Brucella spp.; Ecuador; cattle; competitive ELISA (c-ELISA); risk factors; serological survey; Brucellaspp; Immunology and Allergy; Molecular Biology; Immunology and Microbiology (all); Microbiology (medical); Infectious Diseases; General Immunology and Microbiology
Abstract :
[en] Bovine brucellosis is a worldwide zoonotic contagious disease. According to World Animal Health Information System reports Ecuador has presented an increasing number of bovine brucellosis outbreaks in the continental territory over the past years (756 in 2018 versus 964 in 2021), generating economic losses for producers and causing a risk to public health. A cross-sectional study was conducted to investigate the seroprevalence of bovine brucellosis and associated risk or protective factors between May and June 2018. This stratified random study was implemented in 290 cattle herds located in the 23 provinces of continental Ecuador, which represents a total of 3737 cows aged 24 months or older. A competitive ELISA was used to detect Brucella antibodies. Simultaneously, an epidemiological survey was implemented to assess the brucellosis risk or protective factors. The apparent prevalence of bovine brucellosis at the herd level was 21.3% (95% CI: 16.8-26.6) and 6.2% (95% CI: 5.5-7) at the animal level. Univariate and multivariate logistic regression analyses were performed to determine the relationship between the potential factors associated with the presence of bovine brucellosis. The risk factors identified after multivariate analysis were a surface in ha per herd > 70 ha (OR = 2.73; 95% CI: 1.18-6.32) and the number of parturitions per animal (two or more with OR ≥ 1.8 and p-value ≤ 0.047). On the contrary, the protective factors were the region (farms located in the eastern region) and the absence of reported clinical signs. In addition, in herds where extensive production predominates, farmers have a low level of knowledge, and the farm biosecurity level is low. These results can guide the authorities in managing the risk factors identified, understanding the current epidemiological situation in Ecuador, improving the bovine brucellosis control program and food safety, as well as increase the one-health approach.
Disciplines :
Veterinary medicine & animal health
Author, co-author :
Garrido-Haro, Ana; Agencia de Regulación y Control Fito y Zoosanitario-AGROCALIDAD, Quito 170184, Ecuador ; Research Unit of Epidemiology and Risk Analysis Applied to Veterinary Science (UREAR-ULg), Fundamental and Applied Research for Animals & Health (FARAH) Center, Faculty of Veterinary Medicine, University of Liège, 4000 Liege, Belgium
Barrionuevo-Samaniego, Margoth; Agencia de Regulación y Control Fito y Zoosanitario-AGROCALIDAD, Quito 170184, Ecuador
Moreno-Caballeros, Paola; Agencia de Regulación y Control Fito y Zoosanitario-AGROCALIDAD, Quito 170184, Ecuador
Burbano-Enriquez, Alexandra; Agencia de Regulación y Control Fito y Zoosanitario-AGROCALIDAD, Quito 170184, Ecuador
Sánchez-Vázquez, Manuel J; Pan American Health Organization (PAHO), Pan American Center for Foot and Mouth Disease and Veterinary Public Health (PANAFTOSA), Rio de Janeiro 25020-000, Brazil
Pompei, Julio; Pan American Health Organization (PAHO), Pan American Center for Foot and Mouth Disease and Veterinary Public Health (PANAFTOSA), Rio de Janeiro 25020-000, Brazil
Humblet, Marie-France ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires (DMI)
Ron-Román, Jorge; Grupo de Investigación en Sanidad Animal y Humana (GISAH), Carrera Ingeniería Agropecuaria, Departamento de Ciencias de la Vida y la Agricultura, Universidad de las Fuerzas Armadas ESPE, Sangolquí 171103, Ecuador
Saegerman, Claude ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires (DMI) > Epidémiologie et analyse des risques appliqués aux sciences vétérinaires
Language :
English
Title :
Seroprevalence and Risk Factors Related to Bovine Brucellosis in Continental Ecuador.
Publication date :
05 September 2023
Journal title :
Pathogens
ISSN :
2076-0817
eISSN :
2076-0817
Publisher :
Multidisciplinary Digital Publishing Institute (MDPI), Switzerland
AGROCALIDAD - Agencia de Regulación y Control Fito y Zoosanitario [EC] ARES - Academy for Research and Higher Education [BE]
Funding text :
Our thanks to the Agencia de Regulación y Control Fito y Zoosanitario (AGROCALIDAD), the Ministry of Agriculture and Livestock of Ecuador (MAG), the Panamerican Center for Foot-and-Mouth Disease (PANAFTOSA) and the Belgian Development Cooperation (DGD), within the framework of the Institutional Collaboration in the Brucellosis and Trypanosomosis (Bru-Tryp) Project. Also, our thanks to the laboratory technicians, to the technicians who carried out the sampling at the national level, and to the AGROCALIDAD authorities who support the progress of Ecuador. Finally, this work would not have been possible without the help of the farmers, who collaborated and participated in this study for the benefit of the country and to whom we are grateful for their time and trust.This work was supported by the Agencia de Regulación y Control Fito y Zoosanitario (AGROCALIDAD), the National Brucellosis Program, the Ministry of Agriculture and Livestock of Ecuador (MAG), the Panamerican Centre for Foot-and-Mouth Disease (PANAFTOSA), and the Academy of Research and Higher Education (ARES, Belgium; https://www.ares-ac.be/en/cooperation-au-developpement ; accessed on 1 September 2023) through the Research for Development Project entitled “Establishment of a Platform to support training and awareness, diagnosis and development of a control strategy for brucellosis and trypanosomiasis in Ecuador” (acronym: BruTryp).
OIE Capítulo 3.1.4. Brucelosis (Infección por B. abortus, B. melitensis y B. suis) Available online: https://www.oie.int/es/enfermedad/brucelosis/ (accessed on 5 November 2022)
Khurana S.K. Sehrawat A. Tiwari R. Prasad M. Gulati B. Shabbir M.Z. Chhabra R. Karthik K. Patel S.K. Pathak M. et al. Bovine Brucellosis—A Comprehensive Review Vet. Q. 2021 41 61 88 10.1080/01652176.2020.1868616 33353489
Godfroid J. Al Dahouk S. Pappas G. Roth F. Matope G. Muma J. Marcotty T. Pfeiffer D. Skjerve E. A “One Health” Surveillance and Control of Brucellosis in Developing Countries: Moving Away from Improvisation Comp. Immunol. Microbiol. Infect. Dis. 2013 36 241 248 10.1016/j.cimid.2012.09.001 23044181
Pappas G. Akritidis N. Bosilkovski M. Tsianos E. Brucellosis N. Engl. J. Med. 2005 352 2325 2336 10.1056/NEJMra050570 15930423
Ragan V. Vroegindewey G. Babcock S. International Standards for Brucellosis Prevention and Management Rev. Sci. Tech. 2013 32 189 198 10.20506/rst.32.1.2203
De Figueiredo P. Ficht T.A. Rice-Ficht A. Rossetti C.A. Adams L.G. Pathogenesis and Immunobiology of Brucellosis: Review of Brucella–Host Interactions Am. J. Pathol. 2015 185 1505 1517 10.1016/j.ajpath.2015.03.003
Guerrier G. Daronat J.M. Morisse L. Yvon J.F. Pappas G. Epidemiological and Clinical Aspects of Human Brucella suis Infection in Polynesia Epidemiol. Infect. 2011 139 1621 1625 10.1017/S0950268811001075
Mia M.M. Hasan M. Pory F.S. Occupational Exposure to Livestock and Risk of Tuberculosis and Brucellosis: A Systematic Review and Meta-Analysis One Health 2022 15 100432 10.1016/j.onehlt.2022.100432
Lucero N.E. Ayala S.M. Escobar G.I. Jacob N.R. Brucella Isolated in Humans and Animals in Latin America from 1968 to 2006 Epidemiol Infect 2008 136 496 503 10.1017/S0950268807008795
Dadar M. Tiwari R. Sharun K. Dhama K. Importance of Brucellosis Control Programs of Livestock on the Improvement of One Health Vet. Q. 2021 41 137 151 10.1080/01652176.2021.1894501
Herrera E. Palomares G. Díaz-Aparicio E. Milk Production Increase in a Dairy Farm under a Six-Year Brucellosis Control Program Ann. N. Y. Acad. Sci. 2008 1149 296 299 10.1196/annals.1428.011
Ministerio de Asuntos Exteriores Unión Europea y Cooperación, F Ministerio de Relaciones Exteriores, Indicadores Sociales-Ecuador Available online: https://www.exteriores.gob.es/Documents/FichasPais/Ecuador_FICHA%20PAIS.pdf (accessed on 5 November 2022)
AGROCALIDAD Programa Nacional de Control de Brucelosis y Tuberculosis Bovina Available online: https://www.agrocalidad.gob.ec/39835/ (accessed on 11 January 2022)
AGROCALIDAD Resolucion-0131.Pdf Available online: https://www.agrocalidad.gob.ec/wp-content/uploads/2020/05/resolucion-0131.pdf (accessed on 21 December 2021)
Ministerio de Agricultura y Ganadería Agricultura, La Base de La Economía y La Alimentación–Ministerio de Agricultura y Ganadería Available online: https://www.agricultura.gob.ec/agricultura-la-base-de-la-economia-y-la-alimentacion/ (accessed on 9 February 2023)
AGROCALIDAD Fiebre Aftosa 4.6 Millones Cabezas de Ganado Bovino Recibirán Vacuna Available online: https://www.agrocalidad.gob.ec/fiebre-aftosa-46-millones-cabezas-de-ganado-bovino-recibiran-vacuna/ (accessed on 30 January 2023)
Paredes A. Estudio Epidemiológico y Económico de La Brucelosis En Bovinos de La Parroquia San Pedro de Suma Del Cantón El Carmen de La Provincia de Manabí–Ecuador. Tesis previa a la obtención del Título de Ingeniero Agropecuario., Universidad de las Fuerzas Armadas: Hacienda el Prado Selva Alegre, Sangolquí, Ecuador 2021 Available online: http://repositorio.espe.edu.ec/handle/21000/27345 (accessed on 1 August 2023)
PNSA MAG Programa Nacional de Sanidad Animal del Ministerio de Agricultura y Ganadería Prevalencia de Brucelosis Ministerio de Agricultura y Ganadería Quito, Ecuador 1979
Poulsen K.P. Hutchins F.T. McNulty C.M. Tremblay M. Zabala C. Barragan V. Lopez L. Trueba G. Bethel J.W. Brucellosis in Dairy Cattle and Goats in Northern Ecuador Am. J. Trop. Med. Hyg. 2014 90 712 715 10.4269/ajtmh.13-0362
Carbonero A. Guzmán L.T. García-Bocanegra I. Borge C. Adaszek L. Arenas A. Saa L.R. Seroprevalence and Risk Factors Associated with Brucella Seropositivity in Dairy and Mixed Cattle Herds from Ecuador Trop. Anim. Health Prod. 2018 50 197 203 10.1007/s11250-017-1421-6
Paucar V. Ron-Román J. Benítez-Ortiz W. Celi M. Berkvens D. Saegerman C. Ron-Garrido L. Bayesian Estimation of the Prevalence and Test Characteristics (Sensitivity and Specificity) of Two Serological Tests (RB and SAT-EDTA) for the Diagnosis of Bovine Brucellosis in Small and Medium Cattle Holders in Ecuador Microorganisms 2021 9 1815 10.3390/microorganisms9091815 34576711
Ron-Román J. Ron-Garrido L. Abatih E. Celi-Erazo M. Vizcaíno-Ordóñez L. Calva-Pacheco J. González-Andrade P. Berkvens D. Benítez-Ortíz W. Brandt J. et al. Human Brucellosis in Northwest Ecuador: Typifying Brucella spp., Seroprevalence, and Associated Risk Factors Vector Borne Zoonotic Dis. 2014 14 124 133 10.1089/vbz.2012.1191 24410144
Ron-Román J. Saegerman C. Minda-Aluisa E. Benítez-Ortíz W. Brandt J. Douce R. First Report of Orchitis in Man Caused by Brucella abortus Biovar 1 in Ecuador Am. J. Trop. Med. Hyg. 2012 87 524 528 10.4269/ajtmh.2012.11-0341 22826490
Subsecretaria Nacional de Vigilancia de la Salud Pública Enfermedades Zoonóticas-A239 Brucelosis Ecuador, SE01-24 2020 Available online: https://www.salud.gob.ec/wp-content/uploads/2020/06/BRUSELOSIS-Y-LEPTOSPIRA-SE-24_2020.pdf (accessed on 1 August 2023)
Ron-Roman J. Epidemiological Study of Bovine brucellosis and Its Impact en Santé Publique Dans le Nord-Ouest de l’Equateur Ph.D. Thesis Université de Liège–Faculté de Médecine Vétérinaire Liege, Belgium 2016 ISBN 978-2-87543-095-3
R Foundation for Statistical Computing, R.C. R: A Language and Environment for Statistical Computing R Foundation for Statistical Computing Vienna, Austria 2022
SVANOVIR SVANOVIR Brucella-AB c-ELISA Available online: https://shop.indical.com/en/svanovir-brucella-ab-c-elisa.html (accessed on 10 December 2022)
Martinez B.A.F. Leotti V.B. de Silva G.S.E. Nunes L.N. Machado G. Corbellini L.G. Odds Ratio or Prevalence Ratio? An Overview of Reported Statistical Methods and Appropriateness of Interpretations in Cross-Sectional Studies with Dichotomous Outcomes in Veterinary Medicine Front. Vet. Sci. 2017 4 193 10.3389/fvets.2017.00193
Szumilas M. Explaining Odds Ratios J. Can. Acad. Child. Adolesc. Psychiatry 2010 19 227 229
Vandenbroucke J.P. von Elm E. Altman D.G. Gøtzsche P.C. Mulrow C.D. Pocock S.J. Poole C. Schlesselman J.J. Egger M. STROBE Initiative Strengthening the Reporting of Observational Studies in Epidemiology (STROBE): Explanation and Elaboration Int. J. Surg. 2014 12 1500 1524 10.1016/j.ijsu.2014.07.014
Renault V. Damiaans B. Humblet M.-F. Jiménez Ruiz S. García Bocanegra I. Brennan M.L. Casal J. Petit E. Pieper L. Simoneit C. et al. Cattle Farmers’ Perception of Biosecurity Measures and the Main Predictors of Behaviour Change: The First European-Wide Pilot Study Transbound. Emerg. Dis. 2020 68 3305 3319 10.1111/tbed.13935
Watson P. Petrie A. Statistics for Veterinary and Animal Science 3rd ed. Wiley-Blackwell Oxford, UK 2014 414
El Agrebi N. Steinhauer N. Tosi S. Leinartz L. de Graaf D.C. Saegerman C. Risk and Protective Indicators of Beekeeping Management Practices Sci. Total Environ. 2021 799 149381 10.1016/j.scitotenv.2021.149381
Sutton T. Dassau Sistema de Información Geográfica QGIS Available online: https://www.qgis.org/en/site/forusers/download.html (accessed on 5 January 2023)
Eras R. Lalangui M. The Agricultural Sector in Ecuador: Descriptive Analysis of the Impact on Sustainability by COVID-19 South Fla. J. Dev. 2021 2 4105 4122 10.46932/sfjdv2n3-024
Sanchez A. Vayas T. Mayorga F. Freire C. Sector Ganadero Available online: https://fca.uta.edu.ec/v4.0/images/OBSERVATORIO/dipticos/Diptico_N20.pdf (accessed on 5 November 2022)
Parra V. Tipanluisa D. Prevalencia de Brucelosis en ganado bovino en la Parróquia de San Pedro de Suma Cantón El Carmen Tesis previa a la obtención del Título de Ingeniero Agropecuario Universidad de las Fuerzas Armadas Latacunga, Ecuador 2018
AGROCALIDAD AGROCALIDAD–Fiebre Aftosa Available online: https://www.agrocalidad.gob.ec/FiebreAftosa/ (accessed on 30 January 2023)
Asamblea Nacional de Ecuador Ley Orgánica de Sanidad Agropecuaria Available online: https://www.gob.ec/sites/default/files/regulations/2018-09/Documento_Ley%20Org%C3%A1nica%20de%20Sanidad%20Agropecuaria.pdf (accessed on 1 August 2023)
Rodríguez-Hidalgo R.I. Contreras-Zamora J. Benitez Ortiz W. Guerrero-Viracocha K. Salcan-Guaman H. Minda E. Ron Garrido L. Circulating Strains of Brucella abortus in Cattle in Santo Domingo De Los Tsáchilas Province–Ecuador Front Public Health 2015 3 45 10.3389/fpubh.2015.00045
Zambrano Aguayo M.D. Pérez Ruano M. Seroprevalencia de Brucelosis En Ganado Bovino y En Humanos Vinculados a La Ganadería Bovina En Las Zonas Norte y Centro de La Provincia Manabí, Ecuador Rev. De Salud Anim. 2015 37 164 172
Herrán Ramirez O.L. Azevedo Santos H. Jaramillo Delgado I.L. da Costa Angelo I. Seroepidemiology of Bovine Brucellosis in Colombia’s Preeminent Dairy Region, and Its Potential Public Health Impact Braz. J. Microbiol. 2020 51 2133 2143 10.1007/s42770-020-00377-z 32918242
McDermott J.J. Arimi S.M. Brucellosis in Sub-Saharan Africa: Epidemiology, Control and Impact Vet. Microbiol. 2002 90 111 134 10.1016/S0378-1135(02)00249-3 12414138
Saegerman C. De Waele L. Gilson D. Godfroid J. Thiange P. Michel P. Limbourg B. Vo T.K.-O. Limet J. Letesson J.-J. et al. Evaluation of Three Serum I-ELISAs Using Monoclonal Antibodies and Protein G as Peroxidase Conjugate for the Diagnosis of Bovine Brucellosis Vet. Microbiol. 2004 100 91 105 10.1016/j.vetmic.2004.02.003 15135517
Chacón-Díaz C. Zabalza-Baranguá A. San Román B. Blasco J.-M. Iriarte M. Salas-Alfaro D. Hernández-Mora G. Barquero-Calvo E. Guzmán-Verri C. Chaves-Olarte E. et al. Brucella abortus S19 GFP-Tagged Vaccine Allows the Serological Identification of Vaccinated Cattle PLoS ONE 2021 16 e0260288 10.1371/journal.pone.0260288 34807952
Godfroid J. Nielsen K. Saegerman C. Diagnosis of Brucellosis in Livestock and Wildlife Croat. Med. J. 2010 51 296 305 10.3325/cmj.2010.51.296
Uzal F.A. Carrasco A.E. Nielsen K.H. Evaluation of a Competitive ELISA for the Diagnosis of Bovine Brucellosis Vet. Res. Commun. 1996 20 421 426 10.1007/BF00419179
Vinueza R.L. Durand B. Zanella G. Network Analysis of Cattle Movements in Ecuador Prev. Vet. Med. 2022 201 105608 10.1016/j.prevetmed.2022.105608
Davidson R.M. Control and Eradication of Animal Diseases in New Zealand N. Z. Vet. J. 2002 50 6 12 10.1080/00480169.2002.36259
Godfroid J. Käsbohrer A. Brucellosis in the European Union and Norway at the Turn of the Twenty-First Century Vet. Microbiol. 2002 90 135 145 10.1016/S0378-1135(02)00217-1
Camus E. Incidence clinique de la brucellose bovine dans le Nord de la Côte d’Ivoire Rev. Elev. Méd. Vét. Pays Trop. 1980 33 263 269
Sanogo M. Abatih E. Thys E. Fretin D. Berkvens D. Saegerman C. Risk Factors Associated with Brucellosis Seropositivity among Cattle in the Central Savannah-Forest Area of Ivory Coast Prev. Vet. Med. 2012 107 51 56 10.1016/j.prevetmed.2012.05.010 22704904
Awah-Ndukum J. Mouiche M.M.M. Bayang H.N. Ngwa V.N. Assana E. Feussom K.J.M. Manchang T.K. Zoli P.A. Seroprevalence and Associated Risk Factors of Brucellosis among Indigenous Cattle in the Adamawa and North Regions of Cameroon Vet. Med. Int. 2018 2018 e3468596 10.1155/2018/3468596 29535853
Martinez D.E. Cipolini M.F. Storani C.A. Russo A.M. Martinez E.I. Brucelosis: Prevalencia y Factores de Riesgo Asociados En Bovinos, Bubalinos, Caprinos y Ovinos de Formosa, Argentina Rev. Vet. 2018 29 40 44 10.30972/vet.2912789
Boukary A. Saegerman C. Rigouts L. Matthys F. Berkvens D. Thys E. Preliminary Results of the Study on Zoonotic Brucellosis and Tuberculosis in Niamey Globalization of Tropical Animal Diseases and Public Health Concerns; Proceedings of the 13th AITVM 2010 International Conference, Bangkok, Thailand, 23–26 August 2010 Chulalongkorn University Utrecht, The Netherlands Association of Institutions for Tropical Veterinary Medicine (AITVM) Bangkok, Thailand 2010 22 24 978-616-551-154-4
Saegerman C. Berkvens D. Godfroid J. Walravens K. Chapter 77: Bovine brucellosis Infectious and Parasitic Disease of Livestock Lavoisier et Commonwealth Agricultural Bureau–International Paris, France 2010 991 1011
Lopes L.B. Nicolino R. Haddad J.P. Brucellosis-Risk Factors and Prevalence: A Review Open Vet. Sci. J. 2010 4 72 84 10.2174/1874318801004010072
Omer M.K. Assefaw T. Skjerve E. Tekleghiorghis T. Woldehiwet Z. Prevalence of Antibodies to Brucella spp. and Risk Factors Related to High-Risk Occupational Groups in Eritrea Epidemiol. Infect. 2002 129 85 91 10.1017/S0950268802007215
Ndazigaruye G. Mushonga B. Kandiwa E. Samkange A. Segwagwe B.E. Prevalence and Risk Factors for Brucellosis Seropositivity in Cattle in Nyagatare District, Eastern Province, Rwanda J. South Afr. Vet. Assoc. 2018 89 a1625 10.4102/jsava.v89i0.1625
Chand P. Chhabra R. Herd and Individual Animal Prevalence of Bovine Brucellosis with Associated Risk Factors on Dairy Farms in Haryana and Punjab in India Trop. Anim. Health Prod. 2013 45 1313 1319 10.1007/s11250-013-0362-y 23354992
Boukary A.R. Saegerman C. Abatih E. Fretin D. Alambédji Bada R. De Deken R. Harouna H.A. Yenikoye A. Thys E. Seroprevalence and Potential Risk Factors for Brucella spp. Infection in Traditional Cattle, Sheep and Goats Reared in Urban, Periurban and Rural Areas of Niger PLoS ONE 2013 8 e83175 10.1371/journal.pone.0083175 24358261
Miyashiro S. Scarcelli E. Piatti R.M. Campos F.R. Vialta A. Keid L.B. Dias R.A. Genovez M.E. Detection of Brucella abortus DNA in Illegal Cheese from São Paulo and Minas Gerais and Differentiation of B19 Vaccinal Strain by Means of the Polymerase Chain Reaction (PCR) Braz. J. Microbiol. 2007 38 17 22 10.1590/S1517-83822007000100005
Singh J. Murray R.D. Mshelia G. Woldehiwet Z. The immune status of the bovine uterus during the peripartum period Vet. J. 2008 175 301 309 10.1016/j.tvjl.2007.02.003 17400489
Pacheco W.A. Genovez M.E. Pozzi C.R. Silva L.M.P. Azevedo S.S. Did C.C. Piatti R.M. Pinheiro E.S. Castro V. Miyashiro S. et al. Excretion of Brucella abortus Vaccine B19 Strain during a Reproductive Cycle in Dairy Cows Braz. J. Microbiol. 2012 43 594 601 10.1590/S1517-83822012000200022
Schelling E. Diguimbaye C. Daoud S. Nicolet J. Boerlin P. Tanner M. Zinsstag J. Brucellosis and Q-Fever Seroprevalences of Nomadic Pastoralists and Their Livestock in Chad Prev. Vet. Med. 2003 61 279 293 10.1016/j.prevetmed.2003.08.004
Coelho A.C. Díez J.G. Coelho A.M. Risk Factors for Brucella spp. in Domestic and Wild Animals IntechOpen London, UK 2015 978-953-51-2211-1
Cárdenas L. Peña M. Melo O. Casal J. Risk Factors for New Bovine Brucellosis Infections in Colombian Herds BMC Vet. Res. 2019 15 81 10.1186/s12917-019-1825-9
Acha P.N. Szyfres B. Organizaciónn Panamericana de la Salud Organitzación Mundial de la Salud Zoonosis y Enfermedades Transmisibles Comunes al Hombre y a Los Animales Organizaciónn Mundial de la Salud Washington, DC, USA 2001 978-92-75-31991-8
Givens M.D. Review: Risks of Disease Transmission through Semen in Cattle Animal 2018 12 s165 s171 10.1017/S1751731118000708
Adamu S.G. Atsanda N.N. Tijjani A.O. Usur A.M. Sule A.G. Gulani I.A. Epidemiological study of bovine brucellosis in three senatorial zones of Bauchi State, Nigeria Veter. World 2016 9 48 52 10.14202/vetworld.2016.48-52
Lukambagire A.S. Mendes Â.J. Bodenham R.F. McGiven J.A. Mkenda N.A. Mathew C. Rubach M.P. Sakasaka P. Shayo D.D. Maro V.P. et al. Performance characteristics and costs of serological tests for brucellosis in a pastoralist community of northern Tanzania Sci. Rep. 2021 11 5480 10.1038/s41598-021-82906-w
