Bovine tuberculosis in San Luis Potosi, Mexico: spatial analysis and risk factors
DOI:
https://doi.org/10.12834/VetIt.3405.23070.2Keywords:
Cattle, Spatial distribution, Geographic Information Systems, Bayesian, M. bovisAbstract
A better understanding of the bovine tuberculosis (bTB) spatial distribution and the factors associated with increased risk is required to implement more effective control measures in Mexico. A cross-sectional study based on bTB testing on >1,600 herds in two regions of San Luis Potosi state, Altiplano and Huasteca, during 2018-2021 was conducted for the identification of spatial clustering and of bTB risk factors using the spatial scan statistic test and multivariable logistic regression models. The proportion of herds with at least one reactor was 17.9% in Altiplano and 38.6% in Huasteca, with one high risk cluster (HRC) present in each region. Larger herds (>20 animals) and those included in the HRC were exposed to a significantly increased risk of having at least one reactor in both regions. Given bTB caudal fold test limitations, herd disease freedom median posterior probability was calculated in an empirical Bayesian framework, classifying herds as “likely free” (> 94%) or “inconclusive”, the cluster and regression analysis was repeated, finding similar outcomes. Results demonstrated that certain herds are exposed to higher risk depending on their size and location in both regions, suggesting similar patterns of transmission; these findings can be used to further investigate how the disease spreads in San Luis Potosi.References
Albery, G.F., Kirkpatrick, L., Firth, J.A., Bansal, S., 2021. Unifying spatial and social network analysis in disease ecology. J. Anim. Ecol. 90, 45–61. https://doi.org/10.1111/1365-2656.13356.
Almaw, G., Conlan, A.J.K., Ameni, G., Gumi, B., Alemu, A., Guta, S., Gebre, S., Olani, A., Garoma, A., Shegu, D., Yimesgen, L., Nigussie, D., Wood, J.L.N., Abebe, T., Mihret, A., Berg, S., 2021. The variable prevalence of bovine tuberculosis among dairy herds in Central Ethiopia provides opportunities for targeted intervention. PLoS One 16. https://doi.org/10.1371/JOURNAL.PONE.0254091.
Ávila, D., Rosas, O., Tarango, L., Martínez, J., Santoyo, E., 2011. Conocimiento, uso y valor cultural de seis presas del jaguar (Panthera onca) y su relación con éste, en San Nicolas de los Montes, San Luis Potosí, Mexico. Rev. Mex. Biodivers. 82, 1020–1028.
Baptista, T.F.S., Alves, M.C., Pereira-Dourado, S.M., Costa, G.M., Lopes, E., Bruhn, F.R.P., Braz, M.S., Rocha, C.M.B.M., 2021. Spatial and temporal analyses of culls due to bovine tuberculosis in slaughterhouses of Minas Gerais state, Brazil, 2008 to 2012. Pesqui. Veterinária Bras. 41. https://doi.org/10.1590/1678-5150-PVB-6933.
Barrios-Garcia, H.B., Guizarnotegui-Blanco, J.A., Zapata-Campos, C.C., Almazan-Garcia, C., Gonzalez-Alanis, P., Villareal-Pena, R., Hernandez-Jarguin, A., Miranda-Hernandez, D.U., Martinez-Burnes, J., 2012. Identification of Mycobacterium tuberculosis complex by histopathology and PCR in white-tailed deer (Odocoileus virginianus) in Tamaulipas, Mexico. J. Anim. Vet. Adv. 11, 1036–1040. https://doi.org/10.3923/JAVAA.2012.1036.1040.
Beauvais, W., Orynbayev, M., Guitian, J., 2016. Empirical Bayes estimation of farm prevalence adjusting for multistage sampling and uncertainty in test performance: a Brucella cross-sectional serostudy in southern Kazakhstan. Epidemiol. Infect. 144, 3531–3539. https://doi.org/10.1017/S0950268816001825.
Bezos, J., Casal, C., Romero, B., Schroeder, B., Hardegger, R., Raeber, A.J., López, L., Rueda, P., Domínguez, L., 2014. Current ante-mortem techniques for diagnosis of bovine tuberculosis. Res. Vet. Sci. 97, S44–S52. https://doi.org/10.1016/j.rvsc.2014.04.002.
Broughan, J M, Judge, J., Ely, E., Delahay, R.J., Wilson, G., Clifton-Hadley, R.S., Goodchild, A. V, Bishop, H., Parry, J.E., Downs, S.H., 2016. A review of risk factors for bovine tuberculosis infection in cattle in the UK and Ireland. Epidemiol. Infect. 144, 2899–2926. https://doi.org/10.1017/S095026881600131X.
Broughan, J. M., Maye, D., Carmody, P., Brunton, L.A., Ashton, A., Wint, W., Alexander, N., Naylor, R., Ward, K., Goodchild, A. V., Hinchliffe, S., Eglin, R.D., Upton, P., Nicholson, R., Enticott, G., 2016. Farm characteristics and farmer perceptions associated with bovine tuberculosis incidents in areas of emerging endemic spread. Prev. Vet. Med. 129, 88–98. https://doi.org/10.1016/J.PREVETMED.2016.05.007.
Chenyambuga, S.W., Waiswa, C., Saimo, M., Ngumi, P., Gwakisa, P.S., 2010. Knowledge and perceptions of traditional livestock keepers on tick-borne diseases and sero-prevalence of Theileria parva around Lake Victoria Basin. Livest. Res. Rural Dev. 22.
Ciaravino, G., Laranjo-González, M., Casal, J., Sáez-Llorente, J.L., Allepuz, A., 2021. Most likely causes of infection and risk factors for tuberculosis in Spanish cattle herds. Vet. Rec. 189, no. https://doi.org/10.1002/VETR.140.
De La Cruz, M.L., Perez, A., Bezos, J., Pages, E., Casal, C., Carpintero, J., Romero, B., Dominguez, L., Barker, C.M., Diaz, R., Alvarez, J., 2014. Spatial Dynamics of Bovine Tuberculosis in the Autonomous Community of Madrid, Spain (2010–2012). PLoS One 9, e115632. https://doi.org/10.1371/JOURNAL.PONE.0115632.
Enríquez-Cruz, C., Cruz-Hernández, N.I., Zertuche-Rodríguez, J.L., Uriegas-García, J.L., Toscano-Ruiz, J.E., Flores-Gutiérrez, G.H., 2010. Epidemiology of bovine tuberculosis in Mexico, bordering the United States, at establishment of controlling strategies. Arq. Bras. Med. Vet. Zootec. 62, 1029–1035.
Gay, E., Senoussi, R., Barnouin, J., 2007. A spatial hazard model for cluster detection on continuous indicators of disease: application to somatic cell score. Vet. Res. 38, 585–596. https://doi.org/10.1051/vetres:2007018.
Gobierno Mexico, 1995. Norma Oficial Mexicana NOM-031-ZOO-1995. Campaña Nacional Contra la Tuberculosis Bovina (Mycobacterium bovis). Diario Oficial de la Federación, México.
Gomez-Buendia, A., Pozo, P., Picasso-Risso, C., Branscum, A., Perez, A., Alvarez, J., 2023. Accuracy of Tests for Diagnosis of Animal Tuberculosis: Moving Away from the Golden Calf (and towards Bayesian Models). https://doi.org/10.1155/2023/7615716.
Gutiérrez Reyes, J.A., Casanova, L.G., Torres, C.R., Gallegos, S.L.S., Alarcón, G.J.C., Pezzat, M.M., Martínez, O.P., Chávez, C.E., Suazo, F.M., 2012. Population structure of Mycobacterium bovis isolates from cattle in Mexico. Prev. Vet. Med. 106, 1–8. https://doi.org/10.1016/J.PREVETMED.2012.05.008.
Humblet, M.F., Boschiroli, M.L., Saegerman, C., 2009. Classification of worldwide bovine tuberculosis risk factors in cattle: a stratified approach. Vet. Res. 40, 1–24. https://doi.org/10.1051/VETRES/2009033.
INEGI, 2019. Encuesta Nacional Agropecuaria [WWW Document]. URL https://www.inegi.org.mx/programas/ena/2019/#Tabulados (accessed 1.10.22).
INEGI, 2007. Panorama agropecuario en México: Censo Agropecuario 2007. Aguascalientes, Mexico.
INEGI, Colegio de Posgraduados, 1998. La Ganadería Familiar en México. Aguascalientes, México.
Kara, N.K., Galic, A., 2022. Effects of herd size and bedding surfaces on milk yield and some health problems in dairy cow farms. Large Anim. Rev. 28, 11–14.
Kulldorff, M., 2018. SaTScanTM software for the spatial and space-time statistics.
LaHue, N.P., Baños, J.V., Acevedo, P., Gortázar, C., Martínez-López, B., 2016. Spatially explicit modeling of animal tuberculosis at the wildlife-livestock interface in Ciudad Real province, Spain. Prev. Vet. Med. 128, 101–111. https://doi.org/10.1016/J.PREVETMED.2016.04.011.
López-Rocha, E., Juárez-Álvarez, J., Riego-Ruiz, L., Enciso-Moreno, L., Ortega-Aguilar, F., Hernández-Nieto, J., Enciso-Moreno, J.A., López-Revilla, R., 2013. Genetic diversity of the Mycobacterium tuberculosis Complex in San Luis Potosí, México. BMC Res. Notes 6, 1–11. https://doi.org/10.1186/1756-0500-6-172/TABLES/4.
Marsot, M., Béral, M., Scoizec, A., Mathevon, Y., Durand, B., Courcoul, A., 2016. Herd-level risk factors for bovine tuberculosis in French cattle herds. Prev. Vet. Med. 131, 31–40. https://doi.org/10.1016/j.prevetmed.2016.07.006.
Medrano, C., Boadella, M., Barrios, H., Cantú, A., García, Z., Fuente, J. de la, Gortazar, C., 2012. Zoonotic Pathogens among White-Tailed Deer, Northern Mexico, 2004–2009. Emerg. Infect. Dis. 18, 1372–1374. https://doi.org/10.3201/EID1808.111902.
Mellado, M., Pérez, E., Morales, J.L., Macías-Cruz, U., Avendaño-Reyes, L., Guillén, M., García, J.E., 2021a. Risk factors associated with testing positive for tuberculosis in high-yielding Holstein cows. Trop. Anim. Health Prod. 53, 1–8. https://doi.org/10.1007/s11250-021-02599-1.
Mellado, M., Reséndiz, D., Martínez, A.M., de Santiago, M.A., Véliz, F.G., García, J.E., 2015. Milk yield and reproductive performance of Holstein cows testing positive for bovine tuberculosis. Trop. Anim. Health Prod. 47, 1061–1066. https://doi.org/10.1007/s11250-015-0828-1.
Mellado, M., Treviño, N., Véliz, F.G., Macías-Cruz, U., Avendaño-Reyes, L., De Santiago, A., García, J.E., 2021b. Effect of co-positivity for brucellosis and tuberculosis on milk yield and fertility of Holstein cows. Trop. Anim. Health Prod. 53, 0–7. https://doi.org/10.1007/s11250-021-02952-4.
Milián Suazo, F., García Casanova, L., Romero Torres, C., Cantó Alarcón, G.J., Gutiérrez Reyes, J.A., Gallegos Sosa, S., Mercado Pezzat, M., Mejía Estrada, F.F., Peña Cisneros, A.L., Estrada Chávez, C., Pizano Martínez, O., 2012. Genetic diversity and geographic distribution of Mycobacterium bovis from cattle in Mexico. Rev. Mex. Cienc. Pecu. 3, 459–471.
Miller, R.S., Sweeney, S.J., 2013. Mycobacterium bovis (bovine tuberculosis) infection in North American wildlife: current status and opportunities for mitigation of risks of further infection in wildlife populations. Epidemiol. Infect. 141, 1357–1370. https://doi.org/10.1017/S0950268813000976.
Milne, G., Graham, J., McGrath, J., Kirke, R., McMaster, W., Byrne, A.W., 2022. Investigating Farm Fragmentation as a Risk Factor for Bovine Tuberculosis in Cattle Herds: A Matched Case-Control Study from Northern Ireland. Pathogens 11. https://doi.org/10.3390/pathogens11030299.
Miranda-Aragón, L., Treviño-Garza, E.J., Jiménez-Pérez, J., Aguirre-Calderón, O.A., González-Tagle, M.A., Pompa-García, M., Aguirre-Salado, C.A., 2013. Tasa de deforestación en San Luis Potosí, México (1993-2007). Rev. Chapingo, Ser. Ciencias For. y del Ambient. 19, 201–215. https://doi.org/10.5154/r.rchscfa.2011.06.044.
Munroe, F.A., Dohoo, I.R., McNab, W.B., Spangler, L., 1999. Risk factors for the between-herd spread of Mycobacterium bovis in Canadian cattle and cervids between 1985 and 1994. Prev. Vet. Med. 41, 119–133. https://doi.org/10.1016/S0167-5877(99)00051-3.
Murad, A., Khashoggi, B. F. 2020. Using GIS for Disease Mapping and Clustering in Jeddah, Saudi Arabia. ISPRS International Journal of Geo-Information 9(5), 328. https://doi.org/10.3390/IJGI9050328.
Ord, J.K., Getis, A., 1995. Local Spatial Autocorrelation Statistics: Distributional Issues and an Application. Geogr. Anal. 27, 286–306. https://doi.org/10.1111/J.1538-4632.1995.TB00912.X.
Perea-Razo, C.A., Rodríguez-Hernández, E., Román-Ponce, S.I., Milián-Suazo, F., Robbe-Austerman, S., Stuber, T., Cantó-Alarcón, G.J., 2018. Molecular epidemiology of cattle tuberculosis in mexico through whole-genome sequencing and spoligotyping. PLoS One 13. https://doi.org/10.1371/journal.pone.0201981.
Perera Ortiz, A., Perea, C., Davalos, E., Flores Velázquez, E., Salazar González, K., Rosas Camacho, E., García Latorre, E.A., Salinas Lara, C., Muñiz Salazar, R., Bravo, D.M., Stuber, T.P., Thacker, T.C., Robbe-Austerman, S., 2021. Whole Genome Sequencing Links Mycobacterium bovis From Cattle, Cheese and Humans in Baja California, Mexico. Front. Vet. Sci. 8, 763. https://doi.org/10.3389/FVETS.2021.674307/BIBTEX.
Perez, A.M., Ward, M.P., Torres, P., Ritacco, V., 2002. Use of spatial statistics and monitoring data to identify clustering of bovine tuberculosis in Argentina. Prev. Vet. Med. 56, 63–74. https://doi.org/10.1016/S0167-5877(02)00124-1.
Porphyre, T., Stevenson, M.A., McKenzie, J., 2008. Risk factors for bovine tuberculosis in New Zealand cattle farms and their relationship with possum control strategies. Prev. Vet. Med. 86, 93–106. https://doi.org/10.1016/J.PREVETMED.2008.03.008.
Pozo, P., Vanderwaal, K., Grau, A., Luisa De La Cruz, M., Nacar, J., Bezos, | Javier, Perez, A., Minguez, O., Alvarez, J., 2019. Analysis of the cattle movement network and its association with the risk of bovine tuberculosis at the farm level in Castilla y Leon, Spain. Transbound. Emerg. Dis. 66, 327–340. https://doi.org/10.1111/TBED.13025.
QGIS Development Team, 2022. QGIS Geographic Information System.
R Studio Team, 2022. R Studio: Integrated Development Environment for R.
Redaccion El Universal, 2020. Más de medio millón de ganado bovino en SLP ha sido registrado en el Reemo | San Luis Potosí. El Univers.
Robin, X., Turck, N., Hainard, A., Tiberti, N., Lisacek, F., Sanchez, J.C., Müller, M., 2011. pROC: An open-source package for R and S+ to analyze and compare ROC curves. BMC Bioinformatics 12, 1–8. https://doi.org/10.1186/1471-2105-12-77/TABLES/3.
Rodwell, T.C., Kapasi, A.J., Moore, M., Milian-Suazo, F., Harris, B., Guerrero, L.P., Moser, K., Strathdee, S.A., Garfein, R.S., 2010. Tracing the origins of Mycobacterium bovis tuberculosis in humans in the USA to cattle in Mexico using spoligotyping. Int. J. Infect. Dis. 14. https://doi.org/10.1016/j.ijid.2009.11.037.
Rojas Martínez, C., Loza Rubio, E., Rodríguez Camarillo, S.D., Figueroa Millán, J.V., Aguilar Romero, F., Lagunes Quintanilla, R.E., Morales Álvarez, J.F., Santillán Flores, M.A., Socci Escatell, G.A., Álvarez Martínez, J.A., 2021. Background and perspectives of certain priority diseases affecting cattle farming in Mexico. Rev. Mex. Cienc. Pecu. 12, 111–148. https://doi.org/10.22319/RMCP.V12S3.5848.
SADER, SENASICA, 2021. Análisis Estratégico de Riesgos Sanitarios. Panorama Nacional de Tuberculosis Bovina. Mexico.
Sandoval-Azuara, S.E., Muñiz-Salazar, R., Perea-Jacobo, R., Robbe-Austerman, S., Perera-Ortiz, A., López-Valencia, G., Bravo, D.M., Sanchez-Flores, A., Miranda-Guzmán, D., Flores-López, C.A., Zenteno-Cuevas, R., Laniado-Laborín, R., de la Cruz, F.L., Stuber, T.P., 2017. Whole genome sequencing of Mycobacterium bovis to obtain molecular fingerprints in human and cattle isolates from Baja California, Mexico. Int. J. Infect. Dis. 63, 48–56. https://doi.org/10.1016/j.ijid.2017.07.012.
SENASICA-SAGARPA, 2015. Guía para el seguimiento epidemiológico de la tuberculosis bovina. Ciudad Mexico.
SIAP, 2023. Población ganadera Mexico [WWW Document]. Serv. Inf. Agroaliment. y Pesq. URL https://nube.siap.gob.mx/poblacion_ganadera/ (accessed 11.6.23).
SIAP, 2021. Carne en Canal de Bovino [WWW Document]. Av. Comp. por Prod. la Prod. Pecu. URL http://infosiap.siap.gob.mx/repoAvance_siap_gb/pecCompaEspProd.jsp (accessed 11.6.23).
Tembo, N.F.P., Muma, J.B., Hang’ombe, B., Munyeme, M., 2020. Clustering and spatial heterogeneity of bovine tuberculosis at the livestock/wildlife interface areas in Namwala District of Zambia. Vet. World 13, 478. https://doi.org/10.14202/VETWORLD.2020.478-488.
Torres-Gonzalez, P., Soberanis-Ramos, O., Martinez-Gamboa, A., Chavez-Mazari, B., Teresa Barrios-Herrera, M., Torres-Rojas, M., Pablo Cruz-Hervert, L., Garcia-Garcia, L., Singh, M., Gonzalez-Aguirre, A., Ponce de Leon-Garduñ, A., Sifuentes-Osornio, J., Bobadilla-del-Valle, M., 2013. Prevalence of Latent and Active Tuberculosis among Dairy Farm Workers Exposed to Cattle Infected by Mycobacterium bovis. PLoS Negl. Trop. Dis. 7, e2177. https://doi.org/10.1371/journal.pntd.0002177.
Verdugo Escárcega, D.A., Perea Razo, C.A., González Ruíz, S., Sosa Gallegos, S.L., Milián Suazo, F., Cantó Alarcón, G.J., 2020. Analysis of Bovine Tuberculosis Transmission in Jalisco, Mexico through Whole-genome Sequencing. J. Vet. Res. 64, 51. https://doi.org/10.2478/JVETRES-2020-0010.
Wolff, C., Stevenson, M., Emanuelson, U., Egenvall, A., Lindberg, A., 2011. Spatial patterns of recorded mastitis incidence and somatic cell counts in Swedish dairy cows: implications for surveillance. Geospat. Health 6, 117–123. https://doi.org/10.4081/gh.2011.163.
Zaragoza Bastida, A., Hernández Tellez, M., Bustamante Montes, L.P., Jaramillo Paniagua, J.N., Jaimes Benítes, M.E., Mendoza Barrera, G.E., Ramírez-Durán, N., 2017. Spatial analysis of bovine tuberculosis in the State of Mexico, Mexico. Vet. Ital. 53, 39–46. https://doi.org/10.12834/VetIt.47.133.5.
Zendejas Martínez, H., Milián Suazo, F., Cuador Gil, J.Q., Cruz Bello, G., Anaya Escalera, A.M., Huitrón Márquez, G., García Casanova, L., 2007. Spatial epidemiology of bovine tuberculosis in Mexico. Vet. Ital. 43, 629–34.
