Bovine TB Control Strategies

From an African perspective and keeping the various limitations in mind, there is a number of permutations that could be considered, singly or in combination, to control the disease, as well as to limit the risk of zoonotic infections.

10.3.1 Test-and-Slaughter (TS) Policy

Conventionally, BTB control programs depend on the diagnosis of BTB in cattle through whole-herd testing, slaughtering of test-positive cattle, and quarantine of infected herds. This process is repeated until the disease has finally been eradicated. In many countries, this program initially focused on a voluntary herd testing scheme, followed by area testing, in which all cattle in a specified area were subjected to tuberculin testing at intervals of less than a year (Morris et al. 1994). The program in the USA was initially confined to herds of purebred cattle under the Accredited Herd Plan in which a certificate was issued to herd owners when all cattle in the herd passed repeated tuberculin tests over a period of at least 1 year (Ranney 1960). When a sufficient number of herds were accredited, herd testing was extended into area testing, in which all cattle owners in a county allowed their herds to be tuberculin tested. Cattle positive to the tuberculin test were shipped to slaughter, and herds from which infected animals were removed were placed under movement restriction. The herds were then retested after prescribed periods, until no further reactors were detected or, depending on the number of infected animals in a herd, were totally depopulated. The testing was repeated sequentially at specified intervals until a herd, an area, or a state had no infected animals and could be declared BTB-free.

Focusing on the early detection and slaughter of clinical cases of BTB to remove the sources of infection from within the herd, thereby decreasing the likelihood of in-contact animals to be readily infected, is an important approach. Quarantining an infected herd prevents disease spread beyond that herd. Once the test-and-slaughter programs commenced, the incidence of clinical cases of BTB rapidly declined, reversing the year-on-year increase in the incidence of bovine TB and halting its geographical expansion. In the USA, when the national campaign began in 1917, about 5% of the US cattle population was tuberculous. By 1940, only 0.5% of cattle reacted to the skin test (Martin 1994). It thus became clear that BTB could be eradicated by the use of the tuberculin test to identify infected herds and to clear those herds from infection. As a result, several countries commenced BTB eradica­tion programs, with more or less similar success.

In the 1930s, an estimated 15-20% of the national cattle herd in the UK was infected with M. bovis (Hope and Villarreal-Ramos 2008). The application of the test-and-slaughter policy in high-incidence areas in the 1950s, followed by the nationwide application of control measures in the 1960s, reduced the incidence of BTB to 0.5% in the national herd in 1979. In Spain, the prevalence of TB in cattle was similarly reduced from 1.4 to 0.3% between 1996 and 2005 (Naranjo et al. 2008), although further reduction has proven difficult (Martin-Hernando et al. 2007). In Denmark (Magnus 1966) and Switzerland (Fritsche et al. 2004), where nation­wide, centrally directed eradication programs began in the early 1930s, BTB in cattle was eradicated as long ago as in the 1950s.

The BTB eradication programs in many of the developed countries are regarded as being among the most effective control measures ever mounted against any bacterial disease (Grange et al. 1994). After its initiation about 100 years ago, routine, whole-herd tuberculin testing is still being performed in the UK (and many other countries) at intervals of 1, 2, 3, or 4 years, depending on the BTB risk in the area (Reilly and Courtenay 2007).

A prerequisite of the test-and-slaughter program and the subsequent control of the disease is that, unless executed meticulously and attention given to the various risk factors that favor recurrence, the disease commonly returns. In one instance, about one-third of the M. bovis-infected herds were still positive after the disease was deemed to be eradicated (Roswurm and Ranney 1973) mainly as a consequence of the incorrect performance and interpretation of the tuberculin skin test (Morris et al. 1994). In all the countries that used this form of control, cases of TB detected at slaughter are followed up, and thorough epidemiologic investigations are conducted to determine the source and potential further dissemination of the infection (Wahlstrom and Englund 2006; Drewe et al. 2014; McCluskey et al. 2014). To limit the risk of recurrence, and because of the low sensitivity and specificity when used as an individual-animal test, depopulation of herds with a very high prevalence is favored over test-and-slaughter for the eradication of BTB (Martin 1994).

10.3.1.1 The Current Status of BTB Control Programs in Africa

Bovine TB is poorly controlled in Africa, where economic and sociopolitical factors largely determine the degree to which the disease can be controlled in individual countries. The extent of the current control programs in Africa allows the interven­tions in various countries to be roughly grouped into three categories.

Control Programs on Par with those in the Developed World South Africa is one among a few countries in Africa in which a comprehensive control program has been implemented and sustained for some time.

A comprehensive draft manual outlining the various current programs to deal with the disease in South Africa has been accepted for implementation (DAFF

2016). Participation in the program is voluntary, except that when a herd is found to be infected, it is placed under quarantine until such time that the disease has been eradicated from it. A deficiency in the control program is that it still focuses primarily on commercial farming enterprises; cattle in the informal sector, compris­ing about 50% of cattle in the country, are only tested on an ad hoc basis. In addition, in terms of wildlife, it only addresses the issue of BTB in buffaloes, while a number of other wildlife species, and greater kudus in particular, are infected and may act as maintenance hosts. Kudus that are known to have been infected for about a century have the ability to cross fences and other barriers with ease, may act as maintenance hosts, and can transmit the disease to other species as has happened on a number of occasions. More than 20 different wildlife species are now known to be infected in South Africa, while only the movement of buffaloes is regulated.

Apart from Namibia and Botswana, which both have lucrative meat export markets, and successfully control BTB, the Kingdom of Morocco is the only other country that is relatively well prepared to control BTB. With technical assistance from the FAO, Morocco has strengthened its organizational and technical capacity to conduct surveillance and to control BTB. Laboratory equipment and reagents for BTB diagnosis were supplied, and technical personnel and field veterinarians received adequate training on laboratory and field diagnostics of the disease in cattle. Following that, a national BTB survey was conducted.

Second-Tier Countries These include Algeria (Sahraoui et al. 2009), Egypt (Zahran et al. 2014), Madagascar (Quirin et al. 2001), Mozambique (Moiane et al. 2014), Tanzania (Roug et al. 2014), and Tunisia (Ben Kahla et al. 2011). In these countries, BTB is a notifiable disease, and it is officially controlled by the test-and- slaughter method, but only in registered dairy herds. Unfortunately, animals found positive are not routinely sent for slaughter because of a lack of funds to compensate the owners for their losses following the condemnation of carcasses in abattoirs. Individual animals and herds are not identified, and the movement of cattle cannot be controlled, with the consequence that the programs have a negligible impact on the prevalence and spread of the disease. In, at least, Mozambique and Tanzania, wildlife reservoirs of the infection, which make control even more complex, exist.

Third-Tier Countries The remaining African countries, notably Nigeria (Ejeh et al. 2014), Cameroon (Awah-Ndukum et al. 2012), Burkina Faso (Coulibaly and Yameogo 2000), Niger (Boukary et al. 2012), Uganda (Bernard et al. (2005), Zambia (Malama et al. 2013), and many others, have a statutory policy for the control of BTB, which is either not implemented or very poorly applied. For example, in Nigeria, the control of BTB is the responsibility of the Federal Ministry

of Agriculture and Rural Development, which administers the Animal Diseases (Control) Decree of 1988 (Abubakar et al. 2011), but because of political and socioeconomic constraints, and a lack of awareness, it is inadequately implemented. The only meaningful control measure applied in these countries is limited to meat inspection in the abattoirs in which tuberculous carcasses are fully or partially condemned depending on the extent of the BTB-like lesion detected during inspec­tion. Positive cases are not followed up and no epidemiological investigations are conducted. The detection of infected carcasses at abattoir inspection is more of a public health measure than an attempt to control BTB in the national cattle herd. Owners are also not compensated for carcasses that are condemned, with the result that carcasses with generalized BTB are often declared fit for consumption (Quirin et al. 2001; Asiimwe et al. 2009). In many of these countries, existing meat and milk inspection practices are totally inadequate to protect consumers from consuming M. bovis-infected meat and milk (Ismaila et al. 2015). The general level of compe­tency is reflected by the observation that “these reports were based on slaughter­house scanty records written by unqualified and nonchalant/uncommitted meat inspectors..(Okoro et al. 2014).

10.3.1.2 Legislation and Policy

In addition to knowing what the BTB status of a country is, including its distribution, prevalence, and an understanding of the epidemiology of the disease, there must be a sound policy and effective legislation to control it. Weak enforcement of a veterinary policy is usually the consequence of a lack of capacity, poor advocacy, and the lack of sound evidence of the nature and importance of BTB. Awareness of the poten­tially harmful effects is vitally important, not only for the communities that face daily exposure to them but also for the policy actors and key decision-makers that play a role in preventing the emergence and spread of BTB as it relates to human health, agriculture, and development (Okello and Welburn 2014).

Control programs should be compiled against the background of the specific patterns of the disease in each country, in which the situation may vary substantially and requires information to better inform future testing choices, private biosecurity investments, and vector population control. Unless there is strict enforcement of, and meticulous adherence to, the rules and regulations of all the components, programs are bound to fail, becoming a process of merely going through the motions, and destined to become a complete waste of human and financial resources without any benefit to society.

The lack of policymakers to institute control mechanisms for BTB is often caused by a lack of an understanding of the disease and not knowing what the economic impact is of its presence. There is a disparity in the way in which policymakers and veterinarians approach the control of a disease. Economists focus on increasing human welfare, irrespective of whether the disease is reduced or the farmers ’ welfare is improved. They focus on how the disease affects total economic welfare, consid­ering a variety of economic relationships, the effect of changing incentives, and the implementation of new policies, including animal health policies. For economists, animals are important but are simply part of the production environment. These issues must be addressed by the veterinary authorities if policymakers are to be convinced that there is a need to allocate resources for the control of BTB (Jarvis and Valdes-Donoso 2018).

An integrated, national approach is considered to be essential to effectively control diseases such as BTB in a country, and the successful implementation of BTB control programs depends on the availability of a legal framework allowing enforcement of the control measures (Cousins 2001). It is imperative to understand that the effective control of BTB relies on a high level of competence, requiring continuing education and periodic quality control. The central management should provide detailed technical and administrative guidelines and protocols, and adequate supervision and quality control while conducting the program. The central coordi­nating authority should also set standards and formulate definitions and rules that are practical at all levels to allow the program to be executed.

This implies that the state veterinary services of each country should establish the objectives and goals of BTB control programs according to its specific situation and limitations. These goals and objectives should include the control and activity levels required, the financial needs, and the level of training for field, abattoir, and laboratory personnel, and the responsibility of each stakeholder. In addition, high- quality administrative support is critical for BTB control programs, including the availability of legal procedures to enforce the prescribed activities, particularly the performance of the intradermal tests that is probably one of the most critical steps in the control process, and that supervised slaughtering and meat inspection are cor­rectly done (Moda 2006). These aspects are often insufficiently monitored and prone to result in major differences in the efficiency of the procedures and the reliability of their results that will inevitably determine the degree of success and the cost­effectiveness of the program.

10.3.2 Designing Tuberculin Testing and Control Programs

By the nature of the disease, there is no quick and easy way in which to deal with BTB that will allow its control and eradication from African countries. A number of basic principles apply when using test-and-slaughter programs to control BTB in a country.

Knowledge of the extent, the spread, and the epidemiological features of BTB are essential for designing specific control strategies tailored for the needs of the specific country. In the event that it is not possible to immediately launch a nationwide eradication program, an alternative route could be followed. This would entail focusing on those areas and farming enterprises in which the prevalence of BTB is high and of importance. The first step should thus be to conduct a national survey on which to base these decisions before commencing the program. If this is not possible, the focus should be on those areas that are conducive to the establishment, maintenance, and spread of the disease. It is then advisable to categorize herds and locations based on the BTB risks that they pose and to focus on those that are deemed to be of the greatest importance. The high-risk enterprises include intensive dairy farms and urban and peri-urban smallholder farms, and only once BTB control has been achieved in them, to move on to the known BTB-infected pastoral herds (Asseged et al. 2014).

In many countries, it may not be practicable to test the entire national cattle population. In these countries, the biggest challenge will be to achieve BTB eradi­cation in pastoral areas. Activities in the remote rural areas are hampered by an inadequate road transport system and poor infrastructure, making it difficult, if not impossible, to restrain the animals to do the test. There is also a general apathy of the pastoral stockowners to participate in the testing program and, without compensa­tion, the removal of animals suffering from a disease that they have never heard of or of which they do not comprehend the impact on cattle and humans. Even in South Africa with its more structured approach, it is difficult to convince rural subsistence farmers to return their cattle to a gathering point after three days for assessment and interpretation of the test results.

It is critical too to understand that merely testing cattle and removing reactors do not constitute a control or eradication program. This process includes numerous other activities based on the One Health approach and keeping in mind that eradi­cating BTB from the cattle herds is probably not the main objective for dealing with the disease but that the primary objective is to control zoonotic TB and to contribute to the eradication of TB in humans.

10.3.2.1 Variations of the Test-and-Slaughter Program

The BTB control and eradication programs implemented successfully in the devel­oped countries were all based on the test-and-slaughter approach and related activ­ities. Conducting this type of campaign in developed countries with a sophisticated infrastructure and commercially oriented farms remains a cumbersome process. It is, however, facilitated by the existence of adequate animal identification systems, functional diagnostic laboratories, competent meat inspectors at abattoirs, and the ability to trace the origin of reactors, to limit uncontrolled movement of infected animals and those from infected herds. These practices enable their regulatory veterinary services to conduct these campaigns with relative ease and the confidence that the system will work because of the commitment of stockowners to cooperate in the eradication of the disease. One could use their programs as templates for Africa, but given the many limitations that exist on the continent, it may be prudent to use a template designed by an African country with extensive experience in conducting an eradication scheme. South Africa has been controlling BTB from the beginning of the 1900s and actively from 1969, and its current program framework can be used to give some guidance to other African countries when designing their control and eradication programs. (For more detail on the history of the South African programs, see Chap. 19.)

The points made in the Introduction in the South African BTB Eradication Manual are pertinent to other countries in Africa, and the following extract from it will provide some indication of the logic behind the different programs and how they are integrated (DAFF 2016):

The Bovine Tuberculosis Scheme was officially introduced by the Division of Veterinary Services during 1969 with the purpose of eradicating the disease in the Republic of South Africa.

At the initial stage it was already realized that the need for testing for tuberculosis (TB) in herds varied and that it was largely determined by the type of farming animal husbandry being conducted. In order to incorporate as many stock owners in the scheme as possible, the testing procedures and the various testing programmes were adapted through the years. Such modifications also necessitated changes in the administrative processes and consequent adaptations to the manual.

The various testing programmes as set out in the manual should be regarded as appropriate means of achieving the final objective of the programmes: the total eradication of bTB. In order to reach this goal, thorough planning and careful use of available funds and manpower would be required. Extensive knowledge of the scheme as presented in this manual is a prerequisite for sensible planning and execution of the programme.

The scheme begins with comprehensive guidance to stock owners who wish to join and for his herd to be assigned to the correct testing programme. The previous accreditation programme has been discontinued and replaced by the present scheme. Thus, stud and dairy herds should be incorporated into the Maintenance (old Annual Diagnostic) Programme as many of these require a declaration for the sale of stud animals or milk. Where there is no need for a TB-free declaration or where such a declaration is not of much value to the owner, the incorporation should be into the Surveillance Programme and not the Maintenance Programme. A single negative herd test under the Surveillance Programme makes it possible to test many more herds to track down bovine TB and thereby achieving the final objective sooner.

The various programs are dependent on the use of the tuberculin tests and structured to aid the detection, control, combating, and eventual eradication of BTB. For this purpose, DAFF use the following programs to control BTB in South Africa:

1. Maintenance herd program.

2. Surveillance herd program.

3. Diagnostic testing program (individual animals).

4. Infected herd program.

In South Africa, with the exception of the infected herd program, it is voluntary to join a program. However, if infection is established at the first or later tests, the herd is incorporated in the infected herd program, and although the owner voluntarily participated in the other programs, he/she cannot withdraw in an attempt to avoid further tests and the slaughter of positive reactors. Tests and further action in these herds for the eradication of the infection are compulsory and enforced in terms of the Animal Diseases Act, 1984 (Act No. 35 of 1984).

Only the broad outlines of the various programs will be provided, and the relevant detail, including the test procedures, is available in the detailed TB Control Manual (DAFF 2016).

Maintenance Herd Program This program incorporates all herds that require negative certification. Identification of individual animals in these herds is not required, but the owner may identify his cattle at his own cost. Following the first test, cattle with suspect reactions to the tuberculin test are identified permanently for further tests. Should there be cattle that react positively, the herd is incorporated in the infected herd program in which all the animals are then individually identified by ear tags.

New herds, in which case the initial tests can be done by state officials free of charge, that enter the program must undergo two consecutive negative tests at an interval of not less than 3 months and not more than 6 months, after which a declaration is issued that states that the animals tested negative for tuberculosis on the specific dates of the test. Thereafter all animals of all sexes above the age of 12 months are retested every 2 years.

It is the onus of the stockowner to keep his herd free from tuberculosis during the interim period by not allowing it to become infected, for example, by purchasing cattle with an unknown BTB status or by contact with known or suspected BTB-infected animals.

Surveillance program This program is structured to establish the prevalence of tuberculosis in a certain area and is conducted as a survey at the state’s expense and executed by government officials. Tests in this program should preferably be undertaken on an organized basis, such as testing a whole municipal area until the tuberculosis status of the whole municipality is eventually established.

This program can also accommodate stockowners, at their own expense, that do not want to join the maintenance program but are anxious to determine the tubercu­losis status of their herds. For this purpose, all cattle of all sexes older than 18 months belonging to all the owners on a specific farm (considered to be an epidemiological unit) are subjected to the single intradermal tuberculin test.

In this program, a herd is only tested once except when suspect reactors are detected in which case the whole herd is again tested after 3 months, or the owner may elect to incorporate his herd in the maintenance program. Cattle with suspect reactions to the tuberculin test are identified with ear tags for further tests. Should positive reactors be found with the tuberculin test, the herd is incorporated in the infected herd program.

Following a single reactor-free surveillance test, stockowners should be advised and motivated to keep their herds free from tuberculosis by means of good manage­ment practices, such as purchasing cattle from herds in the maintenance program or having cattle tested for BTB prior to purchasing them and bringing them onto the property.

Diagnostic Herd Program The diagnostic herd program deals with cattle destined for export and for cattle that are at a quarantine station following importation. They are subject to a comparative test with bovine and avian tuberculin done by the officer in charge of the quarantine station. Cattle for export are usually tested at the owner’s expense—regardless of whether the test is conducted by a private or a state veterinarian.

These tests are also conducted when an owner wishes to test one or more of the cattle in a herd that they suspect to be suffering from BTB. Private or state veterinarians do these tests at the stockowner’s expense. Positive reactors found during the test automatically result in the herd being treated in accordance with the requirements of the infected herd program.

Infected Herd Program All herds in which a BTB infection has been diagnosed either during meat inspection, milk examination, postmortem examination, or clin­ically, but especially when positive tuberculin tests have been conducted, are regarded as infected and are placed under quarantine. The necessary steps are then taken to eradicate the infection in the herd and then to keep the herd BTB-free. The manual provides a detailed exposition of the way in which infected herds must be dealt with but stresses that it must be regarded as a guideline as circumstances in each herd will differ and that each herd must thus be treated on its own merits. The activities required in the infected herd program include:

1. Duties of the farmers.

2. Duties of the state veterinarians.

3. Control over the BTB-positive herds.

4. Testing procedures.

5. Dealing with positive reactors.

6. Cleaning and disinfection.

7. Branding of reactors.

8. Quarantine.

9. Permits.

10. Arrangement for dealing with reactors: immediate slaughtering, trial slaughtering, and postponed slaughtering.

11. Milk for human consumption.

12. Clinical cases.

10.3.2.2 Surveillance

Surveillance is a critical initial step in initiating control and eventual eradication of BTB in any country and, even in resource-poor countries, should be executed with as much precision as can be afforded. There are recognized standard procedures for livestock that are mainly dependent on the use of tuberculin testing or abattoir records (with its known limitations).

The process in wildlife is much more complex and usually consists of three independent processes: passive scanning surveillance on hunted wildlife; passive surveillance on animals found dead (road kills), moribund, or with abnormal behav­ior; and active surveillance on hunted or culled animals. Surveillance, and the reliability of the results, in wildlife species is further complicated by unknown geographic dispersion of populations, unknown population densities, difficulties in observing and collecting animals, and the nonrandom selection of the most acces­sible animals leading to potential sampling biases. These activities may be supplemented by active surveillance based on ante-mortal blood testing collected when animals are immobilized for various reasons. The detection of tuberculosis­like lesions in the field has a low sensitivity, and the prevalence of BTB in wildlife species is usually underestimated or not detected (Fitzgerald and Kaneene 2013; Riviere et al. 2015).

10.3.2.3 Movement Restriction and Biosecurity

The imposition of movement restrictions on tuberculin reactors assumes that cattle- to-cattle transmission of BTB is of critical importance. Movement restriction to prevent disease dissemination is an essential component of any BTB control strat­egy, and it can be employed to broadly control the spread of the disease in countries where resources are limited and comprehensive control programs cannot be implemented. There are good examples that this strategy can be used successfully. In the USA, biosecurity and movement restrictions which commenced as early as 1900 to prevent both the entry of infected animals from Europe and their local dissemination played a pivotal role in eliminating BTB on a regional basis (Good and Duignan 2011). Mathematical models similarly highlighted the value of move­ment restrictions. As an example, in Great Britain, the R0 for between-herd spread of BTB in cattle is 1.1 (Cox et al. 2005). That means there would be 11 new infected herds for each 100 existing infected herds, emphasizing that restricting movement of infected or high-risk herds is critical for the control of BTB.

To facilitate the initiation of control programs, attempts should be made to perform pre-movement testing of all animals from herds in high-risk areas (except when they go directly to slaughter). This would aid in the identification of pockets of infection that may exist and prevent the dissemination of large numbers of infected cattle. Hence as a strategy, when initiating the control of BTB in African countries, cattle movement should be regulated by zoning the specific countries or regions into low- and high-risk areas and by prohibiting animal movement from the high- to the low-risk areas (Bourne 2007). This should have a beneficial effect in Africa where there are high (urban/peri-urban)- and low (pastoral)-risk areas and intensive, high- and extensive, low-risk herds. Given the insufficient collaboration at regional and national levels, the lack of quarantine and border control, and the substantial illegal movement across national borders, this strategy is currently bound to be almost impossible to implement and manage unless there is a drastic change of mind and commitment to control BTB and a changed approach to the control of BTB in those regions (FAO 2012).

Test-and-slaughter is not only a practical approach but also is more economical than other BTB control measures (Roswurm and Ranney 1973). Nevertheless, by applying the broad principles of biosecurity, it would be possible to reduce the risk of cattle becoming infected. It is critical that the policy of test-and-slaughter be vigorously applied at all levels and that BTB-positive animals are quarantined and slaughtered as there are many instances where reactors are knowingly sold on the open market, contributing to the further dissemination of the infection (Berrada 1993). Imposing these measures will inevitably require a degree of discipline and compliance that is currently absent from many African countries.

10.3.2.4 Public Awareness

The prevailing ignorance and reluctance to acknowledge the importance of BTB and zoonotic TB is one of the biggest challenges in Africa that will have to be addressed before embarking on control and eradication campaigns if there is to be any hope of success. There is a well-documented lack of knowledge across the continent of the presence and the role of BTB in the health and welfare of its human and animal populations (Munyeme et al. 2010; Tamiru et al. 2013; Tebug et al. 2014; Kidane et al. 2015; Kazoora et al. 2016).

Confinement, poor hygiene, and poor replacement schemes increase the risk of BTB. Therefore, farmers’ education, regarding the nature of BTB, is critical, since most sanitary measures enforced by law are likely to fail if the people do not understand and support them. Hence, commonsense cleanliness of cow sheds, floors, feeding, and water troughs, and maintaining a closed herd at all times are important activities if BTB is to be controlled.

Public awareness campaigns and sensitization of farmers and the general public are key components in the overall strategy when attempting to control zoonotic TB. Specific measures include general hygiene and boiling of milk before consump­tion. A simulation model in Tanzania (Roug et al. 2014) indicated that boiling of milk substantially contributed to reducing human exposure, especially early in the control regimen. Therefore, regulatory authorities in different countries should focus on the implementation of pasteurization or some form of heat treatment of milk to control zoonotic TB even when they lack the ability to control the disease in cattle.

10.4