Abstract
The National Bovine Tuberculosis (bTB) Eradication Program for dairy cattle has been operating in Taiwan for many years and has allowed the prevalence of bTB to decrease gradually. However, 29% of intradermal tuberculin test (ITT)-positive dairy cows were later found to be TB negative based on necropsy, histopathological examination, and mycobacterial isolation results. Studies in Taiwan have indicated that Mycobacterium avium subsp. paratuberculosis (MAP) may lead to false-positive ITT. Due to the high prevalence (over 90%) of paratuberculosis (PTB) serum antibody among Taiwan’s farms, comparative ITT (CITT) has been recommended to differentiate between bTB and PTB infections. In this study, we used ITT, CITT, and enzyme-linked immunosorbent assay (ELISA) to evaluate the prevalence of bTB from 2012 to 2018. We also used pathological and bacterial examination from ITT-positive dairy cows to evaluate CITT’s diagnostic ability and adjust its cutoff point accordingly. After careful selection, 36 cows (including 31 cows from 11 ITT-positive farms and 5 from 2 ITT-negative farms) were examined by CITT. The cutoff point was adjusted using a receiver operating characteristic (ROC) analysis. Overall, our results identified the ITT-positive prevalence in Taiwan as 0.03–0.22%, and PTB-positive prevalence as 54.55–73.53%. The results of sensitivity, specificity, kappa, and ROC analyses have identified the optimal cutoff point for the CITT in Taiwan as ≥ 3 mm. At this cutoff point value, the sensitivity and specificity were 62.5% and 96.43%, respectively. Our findings can be used to reduce the false-positive response rate caused by PTB cross-reaction and accelerate the eradication of bTB in Taiwan.
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References
Aagaard, C., Govaerts, M., Meikle, V., Gutiérrez-Pabello, J.A., McNair, J., Andersen, P., Suárez-Güemes, F., Pollock, J., Espitia, C., Cataldi, A., 2010. Detection of bovine tuberculosis in herds with different disease prevalence and influence of paratuberculosis infection on PPDB and ESAT-6/CFP10 specificity. Preventive Veterinary Medicine, 96,161-169
Awah-Ndukum, J., Temwa, J., Ngu Ngwa, V., Mouiche, M.M., Iyawa, D., Zoli1, P.A., 2016. Interpretation criteria for comparative intradermal tuberculin test for diagnosis of bovine tuberculosis in cattle in Maroua area of Cameroon, Veterinary Medicine International, 2016, 1-8
Bentley, T.G.K., Antonino C., Theodore G.G., 2012, Implications of the impact of prevalence on test thresholds and outcomes: lessons from tuberculosis, BMC research Notes, 5, 1-7
Chen, C.M., 2012. The efficacy of combining intradermal tuberculin test (ITT), Enzyme-linked immunosorbent assay and comparative test on detecting infected cattles of ITT-positive dairy herds, (unpublished Master Thesis, National Pingtung University of Science and Technology)
Chu, C., Lin, H., Su, Y., 2013. Evaluation of different diagnostic methods of mycobacterial infection in intradermal tuberculin testing-positive feedlot cattle and deer, Asian Journal of Animal and Veterinary Advances, 8, 461-472
Council of Agriculture Executive Yuan, Taiwan, Bovine tuberculosis diagnosis method. In Council of Agriculture Executive Yuan Directions, 2017. https://www.baphiq.gov.tw/ws.php?id=16429. Accessed 20 Jan 2020 (In Chinese)
Council of Agriculture Executive Yuan, Taiwan, Annual agricultural statistics. In Official Information, 2019. https://agrstat.coa.gov.tw/sdweb/public/official/OfficialInformation.aspx. Accessed 20 Jan 2020 (In Chinese)
Downs, S.H., Broughan, J.M., Goodchild, A.V., Upton, P.A., Durr, P.A., 2016. Responses to diagnostic tests for bovine tuberculosis in dairy and non-dairy cattle naturally exposed to Mycobacterium bovis in Great Britain, Veterinary Journal, 216, 8-17
Dunn, J.R., Kaneene, J.B., Grooms, D.L., Bolin, S.R., Bolin, C.A., Bruning-Fann, C.S., 2005. Effects of positive results for Mycobacterium avium subsp. paratuberculosis as determined by microbial culture of feces or antibody ELISA on results of caudal fold tuberculin test and interferon-γ assay for tuberculosis in cattle, Journal of the American Veterinary Medical Association, 226, 429-435
Etchechoury, I., Valencia, G.E., Morcillo, N., Sequeira, M.D., Imperiale, B., Lopez, M., Caimi, K., Zumarraga, M.J., Cataldi, A., Romano, M.I., 2010. Molecular typing of Mycobacterium bovis isolates in Argentina: first description of a person-toperson transmission case, Zoonoses Public Health, 57, 375-381
Francis, J., Seiler, R.J., Wilkie, I.W., O’Boyle, D., Lumsden, M.J., Frost, A.J., 1978. The sensitivity and specificity of various tuberculin tests using bovine PPD and other tuberculin, Veterinary Record, 103, 420-425
Gaborick, C.M., Salman, M.D., Ellis, R.P., Triantis, J., 1996. Evaluation of a five-antigen ELISA for diagnosis of tuberculosis in cattle and cervidae, Journal of the American Veterinary Medical Association, 209, 962-966
Huang, C.S., Tsai, S.S., Kuan, N.N., Tu, C., 2011. Prevalence of Mycobacterium avium subsp. paratuberculosis infection in ruminants in Taiwan, Experimental Report Taiwan AHRI, 46, 39-44 (In Chinese)
Jiang, T.S., 1993. Comparison of tuberculin test and bovine γ-interferon detection, (unpublished Master Thesis, National Chung Hsing University)
Jou, R., Huang, W.L., Chiang, C.Y., 2008. Human tuberculosis caused by Mycobacterium bovis, Taiwan, Emerging Infectious Diseases, 14, 515-517
Landis, J.R. and Koch, G.G., 1977. The measurement of observer agreement for categorical data, Biometrics, 33, 159-174
Lauzi, S., Pasotto, D., Amadori, M., Archetti, I.L., Poli, G., Bonizzi, L., 2000. Evaluation of the specificity of the γ-interferon test in Italian bovine tuberculosis-free herds, The Veterinary Journal, 160, 17-24
Li, W.T., 2010. Transmission risk factor and control strategy of bovine paratuberculosis in Taiwan, (unpublished Master Thesis, National Taiwan University)
Lin, H.C., 2010. Diagnosis and phylogenetic analysis of mycobacterial infection and Mycobacterium bovis from intradermal tuberculin test-positive herbivore, (unpublished Master Thesis, National Chiayi University)
Monaghan, M.L., Doherty, M.L., Collins, J.D., Kazda, J.F., Quinn, P.J., 1994. The tuberculin test, Veterinary Microbiology, 40, 111-124
Ngandolo, B.N.R., Müller, B., Diguimbaye-Djaïbe, C., Schiller, I., Marg-Haufe, B., Cagiola, M., Jolley, M., Surujballi, O., Akakpo, A.J., Oesch, B., Zinsstag, J., 2009. Comparative assessment of fluorescence polarization and tuberculin skin testing for the diagnosis of bovine tuberculosis in Chadian cattle, Preventive Veterinary Medicine, 89, 81-89
Pollock, J.M., McNair, J., Welsh, M.D., Girvin, R.M., Kennedy, H.E., Mackie, D.P., Neill, S.D., 2001. Immune responses in bovine tuberculosis, Tuberculosis, 81, 103-107
Pucken, V.B., Knubben-Schweizer, G., Döpfer, D., Groll, A., Hafner-Marx,A., Hörmansdorfer, S., Sauter-Louis, C., Straubinger, R. K., Zimmermann, P., Hartnack, S., 2017. Evaluating diagnostic tests for bovine tuberculosis in the southern part of Germany: A latent class analysis, PLoS One, 12, e0179847
Raffo, E., Steuer, P., Monti, G., Salgado, M., 2017. Effect of Mycobacterium avium subsp. paratuberculosis (MAP) infection on the diagnostic accuracy for Mycobacterium bovis (M. bovis) infection under field conditions in cattle belonging to low M. bovis prevalence herds, Tropical Animal Health and Production, 49, 771-775
Raffo, E., Steuer, P., Tomckowiack, C., Tejeda, C., Collado, B., Salgado, M. 2020. More insights about the interfering effect of Mycobacterium avium subsp. paratuberculosis (MAP) infection on Mycobacterium bovis (M. bovis) detection in dairy cattle. Tropical Animal Health and Production, 52, 1479-1485
Schiller, I., Oesch, B., Vordermeier, H.M., Palmer, M.V., Harris, B.N., Orloski, K.A., Buddle, B.M., Thacker, T.C., Lyashchenko, K.P., Waters, W.R., 2010. Bovine tuberculosis: a review of current and emerging diagnostic techniques in view of their relevance for disease control and eradication, Transboundary and Emerging Diseases, 57, 205-220
Sternberg, S. and Viske, D., 2003. Control strategies for paratuberculosis in Sweden, Acta Veterinaria Scandinavica, 44, 247-249
Tiwari, A., VanLeeuwen, J.A., McKenna, S.L., Keefe, G.P., Barkema, H.W., 2006. Johne’s disease in Canada Part I: clinical symptoms, pathophysiology, diagnosis, and prevalence in dairy herds, Canadian Veterinary Journal, 47, 874-882
Vordermeier, M., Aranaz, A., Pollock, J.M., 2001. Immunodiagnosis of bovine tuberculosis. Summary of a satellite workshop of the Mycobacterium bovis 2000 conference, Cambridge, UK, 17 August 2000, Tuberculosis, 81, 177-180
World Organisation for Animal Health, 2009. Bovine tuberculosis. In: Manual of Diagnostic Tests and Vaccines for Terrestrial Animals, Chapter 3.4.6., 1058–1074
World Organisation for Animal Health, 2018. Paratuberculosis. In: Manual of Diagnostic Tests and Vaccines for Terrestrial Animals, Chapter 3.1.15., 544–559
Wu, Y.H., 1997. Bovine tuberculosis. In: Bovine Disease. (Yi Hsien, Taipei, Taiwan), 141–145. (In Chinese)
Acknowledgements
We thank the Animal Health Research Institute, Council of Agriculture, Executive Yuan for their assistance in conducting M. bovis culture; the Yunlin-Chiayi-Tainan of Animal Disease Diagnostic Center and the National Chiayi University’s College of Veterinary for processing tissue sections and performing acid-fast staining; and the Animal Health Research Institute for sample collection. This manuscript was edited by Wallace Academic Editing and Iris Lai.
Funding
This study was funded by the Council of Agriculture, Executive Yuan of the Republic of China, Taiwan (No. 101AS-10.6.1-BQ-B4, No. 102AS-10.5.1-BQ-B5, No. 103AS-10.3.1-BQ-B4, No. 104AS-10.12.1-BQ-B4, No. 105AS-10.10.1-BQ-B4, No. 106AS-9.9.1-BQ-B3, and No. 107AS-8.7.1-BQ-B3).
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HCL conducted all experiments and analyses. CSC and YCS designed the experiment. YCS and JML supplied the funding. HCL and JML conducted the statistical analyses.
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Lin, HC., Chu, C., Su, Y. et al. Evaluation of using comparative intradermal tuberculin test to diagnose bovine tuberculosis in dairy cattle in Taiwan. Trop Anim Health Prod 54, 79 (2022). https://doi.org/10.1007/s11250-021-03023-4
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DOI: https://doi.org/10.1007/s11250-021-03023-4