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Tuberculosis (Mycobacterium microti) in wild field vole populations

Published online by Cambridge University Press:  16 November 2007

S. BURTHE ,
M. BENNETT ,
A. KIPAR ,
X. LAMBIN ,
A. SMITH ,
S. TELFER  and
M. BEGON
S. BURTHE
Affiliation:
School of Biological Sciences, University of Liverpool, Crown Street, Liverpool L69 7ZB National Centre for Zoonosis Research, Faculty of Veterinary Science, University of Liverpool, Leahurst, Chester High Road, Neston CH64 7TE
M. BENNETT
Affiliation:
National Centre for Zoonosis Research, Faculty of Veterinary Science, University of Liverpool, Leahurst, Chester High Road, Neston CH64 7TE
A. KIPAR
Affiliation:
National Centre for Zoonosis Research, Faculty of Veterinary Science, University of Liverpool, Leahurst, Chester High Road, Neston CH64 7TE
X. LAMBIN
Affiliation:
School of Biological Sciences, University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ
A. SMITH
Affiliation:
School of Biological Sciences, University of Liverpool, Crown Street, Liverpool L69 7ZB National Centre for Zoonosis Research, Faculty of Veterinary Science, University of Liverpool, Leahurst, Chester High Road, Neston CH64 7TE
S. TELFER
Affiliation:
School of Biological Sciences, University of Liverpool, Crown Street, Liverpool L69 7ZB National Centre for Zoonosis Research, Faculty of Veterinary Science, University of Liverpool, Leahurst, Chester High Road, Neston CH64 7TE
M. BEGON*
Affiliation:
School of Biological Sciences, University of Liverpool, Crown Street, Liverpool L69 7ZB
*
*Corresponding author: School of Biological Sciences, The University of Liverpool, Biosciences Building, Crown Street, Liverpool, L69 7ZB, UK. Tel: +44 151 795 4525. Fax: +44 151 795 4408. E-mail: mbegon@liverpool.ac.uk
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Summary

Vole tuberculosis (TB; Mycobacterium microti) is an understudied endemic infection. Despite progressing slowly, it causes severe clinical pathology and overt symptoms in its rodent host. TB was monitored for 2 years in wild field voles in Kielder Forest, UK. The prevalence of characteristic cutaneous TB lesions was monitored longitudinally at 4 sites, with individuals live-trapped and repeatedly monitored. A prevalence of 5·2% of individuals with lesions was recorded (n=2791). In a cross-sectional study, 27 sites were monitored bi-annually, with TB assessed by post-mortem examination for macroscopic lesions, and by culture and histopathology. Seventy-nine voles (10·78%; n=733) were positive for mycobacteria, with the highest prevalence in spring (13·15%; n=327). TB prevalence varied, with between 0% and 50% of voles infected per site. Prevalence increased with age (mass), and apparent seasonality was due to a higher proportion of older animals in spring. Survival analysis supported this result, with cutaneous lesions only manifesting in the advanced stages of infection, and therefore only being found on older voles. The body condition of individuals with lesions declined at the time when the lesion was first recorded, when compared to individuals without lesions, suggesting there may be an acute phase of infection during its advanced stage. Although predicted survival following the appearance of a cutaneous lesion was lower than for uninfected individuals, this was not significant.

Keywords

endemic pathogenMicrotus agrestislongitudinalTBsurvivalwildlife disease

Information

Type
Original Articles
Information
Parasitology , Volume 135 , Issue 3 , March 2008 , pp. 309 - 317
Copyright
Copyright © Cambridge University Press 2007

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References

REFERENCES

Anderson, R. M. and May, R. M. (1979). Population biology of infectious diseases: Part 1. Nature, London 280, 361–367.CrossRefGoogle Scholar
Bates, D. and Maechler, M. (2006). Matrix: a Matrix Package for R. R Package Version 0.995-5.Google Scholar
Bates, D. and Sarkar, D. (2006). lme4: Linear Mixed-Effects Models using S4 Classes. R Package Version 0.995-2.Google Scholar
Bierman, S. M., Fairbairn, J. P., Petty, S. J., Elston, D. A., Tidhar, D. and Lambin, X. (2006). Changes over time in the spatiotemporal dynamics of cyclic populations of field voles (Microtus agrestis L.). American Naturalist 167, 583–590.CrossRefGoogle ScholarPubMed
Burnham, K. P., Anderson, D. R., White, G. C., Brownie, C. and Pollock, K. H. (1987). Design and Analysis of Fish Survival Experiments Based on Release-Recapture Data. American Fisheries Society, Monograph 5. Bethesda, MD, USA.Google Scholar
Burthe, S. J., Telfer, S., Begon, M., Bennett, M., Smith, A. and Lambin, X. (2007). Cowpox virus infection in natural field vole, Microtus agrestis, populations: significant negative impacts on survival. Journal of Animal Ecology (in the Press).Google Scholar
Cavanagh, R. (2001). Interactions between population dynamics, body condition and infectious diseases (cowpox virus and Mycobacterium microti) of wild rodents. Ph.D. thesis. University of Liverpool, UK.Google Scholar
Cavanagh, R., Begon, M., Bennett, M., Ergon, T., Graham, I. M., de Haas, P. E. W., Hart, C. A., Koedam, M., Kremer, K., Lambin, X., Roholl, P. and van Soolingen, D. (2002). Mycobacterium microti infection (vole tuberculosis) in wild rodent populations. Journal of Clinical Microbiology 40, 3281–3285.CrossRefGoogle ScholarPubMed
Cavanagh, R., Lambin, X., Ergon, T., Bennett, M., Graham, I. M., van Soolingen, D. and Begon, M. (2004). Disease dynamics in cyclic populations of field voles (Microtus agrestis): cowpox virus and vole tuberculosis (Mycobacterium microti). Proceedings of the Royal Society of London, B 271, 859–867.CrossRefGoogle ScholarPubMed
Chao, A. and Lee, S. (1991). Estimating population size for continuous time capture-recapture models via sample coverage. Technical Report 91-C-01. Institute of Statistics, National Tsing Hua University, Hsin-Chu, Taiwan, Republic of China.Google Scholar
Chitty, D. (1954). Tuberculosis among wild voles: with a discussion of other pathological conditions among certain mammals and birds. Ecology 35, 227–237.CrossRefGoogle Scholar
Graham, I. M. and Lambin, X. (2002). The impact of weasel predation on cyclic field-vole survival: the specialist predator hypothesis contradicted. Journal of Animal Ecology 71, 946–956.CrossRefGoogle Scholar
Horstkotte, M. A., Sobottka, I., Schewe, C. K., Schafer, P., Laufs, R., Rusch-Gerdes, S. and Niemann, S. (2001). Mycobacterium microti llama-type infection presenting as pulmonary tuberculosis in a human immunodeficiency virus-positive patient. Journal of Clinical Microbiology 39, 406–407.CrossRefGoogle Scholar
Hurvich, C. M. and Tsai, C. L. (1989) Regression and time series model selection in small samples. Biometrika 76, 297–307.CrossRefGoogle Scholar
Kamerbeek, J., Schouls, L., Kolk, A., van Agterveld, M., van Soolingen, D., Kuijper, S., Bunschoten, A., Molhuizen, H., Shaw, R., Goyal, M. and van Emden, J. (1997). Simultaneous detection and strain differentiation of Mycobacterium tuberculosis for diagnosis and epidemiology. Journal of Clinical Microbiology 35, 907–914.CrossRefGoogle Scholar
Lambin, X., Petty, S. J. and MacKinnon, J. L. (2000). Cyclic dynamics in field vole populations and generalist predation. Journal of Animal Ecology 69, 106–118.CrossRefGoogle Scholar
Lambin, X., Elston, D. A., Petty, S. J. and MacKinnon, J. L. (1998). Spatial asynchrony and periodic travelling waves in cyclic populations of field voles. Proceedings of the Royal Society of London, B 265, 1491–1496.CrossRefGoogle Scholar
Lebreton, J. D., Burnham, K. P., Clobert, J. and Anderson, D. R. (1992). Modelling survival and testing biological hypotheses using marked animals: a unified approach with case studies. Ecological Monographs 62, 67–118.CrossRefGoogle Scholar
Magdalena, J., Vachee, A., Supply, P. and Locht, C. (1998). Identification of a new DNA region specific for members of Mycobacterium tuberculosis complex. Journal of Clinical Microbiology 36, 937–943.CrossRefGoogle ScholarPubMed
Manabe, Y. C., Scott, C. P. and Bishai, W. R. (2002). Naturally attenuated, orally administered Mycobacterium microti as a tuberculosis vaccine is better that subcutaneous Mycobacterium bovis BCG. Infection and Immunity 70, 1566–1570.CrossRefGoogle ScholarPubMed
Niemann, S., Harmsen, D., Rusch-Gerdes, S. and Richter, E. (2000). Differentiation of clinical Mycobacterium tuberculosis complex isolates by gyrB DNA sequence polymorphism analysis. Journal of Clinical Microbiology 38, 3231–3234.CrossRefGoogle ScholarPubMed
Otis, D., Burnham, K., White, G. and Anderson, D. (1978). Statistical inference from capture data on closed animal populations. Wildlife Monographs 62, 1–133.Google Scholar
Paterson, S. and Lello, J. (2003). Mixed models: getting the best use of parasitological data. Trends in Parasitology 19, 370–375.CrossRefGoogle ScholarPubMed
Sakamoto, Y., Ishiguro, M. and Kitagawa, G. (1986). Akaike Information Criterion Statistics. KTK Scientific Publishers, Tokyo.Google Scholar
van Embden, J. D. A., Cave, M. D., Crawford, J. T., Dale, J. W., Eisenach, K. D., Gicquel, B., Hermans, P., Martin, C., McAdam, R., Shinnick, T. M. and Small, P. M. (1993). Strain identification of Mycobacterium tuberculosis by DNA fingerprinting: recommendations for a standardized methodology. Journal of Clinical Microbiology 31, 406–409.CrossRefGoogle ScholarPubMed
van Soolingen, D., Hoogenboezem, T., de Haas, P. E. W., Hermans, P. W. M., Koedam, M. A., Teppema, K. S., Brennan, P. J., Besra, G. S., Portaels, F., Top, J., Schouls, L. M. and van Emden, J. D. A. (1997). A novel pathogenic taxon of the Mycobacterium tuberculosis complex, Canetti: characterization of an exceptional isolate from Africa. International Journal of Systematic Bacteriology 47, 1236–1245.CrossRefGoogle ScholarPubMed
van Soolingen, D., van der Zanden, A. G. M., de Haas, P. E. W., Noordhoek, G. T., Kiers, A., Foudraine, N. A., Portaels, F., Kolk, A. H. J., Kremer, K. and van Emden, J. D. A. (1998). Diagnosis of Mycobacterium microti infections among humans by using novel genetic markers. Journal of Clinical Microbiology 36, 1840–1845.CrossRefGoogle ScholarPubMed
Wells, A. Q. (1946). The murine type of tubercle bacillus (the vole acid-fast bacillus). Special Report Series in Medicine, Council of London 259, 1–48.Google Scholar
Wells, A. Q. and Oxon, D. M. (1937). Tuberculosis in wild voles. Lancet I, 1221.CrossRefGoogle Scholar
White, G. C. and Burnham, K. P. (1999). Program MARK: survival estimation from populations of marked animals. Bird Study 46, 120–138.CrossRefGoogle Scholar