Modelling growth of Escherichia coli O157:H7 in fresh-cut lettuce submitted to commercial process conditions: Chlorine washing and modified atmosphere packaging

Food Microbiology

Volumn 33, Issue 2, 2013, Pages 131-138

  Posada Izquierdo, Guiomar D ^a   Pérez Rodríguez, Fernando ^a   López Gálvez, Francisco ^b   Allende, Ana ^b   Selma, María V ^b   Gil, María I ^b   Zurera, Gonzalo ^a  

^a UNIVERSITY OF CÓRDOBA   (Spain)

^b RESEARCH GROUP ON QUALITY   (Spain)

Author keywords

Chlorine; E. coli O157:H7; Fresh cut lettuce; Predictive microbiology

Indexed keywords

CHLORINE; DISINFECTANT AGENT;

ARTICLE; BIOLOGICAL MODEL; CHEMISTRY; DRUG EFFECT; ECONOMICS; ESCHERICHIA COLI O157; EVALUATION; FOOD CONTAMINATION; FOOD PRESERVATION; GROWTH, DEVELOPMENT AND AGING; KINETICS; LETTUCE; METHODOLOGY; MICROBIOLOGY; PACKAGING;

CHLORINE; DISINFECTANTS; ESCHERICHIA COLI O157; FOOD CONTAMINATION; FOOD PRESERVATION; KINETICS; LETTUCE; MODELS, BIOLOGICAL; PRODUCT PACKAGING;

ESCHERICHIA COLI; LACTUCA;

EID: 84871718129     PISSN: 07400020     EISSN: 10959998     Source Type: Journal    
DOI: 10.1016/j.fm.2012.08.010     Document Type: Article

References (56)

1. Abdul-Raouf U.M., Beuchat L.R., Ammar M.R. Survival and growth of Escherichia coli 0157:H7 on salad vegetables. Applied and Environmental Microbiology 1993, 59:1999-2006.
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 1998, 177:1588-1593.
3. Allende A., Selma M.V., López-Gálvez F., Villaescusa R., Gil M.I. Impact of wash water quality on sensory and microbial quality, including Escherichia coli cross contamination, of fresh-cut escarole. Journal of Food Protection 2008, 71:2514-2518.
4. Anonymous Fresh-cut. The sector takes off in a big way but there is still a long road ahead URL:, (accessed 29.02.12). http://www.fruittoday.com/articulos.php%3fid%3d1184161180215227%26idioma%3dE.
5. APHA, (American Public Health Association) Standard Methods for the Examination of Water and Wastewater 1998, American Public Health Association, Washington, DC. 20th ed.
6. Auer J.G. Use of Bioluminescent Escherichia coli O157:H7 to Investigate Chlorine Dioxide Mechanism of Bacterial Inactivation 2009, ETD Collection for Purdue university, Available at:, (accessed 12.07.11). http://docs.lib.purdue.edu/dissertations/AAI3379298/.
7. Baranyi J., Roberts T.A. A dynamic approach to predicting bacterial-growth in food. International Journal of Food Microbiology 1994, 23:277-294.
8. Behrsing J., Winkler S., Franz P., Premier R. Efficacy of chlorine for inactivation of Escherichia coli on vegetables. Postharvest Biology and Technology 2000, 19:187-192.
9. Beuchat L.R. Ecological factors influencing survival and growth of human pathogens on raw fruits and vegetables. Microbes and Infection 2002, 4:413-423.
10. Beuchat L.R., Farber J.N., Garrett E.H., Harris L.J., Parish M.E., Suslow T.V., Busta F.F. Standardization of a method to determine the efficacy of sanitizers in inactivating human pathogenic microorganisms on raw fruits and vegetables. Comprehensive Reviews in Food Science and Food Safety 2003, 2:174-178.
11. Bharathi S., Ramesh M.N., Varadaraj M.C. Predicting the behavioral pattern of Escherichia coli in minimally processed vegetables. Food Control 2001, 12:275-284.
12. Carrasco E., Pérez-Rodríguez F., Valero A., Garcia-Gimeno R.M., Zurera G. Survey of temperature and consumption patterns of fresh-cut leafy green salads: risk factors for Listeriosis. Journal of Food Protection 2007, 70:2407-2412.
13. Carrasco E., Pérez-Rodríguez F., Valero A., Garcia-Gimeno R.M., Zurera G. Growth of Listeria monocytogenes on shredded, ready-to-eat iceberg lettuce. Food Control 2008, 19:487-494.
14. CDC Questions and answers about E. coli O157:H7 outbreak from Fresh Spinach (Center for Disease Control and Prevention), Available from:, (accessed 29.06.12). http://www.cdc.gov/ecoli/2006/september/qa.htm.
15. Danyluk M., Schaffner D. Quantitative assessment of the microbial risk of leafy greens from farm to consumption: preliminary framework, data, and risk estimates. Journal of Food Protection 2011, 74:700-708.
16. Delaquis P., Stewart S., Cazaux S., Toivonen P. Survival and growth of Listeria monocytogenes and Escherichia coli O157:H7 in ready-to-eat iceberg lettuce washed in warm chlorinated water. Journal of Food Protection 2002, 65:459-464.
17. Delaquis P., Bach S., Dinu L.D. Behavior of Escherichia coli O157:H7 in leafy vegetables. Journal of Food Protection 2007, 70:1966-1974.
18. Diaz C., Hotchkiss J.H. Comparative growth of Escherichia coli O157:H7 spoilage organisms and shelf-life of shredded lettuce stored under modified atmospheres. Journal of the Science and Food and Agriculture 1996, 70:433-438.
19. Doyle M.P., Erickson M.C. Summer meeting 2007 - the problems with fresh produce: an overview. Journal of Applied Microbiology 2008, 105:317-330.
20. EFSA (European Food Safety Authority) Urgent advice on the public health risk of Shiga-toxin producing Escherichia coli in fresh vegetables. EFSA Journal 2011, 9(6):2274. Available at:, (accessed March 2012) (50 pp.). http://www.efsa.europa.eu/en/efsajournal/pub/2274.htm, 10.2903/j.efsa.2011.2274.
21. FSA Food Standards Agency Morrisons Recalls Leaf Lettuce, 27 April 2007 Available at:, (accessed 29.10.11). http://www.food.gov.uk/news/newsarchive/2007/apr/morrisalad.
22. Farber J.M. Microbiological aspects of modified atmosphere packaging technology: a review. Journal of Food Protection 1991, 54:58-70.
23. Francis G.A., Thomas C., O'Beirne D. The microbiological safety of mininally processed vegetables. International Journal of Food Science and Nutrition 1999, 34:1-22.
24. Francis G.A., O'Beirne D. Effects of vegetable type, package atmosphere and storage temperature on survival characteristics of E. coli O157:H7 and Listeria monocytogenes. Journal of Industrial Microbiology and Biotechnology 2001, 26:1-6.
25. Geysen S., Escalona V.H., Verlinden B.E., Aertsen A., Geeraerd A.H., Michiels C.W., Van Impe J.F., Nicolaï B.M. Validation of predictive growth models describing superatmospheric oxygen effects on Pseudomonas fluorescens and Listeria innocua on fresh-cut lettuce. International Journal of Food Microbiology 2007, 111:48-58.
26. Gil M.I., Selma M.V., López-Galvez F., Allende A. Fresh-cut product sanitation and wash water disinfection: problems and solutions. International Journal of Food Microbiology 2009, 134:37-45.
27. Jacxsens L., Devlieghere F., Debevere J. Validation of a systematic approach to design equilibrium modified atmosphere packages for fresh-cut produce. Food Science and Technology-Lebensmittel-Wissenschaft & Technologie 1999, 32:425-432.
28. Kader A.A. Prevention of ripening in fruits by use of controlled atmospheres. Food Technology 1980, 34:50-54.
29. Kolling G.L., Matthews K.R. Examination of recovery in vitro and in vivo of nonculturable Escherichia coli O157:H7. Applied and Environmental Microbiology 2001, 67:3928-3933.
30. Kolling G.L., Matthews K.R. Influence of enteric bacteria conditioned media on recovery of Escherichia coli O157:H7 exposed to starvation and sodium hypochlorite. Journal of Applied Microbiology 2007, 103:1435-1441.
31. Koseki S., Isobe S. Prediction of pathogen growth on iceberg lettuce under real temperature history during distribution from farm to table. International Journal of Food Microbiology 2005, 104:239-248.
32. Lee S.-Y., Baek S.-Y. Effect of chemical sanitizer combined with modified atmosphere packaging on inhibiting Escherichia coli O157:H7 in commercial spinach. Food Microbiology 2008, 25:582-587.
33. Li Y., Brackett R.W., Chen J., Beuchat L.R. Survival and growth of Escherichia coli O157:H7 inoculated onto cut lettuce before or after heating in chlorinated water, followed by storage at 5 or 15 C. Journal of Food Protection 2001, 64:305-309.
34. López-Gálvez F., Gil M.I., Truchado P., Selma M.V., Allende A. Cross-contamination of fresh-cut lettuce after a short-term exposure during pre-washing cannot be controlled after subsequent washing with chlorine dioxide or sodium hypochlorite. Food Microbiology 2009, 27:199-204.
35. Lu Z., Zhang L., Lu F., Bie X., Yu Z. Model of microbial growth on fresh-cut lettuce treated with chlorinated water during storage under different temperatures. Journal of Food Process Engineering 2006, 29:106-118.
36. Luo Y., Qiang H., McEvoy J.L., Conway W.S. Fate of Escherichia coli O157:H7 in the presence of indigenous microorganisms on commercially packaged baby spinach, as impacted by storage temperature and time. Journal of Food Protection 2009, 72:2038-2045.
37. McKellar R.C., Delaquis P. Development of a dynamic growth-death model for Escherichia coli O157:H7 in minimally processed leafy green vegetables. International Journal of Food Microbiology 2011, 151:7-14.
38. Montgomery D.C., Peck E.A., Vining G.G. Introduction to Linear Regression Analysis 2006, John Wiley & Sons, Inc., New Jersey. fourth ed.
39. Nauta M.J. Separation of uncertainty and variability in quantitative microbial risk assessment models. International Journal of Food Microbiology 2000, 57:9-18.
40. Oliveira M., Usall J., Solsona C., Alegre I., Viñas I., Abadias M. Effects of packaging type and storage temperature on the growth of foodborne pathogens on shredded 'Romaine' lettuce. Food Microbiology 2010, 27:375-380.
41. Oscar T.P. Quantitative risk assessment model for Salmonella and whole chickens. International Journal of Food Microbiology 2004, 93:231-247.
42. Pérez-Rodríguez F., Valero A., Carrasco E., Garcia R.M., Zurera G. Understanding and modelling bacterial transfer to foods: a review. Trends in Food Science & Technology 2008, 19:131-144.
43. Pérez-Rodríguez F., Campos D., Ryser E.T., Buchholz A.L., Posada-Izquierdo G.D., Marks B.P., Zurera G., Todd E. A mathematical risk model for Escherichia coli O157:H7 cross-contamination of lettuce during processing. Food Microbiology 2011, 8:141-148.
44. Poschet F., Geeraerd A.H., Scheerlinck N., Nicolai B.M., Van Impe J.F. Monte Carlo analysis as a tool to incorporate variation on experimental data in predictive microbiology. Food Microbiology 2003, 20:285-295.
45. Pouillot R., Albert I., Cornu M., Denis J.-B. Estimation of uncertainty and variability in bacterial growth using Bayesian inference. Application to Listeria monocytogenes. International Journal of Food Microbiology 2003, 81:87-104.
46. Rangel J.M., Sparling P.H., Crowe C., Griffin P.M., Swerdlow D.L. Epidemiology of Escherichia coli O157:H7 outbreaks, United States, 1982-2002. Emerging and Infectious Diseases 2005, 11:603-609.
47. Ratkowsky D.A., Olley J., McMeekin T.A., Ball A. Relationship between temperature and growth rate of bacterial cultures. Journal of Bacteriology 1982, 149:1-5.
48. Ross T. Indices for performance evaluation of predictive models in food microbiology. Journal of Applied Bacteriology 1996, 81:501-508.
49. Smyth A.B., Song J., Cameron A.C. Modified atmosphere packaged cut iceberg lettuce: effect of temperature and O-2 partial pressure on respiration and quality. Journal of Agricultural and Food Chemistry 1998, 46:4556-4562.
50. Söderström A., Lindberg A., Andersson Y. EHEC O157 a large E. coli O157 outbreak in Sweden associated with locally produced lettuce. Foodborne Pathogens and Disease 2008, 5:339-349.
51. Takeuchi K., Frank J.F. 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. Journal of Food Protection 2000, 63:434-440.
52. Takeuchi K., Hassan A.N., Frank J.F. Penetration of Escherichia coli O157: H7 into lettuce as influenced by modified atmosphere and temperature. Journal of Food Protection 2001, 64:1820-1823.
53. Taormina P.J., Beuchat L.R. Comparison of chemical treatments to eliminate enterohemorrhagic E. coli O157:H7 on alfalfa seeds. Journal of Food Protection 1999, 62:318-324.
54. Theofel C.G., Harris L.J. Impact of preinoculation culture conditions on the behaviour of Escherichia coli O157:H7 inoculated onto romaine lettuce (lactuca sativa) plants and cut leaf surfaces. Journal of Food Protection 2009, 72:1553-1559.
55. Valero A., Rodríguez M., Carrasco E., Pérez-Rodríguez F., García-Gimeno R.M., Zurera G. Studying the growth boundary and subsequent time to growth of pathogenic Escherichia coli serotypes by turbidity measurements. Food Microbiology 2010, 27:819-828.
56. Zhang G., Li M., Beuchat L.R., Marilyn C.E., Phelan V.H., Doyle M. Evaluation of treatments for elimination of foodborne pathogens on the surface of leaves and roots of lettuce (Lactuca sativa L. Journal of Food Protection 2009, 72:228-234.