Table of Contents Author Guidelines Submit a Manuscript
Canadian Journal of Infectious Diseases and Medical Microbiology
Volume 2016, Article ID 1462405, 8 pages
http://dx.doi.org/10.1155/2016/1462405
Research Article

Subboiling Moist Heat Favors the Selection of Enteric Pathogen Clostridium difficile PCR Ribotype 078 Spores in Food

1Division of Gastroenterology and Liver Disease, Digestive Health Research Institute, Department of Medicine, Case Western Reserve University School of Medicine, Cleveland, OH 44106, USA
2Department of Human Sciences, Human Nutrition, College of Education and Human Ecology, The Ohio State University, Columbus, OH 43210, USA
3Food Animal Health Research Program, Ohio Agricultural Research and Development Center, The Ohio State University, Wooster, OH 44691, USA

Received 29 February 2016; Accepted 26 April 2016

Academic Editor: Maria Tomás

Copyright © 2016 Alexander Rodriguez-Palacios et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. P. N. Wiegand, D. Nathwani, M. H. Wilcox, J. Stephens, A. Shelbaya, and S. Haider, “Clinical and economic burden of Clostridium difficile infection in Europe: a systematic review of healthcare-facility-acquired infection,” Journal of Hospital Infection, vol. 81, no. 1, pp. 1–14, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. T. V. Riley, “Clostridium difficile: a pathogen of the nineties,” European Journal of Clinical Microbiology and Infectious Diseases, vol. 17, no. 3, pp. 137–141, 1998. View at Google Scholar · View at Scopus
  3. Centers for Disease Control and Prevention (CDC), “Surveillance for community-associated clostridium difficile—connecticut,” Morbidity and Mortality Weekly Report (MMWR), vol. 57, no. 13, pp. 340–343, 2008. View at Google Scholar
  4. A. M. Otten, R. J. Reid-Smith, A. Fazil, and J. S. Weese, “Disease transmission model for community-associated Clostridium difficile infection,” Epidemiology and Infection, vol. 138, no. 6, pp. 907–914, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. A. Rodriguez-Palacios, H. R. Staempfli, T. Duffield, and J. S. Weese, “Clostridium difficile in retail ground meat, Canada,” Emerging Infectious Diseases, vol. 13, no. 3, pp. 485–487, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. J. G. Songer, H. T. Trinh, G. E. Killgore, A. D. Thompson, L. C. McDonald, and B. M. Limbago, “Clostridium difficile in retail meat products, USA, 2007,” Emerging Infectious Diseases, vol. 15, no. 5, pp. 819–821, 2009. View at Publisher · View at Google Scholar · View at Scopus
  7. L. C. McDonald, G. E. Killgore, A. Thompson et al., “An epidemic, toxin gene-variant strain of Clostridium difficile,” The New England Journal of Medicine, vol. 353, no. 23, pp. 2433–2441, 2005. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Rupnik, “Is Clostridium difficile-associated infection a potentially zoonotic and foodborne disease?” Clinical Microbiology and Infection, vol. 13, no. 5, pp. 457–459, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. M. Warny, J. Pepin, A. Fang et al., “Toxin production by an emerging strain of Clostridium difficile associated with outbreaks of severe disease in North America and Europe,” The Lancet, vol. 366, no. 9491, pp. 1079–1084, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. A. Goorhuis, D. Bakker, J. Corver et al., “Emergence of Clostridium difficile infection due to a new hypervirulent strain, polymerase chain reaction ribotype 078,” Clinical Infectious Diseases, vol. 47, no. 9, pp. 1162–1170, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. L. H. Gould and B. Limbago, “Clostridium difficile in food and domestic animals: a new foodborne pathogen?” Clinical Infectious Diseases, vol. 51, no. 5, pp. 577–582, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. K. Keel, J. S. Brazier, K. W. Post, S. Weese, and J. G. Songer, “Prevalence of PCR ribotypes among Clostridium difficile isolates from pigs, calves, and other species,” Journal of Clinical Microbiology, vol. 45, no. 6, pp. 1963–1964, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. M. R. Mulvey, D. A. Boyd, D. Gravel et al., “Hypervirulent Clostridium difficile strains in hospitalized patients, Canada,” Emerging Infectious Diseases, vol. 16, no. 4, pp. 678–681, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. A. Rodriguez-Palacios, H. R. Stämpfli, T. Duffield et al., “Clostridium difficile PCR ribotypes in calves, Canada,” Emerging Infectious Diseases, vol. 12, no. 11, pp. 1730–1736, 2006. View at Publisher · View at Google Scholar · View at Scopus
  15. J. S. Weese, R. J. Reid-Smith, B. P. Avery, and J. Rousseau, “Detection and characterization of Clostridium difficile in retail chicken,” Letters in Applied Microbiology, vol. 50, no. 4, pp. 362–365, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. A. Rodriguez-Palacios and J. T. LeJeune, “Moist-heat resistance, spore aging, and superdormancy in Clostridium difficile,” Applied and Environmental Microbiology, vol. 77, no. 9, pp. 3085–3091, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. United States Department of Agriculture (USDA)—Food Safety and Inspection Service, Food Safety Education—Is It Done Yet?http://www.fsis.usda.gov/wps/wcm/connect/c825bac8-c024-4793-be76-159dfb56a88f/IsItDoneYet_Brochure.pdf?MOD=AJPERES.
  18. R. B. Harvey, K. N. Norman, K. Andrews et al., “Clostridium difficile in poultry and poultry meat,” Foodborne Pathogens and Disease, vol. 8, no. 12, pp. 1321–1323, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. D. Metcalf, B. P. Avery, N. Janecko, N. Matic, R. Reid-Smith, and J. S. Weese, “Clostridium difficile in seafood and fish,” Anaerobe, vol. 17, no. 2, pp. 85–86, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. D. S. Metcalf, M. C. Costa, W. M. V. Dew, and J. S. Weese, “Clostridium difficile in vegetables, Canada,” Letters in Applied Microbiology, vol. 51, no. 5, pp. 600–602, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Rodriguez-Palacios, R. J. Reid-Smith, H. R. Staempfli, and J. S. Weese, “Clostridium difficile survives minimal temperature recommended for cooking ground meats,” Anaerobe, vol. 16, no. 5, pp. 540–542, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. D. Wultańska, H. Pituch, P. Obuch-Woszczatyński, F. Meisel-Mikołajczyk, and M. Luczak, “Comparative study of thermoresistance spores of Clostridium difficile strains belonging to different toxigenicity groups,” Medycyna doswiadczalna i mikrobiologia, vol. 56, no. 2, pp. 155–159, 2004. View at Google Scholar · View at Scopus
  23. G. K. Kozak, H. Couture, T. Gleeson et al., “Safe endpoint temperature for cooking whole raw poultry: health Canada recommendation,” Food Protection Trends, vol. 30, no. 10, pp. 580–587, 2010. View at Google Scholar
  24. V. K. Juneja, J. S. Novak, L. Huang, and B. S. Eblen, “Increased thermotolerance of Clostridium perfringens spores following sublethal heat shock,” Food Control, vol. 14, no. 3, pp. 163–168, 2002. View at Publisher · View at Google Scholar · View at Scopus
  25. E. French, A. Rodriguez-Palacios, and J. T. LeJeune, “Enteric bacterial pathogens with zoonotic potential isolated from farm-raised deer,” Foodborne Pathogens and Disease, vol. 7, no. 9, pp. 1031–1037, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. K. N. Norman, R. B. Harvey, H. M. Scott, M. E. Hume, K. Andrews, and A. D. Brawley, “Varied prevalence of Clostridium difficile in an integrated swine operation,” Anaerobe, vol. 15, no. 6, pp. 256–260, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Rodriguez-Palacios, M. Koohmaraie, and J. T. LeJeune, “Prevalence, enumeration, and antimicrobial agent resistance of Clostridium difficile in cattle at harvest in the United States,” Journal of Food Protection, vol. 74, no. 10, pp. 1618–1624, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. A. Rodriguez-Palacios, C. Pickworth, S. Loerch, and J. T. LeJeune, “Transient fecal shedding and limited animal-to-animal transmission of Clostridium difficile by naturally infected finishing feedlot cattle,” Applied and Environmental Microbiology, vol. 77, no. 10, pp. 3391–3397, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. R. D. Rolfe and S. M. Finegold, “Purification and characterization of Clostridium difficile toxin,” Infection and Immunity, vol. 25, no. 1, pp. 191–201, 1979. View at Google Scholar · View at Scopus
  30. P. Bidet, F. Barbut, V. Lalande, B. Burghoffer, and J.-C. Petit, “Development of a new PCR-ribotyping method for Clostridium difficile based on ribosomal RNA gene sequencing,” FEMS Microbiology Letters, vol. 175, no. 2, pp. 261–266, 1999. View at Publisher · View at Google Scholar · View at Scopus
  31. UCLA, Multinomial Logistic Regression. UCLA: Academic Technology Services, Statistical Consulting Group, http://www.ats.ucla.edu/stat/stata/dae/mlogit.htm.
  32. V. K. Juneja, “A comparative heat inactivation study of indigenous microflora in beef with that of Listeria monocytogenes, Salmonella serotypes and Escherichia coli O157:H7,” Letters in Applied Microbiology, vol. 37, no. 4, pp. 292–298, 2003. View at Publisher · View at Google Scholar · View at Scopus
  33. A. Rodriguez-Palacios, S. Borgmann, T. R. Kline, and J. T. LeJeune, “Clostridium difficile in foods and animals: history and measures to reduce exposure,” Animal Health Research Reviews, vol. 14, no. 1, pp. 11–29, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. A. Rodriguez-Palacios, S. Ilic, and J. T. LeJeune, “Clostridium difficile with moxifloxacin/clindamycin resistance in vegetables in Ohio, USA, and prevalence meta-analysis,” Journal of Pathogens, vol. 2014, Article ID 158601, 7 pages, 2014. View at Publisher · View at Google Scholar
  35. D. G. Hoover and A. Rodriguez-Palacios, “Transmission of Clostridium difficile in foods,” Infectious Disease Clinics of North America, vol. 27, no. 3, pp. 675–685, 2013. View at Publisher · View at Google Scholar · View at Scopus
  36. A. Rodriguez-Palacios, R. J. Reid-Smith, H. R. Staempfli et al., “Possible seasonality of Clostridium difficile in retail meat, Canada,” Emerging Infectious Diseases, vol. 15, no. 5, pp. 802–805, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. D. M. Wolf, L. Fontaine-Bodin, I. Bischofs, G. Price, J. Keasling, and A. P. Arkin, “Memory in microbes: quantifying history-dependent behavior in a bacterium,” PLoS ONE, vol. 3, no. 2, Article ID e1700, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. L. Huang and V. K. Juneja, “Thermal inactivation of Escherichia coli O157:H7 in ground beef supplemented with sodium lactate,” Journal of Food Protection, vol. 66, no. 4, pp. 664–667, 2003. View at Google Scholar · View at Scopus
  39. K. M. Wiegand, S. C. Ingham, and B. H. Ingham, “Evaluating lethality of beef roast cooking treatments against Escherichia coli O157:H7,” Journal of Food Protection, vol. 75, no. 1, pp. 48–61, 2012. View at Publisher · View at Google Scholar
  40. A. E. I. de Jong, E. D. van Asselt, M. H. Zwietering, M. J. Nauta, and R. de Jonge, “Extreme heat resistance of food borne pathogens Campylobacter jejuni, Escherichia coli, and Salmonella typhimurium on chicken breast fillet during cooking,” International Journal of Microbiology, vol. 2012, Article ID 196841, 10 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Ghosh, P. Zhang, Y.-Q. Li, and P. Setlow, “Superdormant spores of Bacillus species have elevated wet-heat resistance and temperature requirements for heat activation,” Journal of Bacteriology, vol. 191, no. 18, pp. 5584–5591, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. E. Alfano-Sobsey, D. Sweat, A. Hall et al., “Norovirus outbreak associated with undercooked oysters and secondary household transmission,” Epidemiology and Infection, vol. 140, no. 2, pp. 276–282, 2012. View at Publisher · View at Google Scholar · View at Scopus
  43. E. Barnaud, S. Rogée, P. Garry, N. Rose, and N. Pavio, “Thermal inactivation of infectious hepatitis E virus in experimentally contaminated food,” Applied and Environmental Microbiology, vol. 78, no. 15, pp. 5153–5159, 2012. View at Publisher · View at Google Scholar · View at Scopus
  44. CDC. Centers for Disease Control and Prevention (CDC), “Surveillance for foodborne disease outbreaks—United States, 2006,” Morbidity and Mortality Weekly Report, vol. 58, pp. 609–615, 2009. View at Google Scholar
  45. L. E. Cowen and S. Lindquist, “Hsp90 potentiates the rapid evolution of new traits: drug resistance in diverse fungi,” Science, vol. 309, no. 5744, pp. 2185–2189, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. T. D. Lawley, S. Clare, A. W. Walker et al., “Antibiotic treatment of Clostridium difficile carrier mice triggers a supershedder state, spore-mediated transmission, and severe disease in immunocompromised hosts,” Infection and Immunity, vol. 77, no. 9, pp. 3661–3669, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. A. K. Sethi, W. N. Al-Nassir, M. M. Nerandzic, G. S. Bobulsky, and C. J. Donskey, “Persistence of skin contamination and environmental shedding of Clostridium difficile during and after treatment of C. difficile infection,” Infection Control and Hospital Epidemiology, vol. 31, no. 1, pp. 21–27, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. M. J. Alfa, N. Olson, and L. Buelow-Smith, “Simulated-use testing of bedpan and urinal washer disinfectors: evaluation of Clostridium difficile spore survival and cleaning efficacy,” American Journal of Infection Control, vol. 36, no. 1, pp. 5–11, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. C. P. Gerba, I. L. Pepper, and L. F. Whitehead III, “A risk assessment of emerging pathogens of concern in the land application of biosolids,” Water Science and Technology, vol. 46, no. 10, pp. 225–230, 2002. View at Google Scholar · View at Scopus
  50. R. N. Carmody, G. S. Weintraub, and R. W. Wrangham, “Energetic consequences of thermal and nonthermal food processing,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 48, pp. 19199–19203, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. R. N. Carmody and R. W. Wrangham, “The energetic significance of cooking,” Journal of Human Evolution, vol. 57, no. 4, pp. 379–391, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. R. W. Wrangham, J. H. Jones, G. Laden, D. Pilbeam, and N. Conklin-Brittain, “The raw and the stolen. Cooking and the ecology of human origins,” Current Anthropology, vol. 40, no. 5, pp. 567–594, 1999. View at Publisher · View at Google Scholar
  53. M. Visser, S. Sephri, N. Olson, T. Du, M. R. Mulvey, and M. J. Alfa, “Detection of Clostridium difficile in retail ground meat products in Manitoba,” Canadian Journal of Infectious Diseases and Medical Microbiology, vol. 23, no. 4, pp. 28–30, 2012. View at Publisher · View at Google Scholar
  54. A. N. Jassem, N. Prystajecky, F. Marra et al., “Characterization of Clostridium difficile strains in British Columbia, Canada: a shift from NAP1 majority (2008) to novel strain types (2013) in one region,” Canadian Journal of Infectious Diseases and Medical Microbiology, vol. 2016, Article ID 8207418, 8 pages, 2016. View at Publisher · View at Google Scholar