ARTICLE IN PRESS Research in Veterinary Science ■■ (2014) ■■–■■

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Bovine tuberculosis: Historical perspective

Even though bovine tuberculosis (TB) is a very old acquaintance, and it has been widely studied in the last century, many aspects are still the subject of controversy, starting with its exact definition. Firstly, bovine TB was, in general, defined as the infection caused by Mycobacterium bovis (Braun and Lebek, 1958; Francis, 1958; McMurray, 1941; Schmiedel, 1966, 1968); however, recently a change in this definition was proposed, including now the infection in bovids (including all Bos species, and Bubalus bubalus) and bison (Bison bison) with any of the disease-causing mycobacterial species within the Mycobacterium tuberculosis-complex (Bovine Tuberculosis Subgroup of the Task Force, 2013). Still, the most common causative agent of TB in cattle is M. bovis and to a lesser extent, Mycobacterium caprae (Aranaz et al., 2003; Muller et al., 2013; Rodríguez et al., 2009; Rodriguez et al., 2011). Nowadays, human TB attributable to direct contact with infected cattle is lower than 1% of the confirmed cases in developed countries, mainly due to the heat treatment of the milk and the implementation of veterinary surveillance in the slaughterhouse (Grange and Yates, 1989; Muller et al., 2013). Nevertheless, in developing countries where human and animal TB infection is endemic, and bovine TB control programmes are not implemented, the situation is similar to that described at the beginning of the 20th century when one out of nine deaths were due to TB and 10–20% of them had an animal origin (Muller et al., 2013; Olmstead and Rhode, 2004). In fact, although the zoonotic potential of M. bovis was always suspected, it was not until the 20th century that this was clearly demonstrated. In 1898, Theobald Smith reported that human and bovine TB were infections caused by different bacteria. Some contemporary researchers misunderstood the hypothesis of Smith. In fact, in a conference in London in 1901, Koch reported that the aetiological agent of TB in animals was not a threat for humans. Fortunately, this hypothesis was not accepted without questions and a commission of experts was requested to elucidate this enquiry. Finally, in 1911 this commission concluded that TB could be transmitted between animals and humans. Furthermore, evidence of this transmission was also provided by M. P. Ravenel in 1902, when M. bovis was isolated in tissue samples from children with meningitis. Good diagnostic standards and reliable statistics revealed that between 1901 and 1932, 91% of cervical lymph node and 28% of meningeal TB cases in children under 5 years of age were due to M. bovis (Grange and Yates, 1994), further demonstrating the importance of this zoonosis. Even before the findings of Ravenel, several scientists had already linked TB in humans with the presence of infection in animals and the consumption of non-pasteurized/ boiled milk containing tubercle bacilli was considered as the most probable route of transmission (Collins and Grange, 1983). However,

with the implementation of sanitation practices such as the boiling of milk, and the increasing number of milk pasteurization plants all over the world, the digestive route of the infection became less important. On the other hand, airborne infection continued to be frequent among meat industry and slaughterhouse workers (Robinson et al., 1988), demonstrating the importance of the control of the infection in animals. However, it took 25 years, following the statement by the commission of experts highlighting the risk posed by bovine TB to public health, before the start of the first voluntary TB control programmes in Europe. In Great Britain, in the 1930s, about 40% of all animals slaughtered in public abattoirs had TB lesions and about 0.5% of all dairy cows produced milk containing tubercle bacilli (Collins and Grange, 1983). The first TB control programmes became mandatory in 1950 and were based on a test and slaughter policy using the intradermal test. Bovine TB has been an important issue since the beginning of the European Economic Community (EEC) and the current EU policies regarding eradication of the disease are best understood after considering the progressive development of the relevant European legislation such as the Council Directive 64/432/ECC of 26 June 1964 and subsequent amendments. Moreover, the founding of European organizations such as the Bovine Tuberculosis subgroup of the Task Force (http://, and the EU Reference Laboratory (EU-RL) for Bovine Tuberculosis [Commission Regulation (EC) No 737/2008. http://www.bovinetuberculosis .eu], demonstrate the efforts made to achieve the eradication of bovine TB in Europe. The current EU policy on the eradication of bovine TB is based on two principles: (1) the Member States are primarily responsible for the eradication of bovine TB and may receive community financial support for the eradication programme and (2) eradication of bovine TB in the EU must be a financial target and the Member States must consider eradication as the defined aim (Reviriego Gordejo and Vermeersch, 2006). The historical perspective with regards to bovine TB in the United States (USA) differed significantly from that described in Europe. The Royal Commission on Tuberculosis reported the pathogenicity of bovine TB in 1895 and afterwards, in 1898, the risk of infection by the consumption of milk or other products from infected animals was noted. In fact, cowsheds, butcheries and dairies were considered to be dangerous zones for Public Health and the milk and meat from infected animals were not put on sale. In 1907, Griffith demonstrated the transmission of TB between different animal species and humans, the presence of the bacteria in milk from infected animals without lesions in the udder and the presence of M. tuberculosis (showing low virulence in cattle) in animal products (Royal Commission on Tuberculosis, 1907). All these findings 0034-5288/© 2014 Published by Elsevier Ltd.

Please cite this article in press as: Javier Bezos, Julio Álvarez, Beatriz Romero, Lucía de Juan, Lucas Domínguez, Bovine tuberculosis: Historical perspective, Research in Veterinary Science (2014), doi: 10.1016/j.rvsc.2014.09.003

ARTICLE IN PRESS Preface/Research in Veterinary Science ■■ (2014) ■■–■■


encouraged the establishment of a veterinary public health and the beginning of control programmes for zoonotic diseases based on slaughterhouse surveillance and the pasteurization of milk. In the USA, the bovine TB eradication campaign has been highly successful as the prevalence of TB in cattle has decreased from 5% in 1917 to less than 0.001% in 2009 (Schiller et al., 2010). Complete eradication of bovine TB is not only difficult to achieve in high prevalence countries, but also in countries with low proportions of TB-infected herds. Even in some official tuberculosis free (OTF) countries TB prevalence is currently slightly rising. Trade and wildlife reservoirs both in non-OTF and OTF countries are major factors for re-infections of and spillover to livestock (Schiller et al., 2010, 2011). It is important to highlight that the main basis of the current eradication programmes is a reagent (tuberculin) developed at the end of the 19th century by Koch and initially conceived for the cure of the disease (Good and Duignan, 2011). Nowadays, the intradermal tuberculin test remains as the most important diagnostic tool and the PPD tuberculin is one of the reagents more often used for livestock. Nevertheless, the tuberculin composition is poorly characterized, as significant differences exist with regards to the potency between tuberculins from different manufacturers (Dobbelaer et al., 1983). Moreover, potency testing of the tuberculins is difficult and not well standardized, resulting in high costs and logistical demands. In this sense, the commitment of the European Commission-DG Health and Consumers regarding the standardization of tuberculins is laudable. On the other hand, the lack of an effective vaccine preventing the infection has significantly affected TB eradication. Vaccination is not currently allowed in countries with ongoing official bovine TB eradication programmes due to the interference caused to the official diagnostic tools (Council Directive 78/52/EEC). Nevertheless, it has been proposed as a potential control approach for TB in other species not subjected to eradication programmes, or in countries where these programmes are not economically manageable (Buddle et al., 2013; Canto Alarcon et al., 2013). Nevertheless, great efforts are being made to develop a more effective alternative to the only vaccine commercially available nowadays which was created a century ago (bacillus Calmette–Guérin; BCG) (Buddle et al., 2013). These new vaccines have to be safe and more effective than BCG to be considered as a real option for their potential use in humans and animals. The different reviews included in this special issue focus on the transmission and epidemiology, risk assessment, vaccination, diagnosis and control and vaccination of TB in wildlife, and provide an exhaustive review of all key aspects of bovine TB.

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Javier Bezos a,b, Julio Álvarez c, Beatriz Romero b, Lucía de Juan b,d, Lucas Domínguez b,d a MAEVA SERVET SL. 28749, Alameda del Valle, Madrid, Spain b

Centro de Vigilancia Sanitaria Veterinaria (VISAVET), Universidad Complutense, 28040, Madrid, Spain c

Department of Veterinary Population Medicine, University of Minnesota, St. Paul, MN, USA d

Departamento de Sanidad Animal, Facultad de Veterinaria, Universidad Complutense de Madrid, 28040 Madrid, Spain Tel.: +34 91 394 39 92; fax: +34 91 394 37 95. E-mail address: [email protected]

Please cite this article in press as: Javier Bezos, Julio Álvarez, Beatriz Romero, Lucía de Juan, Lucas Domínguez, Bovine tuberculosis: Historical perspective, Research in Veterinary Science (2014), doi: 10.1016/j.rvsc.2014.09.003

Bovine tuberculosis: historical perspective.

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