1887

Abstract

subspecies () is the causative agent of paratuberculosis, or Johne’s disease, in cattle, with potential involvement in cases of Crohn’s disease in humans. Johne’s disease is found worldwide and is economically important for both beef and dairy industries. In an effort to characterize this important infection in Egypt, we analysed the ecological and genomic features of recent isolates of . In this report, we examined 26 Holstein dairy herds distributed throughout Egypt, from 2010 to 2013. Using PCR analysis of faecal samples, we estimated a mean herd-level prevalence of 65.4 %, with animal-level infection that reached a mean of 13.6 % among animals suffering from diarrhoea. Whole genome sequencing of field isolates identified numerous single nucleotide polymorphisms among field isolates relative to the standard K10 genome. Interestingly, the virulence of isolates from Egypt revealed diverse virulence phenotypes in the murine model of paratuberculosis, with significant differences in tissue colonization, particularly during the chronic stage of infection. Overall, our analysis confirmed that Johne’s disease is a newly identified problem in Egypt and indicated that has potentially diverse genotypes that impact its virulence. Further ecological mapping and genomic analysis of will enhance our understanding of the transmission and evolutionary dynamics of this pathogen under natural field conditions.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000051
2015-04-01
2019-12-06
Loading full text...

Full text loading...

/deliver/fulltext/micro/161/4/807.html?itemId=/content/journal/micro/10.1099/mic.0.000051&mimeType=html&fmt=ahah

References

  1. Amonsin A., Li L. L., Zhang Q., Bannantine J. P., Motiwala A. S., Sreevatsan S., Kapur V.. ( 2004;). Multilocus short sequence repeat sequencing approach for differentiating among Mycobacterium avium subsp. paratuberculosis strains. . J Clin Microbiol 42:, 1694–1702. [CrossRef][PubMed]
    [Google Scholar]
  2. Bannantine J. P., Wu C. W., Hsu C., Zhou S., Schwartz D. C., Bayles D. O., Paustian M. L., Alt D. P., Sreevatsan S. et al. ( 2012;). Genome sequencing of ovine isolates of Mycobacterium avium subspecies paratuberculosis offers insights into host association. . BMC Genomics 13:, 89. [CrossRef][PubMed]
    [Google Scholar]
  3. Barrett D. J., Good M., Hayes M., More S. J.. ( 2006;). The economic impact of Johne's disease in an Irish dairy herd: a case study. . Ir Vet J 59:, 282–286.
    [Google Scholar]
  4. Castellanos E., de Juan L., Domínguez L., Aranaz A.. ( 2012;). Progress in molecular typing of Mycobacterium avium subspecies paratuberculosis. . Res Vet Sci 92:, 169–179. [CrossRef][PubMed]
    [Google Scholar]
  5. Çetinkaya B., Egan K., Harbour D. A., Morgan K. L.. ( 1996;). An abattoir-based study of the prevalence of subclinical Johne’s disease in adult cattle in south west England. . Epidemiol Infect 116:, 373–379. [CrossRef][PubMed]
    [Google Scholar]
  6. Collins M. T.. ( 1996;). Diagnosis of paratuberculosis. . Vet Clin North Am Food Anim Pract 12:, 357–371.[PubMed]
    [Google Scholar]
  7. Collins M. T., Wells S. J., Petrini K. R., Collins J. E., Schultz R. D., Whitlock R. H.. ( 2005;). Evaluation of five antibody detection tests for diagnosis of bovine paratuberculosis. . Clin Diagn Lab Immunol 12:, 685–692.[PubMed]
    [Google Scholar]
  8. Darling A. C., Mau B., Blattner F. R., Perna N. T.. ( 2004;). Mauve: multiple alignment of conserved genomic sequence with rearrangements. . Genome Res 14:, 1394–1403. [CrossRef][PubMed]
    [Google Scholar]
  9. de Juan L., Alvarez J., Romero B., Bezos J., Castellanos E., Aranaz A., Mateos A., Domínguez L.. ( 2006;). Comparison of four different culture media for isolation and growth of type II and type I/III Mycobacterium avium subsp. paratuberculosis strains isolated from cattle and goats. . Appl Environ Microbiol 72:, 5927–5932. [CrossRef][PubMed]
    [Google Scholar]
  10. Eppleston J., Begg D. J., Dhand N. K., Watt B., Whittington R. J.. ( 2014;). Environmental survival of Mycobacterium avium subsp. paratuberculosis in different climatic zones of eastern Australia. . Appl Environ Microbiol 80:, 2337–2342. [CrossRef][PubMed]
    [Google Scholar]
  11. ESRI ( 2011;). ESRI: ArcGIS Desktop. Redlands, CA:: Environmental Systems Research Institute;.
    [Google Scholar]
  12. Forde T., Kutz S., De Buck J., Warren A., Ruckstuhl K., Pybus M., Orsel K.. ( 2012;). Occurrence, diagnosis, and strain typing of Mycobacterium avium subspecies paratuberculosis infection in Rocky Mountain bighorn sheep (Ovis canadensis canadensis) in southwestern Alberta. . J Wildl Dis 48:, 1–11. [CrossRef][PubMed]
    [Google Scholar]
  13. Ghosh P., Hsu C., Alyamani E. J., Shehata M. M., Al-Dubaib M. A., Al-Naeem A., Hashad M., Mahmoud O. M., Alharbi K. B. et al. ( 2012;). Genome-wide analysis of the emerging infection with Mycobacterium avium subspecies paratuberculosis in the Arabian camels (Camelus dromedarius). . PLoS ONE 7:, e31947. [CrossRef][PubMed]
    [Google Scholar]
  14. Ghosh P., Wu C. W., Talaat A. M.. ( 2013;). Key role for the alternative sigma factor, SigH, in the intracellular life of Mycobacterium avium subsp. paratuberculosis during macrophage stress.. Infect Immun 81:, 2242–2257. [CrossRef][PubMed]
    [Google Scholar]
  15. Hines M. E. II, Stabel J. R., Sweeney R. W., Griffin F., Talaat A. M., Bakker D., Benedictus G., Davis W. C., de Lisle G. W. et al. ( 2007;). Experimental challenge models for Johne’s disease: a review and proposed international guidelines. . Vet Microbiol 122:, 197–222. [CrossRef][PubMed]
    [Google Scholar]
  16. Hsu C.-Y., Wu C.-W., Talaat A. M.. ( 2011;). Genome-wide sequence variations among Mycobacterium avium subspecies paratuberculosis isolates: a better understanding of Johne's disease transmission dynamics. . Front Microbiol 2:, 236. [CrossRef][PubMed]
    [Google Scholar]
  17. Kasnitz N., Köhler H., Weigoldt M., Gerlach G. F., Möbius P.. ( 2013;). Stability of genotyping target sequences of Mycobacterium avium subsp. paratuberculosis upon cultivation on different media, in vitro- and in vivo passage, and natural infection. . Vet Microbiol 167:, 573–583. [CrossRef][PubMed]
    [Google Scholar]
  18. Li L., Bannantine J. P., Zhang Q., Amonsin A., May B. J., Alt D., Banerji N., Kanjilal S., Kapur V.. ( 2005;). The complete genome sequence of Mycobacterium avium subspecies paratuberculosis.. Proc Natl Acad Sci U S A 102:, 12344–12349. [CrossRef][PubMed]
    [Google Scholar]
  19. Lombard J. E.. ( 2011;a). Epidemiology and economics of paratuberculosis. . Vet Clin North Am Food Anim Pract 27:, 525–535. [CrossRef][PubMed]
    [Google Scholar]
  20. Lombard J. E.. ( 2011;b). Epidemiology and economics of paratuberculosis. . Vet Clin North Am Food Anim Pract 27:, 525–535. [CrossRef][PubMed]
    [Google Scholar]
  21. Lombard J. E., Gardner I. A., Jafarzadeh S. R., Fossler C. P., Harris B., Capsel R. T., Wagner B. A., Johnson W. O.. ( 2013;). Herd-level prevalence of Mycobacterium avium subsp. paratuberculosis infection in United States dairy herds in 2007. . Prev Vet Med 108:, 234–238. [CrossRef][PubMed]
    [Google Scholar]
  22. Moss M. T., Sanderson J. D., Tizard M. L., Hermon-Taylor J., el-Zaatari F. A., Markesich D. C., Graham D. Y.. ( 1992;). Polymerase chain reaction detection of Mycobacterium paratuberculosis and Mycobacterium avium subsp silvaticum in long term cultures from Crohn’s disease and control tissues. . Gut 33:, 1209–1213. [CrossRef][PubMed]
    [Google Scholar]
  23. Nielsen S. S., Toft N.. ( 2009;). A review of prevalences of paratuberculosis in farmed animals in Europe. . Prev Vet Med 88:, 1–14. [CrossRef][PubMed]
    [Google Scholar]
  24. Perna N. T., Mayhew G. F., Pósfai G., Elliott S., Donnenberg M. S., Kaper J. B., Blattner F. R.. ( 1998;). Molecular evolution of a pathogenicity island from enterohemorrhagic Escherichia coli O157 : H7. . Infect Immun 66:, 3810–3817.[PubMed]
    [Google Scholar]
  25. Pradhan A. K., Mitchell R. M., Kramer A. J., Zurakowski M. J., Fyock T. L., Whitlock R. H., Smith J. M., Hovingh E., Van Kessel J. A. et al. ( 2011;). Molecular epidemiology of Mycobacterium avium subsp. paratuberculosis in a longitudinal study of three dairy herds. . J Clin Microbiol 49:, 893–901. [CrossRef][PubMed]
    [Google Scholar]
  26. Raizman E. A., Fetrow J. P., Wells S. J.. ( 2009;). Loss of income from cows shedding Mycobacterium avium subspecies paratuberculosis prior to calving compared with cows not shedding the organism on two Minnesota dairy farms. . J Dairy Sci 92:, 4929–4936. [CrossRef][PubMed]
    [Google Scholar]
  27. Salem M., Zeid A. A., Hassan D., El-Sayed A., Zschoeck M.. ( 2005;). Studies on Johne’s disease in Egyptian cattle. . J Vet Med B Infect Dis Vet Public Health 52:, 134–137. [CrossRef][PubMed]
    [Google Scholar]
  28. Shin S. J., Wu C.-W., Steinberg H., Talaat A. M.. ( 2006;). Identification of novel virulence determinants in Mycobacterium paratuberculosis by screening a library of insertional mutants. . Infect Immun 74:, 3825–3833. [CrossRef][PubMed]
    [Google Scholar]
  29. Shin S. J., Han J. H., Manning E. J. B., Collins M. T.. ( 2007;). Rapid and reliable method for quantification of Mycobacterium paratuberculosis by use of the BACTEC MGIT 960 system. . J Clin Microbiol 45:, 1941–1948. [CrossRef][PubMed]
    [Google Scholar]
  30. Sonawane G. G., Tripathi B. N.. ( 2013;). Comparison of a quantitative real-time polymerase chain reaction (qPCR) with conventional PCR, bacterial culture and ELISA for detection of Mycobacterium avium subsp. paratuberculosis infection in sheep showing pathology of Johne's disease. . SpringerPlus 2:, 45. [CrossRef][PubMed]
    [Google Scholar]
  31. Stabel J. R., Bosworth T. L., Kirkbride T. A., Forde R. L., Whitlock R. H.. ( 2004;). A simple, rapid, and effective method for the extraction of Mycobacterium paratuberculosis DNA from fecal samples for polymerase chain reaction. . J Vet Diagn Invest 16:, 22–30. [CrossRef][PubMed]
    [Google Scholar]
  32. Stevenson K., Hughes V. M., de Juan L., Inglis N. F., Wright F., Sharp J. M.. ( 2002;). Molecular characterization of pigmented and nonpigmented isolates of Mycobacterium avium subsp. paratuberculosis. . J Clin Microbiol 40:, 1798–1804. [CrossRef][PubMed]
    [Google Scholar]
  33. Talaat A. M., Reimschuessel R., Trucksis M.. ( 1997;). Identification of mycobacteria infecting fish to the species level using polymerase chain reaction and restriction enzyme analysis. . Vet Microbiol 58:, 229–237. [CrossRef][PubMed]
    [Google Scholar]
  34. Tamura K., Dudley J., Nei M., Kumar S.. ( 2007;). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. . Mol Biol Evol 24:, 1596–1599. [CrossRef][PubMed]
    [Google Scholar]
  35. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S.. ( 2013;). MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. . Mol Biol Evol 30:, 2725–2729. [CrossRef][PubMed]
    [Google Scholar]
  36. Wells S. J., Whitlock R. H., Lindeman C. J., Fyock T.. ( 2002;). Evaluation of bacteriologic culture of pooled fecal samples for detection of Mycobacterium paratuberculosis. . Am J Vet Res 63:, 1207–1211. [CrossRef][PubMed]
    [Google Scholar]
  37. Wells S. J., Collins M. T., Faaberg K. S., Wees C., Tavornpanich S., Petrini K. R., Collins J. E., Cernicchiaro N., Whitlock R. H.. ( 2006;). Evaluation of a rapid fecal PCR test for detection of Mycobacterium avium subsp. paratuberculosis in dairy cattle. . Clin Vaccine Immunol 13:, 1125–1130. [CrossRef][PubMed]
    [Google Scholar]
  38. Whittington R. J., Sergeant E. S. G.. ( 2001;). Progress towards understanding the spread, detection and control of Mycobacterium avium subsp paratuberculosis in animal populations. . Aust Vet J 79:, 267–278. [CrossRef][PubMed]
    [Google Scholar]
  39. Whittington R., Marsh I., Choy E., Cousins D.. ( 1998;). Polymorphisms in IS1311, an insertion sequence common to Mycobacterium avium and M. avium subsp. paratuberculosis, can be used to distinguish between and within these species. . Mol Cell Probes 12:, 349–358. [CrossRef][PubMed]
    [Google Scholar]
  40. Wu C.-W., Glasner J., Collins M. T., Naser S., Talaat A. M.. ( 2006;). Whole-genome plasticity among Mycobacterium avium subspecies: insights from comparative genomic hybridizations. . J Bacteriol 188:, 711–723. [CrossRef][PubMed]
    [Google Scholar]
  41. Wu C. W., Schmoller S. K., Shin S. J., Talaat A. M.. ( 2007;). Defining the stressome of Mycobacterium avium subsp. paratuberculosis in vitro and in naturally infected cows. . J Bacteriol 189:, 7877–7886. [CrossRef][PubMed]
    [Google Scholar]
  42. Wynne J. W., Seemann T., Bulach D. M., Coutts S. A., Talaat A. M., Michalski W. P.. ( 2010;). Resequencing the Mycobacterium avium subsp. paratuberculosis K10 genome: improved annotation and revised genome sequence. . J Bacteriol 192:, 6319–6320. [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000051
Loading
/content/journal/micro/10.1099/mic.0.000051
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error