through consump­tion of M. bovis-containing milk and where there is a strong physical bond between humans and their livestock in the pastoral African husbandry settings with exposure to airborne M. bovis-containing aerosols.

Playing down the importance and potential effect of zoonotic tuberculosis in Africa may have serious consequences in the future if the disease in cattle is left uncontrolled. The risk of becoming infected with zoonotic TB is dependent on the prevalence of the disease in cattle. With a low TB prevalence, M. bovis is often considered to be the most common cause of extra-pulmonary TB (EPTB) in humans that is mainly acquired from drinking milk from tuberculous cattle (Dankner and Davis 2000). However, when TB is highly prevalent in the general population (as in Ethiopia), the majority of EPTB cases are caused by M. tuberculosis (Kidane et al.

2002). It is thus necessary to understand the epidemiological role of the pattern of occurrence and prevalence of TB (LoBue et al. 2003) before drawing any firm conclusions from the few isolated studies that are available and are used to create the impression of the limited importance of BTB and zoonotic TB in Africa. These influence policymakers and opportunistically convince them that there is no need to control the infection in either humans or in animals (Beyene et al. 2009; Byarugaba et al. 2009).

10.2.3 The Role of Other Domestic and Wild Animals

Domesticated Animals Mycobacterium bovis is known to infect a large number of other domestic and wild animals. The list of domestic species in which BTB has been diagnosed includes goats (Hiko and Agga 2011), sheep (Opuda-Asibo 1995), camels (Elmossalami et al. 1971), and pigs (Muwonge et al. 2012).

Pastoralists and smallholder crop-livestock farming communities in Africa com­monly practice mixed livestock rearing systems, and close contact between cattle and other livestock species is common. When BTB is highly prevalent in cattle, the disease is likely to spread to other species when intermingling occurs. The detection of identical M. bovis strains in cattle, pigs, and humans along a cattle corridor in Uganda corroborates this assumption (Muwonge et al. 2012). A similar situation exists in Kenya where the prevalence of BTB in camels supplying milk to Nairobi was up to 4.48% (Lamuka et al. 2018). With a few exceptions, the infection in all domesticated species throughout Africa has been epidemiologically linked with infected cattle.

No link between BTB infection in cattle herds and flocks of small ruminants in southern Ethiopia could be established (Tschopp et al. 2011), and the risk of spread between species appears to be limited under those specific circumstances. It is clear, however, that the possibility of becoming infected is area-dependent. In the Somali pastoralist areas of southeastern Ethiopia, a BTB prevalence of 2, 0.4, and 0.2%, respectively, in cattle, camels, and goats and a herd/flock prevalence of 14.3, 3.1, and 2.9% were recorded (Gumi et al. 2012). It is expected, in general, that owing to the low prevalence of BTB in extensive animal husbandry systems, the mixing of various domestic species does not seem to play a significant role in the epidemiology of BTB because of the limited direct contact between species. This suggests that minimum intervention, but with the implementation of biosecurity measures and segregation, would be sufficient to effectively limit the risk of interspecies transmission.

Wildlife During the course of time, it became clear that M. bovis, being a multihost pathogen, has the ability to infect a range of animals, including wildlife in the same ecosystem, thus creating an epidemiologically complex situation in which bi- or multidirectional transmission of the disease can occur. It also became clear, should one of the infected species become a maintenance host, that it is impossible with the current management techniques at our disposal to control and eradicate the infection (Santos et al. 2015). This has been the experience in countries with wildlife reser­voirs such as possums (Trichosurus vulpecula) in New Zealand, Eurasian badgers (Meles meles) in the UK and Ireland, cervids in North America, and wild ungulates, mostly wild boar (Sus scrofa), and red deer (Cervus elaphus) on Continental Europe.

The complexity at the interface varies in that in certain countries a two-host situation exists, while in others a multihost system in which multiple infected species and more than one maintenance host may exist. The role of each of these wildlife species in the overall dynamics of the disease is different due to differences in the persistence of the bacteria in each of the hosts, and behavioral differences (Pilosof et al. 2017). In these situations susceptible species communities are often composed of both domestic and wildlife hosts that include species other than the main reservoir species. The environment itself might contribute to the complexity by maintaining viable mycobacteria of the M. tuberculosis complex (MTC) group in water or soil, thus further complicating the epidemiology of the disease at these interfaces (Gortazar et al. 2015).

Transmission of the infection in ecosystems can be direct or indirect. Direct transmission requires close contact and is expected to play a major role in intraspe­cific transmission, whereas close contact between individuals of different species is usually rare and indirect routes such as predation and environmental contamination are more likely to be important. The way in which transmission takes place is difficult to determine, but environmental contamination of watering and feeding areas may play a major role in the transmission of the disease such as between white­tailed deer and cattle in North America, badgers and cattle in the UK and Ireland, and wild ungulates and cattle in the Iberian Peninsula. In these countries, in particular, it has been impossible to eradicate BTB from cattle, even after the schemes have been in operation for a hundred years or more (Santos et al. 2015).

Although it has been known for almost a century that various species of African wildlife are susceptible to, and become infected with M. bovis (Paine and Martinaglia 1929) (see Chap. 5), their role in the epidemiology and control of the disease has largely been ignored by regulatory authorities and researchers. It is only during the last couple of decades, and against the background of the role of wildlife maintenance hosts in sustaining M. bovis infections in cattle in some of the devel­oped countries, that their potential role in the epidemiology of the disease and its control was recognized and prompted a reappraisal of control measures by some of the African countries. This situation currently prevails in a number of eastern and southern African countries known for their diversity of wildlife. In these areas, African buffaloes (Syncerus caffer) in South Africa, Uganda, Tanzania, Mozam­bique, and Zimbabwe (Woodford 1982; Bengis et al. 2001; Kalema-Zikusoka et al.

2005), greater kudus (Tragelaphus strepsiceros) in South Africa and Tanzania, and Kafue lechwe (Kobus leche kafuensis) on the Kafue flats in Zambia (Gallagher et al. 1972) are known to be maintenance hosts. The risk of transmission from wildlife is particularly high at the wildlife-livestock interface in these countries where bi-directional transmission of the disease has been confirmed. In South Africa in the Kruger National Park (KNP) and Hluhluwe-iMfolozi Park, infection was intro­duced into the ecosystem through direct contact between cattle and buffaloes. The molecular characterization of 189 M. bovis isolates from the two parks showed that the respective epidemics were each caused by a single, but unrelated, M. bovis genotype (Michel et al. 2009). What is of major concern under these circumstances is that bovine tuberculosis and other diseases can spread between buffalo populations across national parks, community land, and countries and thus pose a risk to animal and human health in surrounding wildlife and farming areas (Caron et al. 2016).

Limited information about the role of wildlife in the epidemiology of BTB in Africa exists, but prevalence rates of bovine tuberculosis of up to 50% at herd level are known to occur in Zambia where cattle and Kafue lechwe share grazing and water (Admassu et al. 2015). In South Africa too, transmission of the infection from infected buffaloes to cattle of subsistence farmers at the wildlife-livestock interface has been established, and it is clear that infected wildlife in the conservation areas constitute a risk factor for bovine tuberculosis infection of neighboring cattle, even when the livestock and wildlife are separated by well-maintained disease-control fences. There are growing concerns about the increasing spatial distribution of BTB in South Africa and its spread to an increasing number of wildlife species (Musoke et al. 2015). There is also evidence of clonal expansion of some ancestral strains and of coinfections with two or three M. bovis strains on some of the South African cattle and game farms, which suggested independent introductions of the infection from epidemiologically unrelated sources (Hlokwe et al. 2014). The common element in many of these wildlife hosts appears to be close family groups that spread the disease within the species, and environmental or feed contamination that result in the dissemination of the disease to other wildlife species (Fitzgerald and Kaneene 2013).

It is important to keep in mind that environmental factors also play a role in the dissemination of the disease in these extended and complex ecosystems. In certain infected areas, 55.8% of the water points tested positive for MTC in mud samples, while 8.9% of them were positive in the case of water samples. A higher percentage of MTC-positive samples were found at the smallest waterholes and where cachectic animals, assumed to be in the advanced stage of the disease and actively shedding large numbers of mycobacteria, were identified (Barasona et al. 2017).

There have been a few attempts more recently to detect BTB in wildlife species in other areas of Africa. No infection was found in Ethiopia (Tschopp et al. 2010) or in the Okavango Delta of Northern Botswana (Jori et al. 2013). The extent of the infection in wildlife in most of the African countries is currently unknown, and the importance of the infection in them remains a matter of conjecture. Though cattle remain the major source of infection for other domestic and wild animals (and humans) in many parts of Africa, the role of wildlife should not be ignored because of the lack of information to support such a decision.

Against the background of the known role of infected wildlife hosts in sustaining the infection and interfering with its control and eradication, surveillance programs in various African countries should include wildlife to allow the design of successful strategies to contain the disease. The situation is bound to be different for each individual country, and even within countries, and extrapolation of data between countries may prove to be costly and without benefit. Increasing degrees of diversity should be expected to increase the complexity of the problem, and these factors should be kept in mind when formulating disease-control strategies to manage cattle in ecosystems characterized by seasonally limited resources and intense wildlife­livestock interactions (Sintayehu et al. 2017).

Experience with the presence of wildlife maintenance hosts of BTB in many countries has shown that while M. bovis can be more easily controlled when the disease is limited to livestock species, it is impossible to eradicate once it has spread into ecosystems with established free-ranging wildlife maintenance hosts (Miller and Sweeney 2013). Controlling BTB in wildlife is a major challenge and at this stage almost impossible. Decreasing population densities of wildlife reservoirs of BTB and improving biosecurity to prevent interaction between wild and domestic ani­mals, help to control the lateral spread of the disease, but these methods alone are insufficient to eradicate the disease. Other methods such as focal depopulation of wildlife species, if those species are not endangered or highly valued by the public, are additional strategies that can be employed. It is for these reasons that the South African authorities are attempting to control the movement of African buffa­loes in the wildlife ranching sector across the country and from known BTB-infected conservation areas in an attempt to limit the spread of the disease. Against the background of the extensive spread of the disease to other wildlife species in the country, only focusing on buffaloes may not be sufficient to limit the role of BTB-infected wildlife.

There are two examples of countries that managed to or are in the process of eradicating BTB in the presence of wildlife hosts: Australia and New Zealand. Their successes contrast vividly with those of the UK in which the infection is increasing both in the wildlife hosts and in cattle herds. Regardless of the methods employed, the control of bovine tuberculosis once it establishes itself in a wildlife maintenance host population is generally a long-term commitment (Fitzgerald and Kaneene 2013). Given the experience in those countries in which the disease has been complicated by the presence of a wildlife reservoir, there is no doubt that the African regulatory authorities, when designing control programs without adequate surveil­lance for the presence of the disease in wildlife, will, at their peril, ignore the role of wildlife in the epidemiology of BTB. The reasons for the successful control of the disease while dealing with wildlife maintenance hosts are discussed in detail by Livingstone et al. (2015), and the principles applied may be used as guidelines in countries with similar epidemiological patterns of the disease.

10.2.4 The Challenges of Dealing with BTB in Africa

There is no quick and easy way to control and eradicate BTB. The test-and-slaughter method used by the developed countries in accordance with the recommendations of the OIE forms the basis of all the successfully completed programs that resulted in reducing the prevalence of the disease to very low levels or in its eradication. Conducting such a campaign is a cumbersome process requiring a substantial investment of financial resources, full cooperation of the farming community, access to adequate diagnostic facilities, and competent veterinary human resources. This is where the problem lies with most of the African countries should they consider to attempt to control and eradicate BTB. It is recognized that these programs are exceedingly expensive and thus not easily affordable, and cannot be applied in many parts of the world.

Most African countries do not have the resources to implement and sustain the conventional test-and-slaughter program, and doing nothing remains the status quo (Grange et al. 1994). However, because of the increasing urbanization and need for milk, and the increasing small-scale farming in urban and peri-urban areas, in addition to the intensification caused by the implementation of livestock improve­ment schemes in several African countries, the dynamics and epidemiology of BTB are rapidly changing on the continent, and the problem of BTB is likely to increase in magnitude. There is a perception by most of the veterinary authorities in Africa that although they are aware that BTB and zoonotic TB are present, they are not important. With the limited financial resources and usually inadequate number of veterinary personnel to manage a wide array of animal diseases under unfavorable conditions, they have no option but to focus on more economically important trans­boundary diseases and those that are rapidly fatal and cause many acute deaths in domestic animals and humans (Awad 1962). Most of the countries do not participate in the international trade with livestock and their products, and their lack of partic­ipation in these markets is a further reason why they are not too concerned about the presence of the disease and its limitation on participating in international trade in livestock and their products.

The consequences of doing nothing have been addressed and modeled a number of times. One such study modeled the consequences of various BTB control strategies in Tanzania, including the prospect of doing nothing. The introduction of one infected animal into a herd of 40 animals where no control is applied, will cause the proportion of infected animals to increase to a maximum of 11.3% after 10 years, with an average of 6.7% (Roug et al. 2014). Entertaining this option spells eventual disaster for human and animal health, and control programs in Africa with the current free cross-border movements of cattle, such as in Western Africa according to their trade agreement. Unlimited cross-border movement may become an increasing practice because of the political efforts to create free trading across Africa (BBC News 2015).

To resolve these issues, as there is no alternative, an adaption and phased implementation of permutations of the current test-and-slaughter programs should be considered. There is a number of matters that must be addressed: detection, surveillance, risk factor analysis, mapping and calculating the rate of spread, increasing the knowledge and attitude of both farmers and policymakers, improving the competency of veterinary and abattoir officials, and reducing human exposure by reducing the consumption of raw milk, and reducing the direct contact between humans and potentially infected livestock. It has further been suggested that population-based molecular markers of infectious pathogens be used to assist with developing targeted control strategies in resource-limited settings. These methods focus on the unique host population-driven configurations of pathogen genotype clustering, cluster-size distribution, diversity and spatial distribution to infer contact activity, potential transmission events, and most importantly to identify hot spots of disease on which to focus when setting priority areas in which to commence a control program (Egbe et al. 2017). These data should allow a structured approach to allocate limited resources to deal with the problem, rather than to do nothing.

Following surveillance, and even for surveillance purposes, countries or regions can be subdivided into zones or compartments allowing the control of BTB on a piecemeal and geographic basis. This allows regulatory authorities to design, imple­ment, and manage BTB control programs that have different objectives as a conse­quence of varying epidemiological, economic, social, administrative, and legal factors. Based on these concepts, BTB can be eradicated from parts of a state or country, to allow subpopulations of animals that are kept under different manage­ment or husbandry practices to reach disease-free status independent of the disease status of others. This approach is not without its challenges since the authorities will have to prevent inter- and intraspecific transmission of the infection from neighbor­ing areas. Dealing with wildlife maintenance hosts is another matter and, at this stage, is exceedingly difficult if not impossible. Until the epidemiology and ecology of BTB in the maintenance hosts are understood, and the way in which transmission occurs from the wildlife host to livestock, devising successful control programs remains in the realms of impossibility (Livingstone et al. 2015).

In Africa, it is also necessary too to deal with the lack of the political will to implement the program against the background of poverty, cultural beliefs and customs, illiteracy, high population growth, urbanization, the lack of public aware­ness of the zoonotic implications of BTB, the ongoing social disruption and dis­placement of people and their livestock within and between countries. The biggest problem, perhaps, is the lack of information about the disease that does not allow the authorities to adequately assess its importance, nor to develop a control program that will be executable given the limitations that exist in most of the countries.

The role of livestock in the social structure of many tribes in Africa creates marked resistance to the implementation of eradication programs particularly in those instances where cattle do not appear to be visibly ill. As livestock are highly valued by pastoralists, culling an animal suffering from BTB that does not cause acute clinical signs is perceived as a draconian measure and is experienced as a devastating blow to individual farmers with both emotional and financial implica­tions (Drewe et al. 2014). The remoteness of many of the cattle herds in rural areas that are not accessible by road, and do not have the infrastructure to handle cattle for testing purposes, is a major impediment, as is the requirement for animals after 72 hours to return to a gathering point for the test to be evaluated. Most livestock keepers do not have the monetary means to privately finance their participation in these programs and will not be able to participate without substantial governmental support (Roug et al. 2014). With the exception of few of the countries, no African government is able to do so without substantial international agency and NGO financial support.

10.3