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.
[en] In Ecuador, a national program for bovine brucellosis control has been in implementation since 2008. Given the costs, small- and medium-sized livestock holders are not completely committed to it. The objective of this study was to determine true prevalence (TP) of bovine brucellosis in small- and medium-sized herd populations, as well as the diagnostic sensitivity and specificity of the Rose Bengal (RB) test and the sero-agglutination test (SAT)-EDTA using a Bayesian approach. Between 2011 and 2016, 2733 cattle herds were visited, and 22,592 animal blood samples were taken in nineteen provinces on mainland Ecuador. Bayes-p and deviance information criterion (DIC) statistics were used to select models. Additionally, risk-factor analysis was used for herds according to their brucellosis test status. True prevalence (TP) in herds was estimated by pool testing. National seroprevalence of farms was 7.9% (95% CI: 6.79-9.03), and TP was 12.2% (95% CI: 7.8-17.9). Apparent prevalence (AP) in animals was 2.2% (95% CI: 1.82-2.67), and TP was 1.6% (95% CrI: 1.0-2.4). Similarly, the sensitivity of the RB was estimated at 64.6% (95% CrI: 42.6-85.3) and specificity at 98.9% (95% CrI: 98.6-99.0); for the SAT-EDTA test, sensitivity was 62.3% (95% CrI: 40.0-84.8) and 98.9% (95% CrI: 98.6-99.1) for specificity. Results of the two tests were highly correlated in infected and uninfected animals. Likewise, high spatial variation was observed, with the Coastal Region being the zone with the highest TP at 2.5%. (95% CrI: 1.3-3.8%) in individual animals and 28.2% (95% CI: 15.7-39.8) in herds. Risk factors include herd size, type of production (milk, beef, and mixed), abortions recorded, and vaccination. The results of this study serve to guide authorities to make decisions based on parallel testing at the beginning of a bovine brucellosis program for small livestock holders to increase sensitivity level of the screening tests in Ecuador.
Disciplines :
Veterinary medicine & animal health
Author, co-author :
Paucar, Valeria
Ron-Román, Jorge
Benítez-Ortiz, Washington
Celi, Maritza
Berkvens, Dirk
Saegerman, Claude ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires (DMI) > Epidémiologie et analyse des risques appl. aux sc. vétér.
Ron-Garrido, Lenin
Language :
English
Title :
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.
Publication date :
2021
Journal title :
Microorganisms
eISSN :
2076-2607
Publisher :
Molecular Diversity Preservation International (MDPI), Basel, Switzerland
Spickler, A. Brucelosis; The Center for Food Security & Public Health-Iowa State University: Ames, IA, USA, 2009; pp. 1–15.
European Court of Auditors. Programas de Erradicación, Control y Vigilancia Para Combatir las Enfermedades Animales; Informe Especial no. 06; European Court of Auditors Publications Office: Luxembourg, 2016; ISBN 978-92-872-4483-3.
Torres, H. Programa Nacional de Control de Brucelosis Bovina; Ministerio de Agricultura, Ganadería, Acuacultura y Pesca (MAGAP), Servicio Ecuatoriano de Saniadad Agropecuaria (SESA): Quito, Ecuador, 2008; pp. 3–98.
Carbonero, A.; Guzmán, L.; 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. 2017, 50, 197–203. [CrossRef]
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. [CrossRef]
PNSA; MAG. Programa Nacional de Sanidad Animal del Ministerio de Agricultura y Ganadería; PNSA; MAG: Quito, Ecuador, 1979; pp. 1–72.
Godfroid, J.; Nielsen, K.; Saegerman, C. Diagnosis of brucellosis in livestock and wildlife. Croat. Med. J. 2010, 51, 296–305. [CrossRef]
Yagupsky, P. Detection of brucellae in blood cultures. J. Clin. Microbiol. 1999, 37, 3437–3442. [CrossRef] [PubMed]
Yagupsky, P.; Morata, P.; Colmenero, J.D. Laboratory diagnosis of human brucellosis. Clin. Microbiol. Rev. 2019, 33. [CrossRef]
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. 2007, 136, 496–503. [CrossRef] [PubMed]
Sbriglio, J.L.; Sbriglio, D.H.; Sainz, B.S. Una patología generalmente subdiagnosticada en Humanos y que impacta negativamente en la producción pecuaria y desarrollo de nuestros países. Rev. Bioanálisis 2007, 5, 18–22.
OIE. Brucelosis (Brucella abortus, melitensis y suis). In Manual Terrestre de la OIE (Capítulo 2.14); OIE: Paris, France, 2016; pp. 1–44.
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. [CrossRef]
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. [CrossRef] [PubMed]
Cho, D.; Nam, H.; Kim, J.; Heo, E.; Cho, Y.S.; Hwang, I.; Kim, J.; Jung, S.; More, S.; Kim, J. Quantitative rose bengal test for diagnosis of bovine brucellosis. J. Immunoass. Immunochem. 2010, 31, 120–130. [CrossRef] [PubMed]
Teng, Y.-H.; Teng, J.-J.; Chao, S.; Chao, H.; Waghela, S.D. Comparison of the rose bengal plate and the complement fixation tests with the tube agglutination test for diagnosis of human brucellosis. Open J. Clin. Diagn. 2017, 07, 73–82. [CrossRef]
Smits, H.L.; Kadri, S.M. Brucellosis in India: A deceptive infectious disease. Indian J. Med. Res. 2005, 122, 375–384. [PubMed]
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. Bayesian evaluation of three serological tests for detecting antibodies against Brucella spp. among humans in the northwestern part of ecuador. Am. J. Trop. Med. Hyg. 2019, 100, 1312–1320. [CrossRef] [PubMed]
Cowling, D.W.; Gardner, I.A.; Johnson, W.O. Comparison of methods for estimation of individual-level prevalence based on pooled samples. Prev. Veter. Med. 1999, 39, 211–225. [CrossRef]
Gardner, I.A. The utility of Bayes’ theorem and Bayesian inference in veterinary clinical practice and research. Aust. Veter. J. 2002, 80, 758–761. [CrossRef] [PubMed]
Joseph, L.; Gyorkos, T.W.; Coupal, L. Bayesian estimation of disease prevalence and the parameters of diagnostic tests in the absence of a gold standard. Am. J. Epidemiol. 1995, 141, 263–272. [CrossRef] [PubMed]
Cárdenas, Z.L. La Brucelosis Bovina y Sus Factores de Riesgo: Evaluación a Nivel Mundial y en Colombia. Ph.D. Thesis, Universitat Autònoma de Barcelona, Barcelona, Spain, 2018.
Diallo, A.; Khounsy, S. Subscripciones. 2013, pp. 1–8. Available online: www.oie.int/boutique (accessed on 11 August 2021).
Benítez, W.; Ron-Román, J.; Enríquez, S.; Ron-Garrido, L. Proyecto, Encuesta Nacional Sobre Brucelosis, Tuberculosis y Garrapatas. Available online: http://www.uce.edu.ec/home (accessed on 11 August 2021).
Vizcaino, D.; Estrella, V.; Villareal, V. Instructivo Para los Procesos de Certicación y Recertificación de Predios Libres de Brucelosis y Tuberculosis Bovina. Gest. Manejo Control Enferm. Anim. Programa Nac. Control Brucelosis Tuberc. Bov. 2016, 34, 1–28.
Humphry, R.W.; Cameron, A.; Gunn, G.J. A practical approach to calculate sample size for herd prevalence surveys. Prev. Veter. Med. 2004, 65, 173–188. [CrossRef]
SINAVE. Manual Para la Vigilancia Epidemiológica de la Brucelosis; Secretaria de Salud, Dirección General de Epidemiología: Mexico City, Mexico, 2013; pp. 1–45.
Gardner, I.A.; Stryhn, H.; Lind, P.; Collins, M.T. Conditional dependence between tests affects the diagnosis and surveillance of animal diseases. Prev. Veter. Med. 2000, 45, 107–122. [CrossRef]
Cebul, R.D.; Hershey, J.C.; Williams, S.V. Using multiple tests: Series and parallel approaches. Clin. Lab. Med. 1982, 2, 871–890. [CrossRef]
Avalos, O. Las Pruebas Diagnósticas. Su Aplicación en los Estudios Epidemiológicos. Nefrología 2000, 5, 1–5.
León, E.A.; Duffy, S.J. Pruebas Diagnósticas: Principios y Métodos para su Evaluación e Interpretación. Temas Zoonosis 2006, 3, 4–16.
Berkvens, D.; Speybroeck, N.; Praet, N.; Adel, A.; Lesaffre, E. Estimating disease prevalence in a bayesian framework using probabilistic constraints. Epidemiology 2006, 17, 145–153. [CrossRef] [PubMed]
Branscum, A.; Gardner, I.; Johnson, W. Estimation of diagnostic-test sensitivity and specificity through Bayesian modeling. Prev. Veter. Med. 2005, 68, 145–163. [CrossRef] [PubMed]
R Foundation for Statistical Computing. A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2021.
Gall, D.; Nielsen, K. Serological diagnosis of bovine brucellosis: A review of test performance and cost comparison. Rev. Sci. Tech. l’OIE 2004, 23, 939–1002. [CrossRef]
Abernethy, D.; Menzies, F.; McCullough, S.; McDowell, S.; Burns, K.; Watt, R.; Gordon, A.; Greiner, M.; Pfeiffer, D. Field trial of six serological tests for bovine brucellosis. Veter. J. 2012, 191, 364–370. [CrossRef]
Revelle, W. Psych: Procedures for Personality and Psychological Research; Northwestern University: Evanston, IL, USA, 2020.
Cicchetti, D.V.; Feinstein, A.R. High agreement but low kappa: II. Resolving the paradoxes. J. Clin. Epidemiol. 1990, 43, 551–558. [CrossRef]
Uebersax, J. Raw Agreement Indices; SAS program for multiple binary ratings. Available online: john-uebersax.com (accessed on 11 August 2021).
Venables, W.N.; Ripley, B.D. Modern Applied Statistics with S; Springer: Berlin/Heidelberg, Germany, 2002.
Guzmán-Hernández, R.L.; Contreras-Rodríguez, A.; Ávila-Calderón, E.D.; Morales-García, M.R. Brucelosis: Zoonosis de importancia en México. Rev. Chil. Infectología 2016, 33, 656–662. [CrossRef]
Sanogo, M.; Thys, E.; Achi, Y.L.; Fretin, D.; Michel, P.; Abatih, E.; Berkvens, D.; Saegerman, C. Bayesian estimation of the true prevalence, sensitivity and specificity of the Rose Bengal and indirect ELISA tests in the diagnosis of bovine brucellosis. Veter. J. 2013, 195, 114–120. [CrossRef] [PubMed]
Gelman, A. Prior distributions for variance parameters in hierarchical models (comment on article by browne and draper). Bayesian Anal. 2006, 1, 515–534. [CrossRef]
Shi, D.; Tong, X. The impact of prior information on Bayesian latent basis growth model estimation. SAGE Open 2017, 7. [CrossRef]
Sanogo, M.; Abatih, E.; Saegerman, C. Bayesian versus frequentist methods for estimating true prevalence of disease and diagnostic test performance. Veter. J. 2014, 202, 204–207. [CrossRef] [PubMed]
Holt, H.R.; Eltholth, M.M.; Hegazy, Y.M.; El-Tras, W.F.; Tayel, A.A.; Guitian, J. Brucella spp. infection in large ruminants in an endemic area of Egypt: Cross-sectional study investigating seroprevalence, risk factors and livestock owner’s knowledge, attitudes and practices (KAPs). BMC Public Health 2011, 11, 341. [CrossRef] [PubMed]
Saegerman, C.; De Waele, L.; Gilson, D.; Godfroid, J.; Thiange, P.; Michel, P.; Limbourg, B.; Vo, T.-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. Veter. Microbiol. 2004, 100, 91–105. [CrossRef] [PubMed]
Escrig-Sos, J.; Martinez-Ramos, D.; Miralles-Tena, J.M. Pruebas diagnósticas: Nociones básicas para su correcta interpretación y uso. Cirugía Española 2006, 79, 267–273. [CrossRef]
Talavera, J.O.; Wacher-Rodarte, N.H.; Rivas-Ruiz, R. Investigación clínica II. Estudios de proceso (prueba diagnóstica). Rev. Méd. Inst. Mex. Seguro Soc. 2011, 49, 163–170.
Greiner, M.; Gardner, I. Epidemiologic issues in the validation of veterinary diagnostic tests. Prev. Veter. Med. 2000, 45, 3–22. [CrossRef]
Ponce, J. Acuerdo Ministerial No 394; Ministerio de Agricultura, Ganadería, Acuacultura y Pesca: Quito, Ecuador, 2013; pp. 1–10.
INIAP. La Ganadería de Carne En Ecuador. Publ. Misc. Dep. Econ. Agrícola Ecuad. 1975, 2, 1–28.
Cárdenas, L.; Peña, M.; Melo, O.; Casal, J. Risk factors for new bovine brucellosis infections in Colombian herds. BMC Veter. Res. 2019, 15, 81. [CrossRef]
Jaramillo, V.; Yépez, C. Determinación de Seroprevalencia de Brucelosis Bovina en la Provincia de Pastaza y Posibles Factores de Riesgo Asociados con la Enfermedad. Master’s Thesis, Universidad Central del Ecuador, Quito, Ecuador, 2013; p. 83.
Blasco, J.M. Estado Actual de la Brucelosis en España. Salud Anim. 2002, 12, 22–34.
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. [CrossRef] [PubMed]
Salguero, A. Brucelosis en Bovinos de las Provincias de Carchi, Esmeraldas e Imbabura y Análisis de Factores de Riesgo. Master’s Thesis, Universidad Central del Ecuador, Quito, Ecuador, 2014.
Calderón-Rangel, A.; Angulo-Maza, L.A.; Tique-Salleg, V.P.; Rodríguez-Rodríguez, V.C.; Ensuncho-Hoyos, C.F. Seroprevalencia de brucelosis bovina en dos localidades del Caribe colombiano. Orinoquia 2015, 19, 203. [CrossRef]
Berhe, G.; Belihu, K.; Asfaw, Y. Seroepidemiological investigation of bovine brucellosis in the extensive cattle production system of Tigray region of Ethiopia. Int. J. Appl. Res. Vet. Med. 2007, 5, 65.
Ibrahim, N.; Belihu, K.; Lobago, F.; Bekana, M. Sero-prevalence of bovine brucellosis and its risk factors in Jimma zone of Oromia Region, South-western Ethiopia. Trop. Anim. Health Prod. 2009, 42, 35–40. [CrossRef]
De Alencar Mota, A.L.A.; Ferreira, F.; Neto, J.S.F.; Dias, R.A.; Amaku, M.; Grisi-Filho, J.H.H.; Telles, E.O.; Gonçalves, V.S.P. Large-scale study of herd-level risk factors for bovine brucellosis in Brazil. Acta Trop. 2016, 164, 226–232. [CrossRef]
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. Veter. Med. Int. 2018, 2018, 3468596. [CrossRef]
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. [CrossRef]
Gerbier, G.; Garin-Bastuji, B.; Pouillot, R.; Véry, P.; Cau, C.; Berr, V.; Dufour, B.; Moutou, F. False positive serological reactions in bovine brucellosis: Evidence of the role of Yersinia enterocolitica serotype O:9 in a field trial. Veter. Res. 1997, 28, 375–383.
Kaltungo, B.Y.; Saidu, S.N.A.; Sackey, A.K.B.; Kazeem, H.M. A review on diagnostic techniques for brucellosis. Afr. J. Biotechnol. 2014, 13, 1–10. [CrossRef]
Zhou, B.; Yang, X.J.; Zhao, R.Q.; Huang, R.H.; Wang, Y.H.; Yin, C.P.; Shen, Q.; Schinckel, A.P. Effects of tail docking and teeth clipping on the physiological responses, wounds, behavior, growth, and backfat depth of pigs1. J. Anim. Sci. 2013, 91, 4908–4916. [CrossRef] [PubMed]
Ron-Román, J.; Berkvens, D.; Barzallo-Rivadeneira, D.; Angulo-Cruz, A.; González-Andrade, P.; Minda-Aluisa, E.; Benítez-Ortíz, W.; Brandt, J.; Rodríguez-Hidalgo, R.; Saegerman, C. The unexpected discovery of Brucella abortus Buck 19 vaccine in goats from Ecuador underlines the importance of biosecurity measures. Trop. Anim. Health Prod. 2017, 49, 569–574. [CrossRef]
Young, E.J. Serologic diagnosis of human brucellosis: Analysis of 214 cases by agglutination tests and review of the literature. Clin. Infect. Dis. 1991, 13, 359–372. [CrossRef]
Terán, M.; Maribel, E. Prevalencia Aparente de Brucelosis Bovina a Través de ELISA Indirecto en 48 Fincas de los Cantones rio Verde y Quinindé, Provincia de Esmeraldas; Universidad San Francisco de Ecuador: Quito, Ecuador, 2018.
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. [CrossRef] [PubMed]
Zambrano, D.; Pérez, M. Estudio Epidemiológico de Brucelosis Bovina en la Provincia de Manabí, Ecuador. Ph.D. Thesis, Universidad Agraria de la Habana, San José de las Lajas, Cuba, 2016; p. 164.
Getachew, T.; Sintayehu, G.; Getenet, M.; Fasil, A. Bayesian estimation of sensitivity and specificity of rose bengal, complement fixation, and indirect ELISA tests for the diagnosis of bovine brucellosis in Ethiopia. Veter. Med. Int. 2016, 2016, 8032753. [CrossRef]
Consumers Health Agriculture and Food Executive Agency. Eradication Programme for Bovine Brucellosis; European Commission; Health and Consumers Directorate-General: London, UK, 2012; p. 64.
Aranís, C.; Oporto, J.; Espinoza, M.; Riedel, I.; Pérez, C.; García, P. Utilidad de la determinación de anticuerpos IgG e IgM por ELISA e inmunocaptura en una serie clínica de brucelosis humana. Rev. Chil. Infectología 2008, 25, 116–121. [CrossRef]
Rahman, A.A.; Saegerman, C.; Berkvens, D.; Fretin, D.; Gani, O.; Ershaduzzaman; Ahmed, M.U.; Emmanuel, A. Bayesian estimation of true prevalence, sensitivity and specificity of indirect ELISA, Rose Bengal Test and Slow Agglutination Test for the diagnosis of brucellosis in sheep and goats in Bangladesh. Prev. Veter. Med. 2013, 110, 242–252. [CrossRef]
Dendukuri, N.; Joseph, L. Bayesian approaches to modeling the conditional dependence between multiple diagnostic tests. Biom. 2001, 57, 158–167. [CrossRef]
Landis, J.R.; Koch, G.G. An application of hierarchical kappa-type statistics in the assessment of majority agreement among multiple observers. Biometrics 1977, 33, 363–374. [CrossRef] [PubMed]
Matope, G.; Muma, J.; Toft, N.; Gori, E.; Lund, A.; Nielsen, K.; Skjerve, E. Evaluation of sensitivity and specificity of RBT, c-ELISA and fluorescence polarisation assay for diagnosis of brucellosis in cattle using latent class analysis. Veter. Immunol. Immunopathol. 2011, 141, 58–63. [CrossRef] [PubMed]
Carrasco, E.A.; Uzal, F.A.; Nielsen, K.H. Comparación de cuatro técnicas de ELISA en la evaluación de la respuesta serológica de terneras vacunadas con Brucella abortus cepa. Arch. Med. Vet. 1995, 27, 51–57.
Fosgate, G.T.; Adesiyun, A.A.; Hird, D.W.; Johnson, W.O.; Hietala, S.K.; Schurig, G.G.; Ryan, J. Comparison of serologic tests for detection of Brucella infections in cattle and water buffalo (Bubalus bubalis). Am. J. Veter. Res. 2002, 63, 1598–1605. [CrossRef] [PubMed]
McGiven, J.; Tucker, J.; Perrett, L.; Stack, J.; Brew, S.; MacMillan, A. Validation of FPA and cELISA for the detection of antibodies to Brucella abortus in cattle sera and comparison to SAT, CFT, and iELISA. J. Immunol. Methods 2003, 278, 171–178. [CrossRef]
Reitsma, J.B.; Rutjes, A.W.S.; Khan, K.S.; Coomarasamy, A.; Bossuyt, P.M. A review of solutions for diagnostic accuracy studies with an imperfect or missing reference standard. J. Clin. Epidemiol. 2009, 62, 797–806. [CrossRef]
Vilar, M.J.; Ranta, J.; Virtanen, S.; Korkeala, H. Bayesian estimation of the true prevalence and of the diagnostic test sensitivity and specificity of enteropathogenic yersiniain finnish pig serum samples. BioMed Res. Int. 2015, 2015, 931542. [CrossRef]
