The microbiological efficacy of decontamination methodologies for fresh produce: A review

Food Control

Volumn 32, Issue 2, 2013, Pages 418-427

  Goodburn, Caroline ^a,b   Wallace, Carol A ^a  

^a UNIVERSITY OF CENTRAL LANCASHIRE   (United Kingdom)

^b Florette   (France)

Author keywords

Chlorine decontamination efficacy; Fresh produce and foodborne illness; Fresh produce industrial processing; Fresh produce microbiological decontamination; Fresh produce safety; Fresh produce washing

Indexed keywords

EID: 84873598137     PISSN: 09567135     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.foodcont.2012.12.012     Document Type: Review

References (105)

1. Abadias M., Alegre I., Usall J., Torres R., Viñas Evaluation of alternative sanitizers to chlorine disinfection for reducing foodborne pathogens in fresh-cut apple. Postharvest Biology and Technology 2011, 59:289-297. 10.1016/j.postharvbio.2010.09.014.
2. Abadias M., Cañamas T.P., Asensio A., Angueram M., Viñas I. Microbial quality of commercial 'Golden Delicious' apples throughout production and shelf-life in Lleida (Catalonia, Spain). International Journal of Food Microbiology 2006, 108:404-409.
3. Advisory Committee on the Microbiological Safety of Food Annual report 2011 2011, Retrieved November 2012. http://www.food.gov.uk/multimedia/pdfs/committee/acmsf-report-2011.pdf.
4. Allende A., Martínez B., Selma V., Gil M.I., Suárez J.E., Rodríguez A. Growth and bacteriocin production by lactic acid bacteria in vegetable broth and their effectiveness at reducing Listeria monocytogenes in vitro and in fresh-cut lettuce. Food Microbiology 2007, 24(2007):759-766.
5. Aruscavage D., lee K., Miller S., Lejeune J.T. Interactions affecting the proliferation and control of human pathogens on edible plants. Journal of Food Science 2006, 71:R89-R99.
6. Ashley B.C., Birchfield P.T., Chamberlain B.V., Kotwal R.S., McClellan S.F., Moynihan S., et al. Health concerns regarding consumption of irradiated food. International Journal of Hygiene and Environmental Health 2004, 207(6):493-504.
7. Bailey A.G. Electrostatic atomization of liquids. Science Progress 1974, 61(1):555-585. Oxford.
8. Bari M.L., Nakauma M., Todoriki S., Juneja V.K., Isshiki K., Kawamoto S. Effectiveness of irradiation treatments in inactivating Listeria monocytogenes on fresh vegetables at refrigeration temperature. Journal of Food Protection 2005, 68:318-323.
9. Batterman S., Zhang L., Wang S. Quenching of chlorination disinfection by-product formation in drinking water by hydrogen peroxide. Water Research 2000, 34:1652-1658.
10. Beuchat L.R., Adler B.A., Lang M.M. Efficacy of chlorine and a peroxyacetic acid sanitizer in killing Listeria monocytogenes on iceberg and romaine lettuce using simulated commercial processing conditions. Journal of Food Protection 2004, 67:1238-1242.
11. Beuchat L.R., Pettigrew C.A., Tremblay M.E., Roselle B.J., Scouten A.J. Lethality of chlorine, chlorine dioxide, and a commercial fruit and vegetable sanitizer to vegetative cells and spores of Bacillus cereus and spores of Bacillus thuringiensis. Journal of Food Protection 2004, 67:1702-1708.
12. Beuchat L.R., Ryu J.H. Produce handling and processing practice. Emerging Infectious Diseases 1997, 13:459-465.
13. Bruhn C.M. Consumer acceptance of irradiated food: theory and reality. Radiation Physics and Chemistry 1998, 52(1-6):129-133.
14. Campden & Chorleywood Food Research Association Group Risks of pathogens in ready to eat fruits and salads through the production process 2004, Review No. 44: Campden, UK.
15. Centers for Disease Control and Prevention, CDC E. coli outbreak from fresh spinach 2006, http://www.cdc.gov/ecoli/2006/september/.
16. Chilled Food Association Microbiological guidance for produce suppliers to chilled food manufacturers 2007, Chilled Food Association, London. 2nd ed.
17. Christensen B.E., Tronnes H.N., Vollan K., Smidsrod O., Bakke R. Biofilm removal by low concentration of hydrogen peroxide. Biofouling 1990, 2:165-175.
18. Cleveland J., Montville T.J., Nes I.F., Chikindas M.L. Bacteriocins: safe, natural antimicrobials for food preservation. International Journal of Food Microbiology 2001, 71:1-20.
19. Codex Alimentarius Commission Code of hygienic practice for fresh fruits and vegetables: Adopted 2003. Revision 2010 (new Annex III for fresh leafy vegetables) 2010, Retrieved 13.11.12. http://www.codexalimentarius.net/input/download/standards/./CXP_053e.pdf.
20. Daniel C., Poiret S., Goudercourt D., Dennin V., Leyer G., Pot B. Selecting lactic acid bacteria for their safety and functionality by use of a mouse colitis model. Applied and Environmental Microbiology 2006, 72:5799-5805.
21. De Giusti M., Aurigemma C., Marinelli L., Tufi D., De Medici D., Di Pasquale S., et al. The evaluation of the microbial safety of fresh ready-to-eat vegetables produced by different technologies in Italy. Journal of Applied Microbiology 2010, 109:996-1006.
22. Delaquis P., Stewart J.S., Toivonen P.M.A., Moyls A.L. Effects of warm, chlorinated water on microbial flora of shredded iceberg lettuce. Food Research International 1999, 32:7-14.
23. Du J., Han Y., Linton R.H. Efficacy of chlorine dioxide gas in reducing Escherichia coli 0157:H7 on apple surfaces. Food Microbiology 2003, 20:583-591.
24. Erickson M.C. Internalization of fresh produce by foodborne pathogens. Annual Review of Food Science and Technology 2012, 3:283-319. Epub 2012 Jan 11.
25. European Commission Scientific Committee on Food Risk profile on the microbiological contamination of fruits and vegetables eaten raw 2002, European Commission. http://ec.europa.eu/food/fs/sc/scf/out125_en.pdf.
26. European Food Safety Authority.(EFSA) Shiga toxin-producing E. coli (STEC) o104:H4 2011 outbreaks in Europe: taking stock. EFSA Journal 2011, 9(10):2390. [22pp.]. 10.2903/j.efsa2011.2390.
27. Fan X., Sokorai K.J.B., Engemann J., Gurtler J.B., Liu Y. Inactivation of Listeria innocua, Salmonella typhimurium and Escherichia coli O157:H7 on surface and stem scar areas of tomatoes using in-package ozonation. Journal of Food Protection 2012, 75(9):1611-1618.
28. Fett W.W. Naturally occurring biofilms on alfalfa and other types of sprouts. Journal of Food Protection 2000, 63:625-632.
29. Foley D., Euper M., Caporaso F., Prakash A. Irradiation and chlorination effectively reduces Escherichia coli 0157:H7 inoculated on cilantro (Coriandrum sativum) without negatively affecting quality. Journal of Food Protection 2004, 67:2092-2098.
30. Foley D.M., Rodriguez A., Caporaso L., Prakash F. Reduction of Escherichia coli O157:H7 in shredded iceberg lettuce by chlorination and gamma irradiation. Radiation Physics and Chemistry 2002, 63:391-396.
31. Food and Agriculture Organization of the United Nations Regional Office for Asia and the Pacific Bangkok Processing of fresh-cut tropical fruits and vegetables: A TECHNICAL GUIDE 2010.
32. Food and Drug Aaministration (FDA) U.S. regulatory requirements for irradiating foods 1999 May, http://www.fda.gov/Food/FoodIngredientsPackaging/IrradiatedFoodPackaging/ucm110730.htm.
33. Food and Drug Administration (FDA) Produce safety from production to consumption: 2004 action plan to minimize foodborne illness associated with fresh produce consumption 2004, http://www.fda.gov/Food/FoodSafety/Product-SpecificInformation/FruitsVegetablesJuices/FDAProduceSafetyActivities/ProduceSafetyActionPlan/ucm129487.htm.
34. Food and Drug Administration Irradiation in the production, processing and handling of foods 2008, 21 CFR 179.26. Code of Federal Regulations, Food and Drug Administration, Washington D.C, Available from. http://www.fda.gov/Food/FoodIngredientsPackaging/IrradiatedfoodPackaging/ucm074734.htm.
35. Food and drug administration secondary direct food additives permitted in food for human consumption federal register. Rules and regulations June 26, 2001, Vol. 66. Number 123, pp.33829-33830.
36. Food Drug Administration Nisin preparation: affirmation of GRAS status as a direct human food ingredient. Federal Register 1998, 54:11247-11251.
37. Food Standards Agency FSA nutrient and food based guidelines for UK institutions 2006, Food Standards Agency, London.
38. Foster A. Consumer attitudes to irradiation. Food Control January 1991.
39. Gallup Organization, ABT Associates, Centre for Food Safety and Quality Enhancement, University of Georgia Consumer awareness, knowledge and acceptance of food irradiation 1993, American Meat Institute Foundation, Arlington, Virginia.
40. Ganesh V., Hettiarachchy N.S., Ravichandaran M., Johnson M.G., Griffis C.L., Martin E.M., et al. Electrostatic sprays of food-grade acids and plant extracts are more effective than conventional sprays in decontaminating Salmonella typhimurium on spinach. Journal of Food Science 2010, 75(9):574-579. 10.1111/j.1750-3841.2010.01859.
41. Garcia A., Mount J.R., Davidson P.M. Ozone and chlorine treatment of minimally processed lettuce. Journal of Food Science 2003, 68:2747-2751.
42. 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.
43. Global Gap Global gap standard for integrated farm management. Fruit and vegetables certification 2012, August 2012. http://www1.globalgap.org/cms/front_content.php%3fidart%3d1440, Ed. 4.0-3.
44. Gomes C., Moreira R.G., Castel-Perez E. Radiosensitization of Salmonella spp. And Listeria spp. In ready-to-eat baby spinach leaves. Journal of Food Science 2011, 76(1):141-148. 10.1111/j.1750-3841.2010.01904.
45. Gómez-López V.-M., Ragaert P., Ryckeboer J., Jeyachchandran V., Debevere J., Devlieghere F. Shelf-life of minimally processed cabbage treated with neutral electrolysed oxidising water and stored under equilibrium modified atmosphere. International Journal of Food Microbiology 2007, 117:91-98.
46. Gopal A., Coventry J., Wan J., Roginski H., Ajlouni S. Alternative disinfection techniques to extend the shelf life of minimally processed iceberg lettuce. Food Microbiology 2010, 27:210-219. 10.1016/j.fm.2009.10.006.
47. Gündüz G.T., Gönül S.A., Karapinar Efficacy of myrtle oil against Salmonella typhimurium on fresh produce. International Journal of Food Microbiology 2009, 130:147-150.
48. Gündüz G.T., Gönül S.A., Karapinar M. Efficacy of sumac and oregano in the activation of Salmonella typhimurium on tomatoes. International Journal of Food Microbiology 2010, 141:39-44.
49. Han Y., Linton R.H., Nielson S.S., Nelson P.E. Reduction of Listeria monocytogenes on green peppers (Capsicum annuum L.) by gaseous and aqueous chlorine dioxide and water washing and its growth at 7°C. Journal of Food Protection 2001, 64:1730-1738.
50. Hrudey S.E. Chlorination disinfection by-products, public health risk tradeoffs and me. Water Research 2009, 43:2057-2092. 10.1016/j.watres.2009.02.011.
51. Hsu W.-Y., Simonne A., Jitareerat P., Marshall M.R. Low-dose irradiation improves microbial quality and shelf life of fresh mint (Mentha piperita L.) without compromising visual quality. Journal of Food Science 2010, 75(4):222-230. 10.1111/j.1750-3841.2010.01568.x.
52. Issa-Zacharia A., Kamitano Y., Muhimbula H.S., Ndabikunze B.K. A review of microbiological safety of fruits and vegetables and the introduction of electrolysed water as an alternative to sodium hypochlorite solution. African Journal of Food Science 2010 Dec, 4(13):778-789.
53. Itoh Y., Sugita-Konishi Y., Kasuga F., Inaki M., Hara-kudo Y., Saito N., et al. Enterohemorrhagic Escherichia coli O157:H7 in apple wounds. Journal of Food Protection 1998, 62:1372-1375.
54. Junquiera-Gonçalves M.P., Galotto M.J., Valenzuela X., Dinten C.M., Aguirre P., Miltz J. Perception and view of consumers on food irradiation and the Radura symbol. Radiation Physics and Chemistry 2010, 80:119-122. 10.1016/j.radphyschem.2010.08.001.
55. Khadre M.A., Yousef A.E., Kim J.-G. Microbiological aspects of ozone applications in food: a review. Journal of Food Science 2001, 66:1242-1252.
56. Kim J.-G., Yousef A.E. Inactivation kinetics of foodborne spoilage and pathogenic bacteria by ozone. Journal of Food Science 2000, 65:521-528.
57. Kim J.-G., Yousef A.E., Chism G.W. Use of ozone to inactivate microorganisms on lettuce. Journal of Food Safety 1999, 19:17-34.
58. Kocharunchitt C., Ross T., McNeil D.L. Use of bacteriophages as biocontrol agents to control Salmonella associated with seed sprouts. International Journal of Food Microbiology 2009, 128:453-459.
59. Lang M.M., Harris L.J., Beuchat L.R. 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. Journal of Food Protection 2004, 67:1092-1103.
60. Lee S.,Y., Costello M., Kang D.,H. Efficacy of chlorine dioxide gas as a sanitizer of lettuce leaves. Journal of Food Protection 2004 July, 67(7):1371-1376.
61. Leverentez B., Conway W.S., Camp M.J., Janisiewicz W.J., Abuladze T., Ynag M., et al. Biocontrol of Listeria monocytogenes on fresh cut produce by treatment with lytic bacteriophages and a bacteriocin. Applied and Environmental Microbiology 2003, 69:4519-4526.
62. Little C., Gormley F., Mook P., Gillespie I., Foster K., Harris J., et al. Outbreaks of infection associated with ready-to-eat food 2011, January 2011 (ACM/1014). http://www.food.gov.uk/multimedia/pdfs/committee/acm1014hpa.pdf.
63. Lynch M.F., Tauxe R.V., Hedberg C.W. The growing burden of foodborne outbreaks due to contaminated fresh produce: risks and opportunities. Epidemiology and Infection 2009, 137:307-315. 10.1017/S0950268808001969.
64. Mahmoud b.S.M., Bhagat A.R., Linton R.H. Inactivation kinetics of inoculated Escherichia coli 0157:H7, Listeria monocytogenes and Salmonella enterica on strawberries by chlorine dioxide gas. Food Microbiology 2007, 24:736-744. 10.1016/j.fm.2007.03.006.
65. Mahvi A.H. Application of ultrasonic technology for water and wastewater treatment. Iranian Journal of Public Health 2009, 38(2):1-17.
66. Mahvi A.H., Maleki A., Rezaee R., Safari M. Reduction of humic substances in water by application of ultrasound waves and ultraviolet radiation. Iranian Journal of Environmental Health Science & Engineering 2009, 6(4):233-240.
67. Mintel Mintel fruits and vegetables - UK 2012 Feb, Retrieved 13.11.12. http://store.mintel.com/catalogsearch/result/%3Fq%3Dfruits%2520and%2520vegetables#q%3Dfruits%2520and%2520vegetables%26country%3D7%26published_year%3D555%26cat%3D425.
68. Niemira B.A., Cooke P.H. Escheria coli 0157:H7 biofilm formation on romaine lettuce and spinach leaf surfaces reduces efficacy of irradiation and sodium hypochlorite washes. Journal of Food Science 2010, 75(5):270-277.
69. Niemira B.A., Fan X. Low-dose irradiation of fresh and fresh-cut produce: safety, sensory and shelf life. Food irradiation research and technology 2005, 169-181. Blackwell publishing and the Institute of food Technologists, Ames, Iwoa. C. Sommers, X. Fan (Eds.).
70. Nordion The history of food irradiation 2011, Retrieved November 2012. http://www.nordion.com/documents/The-History-of-Food-Irradiation.pdf.
71. Nou X., Lou Y. Whole-leaf wash improves chlorine efficacy for microbial reduction and prevents pathogen cross-contamination during fresh-cut lettuce processing. Journal of Food Science 2010, 75:283-290. 10.1111/j.1750-3841.2010.01630x.
72. Olaimat A.N., Holley R.A. Factors influencing the microbial safety of fresh produce: a review. Food Microbiology 2012, 32:1-19.
73. ölmez H. Effect of different sanitizing methods and incubation time and temperature on inactivation of Escherichia coli on lettuce. Journal of Food Safety 2010, 30:288-299. 10.1111/j.1745-4565.2009.00206.x.
74. Oms-Oliu G., Aguilo-Aguayó I., Martín-Belloso O., Soliva-Fortuny R. Effects of pulsed light treatments on quality and antioxidant properties of fresh-cut mushrooms (Agaricus bisporus). Postharvest Biology and Technology 2010, 56:216-222.
75. Parish M.E., Beuchat L.R., Suslow T.V., Harris L.J., Garrett E.H., Farber J.N., et al. Methods to reduce/eliminate pathogens from fresh and fresh-cut produce. Comprehensive Reviews in Food Science and Food Safety 2003, 2(Suppl.):161-173.
76. Perry J.J., Yousef A.E. Decontamination of raw foods using ozone-based sanitization techniques. Annual Review of Food Science and Technology 2011, 2:281-298.
77. Rajkovic A., Tomasevic I., Smigic N., Uyttendaele M., Radovanovic R., Devlieghere F. Pulsed UV light as an intervention strategy against Listeria monocytogenes and Escherichia coli 0157:H7 on the surface of a meat slicing knife. Journal of Food Engineering 2010, 100:446-451.
78. Ramos-Villarroel A.Y., Aron-Maftei N., Martín-Belloso O., Soliva-Fortuny R. Influence of spectral distribution on bacterial inactivation and quality changes of fresh-cut watermelon treated with intense light pulses. Postharvest Biology and Technology 2012, 69:32-39.
79. Randazzo C.L., Pitino I., Scifò G.O., Caggia C. 2009, Biopreservation of minimally processed iceberg lettuces using a bacteriocin produced by Lactococcus lactis wild strain. Food Control 2009, 20:756-763.
80. Rico D., Martin-Diana A.B., Barat J.M., Barry-Ryan C. Extending and measuring the quality of fresh-cut fruit and vegetables: a review. Trends in Food Science & Technology 2007, 18:373-386.
81. Rico D., Martin-Diana A.B., Barry-Ryan C., Frias J.M., Henehan G.T.M., Barat J.M. Use of neutral electrolysed water (EW) for quality maintenance and shelf-life extension of minimally processed lettuce. Innovative Food Science and Technologies 2008, 9:37-48.
82. Rodgers S.T., Cash J.N., Siddiq M., Ryser E.T. A comparison of different chemical sanitizers for inactivating Escherichia coli 0157:H7 and Listeria monocytogenes in solution and on apples, lettuce, strawberries, and cantaloupe. Journal of Food Protection 2004, 67:721-731.
83. Rozin P. The meaning of " natural" - process more important than content. Psychological Science 2005, 16:652-658.
84. Sapers G.M. Efficacy of washing and sanitizing methods for disinfection of fresh fruit and vegetable products. Food Technology and Biotechnology 2001, 39(4):305-311.
85. Settanni L., Corsetti A. Application of bacteriocins in vegetable food biopreservation. International Journal of Food Microbiology 2008, 121:123-138.
86. Shen C., Luo Y., Nan X., Bauchan G., Zhou B., Wang Q., et al. Enhanced inactivation of Salmonella and Pseudonomas biofilms on stainless steel by use of T-128, a fresh produce washing aid in chlorinated wash solution 2012, American Society of Microbiology, Published ahead of print 29 June 2012.
87. Smith De Waal C., Bhuiya F. Outbreaks by the numbers: Fruits and vegetables 1990-2005 2009, The Centre for Science in the Public Interest, Available online from. http://www.cspinet.org/foodsafety/IAFPPoster.pdf.
88. Soon J.M., Manning L., Davies W.P., Baines R. Fresh produce associated outbreaks: a call for HACCP on farms. British Food Journal 2012, 114(4):553-597.
89. Stiles M.E., Holzapfel W.H. Lactic acid bacteria of foods and their current taxonomy. International Journal of Food Microbiology 1997 Apr 29, 36(1):1-29.
90. Teisl M.F., Fein S.B., Levy A.S. Information effects on consumer attitudes towards three food technologies: organic production, biotechnology and irradiation. Food Quality and Preference 2009, 20:586-596. 10.1016/j.foodqual.2009.07.001.
91. Trias R., Bañeras L., Badosa E., Montesinos E. Bioprotection of golden delicious apples and iceberg lettuce against foodborne bacterial pathogens by lactic acid bacteria. International Journal of Food Microbiology 2008, 123:50-60.
92. Tzortzakis N.G. Impact of cinnamon oil-enrichment on microbial spoilage of fresh produce. Innovative Food Science and Emerging Technologies 2009, 10:97-102.
93. Viazis S., Akhtar M., Feirtag J., Diez-Gonzalez F. Reduction of Escherichia coli O157:H7 viability on leafy green vegetables by treatment with a bacteriophage mixture and trans-cinnamaldehyde. Food Microbiology 2011, 28:149-157.
94. Villagomez N.S., Herrera E.A.N., Orozco L.R., Wild-Padua G., Iturriaga M.H. Effect of storage time on the efficacy of chemical and irradiation treatments to inactivate Salmonella on cilantro (Coriandrum sativum L.). Journal of Food Safety 2010, 30:584-598. 10.1111/j.1745-4565.2010.00227.x.
95. Wei C.,I., Cook D.L., Kirk J.R. Use of chlorine compounds in the food industry. Food Technology 1985, 39:107-115.
96. World Health Organization (2003a). Diet, nutrition and the prevention of chronic diseases. Report of a Joint WHO/FAO Expert Consultation, WHO Technical Report Series 916. http://www.who.int.
97. World Health Organization (2003b). WHO fruit and vegetable promotion initiative - report of the meeting, Geneva, 25-27 August 2003. http://www.who.int.
98. World Health Organization Silver in drinking-water. Guidelines for drinking-water quality. Health criteria and other supporting information 2003, Vol. 2. World Health organization, Geneva. http://who/SDE/WSH/03.04/14, 2nd ed.
99. World Health Organization Microbiological risk assessment series. Microbiological hazards in fresh fruits and vegetables 2008, http://www.fao.org/ag/AGN/agns/files/FFV_2007.
100. World Health Organization, Food Safety Unit Food safety issues: Surface decontamination of fruits and vegetables eaten raw: a review 1998, World Health Organization, Geneva. http://who/FSF/FOS/98.2.
101. Wu V.C.H., Kim B. Effect of a simple chlorine dioxide method for controlling five foodborne pathogens, yeasts and molds on blueberries. Food Microbiology 2007, 24:794-800.
102. Ye J.X., Kostrzynka M., Dunfield K., Warriner K. Evaluation of a biocontrol preparation consisting of Enterobacter asburiae JX1 and a lytic bacteriophage cocktail to suppress the growth of Salmonella javiana associated with tomatoes. Journal of Food Protection 2009, 72:2284-2292.
103. Ye J.X., Kostrzynka M., Dunfield K., Warriner K. Control of Salmonella on sprouting mung bean and alfalfa seeds by using a biocontrol preparation based on antagonistic bacteria and lytic bacteriophages. Journal of Food Protection 2010, 73:9-17.
104. Zhang S., Faber J.M. The effects of various disinfectants against Listeria monocytogenes on fresh-cut vegetables. Food Microbiology 1996, 13:311-321.
105. Zhang G., Ma L., Beuchat L.R., Erickson M.C., Phelan V.H., Doyle M.P. Lack of internalization of Escherichia coli O157:H7 in lettuce (Lactuca sativa L.) after leaf surface and soil inoculation. Journal of Food Protection 2009, 72:2028-2037.