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Mycobacterium bovis infection: Everything but the cow
Accepted Manuscript Editorial Mycobacterium bovis infection: Everything but the cow J.P. Cassidy PII: DOI: Reference:
S1090-0233(13)00442-5 http://dx.doi.org/10.1016/j.tvjl.2013.09.014 YTVJL 3870
To appear in:
The Veterinary Journal
Please cite this article as: Cassidy, J.P., Mycobacterium bovis infection: Everything but the cow, The Veterinary Journal (2013), doi: http://dx.doi.org/10.1016/j.tvjl.2013.09.014
This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Editorial
Mycobacterium bovis infection: Everything but the cow
There can be few animal diseases, certainly in the United Kingdom, and possibly elsewhere, that generate as much heated scientific debate and political controversy as bovine tuberculosis (bTB). Given that the issues include a heady mixture of ‘a protracted and expensive eradication scheme’, ‘consequences for international trade’, ‘historical zoonosis’, ‘a protected wildlife species’, and a legendary rock guitarist,1 it is perhaps hardly surprising this disease creates so much media attention and public discourse. It has resulted in a particular ‘cultural script’ where scientific evidence and rational argument are frequently trumped by political expediency, ‘custom and practice’, and a host of anthropomorphic attitudes.
Enter this issue of The Veterinary Journal, which potentially adds further complexity to the bTB conundrum by publishing three papers reporting Mycobacterium bovis infection in a multiplicity of domesticated non-bovine mammalian species in the UK, including livestock such as pigs, sheep, goats, llamas and alpacas, as well as companion animals. In their two-part review, Jennifer Broughan and colleagues from the Animal Health and Veterinary Laboratories Agency (Broughan et al., 2013a,b), assess current knowledge of the epidemiology of M. bovis infection in such species; they then present novel data relating to diagnostic submissions for mycobacterial culture, and highlight the challenges posed to detecting and controlling disease in non-bovine animals.
1
See: http://www.theguardian.com/global/2013/aug/24/badger-cull-brian-may-rspca
In a third paper in this issue of The Veterinary Journal, Suzanne Bailey and colleagues at the Bristol Veterinary School report the existence of M. bovis-infected pigs originating from farms with poor biosecurity or where animals are raised outdoors, in the South-West and West-Midland regions of England (Bailey et al., 2013). Intriguingly, these authors found that some of the M. bovis strains found in pigs correlated better with those found in badgers, rather than cattle, raising the possibility that pigs could represent a sentinel for detecting M. bovis infection in wildlife.
So what do these M. bovis-infected domesticated non-bovine/non-wildlife species contribute within the overall ‘black-box’ of epidemiological interactions between cattle, badgers and potentially, other wildlife? At this juncture, the evidence would suggest their role in inter-species disease transmission is relatively small. As Broughan et al. (2013a) indicate, samples from companion and non-bovine farmed animals represent <1% of all samples from which M. bovis is cultured in Great Britain annually, with the caveat that the much more exhaustive active surveillance mechanisms in place to detect infection in cattle are not available for these animals. A further confounding factor has been the introduction of legislation in Great Britain in 2006, requiring animal keepers, meat inspectors and veterinarians to notify authorities of suspect bTB lesions, or the isolation of M. bovis in any mammal excluding human beings. This has inevitably increased disease ascertainment, notwithstanding the fact that the surveillance is passive in nature.
Given the capacity of M. bovis to infect a wide range of species (O'Reilly and Daborn, 1995; Amanfu, 2006), it is perhaps not surprising that bTB has ‘come to the fore’ in animals other than cattle in parallel with the almost doubling of diseased cattle herds in Great Britain between 2004 and 2010.2 This ongoing increase and geographical spread of infection is likely to have had potential ‘spill-over’ effects into contiguous domesticated and wildlife populations. A clearer understanding of how such ‘spill-over’ occurs will dictate what (if any) significance these events have in informing disease control strategies. Previous evidence for the existence of interspecies transmission networks is the concentration and sharing of strains of M. bovis in the same geographical locations by different species (Smith et al., 2003). This study proposed that transmission of M. bovis between cattle and badgers was a ‘two-way street’ and that geographical spread was the result of local, slow ‘diffusion’ of infection between animals over a wide front, as well as by the longer distance transportation of cattle; the latter factor likely to have been significant in the restocking that followed the 2001 foot-and-mouth disease outbreak in the UK (Gilbert et al., 2005; Carrique-Mas, et al., 2008; Johnston et al., 2011).
Improved understanding of the local, behavioural interactions underlying potential ‘transmission events’ will be essential if we are to better appreciate the nature of, and ultimately break or at least manage, these transmission networks. In this context biotelemetry is proving helpful in using proximity data-logging devices to tease-out the complexities of cattle-badger interactions (White et al., 2008; Böhm et al., 2009). Such an approach has flagged individuals in both livestock and wildlife populations with high contact rates, which could act as ‘hubs’ in the spread of disease. See: http://archive.defra.gov.uk/foodfarm/farmanimal/diseases/atoz/tb/documents/btbsurv-report.pdf (accessed 4 August 2011). 2
Biotelemetry is also likely to be useful in supporting or refuting the assumption that the transmission rate of M. bovis infection is positively and linearly related to the density of infectious and susceptible animals. This assumption has been central to the management of bTB in cattle and badgers in the UK to date, drawing on the principle of disease transmission by ‘mass action’, where a reduction in the density of either infectious or susceptible hosts will lead to reduced transmission (White et al., 2008; Böhm et al., 2009). If inter-species interactions at farm level can be identified, this increases the possibility of designing targeted control measures based around high-risk individuals and sub-groups within populations.
The relative importance of disease risk factors is likely to vary between regions given differing domestic and wildlife animal densities, farming practices, and geographical terrain. Bespoke, flexible disease management that reflects local risk, is more likely to be successful in addressing a highly complex, chronic, multispecies disease such as bTB than a ‘one-size-fits-all’ mass control programme. However, such tailored disease control is often difficult to implement within the constraints of statutory regulation.
The eradication of bTB in the UK remains a very challenging, expensive and controversial problem, made all the more intractable by the multitude of factors contributing to its persistence and spread. State veterinarians and other policy makers are in an unenviable position attempting to ‘do the right thing’ based on sometimes conflicting scientific evidence, while at the same time, navigating their way through this often emotionally charged and politically sensitive landscape. Furthermore, the
effects of interventions on the course of chronic diseases such as bTB are typically only seen over the long-term. Careful ongoing surveillance as reported by Bailey et al. (2013) and Brougham et al. (2013a,b), taken together with the epidemiological modelling of cattle movements, the use of biotelemetry to analyse inter-species interactions, and the molecular typing of M. bovis isolates all provide a sound foundation on which to implement and adapt future control strategies. J.P. Cassidy Scientific Editor The Veterinary Journal Pathobiology Section School of Veterinary Medicine University College Dublin Belfield Dublin 4, Ireland E-mail address: [email protected] References
Amanfu, W., 2006. The situation of tuberculosis and tuberculosis control in animals of economic interest. Tuberculosis 86, 330-355. Bailey, S.S., Crawshaw, T.R., Smith, N.H., Palgrave, C.J., 2013. Mycobacterium bovis infection in domestic pigs in Great Britain. The Veterinary Journal, DOI to be inserted Böhm, M. Hutchings, M.R., White, P.C.L., 2009. Dynamic interactions among badgers: Implications for sociality and disease transmission. PLoS One, 4, e5016. Broughan, J.M, Downs, S.H., Crawshaw, T.R., Upton, P.A., Brewer, J., CliftonHadley, R.S., 2013a. Mycobacterium bovis infections in domesticated non-bovine mammalian species. Part 1: Review of epidemiology and laboratory submissions in Great Britain 2004 – 2010. The Veterinary Journal, DOI to be inserted Broughan, J.M, Downs, S.H., Crawshaw, T.R., Upton, P.A., Brewer, J., CliftonHadley, R.S., 2013b. Mycobacterium bovis infections in domesticated non-bovine mammalian species. Part 2: A review of diagnostic methods. The Veterinary Journal, DOI to be inserted Carrique-Mas, J.J., Medley, G.F., Green, L.E., 2008. Risks for bovine tuberculosis in British cattle farms restocked after the foot and mouth disease epidemic of 2001. Preventive Veterinary Medicine, 84, 85–93.
Gilbert, M. Mitchell, A., Bourn, D., Mawdsley, J., Clifton-Hadley, R.S., Wint, W., 2005. Cattle movements and bovine tuberculosis in Great Britain. Nature 435, 491– 496. Johnston, W.T., Vial, F., Gettinby, G., Bourne, F.J., Clifton-Hadley, R.S., Cox, D.R., Crea, P., Donnelly, C.A., McInerney, J.P., Mitchell, A.P. et al., 2011. Herd-level risk factors of bovine tuberculosis in England and Wales after the 2001 foot-and-mouth disease epidemic. International Journal of Infectious Diseases 15, 833-840. O'Reilly, L.M., Daborn, C.J., 1995. The Epidemiology of Mycobacterium bovis infections in animals and man - a review. Tubercle and Lung Disease 76, 1-46. Smith, N.H., Dale, J., Inwald, J., Palmer, S., Gordon, S.V., Hewinson, R.G., Smith, J.M., 2003. The population structure of Mycobacterium bovis in Great Britain: Clonal expansion. Proceedings of the Natural Academy of Sciences of the USA, 100, 15271– 15275. White, P.C.L., Bohm, M., Marion, G., Hutchings, M.R., 2008. Control of bovine tuberculosis in British livestock: There is no ‘silver bullet’. Trends in Microbiology, 16, 420-427.
S1090-0233(13)00442-5 http://dx.doi.org/10.1016/j.tvjl.2013.09.014 YTVJL 3870
To appear in:
The Veterinary Journal
Please cite this article as: Cassidy, J.P., Mycobacterium bovis infection: Everything but the cow, The Veterinary Journal (2013), doi: http://dx.doi.org/10.1016/j.tvjl.2013.09.014
This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Editorial
Mycobacterium bovis infection: Everything but the cow
There can be few animal diseases, certainly in the United Kingdom, and possibly elsewhere, that generate as much heated scientific debate and political controversy as bovine tuberculosis (bTB). Given that the issues include a heady mixture of ‘a protracted and expensive eradication scheme’, ‘consequences for international trade’, ‘historical zoonosis’, ‘a protected wildlife species’, and a legendary rock guitarist,1 it is perhaps hardly surprising this disease creates so much media attention and public discourse. It has resulted in a particular ‘cultural script’ where scientific evidence and rational argument are frequently trumped by political expediency, ‘custom and practice’, and a host of anthropomorphic attitudes.
Enter this issue of The Veterinary Journal, which potentially adds further complexity to the bTB conundrum by publishing three papers reporting Mycobacterium bovis infection in a multiplicity of domesticated non-bovine mammalian species in the UK, including livestock such as pigs, sheep, goats, llamas and alpacas, as well as companion animals. In their two-part review, Jennifer Broughan and colleagues from the Animal Health and Veterinary Laboratories Agency (Broughan et al., 2013a,b), assess current knowledge of the epidemiology of M. bovis infection in such species; they then present novel data relating to diagnostic submissions for mycobacterial culture, and highlight the challenges posed to detecting and controlling disease in non-bovine animals.
1
See: http://www.theguardian.com/global/2013/aug/24/badger-cull-brian-may-rspca
In a third paper in this issue of The Veterinary Journal, Suzanne Bailey and colleagues at the Bristol Veterinary School report the existence of M. bovis-infected pigs originating from farms with poor biosecurity or where animals are raised outdoors, in the South-West and West-Midland regions of England (Bailey et al., 2013). Intriguingly, these authors found that some of the M. bovis strains found in pigs correlated better with those found in badgers, rather than cattle, raising the possibility that pigs could represent a sentinel for detecting M. bovis infection in wildlife.
So what do these M. bovis-infected domesticated non-bovine/non-wildlife species contribute within the overall ‘black-box’ of epidemiological interactions between cattle, badgers and potentially, other wildlife? At this juncture, the evidence would suggest their role in inter-species disease transmission is relatively small. As Broughan et al. (2013a) indicate, samples from companion and non-bovine farmed animals represent <1% of all samples from which M. bovis is cultured in Great Britain annually, with the caveat that the much more exhaustive active surveillance mechanisms in place to detect infection in cattle are not available for these animals. A further confounding factor has been the introduction of legislation in Great Britain in 2006, requiring animal keepers, meat inspectors and veterinarians to notify authorities of suspect bTB lesions, or the isolation of M. bovis in any mammal excluding human beings. This has inevitably increased disease ascertainment, notwithstanding the fact that the surveillance is passive in nature.
Given the capacity of M. bovis to infect a wide range of species (O'Reilly and Daborn, 1995; Amanfu, 2006), it is perhaps not surprising that bTB has ‘come to the fore’ in animals other than cattle in parallel with the almost doubling of diseased cattle herds in Great Britain between 2004 and 2010.2 This ongoing increase and geographical spread of infection is likely to have had potential ‘spill-over’ effects into contiguous domesticated and wildlife populations. A clearer understanding of how such ‘spill-over’ occurs will dictate what (if any) significance these events have in informing disease control strategies. Previous evidence for the existence of interspecies transmission networks is the concentration and sharing of strains of M. bovis in the same geographical locations by different species (Smith et al., 2003). This study proposed that transmission of M. bovis between cattle and badgers was a ‘two-way street’ and that geographical spread was the result of local, slow ‘diffusion’ of infection between animals over a wide front, as well as by the longer distance transportation of cattle; the latter factor likely to have been significant in the restocking that followed the 2001 foot-and-mouth disease outbreak in the UK (Gilbert et al., 2005; Carrique-Mas, et al., 2008; Johnston et al., 2011).
Improved understanding of the local, behavioural interactions underlying potential ‘transmission events’ will be essential if we are to better appreciate the nature of, and ultimately break or at least manage, these transmission networks. In this context biotelemetry is proving helpful in using proximity data-logging devices to tease-out the complexities of cattle-badger interactions (White et al., 2008; Böhm et al., 2009). Such an approach has flagged individuals in both livestock and wildlife populations with high contact rates, which could act as ‘hubs’ in the spread of disease. See: http://archive.defra.gov.uk/foodfarm/farmanimal/diseases/atoz/tb/documents/btbsurv-report.pdf (accessed 4 August 2011). 2
Biotelemetry is also likely to be useful in supporting or refuting the assumption that the transmission rate of M. bovis infection is positively and linearly related to the density of infectious and susceptible animals. This assumption has been central to the management of bTB in cattle and badgers in the UK to date, drawing on the principle of disease transmission by ‘mass action’, where a reduction in the density of either infectious or susceptible hosts will lead to reduced transmission (White et al., 2008; Böhm et al., 2009). If inter-species interactions at farm level can be identified, this increases the possibility of designing targeted control measures based around high-risk individuals and sub-groups within populations.
The relative importance of disease risk factors is likely to vary between regions given differing domestic and wildlife animal densities, farming practices, and geographical terrain. Bespoke, flexible disease management that reflects local risk, is more likely to be successful in addressing a highly complex, chronic, multispecies disease such as bTB than a ‘one-size-fits-all’ mass control programme. However, such tailored disease control is often difficult to implement within the constraints of statutory regulation.
The eradication of bTB in the UK remains a very challenging, expensive and controversial problem, made all the more intractable by the multitude of factors contributing to its persistence and spread. State veterinarians and other policy makers are in an unenviable position attempting to ‘do the right thing’ based on sometimes conflicting scientific evidence, while at the same time, navigating their way through this often emotionally charged and politically sensitive landscape. Furthermore, the
effects of interventions on the course of chronic diseases such as bTB are typically only seen over the long-term. Careful ongoing surveillance as reported by Bailey et al. (2013) and Brougham et al. (2013a,b), taken together with the epidemiological modelling of cattle movements, the use of biotelemetry to analyse inter-species interactions, and the molecular typing of M. bovis isolates all provide a sound foundation on which to implement and adapt future control strategies. J.P. Cassidy Scientific Editor The Veterinary Journal Pathobiology Section School of Veterinary Medicine University College Dublin Belfield Dublin 4, Ireland E-mail address: [email protected] References
Amanfu, W., 2006. The situation of tuberculosis and tuberculosis control in animals of economic interest. Tuberculosis 86, 330-355. Bailey, S.S., Crawshaw, T.R., Smith, N.H., Palgrave, C.J., 2013. Mycobacterium bovis infection in domestic pigs in Great Britain. The Veterinary Journal, DOI to be inserted Böhm, M. Hutchings, M.R., White, P.C.L., 2009. Dynamic interactions among badgers: Implications for sociality and disease transmission. PLoS One, 4, e5016. Broughan, J.M, Downs, S.H., Crawshaw, T.R., Upton, P.A., Brewer, J., CliftonHadley, R.S., 2013a. Mycobacterium bovis infections in domesticated non-bovine mammalian species. Part 1: Review of epidemiology and laboratory submissions in Great Britain 2004 – 2010. The Veterinary Journal, DOI to be inserted Broughan, J.M, Downs, S.H., Crawshaw, T.R., Upton, P.A., Brewer, J., CliftonHadley, R.S., 2013b. Mycobacterium bovis infections in domesticated non-bovine mammalian species. Part 2: A review of diagnostic methods. The Veterinary Journal, DOI to be inserted Carrique-Mas, J.J., Medley, G.F., Green, L.E., 2008. Risks for bovine tuberculosis in British cattle farms restocked after the foot and mouth disease epidemic of 2001. Preventive Veterinary Medicine, 84, 85–93.
Gilbert, M. Mitchell, A., Bourn, D., Mawdsley, J., Clifton-Hadley, R.S., Wint, W., 2005. Cattle movements and bovine tuberculosis in Great Britain. Nature 435, 491– 496. Johnston, W.T., Vial, F., Gettinby, G., Bourne, F.J., Clifton-Hadley, R.S., Cox, D.R., Crea, P., Donnelly, C.A., McInerney, J.P., Mitchell, A.P. et al., 2011. Herd-level risk factors of bovine tuberculosis in England and Wales after the 2001 foot-and-mouth disease epidemic. International Journal of Infectious Diseases 15, 833-840. O'Reilly, L.M., Daborn, C.J., 1995. The Epidemiology of Mycobacterium bovis infections in animals and man - a review. Tubercle and Lung Disease 76, 1-46. Smith, N.H., Dale, J., Inwald, J., Palmer, S., Gordon, S.V., Hewinson, R.G., Smith, J.M., 2003. The population structure of Mycobacterium bovis in Great Britain: Clonal expansion. Proceedings of the Natural Academy of Sciences of the USA, 100, 15271– 15275. White, P.C.L., Bohm, M., Marion, G., Hutchings, M.R., 2008. Control of bovine tuberculosis in British livestock: There is no ‘silver bullet’. Trends in Microbiology, 16, 420-427.