Quantitative transfer of escherichia coli O157: H7 To equipment during small-scale production of fresh-cut leafy greens

Journal of Food Protection

Volumn 75, Issue 7, 2012, Pages 1184-1197

  Buchholz, Annemarie L ^a   Davidson, Gordon R ^a   Marks, Bradley P ^b   Todd, Ewen C D ^c   Ryser, Elliot T ^a  

^a Michigan State University   (United States)

^b Michigan State University   (United States)

^c MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESCHERICHIA COLI; LACTUCA; SPINACIA OLERACEA;

EID: 84863834265     PISSN: 0362028X     EISSN: None     Source Type: Journal    
DOI: 10.4315/0362-028X.JFP-11-489     Document Type: Article

References (63)

1. Beuchat, L. R. 1996. Pathogenic microorganisms associated with fresh produce. J. Food Prot. 59:204-216.
2. Beuchat, L. R. 2002. Ecological factors influencing survival and growth of human pathogens on raw fruits and vegetables. Microbiol. Infect. 4:413-423. (Pubitemid 34270678)
3. Beuchat, L. R., B. B. Adler, and M. M. Lang. 2004. Efficacy of chlorine and a peroxyacetic acid sanitizer in killing Listeria monocytogenes on iceberg and Romaine lettuce using simulated commercial processing conditions. J. Food Prot. 67:1238-1242. (Pubitemid 38751898)
4. Beuchat, L. R., and J. H. Ryu. 1997. Produce handling and processing practices. Emerg. Infect. Dis. 3:459-465. (Pubitemid 127431712)
5. Burnett, A. B., M. H. Iturriaga, E. F. Escartin, C. A. Pettigrew, and L. R. Beuchat. 2004. Influence of variations in methodology on populations of Listeria monocytogenes recovered from lettuce treated with sanitizers. J. Food Prot. 67:742-750. (Pubitemid 38453964)
6. Burnett, S. L., and L. R. Beuchat. 2001. Human pathogens associated with raw produce and unpasteurized juices, and difficulties in decontamination. J. Ind. Microbiol. Biotechnol. 27:104-110. (Pubitemid 33702310)
7. Carmichael, I., I. S. Harper, M. J. Coventry, P. W. J. Taylor, J. Wan, and M. W. Hickey. 1999. Bacterial colonization and biofilm development on minimally processed vegetables. J. Appl. Microbiol. 85:45S-51S. (Pubitemid 29296560)
8. Center for Science in the Public Interest. 2008. CSPI outbreak alert data: Info on produce outbreaks. Available at: Http://www.cspinet.org/new/pdf/ cspi-outbreak-alert.pdf. Accessed 26 May 2011.
9. Center for Science in the Public Interest. 2008. Outbreak alert! 2008. Available at: Http://www.cspinet.org/new/pdf/outbreak-alert-2008-report-final. pdf. Accessed 26 May 2011.
10. Center for Science in the Public Interest. 2009. The ten riskiest foods regulated by the US Food and Drug Administration. Available at: Http://cspinet.org/new/pdf/cspi-top-10-fda.pdf. Accessed 26 May 2011.
11. Chai, L. C., H. Y. Lee, F. M. Ghazali, F. Abu Bakar, P. K. Malakar, M. Nishibuchi, Y. Nakaguchi, and S. Radu. 2008. Simulation of cross-contamination and decontamination of Campylobacter jejuni during handling of contaminated raw vegetables in a domestic kitchen. J. Food Prot. 71:2448-2452.
12. Chase-Topping, M. E., I. J. McKendrick, M. C. Pearce, P. MacDonald, L. Matthews, J. Halliday, L. Allison, D. Fenlon, J. C. Low, G. Gunn, and M. E. Woolhouse. 2007. Risk factors for the presence of high-level shedders of Escherichia coli O157 on Scottish farms. J. Clin. Microbiol. 45:1594-1603. (Pubitemid 46766515)
13. Chen, Y., K. M. Jackson, F. P. Chea, and D. W. Schaffner. 2001. Quantification and variability analysis of bacterial cross-contamination rates in common food service tasks. J. Food Prot. 64:72-80. (Pubitemid 32102896)
14. Davis, H., J. P. Taylor, J. N. Perdue, G. N. Stelma, Jr., J. M. Humphreys, Jr., R. Rowntree III, and K. D. Greene. 1988. A shigellosis outbreak traced to commercially distributed, shredded lettuce. Am. J. Epidemiol. 128:1312-1321. (Pubitemid 19015503)
15. Doyle, M. P., and M. C. Erickson. 2008. Summer meeting 2007-the problems with fresh produce: An overview. J. Appl. Microbiol. 105: 317-330. (Pubitemid 351989429)
16. Farrell, B. L., A. B. Ronner, and A. C. Wong. 1998. Attachment of Escherichia coli O157:H7 in ground beef to meat grinders and survival after sanitation with chlorine and peroxyacetic acid. J. Food Prot. 61:817-822. (Pubitemid 28348601)
17. Fett, W. F. 2000. Naturally occurring biofilms on alfalfa and other types of sprouts. J. Food Prot. 63:625-632. (Pubitemid 30259710)
18. Flores, R. A., and T. E. Stewart. 2004. Empirical distribution models for Escherichia coli O157:H7 in ground beef produced by a mid-size commercial grinder. J. Food Sci. 69:121-126.
19. Flores, R. A., and M. L. Tamplin. 2002. Distribution patterns of Escherichia coli O157:H7 in ground beef produced by a laboratoryscale grinder. J. Food Prot. 65:1894-1902. (Pubitemid 36017020)
20. Fravalo, P., M. J. Laisney, M. O. Gillard, G. Salvat, and M. Chemaly. 2009. Campylobacter transfer from naturally contaminated chicken thighs to cutting boards is inversely related to initial load. J. Food Prot. 72:1836-1840.
21. Friesema, I., G. Sigmundsdottir, K. van der Zwaluw, A. Heuvelink, B. Schimmer, C. de Jager, B. Rump, H. Briem, H. Hardardottir, A. Atladottir, E. Gudmundsdottir, and W. van Pelt. 2008. An international outbreak of Shiga toxin-producing Escherichia coli O157 infection due to lettuce, September-October 2007. Euro. Surveill. 13:19065.
22. Gill, C. O., and T. Jones. 2002. Effects of wearing knitted or rubber gloves on the transfer of Escherichia coli between hands and meat. J. Food Prot. 65:1045-1048. (Pubitemid 34609272)
23. Gorny, J. R. 2006. Microbial contamination of fruits and vegetables, p. 3-32. In G. M. Sapers, J. R. Gorny, and A. E. Yousef (ed.), Microbiology of fruits and vegetables. CRC Press, Boca Raton, FL.
24. Herman, K. M., T. L. Ayers, and M. Lynch. 2008. Foodborne disease outbreaks associated with leafy greens, 1973-2006. International Conference on Emerging Infectious Diseases 2008 slide sessions and poster abstracts. Available at: Http://www.cdc.gov/eid/content/14/3/ ICEID2008.pdf. Accessed 26 May 2011.
25. Hill, V. R., A. L. Polaczyk, D. Hahn, J. Narayanan, T. L. Cromeans, J. M. Roberts, and J. E. Amburgey. 2005. Development of a rapid method for simultaneous recovery of diverse microbes in drinking water by ultrafiltration with sodium polyphosphate and surfactants. Appl. Environ. Microbiol. 71:6878-6884. (Pubitemid 43194177)
26. Ibekwe, A. M., P. M. Watt, P. J. Shouse, and C. M. Grieve. 2004. Fate of Escherichia coli O157:H7 in irrigation water on soils and plants as validated by culture method and real-time PCR. Can. J. Microbiol. 50:1007-1014.
27. Jackson, D. W., K. Suzuki, L. Oakford, J. W. Simecka, M. E. Hart, and T. Romeo. 2002. Biofilm formation and dispersal under the influence of the global regulator CsrA of Escherichia coli. J. Bacteriol. 184:290-301. (Pubitemid 34003309)
28. Jay, M. T., M. Cooley, D. Carychao, G. W. Wiscomb, R. A. Sweitzer, L. Crawford-Miksza, J. A. Farrar, D. K. Lau, J. O'Connell, A. Millington, R. V. Asmundson, E. R. Atwill, and R. E. Mandrell. 2007. Escherichia coli O157:H7 in feral swine near spinach fields and cattle, central California coast. Emerg. Infect. Dis. 13:1908-1911. (Pubitemid 350248495)
29. Jiménez, S. M., M. C. Tiburzi, M. S. Salsi, M. A. Moguilevsky, and M. E. Pirovani. 2009. Survival of Salmonella on refrigerated chicken carcasses and subsequent transfer to cutting board. Lett. Appl. Microbiol. 48:687-691.
30. Kaneko, K., H. Hayashidani, K. Takahashi, Y. Shiraki, S. Limawongpranee, and M. Ogawa. 1999. Bacterial contamination in the environment of food factories processing ready-to-eat fresh vegetables. J. Food Prot. 62:800-804. (Pubitemid 29324231)
31. Keskinen, L. A., A. M. Burke, and B. A. Annous. 2009. Efficacy of chlorine, acidic electrolyzed water and aqueous chlorine dioxide solutions to decontaminate Escherichia coli O157:H7 from lettuce leaves. Int. J. Food Microbiol. 132:134-140.
32. Keskinen, L. A., E. C. Todd, and E. T. Ryser. 2008. Impact of bacterial stress and biofilm-forming ability on transfer of surfacedried Listeria monocytogenes during slicing of delicatessen meats. Int. J. Food Microbiol. 127:298-304.
33. Keskinen, L. A., E. C. Todd, and E. T. Ryser. 2008. Transfer of surface-dried Listeria monocytogenes from stainless steel knife blades to roast turkey breast. J. Food Prot. 71:176-181.
34. Lang, M. M., L. J. Harris, and L. R. Beuchat. 2004. Survival and recovery of Escherichia coli O157:H7, Salmonella, and Listeria monocytogenes on lettuce and parsley as affected by method of inoculation, time between inoculation and analysis, and treatment with chlorinated water. J. Food Prot. 67:1092-1103. (Pubitemid 38751874)
35. Lin, C. M., K. Takeuchi, L. Zhang, C. B. Dohm, J. D. Meyer, P. A. Hall, and M. P. Doyle. 2006. Cross-contamination between processing equipment and deli meats by Listeria monocytogenes. J. Food Prot. 69:71-79. (Pubitemid 43132522)
36. Low, J. C., I. J. McKendrick, C. McKechnie, D. Fenlon, S. W. Naylor, C. Currie, D. G. Smith, L. Allison, and D. L. Gally. 2005. Rectal carriage of enterohemorrhagic Escherichia coli O157 in slaughtered cattle. Appl. Environ. Microbiol. 71:93-97. (Pubitemid 40116255)
37. Meng, J., M. P. Doyle, T. Zhao, and S. Zhao. 2007. Enterohemorrhagic Escherichia coli, p. 260. In M. P. Doyle and L. R. Beuchat (ed.), Food microbiology: Fundamentals and frontiers, 3rd ed. ASM Press, Washington, DC.
38. Montville, R., Y. Chen, and D. W. Schaffner. 2001. Glove barriers to bacterial cross-contamination between hands to food. J. Food Prot. 64:845-849. (Pubitemid 32532749)
39. Montville, R., and D. W. Schaffner. 2003. Inoculum size influences bacterial cross contamination between surfaces. Appl. Environ. Microbiol. 69:7188-7193. (Pubitemid 38585368)
40. Moore, C. M., B. W. Sheldon, and L. A. Jaykus. 2003. Transfer of Salmonella and Campylobacter from stainless steel to Romaine lettuce. J. Food Prot. 66:2231-2236. (Pubitemid 37507057)
41. Morales-Morales, H. A., G. Vidal, J. Olszewski, C. M. Rock, D. Dasgupta, K. H. Oshima, and G. B. Smith. 2003. Optimization of a reusable hollow-fiber ultrafilter for simultaneous concentration of enteric bacteria, protozoa, and viruses from water. Appl. Environ. Microbiol. 69:4098-4102. (Pubitemid 36870070)
42. Pérez Rodriǵuez, F., D. Campos, E. T. Ryser, A. M. Buchholz, B. P. Marks, Z. Gonzalo, and E. C. D. Todd. 2011. A mathematical risk model for Escherichia coli O157:H7 cross-contamination of lettuce during processing. Food Microbiol. 28:694-701.
43. Ravishankar, S., L. Zhu, and D. Jaroni. 2010. Assessing the cross contamination and transfer rates of Salmonella enterica from chicken to lettuce under different food-handling scenarios. Food Microbiol. 7: 791-794.
44. Sapers, G. M. 2001. Efficacy of washing and sanitizing methods for disinfection of fresh fruit and vegetable products. Food Technol. Biotechnol. 39:305-311. (Pubitemid 33671358)
45. Sapers, G. M. 2006. Washing and sanitizing treatments for fruits and vegetables, p. 375-400. In G. M. Sapers, J. R. Gorny, and A. E. Yousef (ed.), Microbiology of fruits and vegetables. CRC Press, Boca Raton, FL.
46. Scott, E., and S. F. Bloomfield. 1990. The survival and transfer of microbial contamination via cloths, hands and utensils. J. Appl. Bacteriol. 68:271-278. (Pubitemid 20241417)
47. Seo, K. H., and J. F. Frank. 1999. Attachment of Escherichia coli O157:H7 to lettuce leaf surface and bacterial viability in response to chlorine treatment as demonstrated by using confocal scanning laser microscopy. J. Food Prot. 62:3-9. (Pubitemid 29051802)
48. Sheen, S., and C. A. Hwang. 2008. Modeling transfer of Listeria monocytogenes from slicer to deli meat during mechanical slicing. Foodborne Pathog. Dis. 5:135-146. (Pubitemid 351535858)
49. Stafford, R. J, B. J. McCall, A. S. Neill, D. S. Leon, G. J. Dorricott, C. D. Towner, and G. R. Micalizzi. 2002. A statewide outbreak of Salmonella Bovismorbificans phage type 32 infection in Queensland. Commun. Dis. Intell. 26:568-573.
50. Takeuchi, K., and J. F. Frank. 2000. Penetration of Escherichia coli O157:H7 into lettuce tissues as affected by inoculum size and temperature and the effect of chlorine treatment on cell viability. J. Food Prot. 63:434-440. (Pubitemid 30208693)
51. Taormina, P. J., L. R. Beuchat, M. C. Erickson, L. Ma, G. Zhang, and M. P. Doyle. 2009. Transfer of Escherichia coli O157:H7 to iceberg lettuce via simulated field coring. J. Food Prot. 72:465-472.
52. U.S. Department of Health and Human Services and U.S. Department of Agriculture. 2005. Dietary guidelines for Americans, 6th ed. U.S. Government Printing Office, Washington, DC.
53. U.S. Food and Drug Administration. 2006. Update: FDA narrows investigation of E. coli O157:H7 outbreak at Taco Bell restaurants. Available at: Http://www.fda.gov/NewsEvents/Newsroom/Press Announcements/2006/ucm108803. htm. Accessed 26 May 2011.
54. U.S. Food and Drug Administration. 2007. FDA and states closer to identifying source of E. coli contamination associated with illness at Taco John's restaurants. Available at: Http://www.fda.gov/NewsEvents/ Newsroom/PressAnnouncements/2007/ucm108827.htm. Accessed 26 May 2011.
55. U.S. Food and Drug Administration. 2009. Guidance for industry: Guide to minimize microbial food safety hazards of leafy greens; draft guidance. Available at: Http://www.fda.gov/Food/Guidance ComplianceRegulatoryInformation/ GuidanceDocuments/Produceand PlanProducts/ucm174200.htm#post. Accessed 26 May 2011.
56. U.S. Food and Drug Administration. 2010. Fresh Express announces precautionary recall of a limited number of cases of Veggie Lovers salad with an expiration date of August 10 due to a possible health risk. Available at: Http://www.fda.gov/Safety/Recalls/ucm221943. htm. Accessed 26 May 2011.
57. U.S. Food and Drug Administration. 2010. Fresh Express announces recall of expired Romaine lettuce products with use-by dates of July 8 to 12 and "S" in the product code due to possible health risk. Available at: Http://www.fda.gov/Safety/Recalls/ucm219057.htm. Accessed 26 May 2011.
58. U.S. Food and Drug Administration. 2010. Fresh Express recalls Romaine-based salads with use-by dates of May 13-16th due to possible health risk. Available at: Http://www.fda.gov/Safety/Recalls/ ucm213247.htm. Accessed 26 May 2011.
59. Vorst, K. L., E. C. D. Todd, and E. T. Ryser. 2004. Improved quantitative recovery of Listeria monocytogenes from stainless steel surfaces using a one-ply composite tissue. J. Food Prot. 67:2212-2217. (Pubitemid 39408834)
60. Vorst, K. L., E. C. D. Todd, and E. T. Ryser. 2006. Transfer of Listeria monocytogenes during mechanical slicing of turkey breast, bologna, and salami. J. Food Prot. 69:619-626.
61. Wachtel, M. R., L. C. Whitehand, and R. E. Mandrell. 2002. Association of Escherichia coli O157:H7 with preharvest leaf lettuce on exposure to contaminated irrigation water. J. Food Prot. 65:18-25. (Pubitemid 34108153)
62. Weissinger, W. R., W. Chantarapanont, and L. R. Beuchat. 2000. Survival and growth of Salmonella baildon in shredded lettuce and diced tomatoes, and effectiveness of chlorinated water as a sanitizer. Int. J. Food Microbiol. 62:123-131.
63. Zhang, G., L. Ma, V. H. Phelan, and M. P. Doyle. 2009. Efficacy of antimicrobial agents in lettuce leaf processing water for control of Escherichia coli O157:H7. J. Food Prot. 72:1392-1397.