Transboundary and Emerging Diseases
REVIEW ARTICLE
Epidemiology Caught in the Causal Web of Bovine Tuberculosis D. U. Pfeiffer Veterinary Epidemiology, Economics & Public Health Group, Royal Veterinary College, University of London, Hertfordshire, UK
Keywords: policy; human behaviour; transdisciplinarity; science; risk governance; wildlife Correspondence: D. U. Pfeiffer. Veterinary Epidemiology, Economics & Public Health Group, Royal Veterinary College, University of London, Hawkshead Lane, North Mymms, Hertfordshire, AL9 7TA, UK. Tel.: +44 (1707) 666205; Fax: +44 (1707) 666574; E-mail: [email protected]
Summary Bovine tuberculosis in domestic cattle in the presence of significant infection levels in wild animal species represents a major challenge for disease control. The use of wild animal population density reduction as part of risk management policies is highly controversial from the perspectives of scientific effectiveness and societal acceptability. The experience in Great Britain in dealing with this problem over the last 20 years demonstrates the need to engage in an integrated approach towards risk governance to more effectively deal with such a complex and contentious multifactorial animal disease problem. As part of this process, the traditional emphasis on bioscientific, in particular epidemiological, research needs to be complemented by relevant social science approaches. In addition, the risk assessment as well as the risk management should have effective participatory elements.
Received for publication December 2, 2012 doi:10.1111/tbed.12105
Context Mycobacterium bovis causes one of the most widespread zoonotic bacterial infections in mammal species. It is likely to occur in most countries around the world, in many of these at very low prevalence due to the implementation of control or eradication programmes over long periods of time. A major complicating factor preventing its eradication is its occurrence in wild mammal species. The complexity of the challenge has been demonstrated in particular in New Zealand, the United Kingdom, the Republic of Ireland and USA’s Michigan state where M. bovis still occurs at levels that do not currently allow eradication (Pfeiffer, 2008; Humblet et al., 2009; Okafor et al., 2011). The intent to control or eradicate an infectious disease needs to be underpinned by a sound risk management policy. The development of the policy is the responsibility of the risk managers who have to consider the available financial resources and the outcomes of risk assessments. A key requirement is sufficient knowledge about the underlying biological and non-biological processes that allow the implementation of risk mitigation measures that result in effective reduction in risk of transmission of the infectious 104
organism. Unfortunately, even from a purely biological perspective, there are in almost all instances significant knowledge gaps which result in uncertainty in relation to the likelihood of particular risk mitigation measures being successful (Fish et al., 2011). It should also be recognized that such measures can be highly effective even if the disease’s epidemiology is poorly understood, for example, if vaccine is available which is highly effective, easily applied and low cost. But even if effective risk mitigation options are available, the policy may still be unsuccessful in the absence of adequate financial or staff resources, effective legislation/governance or adequate support by important stakeholders. If there is variation amongst stakeholders in relation to the acceptance of different risk mitigation options, the ever present uncertainty in relation to effectiveness of these risk mitigation measures is then often used to emphasize the need for better scientific evidence and to justify non-compliance (Enticott and Franklin, 2009; Grant, 2009; Carstensen et al., 2011; Spencer, 2011; Wilkinson et al., 2011). It is for risk managers to recognize the social role of scientific uncertainty and that, in the design of effective control strategies, science may often be less important than values and cultural attitudes (Jamieson, 1996).
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Why Worry? The acceptance of a policy amongst stakeholders and therefore its success is closely linked to its purpose. In the case of bovine tuberculosis, risk management is conducted primarily to be able to trade cattle and associated products with countries that are considered free from bovine tuberculosis. The zoonotic potential of M. bovis was the reason why national control programmes were introduced during the last century. But due to the combination of widespread pasteurization of milk and reduction in infection levels in cattle through control programmes this risk is now considered to be minimal. In the United Kingdom, M. bovis diagnoses in humans have varied between 20 and 50 individuals per year, and almost all of them were unrelated to animal exposure while in the UK. At the same time, M. tuberculosis diagnoses in humans have increased from around 5500 to almost 8000 per year (source: UK Health Protection Agency). Other reasons for control or eradication policies of M. bovis are the adverse effects on animal productivity and welfare, and wild animal conservation. The importance and acceptance of the programme purpose for the different stakeholder groups influences the justification of specific risk mitigation measures and their cost. In Great Britain, the tuberculosis breakdown risk amongst previously M. bovisfree cattle herds tested during any year has increased from about 2.3% in 1998 to just over 5% in 2010, whilst the total annual government expenditure increased from about £25 million to about £120 million during the same period (source: www.defra.gov.uk). This enormous surveillance, control and research effort involved performing 7.6 million tests in cattle in 2011 which resulted in slaughter of about 34 000 cattle, relative to 2.2 million tests in 1996 and 3 776 cattle slaughtered (source: www.defra.gov.uk). When considering this tuberculosis control intensity, it needs to also be taken into account that it is concentrated in the southwest of England and in Wales. The spatial extent of this area has continuously increased over the last 10–15 years, despite the enormous resources invested by government and farmers. What is the Epidemiological Problem? The epidemiology of M. bovis represents a classic disease problem involving multiple host species between which infection is flowing in most instances bidirectionally, with usually different weights attributed to the directions. The absolute and relative magnitude of each of these weights is still subject to significant uncertainty. A key requirement for successful control is an understanding of the role of the different host species, specifically in terms of them being able to maintain infection within local populations, that is, being reservoir hosts, or acting as spillover hosts, who are unable
Epidemiology and TB Policy
to maintain infection without continued introduction from other species. A risk mitigation measure will usually aim at changing a reservoir to a spillover host (Pfeiffer, 2008; Nugent, 2011). The countries that have a widely recognized bovine tuberculosis problem all share the presence of wildlife reservoir species. In New Zealand, it is the Australian brushtailed possum, in USA’s Michigan state, it is white-tailed deer, and in the United Kingdom and the Republic of Ireland, it is the European badger (Pfeiffer, 2008). In all these cases, other wild animal species and cattle are also involved, and on extremely rare occasions, if ever, humans. A subject of scientific and non-scientific debate has been the frequency and direction of infection flow between cattle and the relevant wild animal reservoir species and also the importance of spread amongst cattle. In New Zealand and the Republic of Ireland, there is agreement amongst almost all stakeholders that the respective wild animal reservoir species is primarily responsible for the continued presence of M. bovis in domestic cattle (Morris and Pfeiffer, 1995; More and Good, 2006). In Michigan state, there is disagreement between stakeholders such as hunters and farmers about their role (Carstensen et al., 2011). The situation in Great Britain has resulted in significant tensions in society, specifically between those prioritizing protection of wildlife and those attributing the need to control tuberculosis in wildlife to eradicate cattle tuberculosis higher priority (Zuckerman, 1980; Dunnet et al., 1986; Krebs, 1997; Spencer, 2011). It could be argued that whilst there is no complete understanding of the epidemiology of M. bovis in these countries, it should still be sufficient to be able to control the disease. In all cases, the infection seems to occur within infected metapopulations of the respective wild animal reservoir species at overall prevalence levels of 5–20%, but clusters of higher infection occur within these populations, as a result of variation in social contact structures and environmental conditions. Transmission within these populations occurs through direct or indirect contact. Spatial spread is influenced by the dispersal of young animals, in particular males. Contact between the wild animal reservoir and cattle is typically infrequent and is likely to be indirect, for example, through environmental contamination. Although it needs to be noted that there are epidemiological scenarios where wild animal to livestock transmission may be more frequent, such as between wild possums and farmed deer in New Zealand due to behavioural factors. In this multifactorial causal web, effective implementation of classical control measures applied to cattle should, in general, not allow significant cattle–cattle transmission to occur, that is, they should become spillover hosts. Yet, it has become apparent, particularly in Great Britain, that cattle-to-cattle transmission still makes a contribution to the
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disease epidemiology which cannot be ignored (Krebs, 1997; Independent Scientific Group on Cattle TB, 2007). What Can be Done? The classic control measures for cattle tuberculosis are diagnostic testing and slaughter of test-positive animals, combined with movement control of infected herds and post-mortem inspection of cattle at the abattoir for presence of typical tissue lesions. It is important to note that the response to positive test results or detection of lesions at the individual animal level always also applies to the herd, because the assumption is being made that if one animal tests positive or has lesions at the abattoir, there is an increased risk of there being more infected animals within that herd, even if they have already been tested. The most widely used diagnostic method is the tuberculin test, which is known to have limited sensitivity (de la Rua-Domenech et al., 2006; Schiller et al., 2010). But the test is still considered to be adequate, particularly if applied at the herd level, because that compensates somewhat for the moderate individual animal sensitivity. The question arises why this set of control measures, if applied according to recommended international standards, has been used successfully in most countries, but not in the presence of a significant reservoir in wildlife species. It does indeed seem that the re-introduction of infection from wildlife, even if occurring relatively infrequently, exposes the shortcomings of the diagnostic test. Unfortunately, more sensitive diagnostic tests, such as gamma interferon, are not yet cost-effective for large-scale routine testing (Schiller et al., 2011). The obvious answer to protecting cattle from infection would be their vaccination, but that is not possible because the currently available vaccine would prevent differentiation between diagnostic reaction caused by infection and vaccination (Waters et al., 2012). Given the above, measures need to be applied to prevent the re-introduction of infection from wildlife reservoirs to cattle (and vice versa). These can be physical separation of populations, such as by the use of fences or avoiding keeping cattle in areas of particularly high densities of the wildlife reservoir (Phillips et al., 2003; Wilson et al., 2011). If feasible, the goal should be to eradicate the infection from the wildlife reservoir species. This can be done by reducing the number of susceptible animals below a given threshold, which can be achieved either by vaccination or reduction in population density (O’Brien et al., 2011). Simulation modelling allows determination of the required threshold, below which infection is believed to eventually disappear. Vaccination of wild animal populations is a major technological and logistical challenge, in terms of the vaccine development and delivery that achieves the necessary sustained vaccination coverage. It has only rarely been used successfully, and where that has 106
happened, it was very costly, such as in the case of rabies in foxes in continental Europe (Muller et al., 2012). This leaves the option of population density reduction, which can be achieved by fertility control or increasing mortality. The latter is the technique which has been used in New Zealand, the Republic of Ireland and in Great Britain. The use of the population reduction method has resulted in much controversy, particularly in Great Britain. In this country, various population control methods including gassing, snaring, cage trapping and shooting were used between 1971 and 1997 (Krebs, 1997). Population density control was discontinued between 1998 and 2007, when a large-scale scientific study for investigating the impact of badger population reduction on cattle tuberculosis was conducted. This randomized badger culling trial (RBCT) was funded by the British government at a total cost of £49 million and coordinated by the Independent Scientific Group (ISG), which was purposely selected to consist of scientists independent from government. Details in relation to the study and its conclusions are provided in the report produced by the ISG (Independent Scientific Group on Cattle TB, 2007), as well as in a series of peer-reviewed scientific publications (Woodroffe et al., 2006, 2009; Donnelly et al., 2007; Jenkins et al., 2010). The findings from this study included confirmation that badgers contribute to cattle TB but also that whilst removal of badgers within a geographical area reduces cattle TB incidence, it appears to increase in the border of the removal area. It was concluded that badger removal was not cost-effective and that instead, a TB vaccine for cattle should be developed and the cattle testing regime and methods should be improved. After examining this report, the British government’s Chief Scientist Professor Sir David King came to a slightly different conclusion, in that in areas of high and sustained TB incidence badger removal would still be a useful control measure (King, 2007). The Labour government decided for England in 2008, after much deliberation and consultation of expert scientists, that no badger removal policy should be introduced; instead, research targeted at development of badger and cattle vaccines would be funded. In the same year, the Welsh government developed a national control strategy involving badger population reduction together with various cattle measures. Badger welfare groups challenged the legality of this policy in court through a judicial review, which eventually failed. But the policy was not implemented, because after a change of government in Wales, it was decided in 2011, after commissioning a report from a group of scientists, to abandon badger population reduction and instead to apply the newly developed badger TB vaccine together with various cattle control measures. In contrast, the conservative/liberal British coalition government decided in 2011 for England to introduce a farmer
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led badger removal policy (Anonymous, 2011). This decision was also challenged by badger welfare groups, but the judicial review failed in 2012. The first badger removal operations should have commenced in autumn 2012, amongst threats from badger welfare groups to disrupt these activities, but they were postponed until summer 2013 when it was discovered that badger numbers in the designated areas were higher than expected, and therefore, the targeted level of badger population reduction could not be achieved. As a consequence of no decision having been made over a period of 10 years whilst the RBCT was being conducted and the variation in interpretation of the scientific evidence generated by this enormously costly scientific field study, political decision-makers found it difficult to develop policies which would be able to receive broad support amongst stakeholders. In fact, it could be argued that public opinion in Great Britain is at least as divided now as it was before the trial commenced in the last century. It has even been suggested that the situation has turned into a conflict between urban and rural communities (Brumfiel, 2012; Cassidy, 2012). What are the Lessons for Risk Assessment and Management? There are often unrealistic expectations amongst stakeholders, particularly policy makers, in terms of what knowledge ‘science’ can generate and to what extent that will determine the effectiveness of the resulting policy (Jamieson, 1996). Science is considered to be implicitly rational and objective, and able to eventually come up with solutions for most of society’s problems. In reality, science and its outputs are subject to ignorance, ambiguity and uncertainty, and therefore, at any point in time, there may well be several ‘valid’ scientific standpoints in relation to how a particular system functions (Van den Hove, 2007; Renn et al., 2011; Rivera-Ferre and Ortega-Cerda, 2011). The latter situation is a very common scenario and represents a major communication challenge for decision-makers. A particular problem has been the emphasis on the desire amongst policy makers for ‘accurate’ quantitative measurement in risk assessment, compounded by professional boundary issues which prevent appropriate representation of underlying system properties (Gieryn, 1983; Mikes, 2011). Recent experience, particularly during the climate change debate, has shown that development of effective policies requires adopting an integrated risk governance perspective in recognition of the complexity of the science–policy interface (Renn, 2005; Assmuth et al., 2010; Aven and Renn, 2010; Renn et al., 2011). This post-modern perspective of the role of science in policy development should result in more effective decision-making, and not, as predicted by Kuntz (2012), in arbitrary decisions.
Epidemiology and TB Policy
When seeking a risk management solution for dealing with infectious disease risks, most stakeholders will assume that the biosciences alone hold the answer (Enticott, 2001). In the case of the bovine tuberculosis disease problem in Great Britain, epidemiological research was expected to fulfil that role (Krebs, 1997). But whilst epidemiology has made an important contribution towards generating relevant knowledge based on biomedical principles, its methodological tools and underlying epistemiological principles are less useful for examining the drivers of human behaviour. This shortcoming becomes particularly apparent when dealing with complex and contentious multifactorial problems such as bovine tuberculosis in domestic cattle. In such situations, which are usually characterized by significant uncertainties in relation to impacts of different policy options and understanding of underlying disease risks, transdisciplinary approaches become essential (Stirling, 2007, 2012; Pohl, 2008). This involves integrated research linking different scientific disciplines, particularly the natural together with the social sciences, both in the risk assessment and management contexts (Strang, 2009). But apart from integration, research and policy development need to have participatory components by involving non-academic stakeholders, specifically those affected by the policy decisions (Max-Neef, 2005; Tress et al., 2006; Dreyer and Renn, 2009; Renn et al., 2011). It should be noted that the British government, particularly over the last 10–15 years, has engaged in extensive communication with stakeholders during the policy development process, through public consultations, advisory groups and public meetings. More specifically, the integrated nature of zoonotic disease systems involving wildlife, livestock and humans needs to be recognized so that effective prevention and control policies can be developed. Particular emphasis has to be placed on the human behavioural drivers influencing transmission dynamics, because being able to change these is often key to successful risk management. Such changes are more likely to occur if the relevant stakeholders accept that they themselves have a role to play and want the management of the risk. This is unlikely to be achieved by top-down and authoritarian prescriptive approaches. In contrast, a participatory approach is required that achieves a common purpose and aims to develop shared solutions (Falk and Wallace, 2011; Renn et al., 2011). In the case of bovine tuberculosis in Great Britain, identifying common purpose across stakeholder groups will be impossible given that the justification of aiming for disease eradication can be questioned (Torgerson and Torgerson, 2008; Torgerson, 2010). The effectiveness of risk communication is strongly influenced by trust and credibility (Aven and Renn, 2010). The language used for communicating scientific evidence to stakeholders is often poorly effective, and the benefit of using narratives rather than rational science-based
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explanation in this process has been emphasized (Meisel and Karlawish, 2011). Furthermore, it is important that during the policy development process, the breadth of available management tools are utilized, in particular those which are non-regulatory or non-fiscal. In this context, the value of so-called behavioural ‘nudges’ as policy tools in dealing with human behaviour change has now been recognized (Science and Technology Select Committee House of Lords, 2011). The stakeholders involved in M. bovis control traditionally have primarily been the livestock farming and veterinary professions, animal health scientists and government animal health authorities. Only during the last 15–20 years have others such as wildlife protection groups or scientists from other disciplines become influential stakeholders, specifically in countries with significant tuberculosis infection in wild animals. The relationship between these stakeholder groups influences control policy effectiveness. The communication amongst the original group of stakeholders was based around a single primary objective, that is, to eradicate cattle tuberculosis, which simplified policy development and implementation processes, as evidenced in New Zealand. The addition of, for example, the wildlife protection groups in Great Britain resulted in a more complex decision-making landscape, with the societal acceptability of this objective being questioned. The challenge for institutions responsible for animal disease control will be to adopt participatory approaches that are underpinned by sound social science complementing the traditional dominance of veterinary and animal science in animal health risk governance. One caveat that needs to be emphasized is that an integrated approach based on intensive stakeholder involvement is no guarantee for success, in the sense of, say, being able to eradicate bovine tuberculosis. But, it should increase the likelihood that decision-makers are able to define a policy that is acceptable to most if not all relevant stakeholders, even if it does not achieve the desired outcome. It also needs to be taken into consideration that integrated research is a relatively new field and the majority of researchers, particularly in the biosciences, will have to develop the skills and experience required for working successfully in such projects. Conclusion The challenge for control policies for bovine tuberculosis in situations with significant wildlife reservoirs is not only the uncertainty associated with epidemiological mechanisms driving the disease process, but also the variation in public perception about the acceptability and effectiveness of the available control options. The answer to this dilemma should not be to continue to primarily invest in more 108
epidemiological and immunological research, but rather to acknowledge and also research the importance and diversity of drivers influencing human behaviour, which also are part of the causal web of bovine tuberculosis. In addition, the approach to risk assessment and management needs to be based on integrated risk governance principles that include participatory elements, so that stakeholders can be constructively engaged throughout the process. Conflicts of Interest The author has no conflicts of interest to declare. References Anonymous, 2011: The Government’s Policy on Bovine TB and Badger Control in England. Department for Environment, Food and Rural Affairs, London, UK. Assmuth, T., M. Hilden, and C. Benighaus, 2010: Integrated risk assessment and risk governance as socio-political phenomena: a synthetic view of the challenges. Sci. Total Environ. 408, 3943–3953. Aven, T., and O. Renn, 2010: Risk Management and Governance. Springer Verlag, Heidelberg, Germany. Brumfiel, G., 2012: Badger battle erupts in England. Nature 490, 317–318. Carstensen, M., D. J. O’Brien, and S. M. Schmitt, 2011: Public acceptance as a determinant of management strategies for bovine tuberculosis in free-ranging U.S. wildlife. Vet. Microbiol. 151, 200–204. Cassidy, A., 2012: Vermin, victims and disease: UK framings of badgers in and beyond the bovine TB controversy. Sociol. Ruralis 52, 192–214. Donnelly, C. A., G. Wei, W. T. Johnston, D. R. Cox, R. Woodroffe, F. J. Bourne, C. L. Cheeseman, R. S. CliftonHadley, G. Gettinby, P. Gilks, H. E. Jenkins, A. M. Le Fevre, J. P. McInerney, and W. I. Morrison, 2007: Impacts of widespread badger culling on cattle tuberculosis: concluding analyses from a large-scale field trial. Int. J. Infect. Dis. 11, 300–308. Dreyer, M., and O. Renn, 2009: A structured approach to participation. In: Dreyer, M., and O. Renn (eds), Food Safety Governance - Integrating Science, Precaution and Public Involvement, pp. 111–120. Springer Verlag, Berlin, Germany. Dunnet, G. M., D. M. Jones, and J. P. McInerney, 1986: Badgers and Bovine Tuberculosis - Review of Policy. Her Majesty’s Stationery Office, London, UK. Enticott, G., 2001: Calculating nature: the case of badgers, bovine tuberculosis and cattle. J. Rural. Stud. 17, 149–164. Enticott, G., and A. Franklin, 2009: Biosecurity, expertise and the institutional void: the case of bovine tuberculosis. Sociol. Ruralis 49, 375–393. Falk, I., and R. Wallace, 2011: Managing plant biosecurity across borders. In: Falk, I., R. Wallace, and M. L. Ndoen (eds), Man-
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REVIEW ARTICLE
Epidemiology Caught in the Causal Web of Bovine Tuberculosis D. U. Pfeiffer Veterinary Epidemiology, Economics & Public Health Group, Royal Veterinary College, University of London, Hertfordshire, UK
Keywords: policy; human behaviour; transdisciplinarity; science; risk governance; wildlife Correspondence: D. U. Pfeiffer. Veterinary Epidemiology, Economics & Public Health Group, Royal Veterinary College, University of London, Hawkshead Lane, North Mymms, Hertfordshire, AL9 7TA, UK. Tel.: +44 (1707) 666205; Fax: +44 (1707) 666574; E-mail: [email protected]
Summary Bovine tuberculosis in domestic cattle in the presence of significant infection levels in wild animal species represents a major challenge for disease control. The use of wild animal population density reduction as part of risk management policies is highly controversial from the perspectives of scientific effectiveness and societal acceptability. The experience in Great Britain in dealing with this problem over the last 20 years demonstrates the need to engage in an integrated approach towards risk governance to more effectively deal with such a complex and contentious multifactorial animal disease problem. As part of this process, the traditional emphasis on bioscientific, in particular epidemiological, research needs to be complemented by relevant social science approaches. In addition, the risk assessment as well as the risk management should have effective participatory elements.
Received for publication December 2, 2012 doi:10.1111/tbed.12105
Context Mycobacterium bovis causes one of the most widespread zoonotic bacterial infections in mammal species. It is likely to occur in most countries around the world, in many of these at very low prevalence due to the implementation of control or eradication programmes over long periods of time. A major complicating factor preventing its eradication is its occurrence in wild mammal species. The complexity of the challenge has been demonstrated in particular in New Zealand, the United Kingdom, the Republic of Ireland and USA’s Michigan state where M. bovis still occurs at levels that do not currently allow eradication (Pfeiffer, 2008; Humblet et al., 2009; Okafor et al., 2011). The intent to control or eradicate an infectious disease needs to be underpinned by a sound risk management policy. The development of the policy is the responsibility of the risk managers who have to consider the available financial resources and the outcomes of risk assessments. A key requirement is sufficient knowledge about the underlying biological and non-biological processes that allow the implementation of risk mitigation measures that result in effective reduction in risk of transmission of the infectious 104
organism. Unfortunately, even from a purely biological perspective, there are in almost all instances significant knowledge gaps which result in uncertainty in relation to the likelihood of particular risk mitigation measures being successful (Fish et al., 2011). It should also be recognized that such measures can be highly effective even if the disease’s epidemiology is poorly understood, for example, if vaccine is available which is highly effective, easily applied and low cost. But even if effective risk mitigation options are available, the policy may still be unsuccessful in the absence of adequate financial or staff resources, effective legislation/governance or adequate support by important stakeholders. If there is variation amongst stakeholders in relation to the acceptance of different risk mitigation options, the ever present uncertainty in relation to effectiveness of these risk mitigation measures is then often used to emphasize the need for better scientific evidence and to justify non-compliance (Enticott and Franklin, 2009; Grant, 2009; Carstensen et al., 2011; Spencer, 2011; Wilkinson et al., 2011). It is for risk managers to recognize the social role of scientific uncertainty and that, in the design of effective control strategies, science may often be less important than values and cultural attitudes (Jamieson, 1996).
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Why Worry? The acceptance of a policy amongst stakeholders and therefore its success is closely linked to its purpose. In the case of bovine tuberculosis, risk management is conducted primarily to be able to trade cattle and associated products with countries that are considered free from bovine tuberculosis. The zoonotic potential of M. bovis was the reason why national control programmes were introduced during the last century. But due to the combination of widespread pasteurization of milk and reduction in infection levels in cattle through control programmes this risk is now considered to be minimal. In the United Kingdom, M. bovis diagnoses in humans have varied between 20 and 50 individuals per year, and almost all of them were unrelated to animal exposure while in the UK. At the same time, M. tuberculosis diagnoses in humans have increased from around 5500 to almost 8000 per year (source: UK Health Protection Agency). Other reasons for control or eradication policies of M. bovis are the adverse effects on animal productivity and welfare, and wild animal conservation. The importance and acceptance of the programme purpose for the different stakeholder groups influences the justification of specific risk mitigation measures and their cost. In Great Britain, the tuberculosis breakdown risk amongst previously M. bovisfree cattle herds tested during any year has increased from about 2.3% in 1998 to just over 5% in 2010, whilst the total annual government expenditure increased from about £25 million to about £120 million during the same period (source: www.defra.gov.uk). This enormous surveillance, control and research effort involved performing 7.6 million tests in cattle in 2011 which resulted in slaughter of about 34 000 cattle, relative to 2.2 million tests in 1996 and 3 776 cattle slaughtered (source: www.defra.gov.uk). When considering this tuberculosis control intensity, it needs to also be taken into account that it is concentrated in the southwest of England and in Wales. The spatial extent of this area has continuously increased over the last 10–15 years, despite the enormous resources invested by government and farmers. What is the Epidemiological Problem? The epidemiology of M. bovis represents a classic disease problem involving multiple host species between which infection is flowing in most instances bidirectionally, with usually different weights attributed to the directions. The absolute and relative magnitude of each of these weights is still subject to significant uncertainty. A key requirement for successful control is an understanding of the role of the different host species, specifically in terms of them being able to maintain infection within local populations, that is, being reservoir hosts, or acting as spillover hosts, who are unable
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to maintain infection without continued introduction from other species. A risk mitigation measure will usually aim at changing a reservoir to a spillover host (Pfeiffer, 2008; Nugent, 2011). The countries that have a widely recognized bovine tuberculosis problem all share the presence of wildlife reservoir species. In New Zealand, it is the Australian brushtailed possum, in USA’s Michigan state, it is white-tailed deer, and in the United Kingdom and the Republic of Ireland, it is the European badger (Pfeiffer, 2008). In all these cases, other wild animal species and cattle are also involved, and on extremely rare occasions, if ever, humans. A subject of scientific and non-scientific debate has been the frequency and direction of infection flow between cattle and the relevant wild animal reservoir species and also the importance of spread amongst cattle. In New Zealand and the Republic of Ireland, there is agreement amongst almost all stakeholders that the respective wild animal reservoir species is primarily responsible for the continued presence of M. bovis in domestic cattle (Morris and Pfeiffer, 1995; More and Good, 2006). In Michigan state, there is disagreement between stakeholders such as hunters and farmers about their role (Carstensen et al., 2011). The situation in Great Britain has resulted in significant tensions in society, specifically between those prioritizing protection of wildlife and those attributing the need to control tuberculosis in wildlife to eradicate cattle tuberculosis higher priority (Zuckerman, 1980; Dunnet et al., 1986; Krebs, 1997; Spencer, 2011). It could be argued that whilst there is no complete understanding of the epidemiology of M. bovis in these countries, it should still be sufficient to be able to control the disease. In all cases, the infection seems to occur within infected metapopulations of the respective wild animal reservoir species at overall prevalence levels of 5–20%, but clusters of higher infection occur within these populations, as a result of variation in social contact structures and environmental conditions. Transmission within these populations occurs through direct or indirect contact. Spatial spread is influenced by the dispersal of young animals, in particular males. Contact between the wild animal reservoir and cattle is typically infrequent and is likely to be indirect, for example, through environmental contamination. Although it needs to be noted that there are epidemiological scenarios where wild animal to livestock transmission may be more frequent, such as between wild possums and farmed deer in New Zealand due to behavioural factors. In this multifactorial causal web, effective implementation of classical control measures applied to cattle should, in general, not allow significant cattle–cattle transmission to occur, that is, they should become spillover hosts. Yet, it has become apparent, particularly in Great Britain, that cattle-to-cattle transmission still makes a contribution to the
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disease epidemiology which cannot be ignored (Krebs, 1997; Independent Scientific Group on Cattle TB, 2007). What Can be Done? The classic control measures for cattle tuberculosis are diagnostic testing and slaughter of test-positive animals, combined with movement control of infected herds and post-mortem inspection of cattle at the abattoir for presence of typical tissue lesions. It is important to note that the response to positive test results or detection of lesions at the individual animal level always also applies to the herd, because the assumption is being made that if one animal tests positive or has lesions at the abattoir, there is an increased risk of there being more infected animals within that herd, even if they have already been tested. The most widely used diagnostic method is the tuberculin test, which is known to have limited sensitivity (de la Rua-Domenech et al., 2006; Schiller et al., 2010). But the test is still considered to be adequate, particularly if applied at the herd level, because that compensates somewhat for the moderate individual animal sensitivity. The question arises why this set of control measures, if applied according to recommended international standards, has been used successfully in most countries, but not in the presence of a significant reservoir in wildlife species. It does indeed seem that the re-introduction of infection from wildlife, even if occurring relatively infrequently, exposes the shortcomings of the diagnostic test. Unfortunately, more sensitive diagnostic tests, such as gamma interferon, are not yet cost-effective for large-scale routine testing (Schiller et al., 2011). The obvious answer to protecting cattle from infection would be their vaccination, but that is not possible because the currently available vaccine would prevent differentiation between diagnostic reaction caused by infection and vaccination (Waters et al., 2012). Given the above, measures need to be applied to prevent the re-introduction of infection from wildlife reservoirs to cattle (and vice versa). These can be physical separation of populations, such as by the use of fences or avoiding keeping cattle in areas of particularly high densities of the wildlife reservoir (Phillips et al., 2003; Wilson et al., 2011). If feasible, the goal should be to eradicate the infection from the wildlife reservoir species. This can be done by reducing the number of susceptible animals below a given threshold, which can be achieved either by vaccination or reduction in population density (O’Brien et al., 2011). Simulation modelling allows determination of the required threshold, below which infection is believed to eventually disappear. Vaccination of wild animal populations is a major technological and logistical challenge, in terms of the vaccine development and delivery that achieves the necessary sustained vaccination coverage. It has only rarely been used successfully, and where that has 106
happened, it was very costly, such as in the case of rabies in foxes in continental Europe (Muller et al., 2012). This leaves the option of population density reduction, which can be achieved by fertility control or increasing mortality. The latter is the technique which has been used in New Zealand, the Republic of Ireland and in Great Britain. The use of the population reduction method has resulted in much controversy, particularly in Great Britain. In this country, various population control methods including gassing, snaring, cage trapping and shooting were used between 1971 and 1997 (Krebs, 1997). Population density control was discontinued between 1998 and 2007, when a large-scale scientific study for investigating the impact of badger population reduction on cattle tuberculosis was conducted. This randomized badger culling trial (RBCT) was funded by the British government at a total cost of £49 million and coordinated by the Independent Scientific Group (ISG), which was purposely selected to consist of scientists independent from government. Details in relation to the study and its conclusions are provided in the report produced by the ISG (Independent Scientific Group on Cattle TB, 2007), as well as in a series of peer-reviewed scientific publications (Woodroffe et al., 2006, 2009; Donnelly et al., 2007; Jenkins et al., 2010). The findings from this study included confirmation that badgers contribute to cattle TB but also that whilst removal of badgers within a geographical area reduces cattle TB incidence, it appears to increase in the border of the removal area. It was concluded that badger removal was not cost-effective and that instead, a TB vaccine for cattle should be developed and the cattle testing regime and methods should be improved. After examining this report, the British government’s Chief Scientist Professor Sir David King came to a slightly different conclusion, in that in areas of high and sustained TB incidence badger removal would still be a useful control measure (King, 2007). The Labour government decided for England in 2008, after much deliberation and consultation of expert scientists, that no badger removal policy should be introduced; instead, research targeted at development of badger and cattle vaccines would be funded. In the same year, the Welsh government developed a national control strategy involving badger population reduction together with various cattle measures. Badger welfare groups challenged the legality of this policy in court through a judicial review, which eventually failed. But the policy was not implemented, because after a change of government in Wales, it was decided in 2011, after commissioning a report from a group of scientists, to abandon badger population reduction and instead to apply the newly developed badger TB vaccine together with various cattle control measures. In contrast, the conservative/liberal British coalition government decided in 2011 for England to introduce a farmer
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led badger removal policy (Anonymous, 2011). This decision was also challenged by badger welfare groups, but the judicial review failed in 2012. The first badger removal operations should have commenced in autumn 2012, amongst threats from badger welfare groups to disrupt these activities, but they were postponed until summer 2013 when it was discovered that badger numbers in the designated areas were higher than expected, and therefore, the targeted level of badger population reduction could not be achieved. As a consequence of no decision having been made over a period of 10 years whilst the RBCT was being conducted and the variation in interpretation of the scientific evidence generated by this enormously costly scientific field study, political decision-makers found it difficult to develop policies which would be able to receive broad support amongst stakeholders. In fact, it could be argued that public opinion in Great Britain is at least as divided now as it was before the trial commenced in the last century. It has even been suggested that the situation has turned into a conflict between urban and rural communities (Brumfiel, 2012; Cassidy, 2012). What are the Lessons for Risk Assessment and Management? There are often unrealistic expectations amongst stakeholders, particularly policy makers, in terms of what knowledge ‘science’ can generate and to what extent that will determine the effectiveness of the resulting policy (Jamieson, 1996). Science is considered to be implicitly rational and objective, and able to eventually come up with solutions for most of society’s problems. In reality, science and its outputs are subject to ignorance, ambiguity and uncertainty, and therefore, at any point in time, there may well be several ‘valid’ scientific standpoints in relation to how a particular system functions (Van den Hove, 2007; Renn et al., 2011; Rivera-Ferre and Ortega-Cerda, 2011). The latter situation is a very common scenario and represents a major communication challenge for decision-makers. A particular problem has been the emphasis on the desire amongst policy makers for ‘accurate’ quantitative measurement in risk assessment, compounded by professional boundary issues which prevent appropriate representation of underlying system properties (Gieryn, 1983; Mikes, 2011). Recent experience, particularly during the climate change debate, has shown that development of effective policies requires adopting an integrated risk governance perspective in recognition of the complexity of the science–policy interface (Renn, 2005; Assmuth et al., 2010; Aven and Renn, 2010; Renn et al., 2011). This post-modern perspective of the role of science in policy development should result in more effective decision-making, and not, as predicted by Kuntz (2012), in arbitrary decisions.
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When seeking a risk management solution for dealing with infectious disease risks, most stakeholders will assume that the biosciences alone hold the answer (Enticott, 2001). In the case of the bovine tuberculosis disease problem in Great Britain, epidemiological research was expected to fulfil that role (Krebs, 1997). But whilst epidemiology has made an important contribution towards generating relevant knowledge based on biomedical principles, its methodological tools and underlying epistemiological principles are less useful for examining the drivers of human behaviour. This shortcoming becomes particularly apparent when dealing with complex and contentious multifactorial problems such as bovine tuberculosis in domestic cattle. In such situations, which are usually characterized by significant uncertainties in relation to impacts of different policy options and understanding of underlying disease risks, transdisciplinary approaches become essential (Stirling, 2007, 2012; Pohl, 2008). This involves integrated research linking different scientific disciplines, particularly the natural together with the social sciences, both in the risk assessment and management contexts (Strang, 2009). But apart from integration, research and policy development need to have participatory components by involving non-academic stakeholders, specifically those affected by the policy decisions (Max-Neef, 2005; Tress et al., 2006; Dreyer and Renn, 2009; Renn et al., 2011). It should be noted that the British government, particularly over the last 10–15 years, has engaged in extensive communication with stakeholders during the policy development process, through public consultations, advisory groups and public meetings. More specifically, the integrated nature of zoonotic disease systems involving wildlife, livestock and humans needs to be recognized so that effective prevention and control policies can be developed. Particular emphasis has to be placed on the human behavioural drivers influencing transmission dynamics, because being able to change these is often key to successful risk management. Such changes are more likely to occur if the relevant stakeholders accept that they themselves have a role to play and want the management of the risk. This is unlikely to be achieved by top-down and authoritarian prescriptive approaches. In contrast, a participatory approach is required that achieves a common purpose and aims to develop shared solutions (Falk and Wallace, 2011; Renn et al., 2011). In the case of bovine tuberculosis in Great Britain, identifying common purpose across stakeholder groups will be impossible given that the justification of aiming for disease eradication can be questioned (Torgerson and Torgerson, 2008; Torgerson, 2010). The effectiveness of risk communication is strongly influenced by trust and credibility (Aven and Renn, 2010). The language used for communicating scientific evidence to stakeholders is often poorly effective, and the benefit of using narratives rather than rational science-based
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explanation in this process has been emphasized (Meisel and Karlawish, 2011). Furthermore, it is important that during the policy development process, the breadth of available management tools are utilized, in particular those which are non-regulatory or non-fiscal. In this context, the value of so-called behavioural ‘nudges’ as policy tools in dealing with human behaviour change has now been recognized (Science and Technology Select Committee House of Lords, 2011). The stakeholders involved in M. bovis control traditionally have primarily been the livestock farming and veterinary professions, animal health scientists and government animal health authorities. Only during the last 15–20 years have others such as wildlife protection groups or scientists from other disciplines become influential stakeholders, specifically in countries with significant tuberculosis infection in wild animals. The relationship between these stakeholder groups influences control policy effectiveness. The communication amongst the original group of stakeholders was based around a single primary objective, that is, to eradicate cattle tuberculosis, which simplified policy development and implementation processes, as evidenced in New Zealand. The addition of, for example, the wildlife protection groups in Great Britain resulted in a more complex decision-making landscape, with the societal acceptability of this objective being questioned. The challenge for institutions responsible for animal disease control will be to adopt participatory approaches that are underpinned by sound social science complementing the traditional dominance of veterinary and animal science in animal health risk governance. One caveat that needs to be emphasized is that an integrated approach based on intensive stakeholder involvement is no guarantee for success, in the sense of, say, being able to eradicate bovine tuberculosis. But, it should increase the likelihood that decision-makers are able to define a policy that is acceptable to most if not all relevant stakeholders, even if it does not achieve the desired outcome. It also needs to be taken into consideration that integrated research is a relatively new field and the majority of researchers, particularly in the biosciences, will have to develop the skills and experience required for working successfully in such projects. Conclusion The challenge for control policies for bovine tuberculosis in situations with significant wildlife reservoirs is not only the uncertainty associated with epidemiological mechanisms driving the disease process, but also the variation in public perception about the acceptability and effectiveness of the available control options. The answer to this dilemma should not be to continue to primarily invest in more 108
epidemiological and immunological research, but rather to acknowledge and also research the importance and diversity of drivers influencing human behaviour, which also are part of the causal web of bovine tuberculosis. In addition, the approach to risk assessment and management needs to be based on integrated risk governance principles that include participatory elements, so that stakeholders can be constructively engaged throughout the process. Conflicts of Interest The author has no conflicts of interest to declare. References Anonymous, 2011: The Government’s Policy on Bovine TB and Badger Control in England. Department for Environment, Food and Rural Affairs, London, UK. Assmuth, T., M. Hilden, and C. Benighaus, 2010: Integrated risk assessment and risk governance as socio-political phenomena: a synthetic view of the challenges. Sci. Total Environ. 408, 3943–3953. Aven, T., and O. Renn, 2010: Risk Management and Governance. Springer Verlag, Heidelberg, Germany. Brumfiel, G., 2012: Badger battle erupts in England. Nature 490, 317–318. Carstensen, M., D. J. O’Brien, and S. M. Schmitt, 2011: Public acceptance as a determinant of management strategies for bovine tuberculosis in free-ranging U.S. wildlife. Vet. Microbiol. 151, 200–204. Cassidy, A., 2012: Vermin, victims and disease: UK framings of badgers in and beyond the bovine TB controversy. Sociol. Ruralis 52, 192–214. Donnelly, C. A., G. Wei, W. T. Johnston, D. R. Cox, R. Woodroffe, F. J. Bourne, C. L. Cheeseman, R. S. CliftonHadley, G. Gettinby, P. Gilks, H. E. Jenkins, A. M. Le Fevre, J. P. McInerney, and W. I. Morrison, 2007: Impacts of widespread badger culling on cattle tuberculosis: concluding analyses from a large-scale field trial. Int. J. Infect. Dis. 11, 300–308. Dreyer, M., and O. Renn, 2009: A structured approach to participation. In: Dreyer, M., and O. Renn (eds), Food Safety Governance - Integrating Science, Precaution and Public Involvement, pp. 111–120. Springer Verlag, Berlin, Germany. Dunnet, G. M., D. M. Jones, and J. P. McInerney, 1986: Badgers and Bovine Tuberculosis - Review of Policy. Her Majesty’s Stationery Office, London, UK. Enticott, G., 2001: Calculating nature: the case of badgers, bovine tuberculosis and cattle. J. Rural. Stud. 17, 149–164. Enticott, G., and A. Franklin, 2009: Biosecurity, expertise and the institutional void: the case of bovine tuberculosis. Sociol. Ruralis 49, 375–393. Falk, I., and R. Wallace, 2011: Managing plant biosecurity across borders. In: Falk, I., R. Wallace, and M. L. Ndoen (eds), Man-
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