Survival of acid-adapted or nonadapted Escherichia coli O157:H7 in apple wounds and surrounding tissue following chemical treatments and storage

International Journal of Food Microbiology

Volumn 90, Issue 1, 2004, Pages 51-61

  Stopforth, Jarret D ^a   Ikeda, Jack S ^a,b   Kendall, Patricia A ^a   Sofos, John N ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Acid adaptation; Apple wounds; Chemical treatment; Escherichia coli; O157:H7

Indexed keywords

ACETIC ACID; AGAR; GREEN FLUORESCENT PROTEIN; HYDROGEN PEROXIDE; HYPOCHLORITE SODIUM; RIFAMPICIN; TOPICAL ANTIINFECTIVE AGENT; WATER;

ADAPTATION; ANTIBIOTIC RESISTANCE; APPLE; ARTICLE; BACTERIAL COUNT; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL SURVIVAL; COMPARATIVE STUDY; DISINFECTION; DRUG EFFECT; ESCHERICHIA COLI; ESCHERICHIA COLI O157; FOOD CONTROL; FOOD PRESERVATION; FRUIT STORAGE; GROWTH, DEVELOPMENT AND AGING; INOCULATION; METHODOLOGY; MICROBIOLOGY; NONHUMAN; PATHOGENESIS; PH; SAMPLING; SOYBEAN; TEMPERATURE; TIME;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MALUS X DOMESTICA;

EID: 0346220377     PISSN: 01681605     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0168-1605(03)00171-5     Document Type: Article

References (56)

1. Abdul-Raouf U.M., Beuchat L.R., Ammar M.S. Survival and growth of Escherichia coli O157:H7 on salad vegetables. Applied and Environmental Microbiology. 59:1993;1999-2006.
2. Ackers M.-L., Mahon B.E., Leahy E., Goode B., Damrow T., Hayes P.S., Bibb W.F., Rice D.H., Barrett T.J., Hutwagner L., Griffin P.M., Slutsker L. An outbreak of Escherichia coli O157:H7 infections associated with leaf lettuce consumption. Journal of Infectious Diseases. 177:1998;1588-1593.
3. Annous B.A., Sapers G.M., Mattrazzo A.M., Riordan D.C.R. Efficacy of washing with a commercial flatbed brush washer, using conventional and experimental washing agents, in reducing populations of Escherichia coli on artificially inoculated apples. Journal of Food Protection. 64:2001;159-163.
4. Arnold K.W., Kaspar C.W. Starvation- and stationary-phase-induced acid tolerance in Escherchia coli O157:H7. Applied and Environmental Microbiology. 61:1995;2037-2039.
5. Behrsing J., Winkler S., Franz P., Premier R. Efficacy of chlorine for inactivation of Escherichia coli on vegetables. Postharvest Biology and Technology. 19:2000;187-192.
6. Benjamin M.M., Datta A.R. Acid tolerance of enterohemorrhagic Escherichia coli. Applied and Environmental Microbiology. 61:1995;1669-1672.
7. Berry E.D., Cutter C.N. Effects of acid adaptation of Escherchia coli O157:H7 on efficacy of acetic acid spray washes to decontaminate beef carcass tissue. Applied Environmental Microbiology. 66:2000;1493-1498.
8. Besser R.E., Lett S.M., Weber J.T., Doyle M.P., Barrett T.J., Wells J.G., Griffin P.M. An outbreak of diarrhea and hemolytic uremic syndrome from Escherichia coli O157:H7 in fresh-pressed cider. Journal of American Medical Association. 269:1993;2217-2220.
9. Beuchat L.R. Pathogenic microorganisms associated with fresh produce. Journal of Food Protection. 59:1996;204-206.
10. Beuchat L.R., Nail B.V., Adler B.B., Clavero M.R.S. Efficacy of spray application of chlorinated water in killing pathogenic bacteria on raw apples, tomatoes, and lettuce. Journal of Food Protection. 61:1998;1305-1311.
11. Buchanan R.L., Edelson S.G. Culturing enterohemorrhagic Escherichia coli in the presence and absence of glucose as a simple means of evaluating the acid tolerance of stationary-phase cells. Applied and Environmental Microbiology. 62:1996;4009-4013.
12. Buchanan R.L., Edelson S.G., Miller R.L., Sapers G.M. Contamination of intact apples after immersion in an aqueous environment containing Escherichia coli O157:H7. Journal of Food Protection. 62:1999;444-450.
13. Burnett S.L., Beuchat L.R. Differentiation of viable and dead Escherichia coli O157:H7 cells on and in apple structures and tissues following chlorine treatment. Journal of Food Protection. 65:2002;251-259.
14. Burnett S.L., Chen J., Beuchat L.R. Attachment of Escherichia coli O157:H7 to the surfaces and internal structures of apples as detected by confocal scanning laser microscopy. Applied and Environmental Microbiology. 66:2000;4679-4687.
15. CDC (Centers for Disease Control and Prevention) Outbreak of E. coli O157:H7 infections associated with drinking unpasteurized commercial apple juice - October 1996. Morbidity and Mortality Weekly Report. 45:1996;975.
16. CDC (Centers for Disease Control and Prevention) Outbreaks of Escherichia coli O157:H7 infection and cryptosporidiosis associated with drinking unpasteurized apple cider - Connecticut and New York, October 1996. Morbidity and Mortality Weekly Report. 46:1997;4-8.
17. CFR (Code of Federal Regulations) Chemicals used in washing or to assist in the peeling of fruits and vegetables. (21 CFR 173.315) Code of Federal Regulations, Title 21. 1999;Office of Federal Register, U.S. Government Printing Office, Washington, DC.
18. CFR (Code of Federal Regulations) Hydrogen peroxide. (21 CFR 184.1366) Code of Federal Regulations, Title 21. 1999;Office of Federal Register, U.S. Government Printing Office, Washington, DC.
19. Cherry J.P. Improving the safety of fresh produce with antimicrobials. Food Technology. 53:1999;54-59.
20. Del Rosario B.A., Beuchat L.R. Survival and growth of enterohemorrhagic Escherichia coli O157:H7 in cantaloupe and watermelon. Journal of Food Protection. 58:1995;105-107.
21. Dingman D.W. Growth of Escherichia coli O157:H7 in bruised apple (Malus domestica) tissue as influenced by cultivar, date of harvest, and source. Applied and Environmental Microbiology. 66:2000;1077-1083.
22. Doores S. Food Safety: Current Status and Future Needs. 1999;American Academy of Microbiology, Washington, DC.
23. Elder R.O., Keen J.E., Siragusa G.R., Barkocy-Gallagher G.A., Koohmarie M., Laegreid W.W. Correlation of enterohemorrhagic Escherichia coli O157:H7 prevalence in feces, hides, and carcasses of beef cattle during processing. Proceedings of the National Academy of Sciences. 97:2000;2999-3003.
24. FDA (Food and Drug Administration) Hazard analysis and critical control point (HACCP); procedures for the safe and sanitary processing and importing of juice. Federal Register. 63:1998;20450-20486.
25. Fleischman G.J., Bator C., Merker R., Keller S.E. Hot water immersion to eliminate Escherichia coli O157:H7 on the surface of whole apples: thermal effects and efficacy. Journal of Food Protection. 64:2001;451-455.
26. Foster J.W., Hall H.K. Adaptive acidification tolerance response of Salmonella typhimurium. Journal of Bacteriology. 172:1990;771-778.
27. Janisiewicz W.J., Conway W.S., Brown M.W., Sapers G.M., Fratamico P., Buchanan R.L. Fate of Escherichia coli O157:H7 on fresh-cut apple tissue and its potential for transmission by fruit flies. Applied and Environmental Microbiology. 65:1999;1-5.
28. Janisiewicz W.J., Conway W.S., Leverentz B. Biological control of postharvest decays of apple can prevent growth of Escherichia coli O157:H7 in apple wounds. Journal of Food Protection. 62:1999;1372-1375.
29. Jolivet-Gougeon A., Braux A.S., Sauvager F., Arturo-Schaan M., Cormier M. Influence of peracetic acid on Escherichia coli H10407 strain in laboratory microcosms. Canadian Journal of Microbiology. 42:1996;60-65.
30. Karapinar M., Gonul S.A. Removal of Yersinia enterocolitica from fresh parsley by washing with acetic acid or vinegar. International Journal of Food Microbiology. 16:1992;261-264.
31. Lang M.M., Ingham S.C., Ingham B.H. Verifying apple cider plant sanitation and hazard analysis critical control point programs: choice of indicator bacteria and testing methods. Journal of Food Protection. 62:1999;887-893.
32. Leyer G.J., Wang L.-L., Johnson E.A. Acid adaptation of Escherichia coli O157:H7 increases survival in acidic foods. Applied and Environmental Microbiology. 61:1995;3752-3755.
33. Liao C.-H., Sapers G.M. Attachment and growth of Salmonella Chester on apple fruits and in vivo response of attached bacteria to sanitizer treatments. Journal of Food Protection. 63:2000;876-883.
34. Lin C.-M., Kim J., Du W.-X., Wei C.-I. Bactericidal acitivity of isothiocyanate against pathogens on fresh produce. Journal of Food Protection. 63:2000;25-30.
35. Marriott N.G. Principles of Food Sanitation. 3rd ed. 1994;Chapman & Hall, New York.
36. McLellan M.R., Splittstoesser D.F. Reducing risk of E. coli in apple cider. Food Technology. 50:1996;174.
37. Mead P.S., Slutsker L., Dietz V., McCaig L.F., Bresee J.S., Shapiro S., Griffin P.M., Tauxe R.V. Food-related illness and death in the United States. Emerging Infectious Diseases. 5:1999;607-625.
38. Miller L.G., Kaspar C.W. Escherichia coli O157:H7 acid tolerance and survival in apple cider. Journal of Food Protection. 57:1994;460-464.
39. NACMCF (National Advisory Committee on Microbiological Criteria for Foods) Recommendations for Controlling the Transmission of Pathogenic Microorganisms in Juices. 1997;USDA Food Safety and Inspection Services, Washington, DC.
40. Park S., Worobo R.W., Durst R.A. Escherichia coli O157:H7 as an emerging foodborne pathogen: a literature review. Critical Reviews in Food Science and Nutrition. 39:1999;481-502.
41. Peters, D.L., 1995. Control of enteric pathogenic bacteria on fresh produce. MS thesis, University of Nebraska.
42. Riordan D.C.R., Sapers G.M., Annous B.A. The survival of Escherichia coli O157:H7 in the presence of Penicillium expansum and Glomerella cingulata in wounds on apple surfaces. Journal of Food Protection. 63:2000;1637-1642.
43. Samelis J., Sofos J.N., Kendall P.A., Smith G.C. Effect of acid adaptation on survival of Escherichia coli O157:H7 in meat decontamination washing fluids and potential effects of organic acid interventions on the microbial ecology of the meat plant environment. Journal of Food Protection. 65:2002;33-40.
44. Sapers G.M., Simmons G.F. Hydrogen peroxide disinfection of minimally processed fruits and vegetables. Food Technology. 52:1998;48-52.
45. Sapers G.M., Miller R.L., Mattrazzo A.M. Effectiveness of sanitizing agents in inactivating Escherichia coli in golden delicious apples. Journal of Food Science. 64:1999;734-737.
46. Sapers G.M., Miller R.L., Jantschke M., Mattrazzo A.M. Factors limiting the efficacy of hydrogen peroxide washes for decontamination of apples containing Escherichia coli. Journal of Food Science. 65:2000;529-532.
47. SAS Institute, 2001. SAS/STAT® User's Guide, SAS system, Version 8.2. SAS Institute, Cary, NC.
48. Suarez A., Güttler A., Strätz M., Staendner L.H., Timmis K.N., Guzmán C.A. Green fluorescent protein-based reporter systems for genetic analysis of bacteria including monocopy applications. Gene. 196:1997;69-74.
49. Takeuchi K., Frank J.F. Quantitative determination of the role of lettuce leaf structures in protecting Escherichia coli O157:H7 from chlorine disinfection. Journal of Food Protection. 64:2001;147-151.
50. Tauxe R., Kruse H., Hedberg C., Potter M., Madden J., Wachsmuth K. Microbial hazards and emerging issues associated with produce: a preliminary report to the National Advisory Committee on Microbiologic Criteria for Foods. Journal of Food Protection. 60:1997;1400-1408.
51. Waterman S.R., Small P.L.C. Acid-sensitive enteric pathogens are protected from killing under extremely acidic conditions of pH 2.5 when they are inoculated onto certain solid food sources. Applied and Environmental Microbiology. 64:1998;3882-3886.
52. Wisniewsky M.A., Glatz B.A., Gleason M.L., Reitmeier C.A. Reduction of Escherichia coli O157:H7 counts on whole fresh apples by treatment with sanitizers. Journal of Food Protection. 63:2000;703-708.
53. Wright J.R., Sumner S.S., Hackney C.R., Pierson M.D., Zoecklein B.W. Reduction of Escherichia coli O157:H7 on apples using wash and chemical sanitizer treatments. Dairy, Food, and Environmental Sanitation. 20:2000;120-126.
54. Wright J.R., Sumner S.S., Hackney C.R., Pierson M.D., Zoecklein B.W. Efficacy of ultraviolet light for reducing Escherichia coli O157:H7 in unpasteurized apple cider. Journal of Food Protection. 63:2000;563-567.
55. Zhang S., Farber J.M. The effects of various disinfectants against Listeria monocytogenes on fresh-cut vegetables. Food Microbiology. 13:1996;311-321.
56. Zhao T., Doyle M.P., Besser R.E. Fate of enterohemmorrhagic Escherichia coli O157:H7 in apple cider with and without preservatives. Applied and Environmental Microbiology. 59:1993;2526-2530.