Bovine tuberculosis (Mycobacterium bovis) in British farmland wildlife: the importance to agriculture

Bovine tuberculosis (bTB) is an important disease of cattle and an emerging infectious disease of humans. Cow- and badger-based control strategies have failed to eradicate bTB from the British cattle herd, and the incidence is rising by about 18% per year. The annual cost to taxpayers in Britain is currently £74 million. Research has focused on the badger as a potential bTB reservoir, with little attention being paid to other mammals common on farmland. We have conducted a systematic survey of wild mammals (n=4393 individuals) present on dairy farms to explore the role of species other than badgers in the epidemiology of bTB. Cultures were prepared from 10 397 samples (primarily faeces, urine and tracheal aspirates). One of the 1307 bank voles (Clethrionomys glareolus) live-sampled, and three of the 43 badgers (Meles meles), yielded positive isolates of Mycobacterium bovis. This is the first time the bacterium has been isolated from the bank vole. The strain type was the same as that found in cattle and badgers on the same farm. However, our work indicates that the mean prevalence of infectious individuals among common farmland wildlife is extremely low (the upper 95% confidence interval is ≤2.0 for all of the abundant species). Mathematical models illustrate that it is highly unlikely the disease could be maintained at such low levels. Our results suggest that these animals are relatively unimportant as reservoirs of bTB, having insufficient within-species (or within-group) transmission to sustain the infection, though occasional spill-overs from cattle or badgers may occur.

[1]  E. Gould,et al.  Persistence and transmission of tick-borne viruses: Ixodes ricinus and louping-ill virus in red grouse populations , 1995, Parasitology.

[2]  B Grenfell,et al.  Space, persistence and dynamics of measles epidemics. , 1995, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[3]  B. Bang Tuberculosis in Cattle , 1884, The Journal of Comparative Medicine and Surgery.

[4]  B. Everitt,et al.  Statistical methods for rates and proportions , 1973 .

[5]  J. Hanzák,et al.  Mammals of Britain and Europe , 1974 .

[6]  Andrew P. Dobson,et al.  Microparasite transmission and persistence , 2002 .

[7]  S. Fitzgerald,et al.  Bovine Tuberculosis in Michigan Wildlife and Livestock , 2002, Annals of the New York Academy of Sciences.

[8]  J. Wilesmith,et al.  The occurrence of Mycobacterium bovis infection in cattle in and around an area subject to extensive badger (Meles meles) control , 1995, Epidemiology and Infection.

[9]  D. H. Williams,et al.  The impact of badger removal on the control of tuberculosis in cattle herds in Ireland. , 2005, Preventive veterinary medicine.

[10]  J. Camp Tuberculosis in animals and man : a study in comparative pathology , 1958 .

[11]  E. B. Wilson Probable Inference, the Law of Succession, and Statistical Inference , 1927 .

[12]  A. Somoskövi,et al.  Comparison of the Mycobacteria Growth Indicator Tube with MB Redox, Löwenstein-Jensen, and Middlebrook 7H11 Media for Recovery of Mycobacteria in Clinical Specimens , 1999, Journal of Clinical Microbiology.

[13]  C. Buchrieser,et al.  A new evolutionary scenario for the Mycobacterium tuberculosis complex , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[14]  P. Cichero,et al.  Use of BACTEC MGIT 960 for Recovery of Mycobacteria from Clinical Specimens: Multicenter Study , 1999, Journal of Clinical Microbiology.

[15]  Roy M. Anderson,et al.  The Population Dynamics of Microparasites and Their Invertebrate Hosts , 1981 .

[16]  R. Delahay,et al.  The status of Mycobacterium bovis infection in UK wild mammals: a review. , 2002, Veterinary journal.

[17]  C. Collins,et al.  Tuberculosis bacteriology: organization and practice. , 1997 .

[18]  J. Pollock,et al.  Pathogenesis of tuberculosis in cattle. , 2001, Tuberculosis.

[19]  G C Smith,et al.  Models of Mycobacterium bovis in wildlife and cattle. , 2001, Tuberculosis.

[20]  S. Rüsch-Gerdes,et al.  Comparison of the Mycobacteria Growth Indicator Tube (MGIT) with radiometric and solid culture for recovery of acid-fast bacilli , 1997, Journal of clinical microbiology.

[21]  S. Harris,et al.  Handbook of British Mammals , 1996 .

[22]  J. Grange Mycobacterium bovis infection in human beings. , 2001, Tuberculosis.

[23]  S. Wolfensohn,et al.  Handbook of Laboratory Animal Management and Welfare , 1994 .

[24]  O. Zuckerman Badgers, Cattle and Tuberculosis , 1980 .

[25]  M. Holdiness Mycobacterium bovis infection. , 1985, Archives of internal medicine.

[26]  Peter J. Hudson,et al.  The ecology of wildlife diseases , 2002 .

[27]  S. Wolfensohn,et al.  Use of inhalation anaesthesia for wild mammals in the field , 2002, Veterinary Record.

[28]  G. Gettinby,et al.  Impact of localized badger culling on tuberculosis incidence in British cattle , 2003, Nature.

[29]  S. Cole,et al.  Identification of variable regions in the genomes of tubercle bacilli using bacterial artificial chromosome arrays , 1999, Molecular microbiology.

[30]  A. Griffith Infections of Wild Animals with Tubercle Bacilli and other Acid-Fast Bacilli , 1939, Proceedings of the Royal Society of Medicine.

[31]  F. Baquero,et al.  Mycobacterium tuberculosis subsp. caprae subsp. nov.: a taxonomic study of a new member of the Mycobacterium tuberculosis complex isolated from goats in Spain. , 1999, International journal of systematic bacteriology.

[32]  M. Domingo,et al.  Spacer oligonucleotide typing of Mycobacterium bovis strains from cattle and other animals: a tool for studying epidemiology of tuberculosis , 1996, Journal of clinical microbiology.

[33]  C. E. Miller,et al.  Mycobacterium bovis (bovine TB) exposure as a recreational risk for hunters: results of a Michigan Hunter Survey, 2001. , 2003, The international journal of tuberculosis and lung disease : the official journal of the International Union against Tuberculosis and Lung Disease.

[34]  F. Drobniewski,et al.  Mycobacterium bovis Infection, United Kingdom , 2004, Emerging infectious diseases.

[35]  J. Álvarez,et al.  Bovine Tuberculosis (Mycobacterium bovis) in Wildlife in Spain , 2004, Journal of Clinical Microbiology.

[36]  J. Kirshner The tuberculin test. , 1960, The Journal of the Albert Einstein Medical Center, Philadelphia.

[37]  D. Young,et al.  Bovine Tuberculosis in Cattle and Badgers , 1997 .

[38]  J. Wilesmith,et al.  Mycobacterium bovis in the European badger (Meles meles): epidemiological findings in tuberculous badgers from a naturally infected population , 1993, Epidemiology and Infection.

[39]  J. Wilesmith,et al.  Bovine tuberculosis in domestic and wild mammals in an area of Dorset. I. Tuberculosis in cattle , 1982, Journal of Hygiene.

[40]  Toni Bayans Handbook of Laboratory Animal Management and Welfare, 2nd ed. , 2000 .