[en] Diagnosis of bovine tuberculosis in cattle is challenging due to complex immune host response to infection that limit the performance of available diagnostic tests. In this study, performance of two commercial serological assays developed to detect bovine tuberculosis were evaluated: Enferplex Bovine TB antibody kit including 11 antigens (EnferGroup, Ireland) and IDEXX M. bovis Ab kit (IDEXX, USA). The specificity value obtained with the ELISA IDEXX M. bovis Ab test was 97.1%, whereas it was 97.1% and 95.1% for the high specificity and sensitivity settings, respectively, with the Enferplex Bovine TB antibody kit. The sensitivity of the multiplexed Enferplex Bovine TB antibody test for SICCT-positive animals was higher (N = 172; 51.7% and 58.7% with high specificity and sensitivity settings, respectively) compared to the ELISA IDEXX M. bovis Ab test (sensitivity of 36.6%). "Antigen profiles" generated by the multiplexed Enferplex method showed that five out of 11 antigens present in the test were mostly identified as positive sera in cattle originating from bTB-outbreaks. In comparison, unique profiles appeared to be correlated with false positive results. However additional studies are needed to confirm the observed antigen profiles, and their potential use as an additional diagnostic tool. Serial interpretation of the two serological tests produced higher diagnostic specificity (>99%), reducing false positive results, which is essential for a screening test when the prevalence of bovine tuberculosis is low.
Disciplines :
Veterinary medicine & animal health
Author, co-author :
Moens, Charlotte; Veterinary Bacteriology Service, Sciensano, Brussels B-1050, Belgium, Louvain Institute of Biomolecular Science and Technology, Université Catholique de Louvain, Louvain-la-Neuve B-1348, Belgium
Saegerman, Claude ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires (DMI) > Epidémiologie et analyse des risques appliqués aux sciences vétérinaires
FOD Volksgezondheid - Federale Overheidsdienst Volksgezondheid - Veiligheid van de Voetselketen en Leefmilieu
Funding text :
The research that yielded these results, was funded by the Belgian Federal Public Service of Health, Food Chain Safety and Environment through the contract RT 18/01 DIBOTUB. Preliminary results were presented as a poster at the Seventh International Conference on Mycobacterium bovis, Galway, 7-10 June 2022. We thank members from “Association Régionale de Santé et d'Identification Animales” (ARSIA) for providing the serum samples used in this study. We also thank Ana Soares, Philippe Vannoorenberghe, Damien Desqueper, and Willem Van Campe for providing technical assistance.The research that yielded these results, was funded by the Belgian Federal Public Service of Health , Food Chain Safety and Environment through the contract RT 18/01 DIBOTUB . Preliminary results were presented as a poster at the Seventh International Conference on Mycobacterium bovis, Galway, 7-10 June 2022. We thank members from “Association Régionale de Santé et d'Identification Animales” (ARSIA) for providing the serum samples used in this study. We also thank Ana Soares, Philippe Vannoorenberghe, Damien Desqueper, and Willem Van Campe for providing technical assistance.
Amadori, M., Lyashchenko, K.P., Gennaro, M.L., Pollock, J.M., Zerbini, I., Use of recombinant proteins in antibody tests for bovine tuberculosis. Vet. Microbiol. 85 (2002), 379–389.
Bermingham, M.L., Bishop, S.C., Woolliams, J.A., Pong-Wong, R., Allen, A.R., McBride, S.H., Ryder, J.J., Wright, D.M., Skuce, R.A., McDowell, S.W., Glass, E.J., Genome-wide association study identifies novel loci associated with resistance to bovine tuberculosis. Heredity 112 (2014), 543–551.
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., A review of risk factors for bovine tuberculosis infection in cattle in the UK and Ireland. Epidemiol. Infect. 144 (2016), 2899–2926.
Caminiti, A., Panorama 2019-1: The Socio-Economic Costs of Bovine Tuberculosis. 2019, Bulletin OIE.
Casal, C., Díez-Guerrier, A., Álvarez, J., Rodriguez-Campos, S., Mateos, A., Linscott, R., Martel, E., Lawrence, J.C., Whelan, C., Clarke, J., O'Brien, A., Domínguez, L., Aranaz, A., Strategic use of serology for the diagnosis of bovine tuberculosis after intradermal skin testing. Vet. Microbiol. 170 (2014), 342–351.
Cassidy, J.P., The pathogenesis and pathology of bovine tuberculosis with insights from studies of tuberculosis in humans and laboratory animal models. Vet. Microbiol. 112 (2006), 151–161.
Dean, G.S., Rhodes, S.G., Coad, M., Whelan, A.O., Cockle, P.J., Clifford, D.J., Hewinson, R.G., Vordermeier, H.M., Minimum infective dose of Mycobacterium bovis in cattle. Infect. Immun. 73 (2005), 6467–6471.
Domingo, M., Vidal, E., Marco, A., Pathology of bovine tuberculosis. Res. Vet. Sci. 97 (2014), S20–S29.
EFSA, Scientific opinion on the public health hazards to be covered by inspection of meat (bovine animals). EFSA J., 11(6), 2013, 3266.
Federal Agency for the Safety of the Food Chain (FASFC), Scientific Committee Opinion 2015/11: Evaluation of the Belgian Bovine Tuberculosis Control Program. https://www.favv-afsca.be/scientificcommittee/opinions/2016/_documents/Opinion12-2016_Tuberculose.pdf, 2016, 2016.
Fifis, T., Costopoulos, C., Corner, L.A., Wood, P.R., Serological reactivity to Mycobacterium bovis protein antigens in cattle. Vet. Microbiol. 30 (1992), 343–354.
Gcebe, N., Michel, A., Gey van Pittius, N.C., Rutten, V., Comparative genomics and proteomic analysis of four non-tuberculous mycobacterium species and mycobacterium tuberculosis complex: occurrence of shared immunogenic proteins. Front. Microbiol., 7, 2016, 795.
Hirpa, E., Ameni, G., Lawrence, J.C., Tafess, K., Worku, A., Sori, T., Zewdie, O., Performance evaluation of Mycobacterium bovis antibody test for the diagnosis of bovine tuberculosis in Ethiopia. Acad. J. Anim. Disease. 3 (2014), 33–38.
Humblet, M.-F., Boschiroli, M.L., Saegerman, C., Classification of worldwide bovine tuberculosis risk factors in cattle: a stratified approach. Vet. Res., 40, 2009, 50.
Infantes-Lorenzo, J.A., Moreno, I., de los Risalde, M.Á., Roy, Á., Villar, M., Romero, B., Ibarrola, N., de la Fuente, J., Puentes, E., de Juan, L., Gortázar, C., Bezos, J., Domínguez, L., Domínguez, M., Proteomic characterisation of bovine and avian purified protein derivatives and identification of specific antigens for serodiagnosis of bovine tuberculosis. Clin. Proteomics, 14, 2017, 36.
Lightbody, K.A., Skuce, R.A., Neill, S.D., Pollock, J.M., Mycobacterial antigen-specific antibody responses in bovine tuberculosis: an ELISA with potential to confirm disease status. Vet. Rec. 142 (1998), 295–300.
Lyashchenko, K.P., Pollock, J.M., Colangeli, R., Gennaro, M.L., Diversity of antigen recognition by serum antibodies in experimental bovine tuberculosis. Infect. Immun., 66, 1998, 5344.
Lyashchenko, K., Whelan, A.O., Greenwald, R., Pollock, J.M., Andersen, P., Hewinson, R.G., Vordermeier, H.M., Association of Tuberculin-Boosted Antibody Responses with pathology and cell-mediated immunity in cattle vaccinated with Mycobacterium bovis BCG and infected with M. bovis. Infect. Immun. 72 (2004), 2462–2467.
Lyashchenko, K.P., Grandison, A., Keskinen, K., Sikar-Gang, A., Lambotte, P., Esfandiari, J., Ireton, G.C., Vallur, A., Reed, S.G., Jones, G., Vordermeier, H.M., Stabel, J.R., Thacker, T.C., Palmer, M.V., Waters, W.R., Identification of novel antigens recognized by serum antibodies in Bovine tuberculosis. Clin. Vaccine Immunol., 2017, 24.
Lyashchenko, K.P., Greenwald, R., Sikar-Gang, A., Sridhara, A.A., Johnathan, A., Lambotte, P., Esfandiari, J., Maggioli, M.F., Thacker, T.C., Palmer, M.V., Waters, W.R., Early detection of circulating antigen and IgM-associated immune complexes during experimental Mycobacterium bovis infection in cattle. Clin. Vaccine Immunol., 2017, 24.
McCallan, L., Brooks, C., Couzens, C., Young, F., McNair, J., Byrne, A.W., Assessment of serological tests for diagnosis of bovine tuberculosis. Vet. Rec., 181, 2017, 90.
McCallan, L., Brooks, C., Barry, C., Couzens, C., Young, F.J., McNair, J., Byrne, A.W., Serological test performance for bovine tuberculosis in cattle from herds with evidence of on-going infection in Northern Ireland. PLoS One, 16, 2021, e0245655.
Mcnair, J., Corbett, D.M., Girvin, R.M., Mackie, D.P., Pollock, J.M., Characterization of the early antibody response in bovine tuberculosis: MPB83 is an early target with diagnostic potential: antibody responses in bovine Tb. Scand. J. Immunol. 53 (2001), 365–371.
OIE, OIE Procedure for Registration of Diagnostic kits : IDEXX M. bovis Antibody Test kit. https://www.woah.org/app/uploads/2021/03/oie-register-mbat-abstract-v1-06-2012.pdf, 2012.
OIE, OIE Procedure for Registration of Diagnostic kits : Enferplex Bovine TB antibody kit. https://www.woah.org/app/uploads/2021/03/oie20abstract2026-07-19.pdf, 2019.
Pérez-Morote, R., Pontones-Rosa, C., Gortázar-Schmidt, C., Muñoz-Cardona, Á.I., Quantifying the economic impact of bovine tuberculosis on livestock farms in South-Western Spain. Animals, 10, 2020, 2433.
Pollock, J.M., Neill, S.D., Mycobacterium boviss infection and tuberculosis in cattle. Vet. J. 163 (2002), 115–127.
Trost, B., Stuber, T., Surujballi, O., Nelson, J., Robbe Austerman, S., Smith, N.H., Desautels, L., Tikoo, S.K., Griebel, P., Investigation of the cause of geographic disparities in IDEXX ELISA sensitivity in serum samples from Mycobacterium bovis-infected cattle. Sci. Rep., 6, 2016, 22763.
Varela-Castro, L., Barral, M., Arnal, M.C., Fernández de Luco, D., Gortázar, C., Garrido, J.M., Sevilla, I.A., Beyond tuberculosis: diversity and implications of non-tuberculous mycobacteria at the wildlife–livestock interface. Transbound. Emerg. Dis. 69 (2022), e2978–e2993.
Waters, W.R., Palmer, M.V., Thacker, T.C., Bannantine, J.P., Vordermeier, H.M., Hewinson, R.G., Greenwald, R., Esfandiari, J., McNair, J., Pollock, J.M., Andersen, P., Lyashchenko, K.P., Early antibody responses to experimental Mycobacterium bovis infection of cattle. Clin. Vaccine Immunol. 13 (2006), 648–654.
Waters, W.R., Buddle, B.M., Vordermeier, H.M., Gormley, E., Palmer, M.V., Thacker, T.C., Bannantine, J.P., Stabel, J.R., Linscott, R., Martel, E., Milian, F., Foshaug, W., Lawrence, J.C., Development and evaluation of an enzyme-linked immunosorbent assay for use in the detection of bovine tuberculosis in cattle. Clin. Vaccine Immunol., 18, 2011, 7.
Waters, W.R., Vordermeier, H.M., Rhodes, S., Khatri, B., Palmer, M.V., Maggioli, M.F., Thacker, T.C., Nelson, J.T., Thomsen, B.V., Robbe-Austerman, S., Bravo Garcia, D.M., Schoenbaum, M.A., Camacho, M.S., Ray, J.S., Esfandiari, J., Lambotte, P., Greenwald, R., Grandison, A., Sikar-Gang, A., Lyashchenko, K.P., Potential for rapid antibody detection to identify tuberculous cattle with non-reactive tuberculin skin test results. BMC Vet. Res., 13, 2017, 164.
Welby, S., Cargnel, M., Saegerman, C., Quantitative decision making in animal health surveillance: bovine tuberculosis surveillance in Belgium as case study. Transbound. Emerg. Dis. 69 (2022), e119–e129.
Welsh, M.D., Cunningham, R.T., Corbett, D.M., Girvin, R.M., McNair, J., Skuce, R.A., Bryson, D.G., Pollock, J.M., Influence of pathological progression on the balance between cellular and humoral immune responses in bovine tuberculosis. Immunology 114 (2005), 101–111.
Whelan, C., Shuralev, E., O'Keeffe, G., Hyland, P., Kwok, H.F., Snoddy, P., O'Brien, A., Connolly, M., Quinn, P., Groll, M., Watterson, T., Call, S., Kenny, K., Duignan, A., Hamilton, M.J., Buddle, B.M., Johnston, J.A., Davis, W.C., Olwill, S.A., Clarke, J., Multiplex immunoassay for serological diagnosis of Mycobacterium bovis infection in cattle. Clin. Vaccine Immunol. 15 (2008), 1834–1838.
Whelan, C., Whelan, A.O., Shuralev, E., Kwok, H.F., Hewinson, G., Clarke, J., Vordermeier, H.M., Performance of the Enferplex TB assay with cattle in Great Britain and assessment of its suitability as a test to distinguish infected and vaccinated animals. Clin. Vaccine Immunol., 17, 2010, 813.
