DOI QR코드

DOI QR Code

Comparative analysis of serological tests and fecal detection in the diagnosis of Mycobacterium avium subspecies paratuberculosis infection

  • Park, Hong-Tae (Department of Infectious Diseases, College of Veterinary Medicine, Seoul National University) ;
  • Ha, Seungmin (Department of Animal Resources Development, National Institute of Animal Science, Rural Development Administration) ;
  • Park, Hyun-Eui (Department of Infectious Diseases, College of Veterinary Medicine, Seoul National University) ;
  • Shim, Soojin (Department of Infectious Diseases, College of Veterinary Medicine, Seoul National University) ;
  • Hur, Tai Young (Department of Animal Resources Development, National Institute of Animal Science, Rural Development Administration) ;
  • Yoo, Han Sang (Department of Infectious Diseases, College of Veterinary Medicine, Seoul National University)
  • Received : 2020.05.11
  • Accepted : 2020.07.09
  • Published : 2020.09.30

Abstract

Johne's disease (JD) caused by Mycobacterium avium subspecies paratuberculosis (MAP) is a chronic, wasting infectious disease in ruminants that causes enormous economic losses to the dairy and beef cattle industries. The most effective way to eradicate JD is to detect infected individuals as early as possible and remove them from the herd. However, it is difficult to detect infected individuals early with the currently using diagnostic methods. Two serological diagnostic kits commercially used worldwide and a fecal detection test were compared using 298 serum samples and feces of cattle in this study to present an efficient diagnostic method. Although there was a high correlation between the 2 serological diagnostic kits (R2 = 0.7473), kit A showed a higher serological positive rate. However, the correlation between fecal tests and serological diagnosis was very low. MAP was also detected in fecal tests in many serologically negative individuals. In the periodical diagnosis of JD, MAP was detected in the feces of only cows with the higher antibody titer to MAP. These results suggest that for effective eradication of JD, early detection of infected individuals by fecal tests together with the serological tests currently in use and by removal of infected individuals are needed.

Keywords

References

  1. Manning EJ. Mycobacterium avium subspecies paratuberculosis: a review of current knowledge. J Zoo Wildl Med 2001;32:293-304. https://doi.org/10.1638/1042-7260(2001)032[0293:MASPAR]2.0.CO;2
  2. Britton LE, Cassidy JP, O'Donovan J, Gordon SV, Markey B. Potential application of emerging diagnostic techniques to the diagnosis of bovine Johne's disease (paratuberculosis). Vet J 2016;209:32-39. https://doi.org/10.1016/j.tvjl.2015.10.033
  3. Fecteau ME. Paratuberculosis in Cattle. Vet Clin North Am Food Anim Pract 2018;34:209-222. https://doi.org/10.1016/j.cvfa.2017.10.011
  4. Kudahl AB, Nielsen SS, Ostergaard S. Economy, efficacy, and feasibility of a risk-based control program against paratuberculosis. J Dairy Sci 2008;91:4599-4609. https://doi.org/10.3168/jds.2008-1257
  5. Marce C, Beaudeau F, Bareille N, Seegers H, Fourichon C. Higher non-return rate associated with Mycobacterium avium subspecies paratuberculosis infection at early stage in Holstein dairy cows. Theriogenology 2009;71:807-816. https://doi.org/10.1016/j.theriogenology.2008.10.017
  6. Smith RL, Strawderman RL, Schukken YH, Wells SJ, Pradhan AK, Espejo LA, Whitlock RH, Van Kessel JS, Smith JM, Wolfgang DR, Grohn YT. Effect of Johne's disease status on reproduction and culling in dairy cattle. J Dairy Sci 2010;93:3513-3524. https://doi.org/10.3168/jds.2009-2742
  7. Grant IR, Ball HJ, Rowe MT. Incidence of Mycobacterium paratuberculosis in bulk raw and commercially pasteurized cows' milk from approved dairy processing establishments in the United Kingdom. Appl Environ Microbiol 2002;68:2428-2435. https://doi.org/10.1128/AEM.68.5.2428-2435.2002
  8. Grant IR. Zoonotic potential of Mycobacterium avium ssp. paratuberculosis: the current position. J Appl Microbiol 2005;98:1282-1293. https://doi.org/10.1111/j.1365-2672.2005.02598.x
  9. Aly SS, Thurmond MC. Evaluation of Mycobacterium avium subsp paratuberculosis infection of dairy cows attributable to infection status of the dam. J Am Vet Med Assoc 2005;227:450-454. https://doi.org/10.2460/javma.2005.227.450
  10. National Research Council (US) Committee on Diagnosis and Control of Johne's Disease. Diagnosis and Control of Johne's Disease. Washington, D.C., National Academies Press, 2003.
  11. Sweeney RW, Whitlock RH, Rosenberger AE. Mycobacterium paratuberculosis cultured from milk and supramammary lymph nodes of infected asymptomatic cows. J Clin Microbiol 1992;30:166-171. https://doi.org/10.1128/jcm.30.1.166-171.1992
  12. Streeter RN, Hoffsis GF, Bech-Nielsen S, Shulaw WP, Rings DM. Isolation of Mycobacterium paratuberculosis from colostrum and milk of subclinically infected cows. Am J Vet Res 1995;56:1322-1324.
  13. van Esker MH, Koets AP. Application of transcriptomics to enhance early diagnosis of Mycobacterium infections, with an emphasis on Mycobacterium avium ssp. paratuberculosis. Vet Sci 2019;6:59. https://doi.org/10.3390/vetsci6030059
  14. Arango-Sabogal JC, Fecteau G, Pare J, Roy JP, Labrecque O, Cote G, Wellemans V, Schiller I, Dendukuri N, Buczinski S. Estimating diagnostic accuracy of fecal culture in liquid media for the detection of Mycobacterium avium subsp. paratuberculosis infections in Quebec dairy cows: a latent class model. Prev Vet Med 2018;160:26-34. https://doi.org/10.1016/j.prevetmed.2018.09.025
  15. Prendergast DM, Pearce RA, Yearsley D, Ramovic E, Egan J. Evaluation of three commercial PCR kits for the direct detection of Mycobacterium avium subsp. paratuberculosis (MAP) in bovine faeces. Vet J 2018;241:52-57. https://doi.org/10.1016/j.tvjl.2018.09.013
  16. Buczinski S, Arsenault J, Kostoulas P, Corbiere F, Fecteau G, Dendukuri N. Accuracy of paratuberculosis diagnostic tests in small ruminants: protocol for a systematic review and metaanalysis. Anim Health Res Rev 2019;20:98-102. https://doi.org/10.1017/s1466252319000082
  17. Gupta SK, Maclean PH, Ganesh S, Shu D, Buddle BM, Wedlock DN, Heiser A. Detection of microRNA in cattle serum and their potential use to diagnose severity of Johne's disease. J Dairy Sci 2018;101:10259-10270. https://doi.org/10.3168/jds.2018-14785
  18. de Souza GD, Rodriguez AB, Romano MI, Ribeiro ES, Oelemann WM, da Rocha DG, da Silva WD, Lasunskaia EB. Identification of the Apa protein secreted by Mycobacterium avium subsp. paratuberculosis as a novel fecal biomarker for Johne's disease in cattle. Pathog Dis 2018;76:fty063.
  19. Li L, Bannantine JP, Campo JJ, Randall A, Grohn YT, Schilling MA, Katani R, Radzio-Basu J, Easterling L, Kapur V. Identification of sero-diagnostic antigens for the early diagnosis of Johne's disease using MAP protein microarrays. Sci Rep 2019;9:17573. https://doi.org/10.1038/s41598-019-53973-x
  20. Nielsen SS, Toft N. Ante mortem diagnosis of paratuberculosis: a review of accuracies of ELISA, interferon-${\gamma}$ assay and faecal culture techniques. Vet Microbiol 2008;129:217-235. https://doi.org/10.1016/j.vetmic.2007.12.011
  21. Facciuolo A, Kelton DF, Mutharia LM. Novel secreted antigens of Mycobacterium paratuberculosis as serodiagnostic biomarkers for Johne's disease in cattle. Clin Vaccine Immunol 2013;20:1783-1791. https://doi.org/10.1128/CVI.00380-13
  22. Park HT, Shin MK, Sung KY, Park HE, Cho YI, Yoo HS. Effective DNA extraction method to improve detection of Mycobacterium avium subsp. paratuberculosis in bovine feces. Korean J Vet Res 2014;54:55-57. https://doi.org/10.14405/kjvr.2014.54.1.55
  23. Sevilla IA, Garrido JM, Molina E, Geijo MV, Elguezabal N, Vazquez P, Juste RA. Development and evaluation of a novel multicopy-element-targeting triplex PCR for detection of Mycobacterium avium subsp. paratuberculosis in feces. Appl Environ Microbiol 2014;80:3757-3768. https://doi.org/10.1128/AEM.01026-14
  24. Fry MP, Kruze J, Collins MT. Evaluation of four commercial enzyme-linked immunosorbent assays for the diagnosis of bovine paratuberculosis in Chilean dairy herds. J Vet Diagn Invest 2008;20:329-332. https://doi.org/10.1177/104063870802000311
  25. Collins MT, Wells SJ, Petrini KR, Collins JE, Schultz RD, Whitlock RH. Evaluation of five antibody detection tests for diagnosis of bovine paratuberculosis. Clin Diagn Lab Immunol 2005;12:685-692. https://doi.org/10.1128/CDLI.12.6.685-692.2005
  26. DeKuiper JL, Coussens PM. Inflammatory Th17 responses to infection with Mycobacterium avium subspecies paratuberculosis (MAP) in cattle and their potential role in development of Johne's disease. Vet Immunol Immunopathol 2019;218:109954. https://doi.org/10.1016/j.vetimm.2019.109954
  27. Manning EJ, Collins MT. Mycobacterium avium subsp. paratuberculosis: pathogen, pathogenesis and diagnosis. Rev Sci Tech 2001;20:133-150. https://doi.org/10.20506/rst.20.1.1275
  28. Koets A, Rutten V, Hoek A, van Mil F, Muller K, Bakker D, Gruys E, van Eden W. Progressive bovine paratuberculosis is associated with local loss of CD4+ T cells, increased frequency of gamma delta T cells, and related changes in Tcell function. Infect Immun 2002;70:3856-3864. https://doi.org/10.1128/IAI.70.7.3856-3864.2002
  29. Begg DJ, Plain KM, de Silva K, Gurung R, Gunn A, Purdie AC, Whittington RJ. Immunopathological changes and apparent recovery from infection revealed in cattle in an experimental model of Johne's disease using a lyophilised culture of Mycobacterium avium subspecies paratuberculosis. Vet Microbiol 2018;219:53-62. https://doi.org/10.1016/j.vetmic.2018.03.029