Advertisement

Is the transmission of Mycobacterium avium subspecies paratuberculosis (MAP) infection through milk intended to feed calves an overlooked item in paratuberculosis control programs?

  • Pamela Steuer
  • Bernardita Collado
  • Carolina Avilez
  • Carlos Tejeda
  • Juan P. Soto
  • Miguel SalgadoEmail author
Regular Articles

Abstract

As in many parts of the world, Chile shows a high Mycobacterium avium subsp. paratuberculosis (MAP) infection rate. Evidently, the control recommendations have been inefficient. In the author’s opinion, the potential risk of MAP transmission to susceptible calves through milk consumption is largely overlooked. Two observational studies were performed, one to confirm MAP shedding in young stock in a high MAP-infected dairy herd and MAP load in milk intended to feed these calves was estimated. In parallel, in a second study, we estimated the relationship between MAP herd seroprevalence and the cow MAP shedding level as well as the presence of this pathogen in milk used to feed dairy calves. In the first study, 53.7% of cows and 22.5% of calves showed positive culture results. Among all cows tested, 9 (2.19%) animals had a positive serum ELISA, and MAP load in milk reached 106 bacteria/mL. In the second study, three seroprevalence categories were established as follows: high (≥ 9%), medium (> 5% and ≤ 9%), and low (≤ 5%). Statistical significant differences among these categories were observed. Animals from the high seroprevalence category shed significantly more MAP than the others. However, in the low category, heavy shedder animals were also observed. Finally, in all study herds, MAP presence in milk intended to feed calves was reported, even from herds without ELISA-positive animals.

Keywords

Paratuberculosis Control Milk ELISA Observational studies 

Notes

Funding information

This work was supported by FONDECYT Grant (1161633) and DID S-2015-48 grant. Pamela Steuer was the recipient of a Doctoral Studentship from the Chilean government (CONICYT) during the present study and it was part of a Doctoral Thesis of the Universidad Austral de Chile.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The study was carried out in strict accordance with the recommendations in the Guide of Use of Animals for Research of Universidad Austral de Chile (www.uach.cl/direccion/investigacion/uso_animales.htm).

References

  1. Bastida, F. and Juste, R.A., 2011. Paratuberculosis control: a review with a focus on vaccination, Journal of Immune Based Therapies and Vaccines, 9:8, 1–17.Google Scholar
  2. Beaudeau, F., Belliard, M., Joly, A. and Seegers, H., 2007. Reduction in milk yield associated with Mycobacterium avium subspecies paratuberculosis (Map) infection in dairy cows, Veterinary Research, 38, 625–634.CrossRefPubMedGoogle Scholar
  3. Chiodini, R.J., Chamberlin, W.M., Sarosiek, J. and McCallum, R.W., 2012. Crohn’s disease and the mycobacterioses: a quarter century later: causation or simple association?, Critical Reviews in Microbiology, 38, 52–93.CrossRefPubMedGoogle Scholar
  4. Collins, M.T., 2003. Paratuberculosis: review of present knowledge, Acta Veterinaria Scandinavica, 44, 217–221.PubMedGoogle Scholar
  5. Collins, M.T., Eggleston, V. and Manning, E.J.B., 2010. Successful control of Johne’s disease in nine dairy herds: Results of a six-year field trial, Journal of Dairy Science, 93, 1638–1643.CrossRefPubMedGoogle Scholar
  6. Cossu, D., Cocco, E., Paccagnini, D., Masala, S., Ahmed, N., Frau, J., Marrosu, M., Sechi, L.A., 2011. Association of Mycobacterium avium subsp. paratuberculosis with Multiple Sclerosis in Sardinian Patients, PloS One, 6, 1–6.CrossRefGoogle Scholar
  7. Dohoo, I., 2003. Screening and Diagnostic Test. In: I. Dohoo, W. Martin, H. Stryhn (eds), Veterinary Epidemiologic Research, AVC Inc., Charlottetown, Prince Edward Island, Canada, 85–113.Google Scholar
  8. Dzieciol, M., Volgger, P., Khol, J., Baumgartner, W., Wagner, M. and Hein, I., 2010. A novel real-time PCR assay for specific detection and quantification of Mycobacterium avium subsp. paratuberculosis in milk with the inherent possibility of differentiation between viable and dead cells, BMC Research Notes, 3:251, 1–8.Google Scholar
  9. Fecteau, M-E., 2018. Paratuberculosis in cattle. Veterinary Clinics: Food Animal Practice, 34, 209–222.Google Scholar
  10. Foddai, A., Elliott, C.T. and Grant, I.R., 2010. Maximizing capture efficiency and specificity of magnetic separation for Mycobacterium avium subsp. paratuberculosis cells, Applied Environmental Microbiology, 76, 7550–7558.CrossRefPubMedGoogle Scholar
  11. Garry, F., 2011. Control of paratuberculosis in dairy herds, Veterinary Clinics: Food Animal Practice, 27, 599–607.Google Scholar
  12. Giese and Ahrens, 2000. Detection of Mycobacterium avium subsp. Paratuberculosis in milk from clinically affected cows by PCR and culture, Veterinary Microbiology, 77, 291–297.Google Scholar
  13. Grant, I.R., Ball, H.J., Neil, S.D. and Rowe, M.T., 1996. Inactivation of Mycobacterium paratuberculosis in cows’ milk at pasteurization temperatures, Applied Environmental Microbiology, 62, 2631–2636.Google Scholar
  14. Grant, I.R., Hitchings, E.I., McCartney, A., Ferguson, F. and Rowe, M.T., 2002. Effect of commercial-scale high temperature, short-time pasteurization on the viability of Mycobacterium paratuberculosis in naturally infected cows’ milk, Applied Environmental Microbiology, 68, 602–607.CrossRefPubMedGoogle Scholar
  15. Grant, I.R., Williams, A.G., Rowe, M.T. and Muir, D.D., 2005. Efficacy of various pasteurization time temperature conditions in combination with homogenization on inactivation of Mycobacterium avium subsp. paratuberculosis in milk, Applied Environmental Microbiology, 71, 2853–2861.CrossRefPubMedGoogle Scholar
  16. Grant, I.R., Foddai, A., Tarrant, J., Kunkel, B., Hartmann, F.A., McGuirk, S., Hansen, C., Talaat, A.M. and Collins, M.T., 2017. Viable Mycobacterium avium ssp. paratuberculosis isolated from calf milk replacer, Journal of Dairy Science, 100, 1–13.CrossRefGoogle Scholar
  17. Jubb, T.F., Sergeant, E.S., Callinan, A.P. and Galvin, J., 2004. Estimate of the sensitivity of an ELISA used to detect Johne’s disease in Victorian dairy cattle herds, Australian Veterinary Journal, 82, 569–573.CrossRefPubMedGoogle Scholar
  18. Kruze, J., Monti, G., Schulze, F., Mella, A. and Leiva, S., 2013. Herd-level prevalence of Mycobacterium avium subsp paratuberculosis infection in dairy herds of southern Chile determined by culture of environmental fecal samples and bulk-tank milk qPCR, Preventive Veterinary Medicine, 111, 19–24.CrossRefGoogle Scholar
  19. Kudahl, A.B., Nielsen, B. and Østergaard, S., 2011. Strategies for time of culling in control of paratuberculosis in dairy herds, Journal of Dairy Science, 94, 3824–3834.CrossRefPubMedGoogle Scholar
  20. Lombard, J.E., 2011. Epidemiology and Economics of Paratuberculosis, Veterinary Clinics: Food Animal Practice, 27, 525–535.Google Scholar
  21. Manning, E.J. and Collins, M.T., 2001. Mycobacterium avium subsp. paratuberculosis: pathogen, pathogenesis and diagnosis, Revue scientifique et technique (International Office of Epizootics), 20, 133–150.Google Scholar
  22. Mortier, R., Barkema, H., Orsel, K., Wolf, R. and De Buck, J., 2014. Shedding patterns of dairy calves experimentally infected with Mycobacterium avium subsp. paratuberculosis, Veterinary Research, 45, 71, 1–9.Google Scholar
  23. Naser, S.A, Thanigachalam, S., Dow, C.T., Collins, M.T., 2013. Exploring the role of Mycobacterium avium subspecies paratuberculosis in the pathogenesis of type 1 diabetes mellitus: a pilot study, Gut Pathogens, 5, 1–7.CrossRefGoogle Scholar
  24. R Core Team, 2014. R: A Language and Environment for Statistical Computing. http://www.R-project.org.
  25. Salgado, M., Steuer, P., Troncoso, E. and Collins, M.T., 2013. Evaluation of PMS–PCR technology for detection of Mycobacterium avium subsp. paratuberculosis directly from bovine fecal specimens, Veterinary Microbiology, 167, 725–728.CrossRefPubMedGoogle Scholar
  26. Salgado, M., Verdugo, C., Heuer, C., Castillo, P. and Zamorano, P., 2014. A novel low cost method for Mycobacterium avium SUBSP. paratuberculosis DNA extraction from an automated broth culture system for a real time PCR confirmation, Journal of Veterinary Science, 15, 233–239.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Stratmann, J., Strommenger, B., Stevenson, K. and Gerlach, G.F., 2002. Development of a Peptide-Mediated Capture PCR for Detection of Mycobacterium aviumsubsp. paratuberculosis in Milk, Journal of Clinical Microbiology, 40, 4244–4250.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Stratmann, J., Dohmann, K., Heinzmann, J. and Gerlach, G.F., 2006. Peptide aMptD-Mediated Capture PCR for Detection of Mycobacterium avium subsp. paratuberculosis in Bulk Milk Samples, Applied Environmental Microbiology, 72, 5150–5158.CrossRefPubMedGoogle Scholar
  29. Sweeney, R.W., 1996. Transmission of paratuberculosis, Veterinaty Clinics: Food Animal Practice, 12, 305–312.Google Scholar
  30. Sweeney, R.W., 2011. Pathogenesis of Paratuberculosis, Veterinaty Clinics: Food Animal Practice, 27, 537–546.Google Scholar
  31. Sweeney, R.W., 2015. Paratuberculosis (Johne’s disease). In: B.P., Smith (ed), Large animal internal medicine (Elsevier, St. Louis, 5th edition), 834-837.Google Scholar
  32. Sweeney, R.W., Whitlock, R.H. and Rosenberg, A.E., 1992. Mycobacterium avium subsp. paratuberculosis cultured from milk and supramamammary lymph nodes of infected asymptomatic cows, Journal of Clinical Microbiology, 30, 166–171.PubMedPubMedCentralGoogle Scholar
  33. van Schaik, G., Haro, F., Mella, A. and Kruze, J., 2007. Bayesian analysis to validate a commercial ELISA to detect paratuberculosis in dairy herds of southern Chile, Preventive Veterinary Medicine, 79, 59–69.CrossRefPubMedGoogle Scholar
  34. Verdugo, C., Valdes, M.F. and Salgado, M., 2018. Within-herd prevalence and clinical incidence distributions of Mycobacterium avium subspecies paratuberculosis infection on dairy herds in Chile, Preventive Veterinary Medicine, 154, 113–118.CrossRefPubMedGoogle Scholar
  35. Villarino, M.A., Scott, H.M. and Jordan, E.R., 2011. Influence of parity at time of detection of serologic antibodies to Mycobacterium avium subspecies paratuberculosis on reduction in daily and lifetime milk production in Holstein cows, Journal of Animal Science, 89, 267–276.CrossRefPubMedGoogle Scholar
  36. Whitlock, R.H. and Buergelt, C., 1996. Preclinical and clinical manifestations of paratuberculosis (including pathology), Veterinary Clinics: Food Animal Practice, 12, 345–356.Google Scholar
  37. Windsor, P.A. and Whittington, R.J., 2010. Evidence for age susceptibility of cattle to Johne’s disease, The Veterinary Journal, 184, 37–44.CrossRefPubMedGoogle Scholar
  38. Wolf, R., Orsel, K., De Buck, J. and Barkema, H., 2015. Calves shedding Mycobacterium avium subsp. paratuberculosis are common on infected dairy herds, Veterinary Research, 46:71, 1–9.Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Pamela Steuer
    • 1
    • 2
  • Bernardita Collado
    • 1
    • 2
  • Carolina Avilez
    • 1
  • Carlos Tejeda
    • 1
    • 2
  • Juan P. Soto
    • 3
  • Miguel Salgado
    • 1
    Email author
  1. 1.Instituto de Medicina Preventiva Veterinaria, Facultad de Ciencias VeterinariasUniversidad Austral de ChileValdiviaChile
  2. 2.Escuela de Graduados, Facultad de Ciencias VeterinariasUniversidad Austral de ChileValdiviaChile
  3. 3.ProlesurLos LagosChile

Personalised recommendations