Abstract
Bovine tuberculosis (bTB) causes significant losses to farming economies worldwide. A better understanding on the epidemiology of this disease and the role that the different hosts develop in the maintenance and spread of bTB is vital to control this zoonotic disease. This study reports the spoligotype diversity and temporal evolution of Mycobacterium tuberculosis Complex (MTBC) isolates obtained from Extremadura (southern Spain). Genotyping data of Mycobacterium bovis (n = 2102) and Mycobacterium caprae (n = 96) isolates from cattle and wildlife species, collected between 2008 and 2012, were used in this study. The isolates resulted clustered into 88 spoligotypes which varied largely in frequency and occurrence in the three hosts. The 20 most frequent patterns represented 91.99 % of the isolates, the spoligotype SB0121 being the clearly predominant and most widely dispersed geographically. The major variety of the spoligotype patterns (78 out of 88) was isolated from the cattle, in fact 50 (56.83 %) of the patterns were found only in this species. Within the spoligotypes shared between the cattle and wildlife species, 17 patterns (1747 isolates) were shared with wild boar and Iberian red deer, 10 patterns (308 isolates) were exclusively shared with wild boar, and only one pattern (two isolates) was shared exclusively with Iberian red deer. The significant number of spoligotypes shared between the three hosts (79.49 %) highlights the components of the multi-host system that allows the bTB maintenance in our study area. The greater percentage of isolates shared by the wild boar and cattle (93.50 %) supports the role of wild boar as main maintenance host for bTB in cattle. These results could be extrapolated to areas with a similar epidemiological scenario and could be helpful for other countries where wild reservoirs represent a handicap for the successful eradication of bTB from livestock.
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References
Acevedo, P., Romero, B., Vicente, J., Caracappa, S., Galluzzo, P., Marineo, S., Vicari, D., Torina, A., Casal, C., de la Fuente, J., and Gortazar, C., 2013. Tuberculosis Epidemiology in Islands: Insularity, Hosts and Trade, PLoS ONE, 8,
Aranaz, A., Liébana, E., Gomez-Mampaso, E., Galán, J.C., Cousins, D., Ortega, A., Blázquez, J., Baquero, F., Mateos, A., Súarez, G., and Domínguez, L., 1999. Mycobacterium tuberculosis subsp. caprae subsp. nov.: A taxonomic study of a new member of the Mycobacterium tuberculosis complex isolated from goats in Spain, International Journal of Systematic Bacteriology, 49, 1263--1273
Aranaz, A., Cousins, D., Mateos, A., and Domínguez, L., 2003. Elevation of Mycobacterium tuberculosis subsp. caprae Aranaz et al. 1999 to species rank as Mycobacterium caprae comb. nov., sp. nov, International Journal of Systematic and Evolutionary Microbiology, 53, 1785--1789
Corner, L.A., and Trajstman, A.C., 1988. An evaluation of 1-hexadecylpyridinium chloride as a decontaminant in the primary isolation of Mycobacterium bovis from bovine lesions, Veterinary Microbiology, 18, 127--134
Corner, L.A.L., 2006. The role of wild animal populations in the epidemiology of tuberculosis in domestic animals: How to assess the risk, Veterinary Microbiology, 112, 303--312
Cunha, M.V., Matos, F., Canto, A., Albuquerque, T., Alberto, J.R., Aranha, J.M., Vieira-Pinto, M., and Botelho, A., 2012. Implications and challenges of tuberculosis in wildlife ungulates in Portugal: A molecular epidemiology perspective, Research in Veterinary Science, 92, 225--235
de la Cruz, M.L., Perez, A., Bezos, J., Pages, E., Casal, C., Carpintero, J., Romero, B., Domínguez, L., Barker, C.M., Diaz, R., and Alvarez, J., 2014. Spatial dynamics of bovine tuberculosis in the Autonomous Community of Madrid, Spain (2010–2012), PLoS ONE, 9
Delahay, R., 2015. Control of bovine tuberculosis in New Zealand in the face of a wildlife host: a compiled review of 50 years of programme policy, design and research, New Zealand Veterinary Journal, 63, 2--3
de la Rua-Domenech, R., 2006. Human Mycobacterium bovis infection in the United Kingdom: Incidence, risks, control measures and review of the zoonotic aspects of bovine tuberculosis, Tuberculosis, 86, 77--109
de la Rua-Domenech, R., Goodchild, A.T., Vordermeier, H.M., Hewinson, R.G., Christiansen, K.H., and Clifton-Hadley, R.S., 2006. Ante mortem diagnosis of tuberculosis in cattle: A review of the tuberculin tests, interferon gamma assay and other ancillary diagnostic techniques, Research in Veterinary Science, 81, 190--210
Duarte, E.L., Domingos, M., Amado, A., and Botelho, A., 2008. Spoligotype diversity of Mycobacterium bovis and Mycobacterium caprae animal isolates, Veterinary Microbiology, 130, 415--421
García-Jiménez, W.L., Benítez-Medina, J.M., Martínez, R., Carranza, J., Cerrato, R., García-Sánchez, A., Risco, D., Moreno, J.C., Sequeda, M., Gómez, L., Fernández-Llario, P., and Hermoso-de-Mendoza, J., 2015. Non-tuberculous mycobacteria in wild boar (Sus scrofa) from southern Spain: Epidemiological, clinical and diagnostic concerns, Transboundary and Emerging Diseases, 62, 72--80
Good, M., Clegg, T.A., Duignan, A., and More, S.J., 2011. Impact of the national full herd depopulation policy on the recurrence of bovine tuberculosis in Irish herds, 2003 to 2005, Veterinary Record, 169, 581
Haddad, N., Ostyn, A., Karoui, C., Masselot, M., Thorel, M.F., Hughes, S.L., Inwald, J., Hewinson, R.G., and Durand, B., 2001. Spoligotype diversity of Mycobacterium bovis strains isolated in France from 1979 to 2000, Journal of Clinical Microbiology, 39, 3623--3632
Hermoso de Mendoza, J., Parra, A., Tato, A., Alonso, J.M., Rey, J.M., Peña, J., García-Sánchez, A., Larrasa, J., Teixidó, J., Manzano, G., Cerrato, R., Pereira, G., Fernández-Llario, P., and Hermoso de Mendoza, M., 2006. Bovine tuberculosis in wild boar (Sus scrofa), red deer (Cervus elaphus) and cattle (Bos taurus) in a Mediterranean ecosystem (1992–2004), Preventive Veterinary Medicine, 74, 239--247
Hunter, P.R., and Gaston, M.A., 1988. Numerical index of the discriminatory ability of typing systems: An application of Simpson’s index of diversity, Journal of Clinical Microbiology, 26, 2465--2466
Kamerbeek, J., Schouls, L., Kolk, A., van Agterveld, M., van Soolingen, D., Kuijper, S., Bunschoten, A., Molhuizen, H., Shaw, R., Goyal, M., and van Embden, J., 1997. Simultaneous detection and strain differentiation of Mycobacterium tuberculosis for diagnosis and epidemiology, Journal of Clinical Microbiology, 35, 907--914
Kelly, R.F., Hamman, S.M., Morgan, K.L., Nkongho, E.F., Ngwa, V.N., Tanya, V., Andu, W.N., Sander, M., Ndip, L., Handel, I.G., Mazeri, S., Muwonge, A., and Bronsvoort, B.M.D.C., 2016. Knowledge of bovine tuberculosis, cattle husbandry and dairy practices amongst pastoralists and small-scale dairy farmers in Cameroon, PLoS ONE, 11
Kremer, K., Van Soolingen, D., Frothingham, R., Haas, W.H., Hermans, P.W.M., Martín, C., Palittapongarnpim, P., Plikaytis, B.B., Riley, L.W., Yakrus, M.A., Musser, J.M., and Van Embden, J.D.A., 1999. Comparison of methods based on different molecular epidemiological markers for typing of Mycobacterium tuberculosis complex strains: Interlaboratory study of discriminatory power and reproducibility, Journal of Clinical Microbiology, 37, 2607--2618
Liébana, E., Aranaz, A., Francis, B., and Cousins, D., 1996. Assessment of genetic markers for species differentiation within the Mycobacterium tuberculosis complex, Journal of Clinical Microbiology, 34, 933--938
Ministerio de Agricultura, Alimentación y Medio Ambiente (MAGRAMA). Programa Nacional de Erradicacion de Tuberculosis Bovina presentado por España para el año 2012.(http://rasve.mapa.es/publica/programas/NORMATIVA%20Y%20PROGRAMAS%5CPROGRAMAS%5C2012%5CTUBERCULOSIS%20BOVINA%5CPROGRAMA%20TB%202012.PDF)
Naranjo, V., Gortazar, C., Vicente, J., and de la Fuente, J., 2008. Evidence of the role of European wild boar as a reservoir of Mycobacterium tuberculosis complex, Veterinary Microbiology, 127, 1--9
Parra, A., Larrasa, J., García, A., Alonso, J.M., and Hermoso de Mendoza, J., 2005. Molecular epidemiology of bovine tuberculosis in wild animals in Spain: A first approach to risk factor analysis, Veterinary Microbiology, 110, 293--300
Rodríguez, S., Bezos, J., Romero, B., de Juan, L., Álvarez, J., Castellanos, E., Moya, N., Lozano, F., Javed, M.T., Sáez-Llorente, J.L., Liébana, E., Mateos, A., Domínguez, L., and Aranaz, A., 2011. Mycobacterium caprae infection in livestock and wildlife, Spain, Emerging Infectious Disease, 17, 532--535
Rodríguez, S., Romero, B., Bezos, J., de Juan, L., Álvarez, J., Castellanos, E., Moya, N., Lozano, F., González, S., Sáez-Llorente, J., Mateos, A., Domínguez, L., and Aranaz, A., 2010. High spoligotype diversity within a Mycobacterium bovis population: Clues to understanding the demography of the pathogen in Europe, Veterinary Microbiology, 141, 89--95
Romero, B., Aranaz, A., Sandoval, A., Álvarez, J., de Juan, L., Bezos, J., Sánchez, C., Galka, M., Fernández, P., Mateos, A., and Domínguez, L., 2008. Persistence and molecular evolution of Mycobacterium bovis population from cattle and wildlife in Doñana National Park revealed by genotype variation, Veterinary Microbiology, 132, 87--95
Skuce, R.A., and Neill, S.D., 2001. Molecular epidemiology of Mycobacterium bovis: Exploiting molecular data, Tuberculosis, 81, 169--175
Smith, N.H., Gordon, S.V., de la Rua-Domenech, R., Clifton-Hadley, R.S., and Hewinson, R.G., 2006a. Bottlenecks and broomsticks: The molecular evolution of Mycobacterium bovis, Nature Reviews Microbiology, 4, 670--681
Smith, N.H., Kremer, K., Inwald, J., Dale, J., Driscoll, J.R., Gordon, S.V., Van Soolingen, D., Glyn Hewinson, R., and Maynard Smith, J., 2006b. Ecotypes of the Mycobacterium tuberculosis complex, Journal of Theoretical Biology, 239, 220--225
Vordermeier, H.M., Jones, G.J., Buddle, B.M., Hewinson, R.G., and Villarreal-Ramos, B., 2016. Bovine tuberculosis in cattle: Vaccines, DIVA tests, and host biomarker discovery, Annual Review of Animal Biosciences, 4, 87--109
Wilton, S., and Cousins, D., 1992. Detection and identification of multiple mycobacterial pathogens by DNA amplification in a single tube, PCR Methods and Applications, 1, 269--273
Acknowledgments
This study was supported by the Ministerio de Ciencia e Innovación (Gobierno de España) PS0900513 and Junta de Extremadura (PDT09A046, GRU10142 and Ref: 11N2999FD002).
W.L. García-Jiménez acknowledges the Junta de Extremadura and the European Social Fund for his research contract (PO14022).
A. Garcia acknowledges his contract TA13003 (Junta de Extremadura and the European Social Fund).
We would like to thank the Extremadura Regional Animal Health authorities that have made this study possible by submitting samples and epidemiological information.
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Waldo L. García-Jiménez and María Cortés contributed equally to this work.
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García-Jiménez, W.L., Cortés, M., Benítez-Medina, J.M. et al. Spoligotype diversity and 5-year trends of bovine tuberculosis in Extremadura, southern Spain. Trop Anim Health Prod 48, 1533–1540 (2016). https://doi.org/10.1007/s11250-016-1124-4
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DOI: https://doi.org/10.1007/s11250-016-1124-4