Antagonistic effect of Pseudomonas graminis CPA-7 against foodborne pathogens in fresh-cut apples under simulated commercial conditions

Food Microbiology

Volumn 33, Issue 2, 2013, Pages 139-148

  Alegre, Isabel ^a   Viñas, Inmaculada ^a   Usall, Josep ^b   Anguera, Marina ^b   Altisent, Rosa ^b   Abadias, Maribel ^b  

^a UNIVERSITY OF LLEIDA   (Spain)

^b IRTA   (Spain)

Author keywords

Biocontrol; Biopreservation; Escherichia coli O157:H7; Listeria monocytogenes; Minimally processed apples; Salmonella

Indexed keywords

ANTIBIOSIS; ARTICLE; ECONOMICS; EVALUATION; FOOD PRESERVATION; FRUIT; GROWTH, DEVELOPMENT AND AGING; LISTERIA MONOCYTOGENES; MALUS; METHODOLOGY; MICROBIOLOGY; PHYSIOLOGY; PRUNUS; PSEUDOMONAS; SALMONELLA;

ANTIBIOSIS; FOOD PRESERVATION; FRUIT; LISTERIA MONOCYTOGENES; MALUS; PRUNUS; PSEUDOMONAS; SALMONELLA;

ESCHERICHIA COLI; LISTERIA MONOCYTOGENES; MALUS X DOMESTICA; PRUNUS PERSICA; PSEUDOMONAS; PSEUDOMONAS GRAMINIS; SALMONELLA;

EID: 84871715301     PISSN: 07400020     EISSN: 10959998     Source Type: Journal    
DOI: 10.1016/j.fm.2012.09.007     Document Type: Article

References (59)

1. Abadias M., Cañamas T.P., Asensio A., Anguera 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.
2. Abadias M., Usall J., Anguera M., Solsona C., Viñas I. Microbiological quality of fresh, minimally-processed fruit and vegetables, and sprouts from retail establishments. International Journal of Food Microbiology 2008, 123:121-129.
3. Abadias M., Usall J., Alegre I., Torres R., Viñas I. Fate of Escherichia coli in apple and reduction of its growth using the postharvest biocontrol agent Candida sake CPA-1. Journal of the Science of Food and Agriculture 2009, 89:1526-1533.
4. Abadias M., Alegre I., Usall J., Torres R., Vinas I. Evaluation of alternative sanitizers to chlorine disinfection for reducing foodborne pathogens in fresh-cut apple. Postharvest Biology and Technology 2011, 59:289-297.
5. Abbott J.A., Saftner R.A., Gross K.C., Vinyard B.T., Janick J. Consumer evaluation and quality measurement of fresh-cut slices of 'Fuji,' 'Golden Delicious,' 'GoldRush,' and 'Granny Smith' apples. Postharvest Biology and Technology 2004, 33:127-140.
6. Alegre I., Abadias M., Anguera M., Oliveira M., Viñas I. Factors affecting growth of foodborne pathogens on minimally processed apples. Food Microbiology 2010, 27:70-76.
7. Alegre I., Abadias M., Anguera M., Usall J., Viñas I. Fate of Escherichia coli O157:H7, Salmonella and Listeria innocua on minimally-processed peaches under different storage conditions. Food Microbiology 2010, 27:862-868.
8. Alegre I., Vinas I., Usall J., Anguera M., Abadias M. Microbiological and physicochemical quality of fresh-cut apple enriched with the probiotic strain Lactobacillus rhamnosus GG. Food Microbiology 2011, 28:59-66.
9. Alegre, I., Vinas, I., Usall, J., Teixidó, N., Figge, M.J., Abadias, M. Control of foodborne pathogens on fresh-cut fruit by a novel strain of Pseudomonas graminis, in press.
10. Allende A., Selma M.V., López-Gálvez F., Villaescusa R., Gil M.I. Role of commercial sanitizers and washing systems on epiphytic microorganisms and sensory quality of fresh-cut escarole and lettuce. Postharvest Biology and Technology 2008, 49:155-163.
11. Álvarez-Ordóñez A., Fernández A., Bernardo A., López M. Acid tolerance in Salmonella typhimurium induced by culturing in the presence of organic acids at different growth temperatures. Food Microbiology 2010, 27:44-49.
12. Ayala-Zavala J.F., Oms-Oliu G., Odriozola-Serrano I., González-Aguilar G.A., Álvarez-Parrilla E., Martín-Belloso O. Bio-preservation of fresh-cut tomatoes using natural antimicrobials. European Food Research and Technology 2008, 226:1047-1055.
13. Beuchat L.R. Surface Decontamination of Fruit and Vegetables Eaten Raw: a Review 1998, Available at:, (accessed 22.04.10.). http://www.who.int/foodsafety/publications/fs_management/en/surface_decon.pdf.
14. Beuchat L.R., Brackett R.E. Survival and growth of Listeria monocytogenes on lettuce as influenced by shredding, chlorine treatment, modified atmosphere packaging and temperature. Journal of Food Science 1990, 55:755-758.
15. Bhagwat A.A., Saftner R.A., Abbott J.A. Evaluation of wash treatments for survival of foodborne pathogens and maintenance of quality characteristics of fresh-cut apple slices. Food Microbiology 2004, 21:319-326.
16. Brackett R.E. Shelf stability and safety of fresh produce as influence by sanitation and disinfection. Journal of Food Protection 1992, 55:808-814.
17. Buck J.W., Walcott R.R., Beuchat L.R. Recent trends in microbiological safety of fruits and vegetables. Plant Health Progress January 2003, 1-10.
18. Centers for Disease Control and Prevention (CDC) Anual Listing of Foodborne Disease Outbraks, United States, 1990-2004 2007, Available at:, (accessed 10.07.09.). http://www.cdc.gov/foodborneoutbreaks/outbreak_data.htm.
19. EU Scientific Comitee on Food Risk Profile of the Microbiological Contamination of Fruits and Vegetables Eaten Raw 2002, Available at:, (accessed 05.05.09.). http://europa.eu.int/comm/food/fs/sc/scf/out123_en.pdfs.
20. Farber J.M. Microbiological aspects of modified-atmosphere packaging technology: a review. Journal of Food Protection 1991, 54:58-70.
21. Gahan C.G.M., Odriscoll B., Hill C. Acid adaptation of Listeria monocytogenes can enhance survival in acidic foods and during milk fermentation. Applied and Environmental Microbiology 1996, 62:3128-3132.
22. Gorny J.R. New opportunities for fresh-cut apples. Fresh Cut 2003, 11:14-15.
23. Gorny J.R. A summary of CA and MA requirements and recommendations for fresh-cut (minimally processed) fruits and vegetables. Proceedings of the 8th International Controlled Atmosphere Research Conference 2003, vols. I and II:609-614.
24. Gorny J.R., Gil M.I., Kader A.A. Postharvest physiology and quality maintenance of fresh-cut pears. Postharvest '96-Proceedings of the International Postharvest Science Conference 1998, 231-236. International Society Horticultural Science, Leuven 1. R. Bieleski, W.A. Laing, C.J. Clark (Eds.).
25. Gorny J.R., Hess-Pierce B., Cifuentes R.A., Kader A.A. Quality changes in fresh-cut pear slices as affected by controlled atmospheres and chemical preservatives. Postharvest Biology and Technology 2002, 24:271-278.
26. Gunes G.G., Hotchkiss J.H. Growth and survival of Escherichia coli O157:H7 on fresh-cut apples in modified atmospheres at abusive temperatures. Journal of Food Protection 2002, 65:1641-1645.
27. Harris L.J., Farber J.N., Beuchat L.R., Parish M.E., Suslow T.V., Garrett E.H., Busta F.F. Outbreaks associated with fresh produce: incidence, growth, and survival of pathogens in fresh and fresh-cut produce. Comprehensive Reviews in Food Science and Food Safety 2003, 2:78-141.
28. Jacxsens L., Devlieghere F., Falcato P., Debevere J. Behavior of Listeria monocytogenes and Aeromonas spp. on fresh-cut produce packaged under equilibrium-modified atmosphere. Journal of Food Protection 1999, 62:1128-1135.
29. 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 1999, 62:1372-1375.
30. Koseki S., Itoh K. Prediction of microbial growth in fresh-cut vegetables treated with acidic electrolyzed water during storage under various temperature conditions. Journal of Food Protection 2001, 64:1935-1942.
31. Koutsoumanis K.P., Sofos J.N. Comparative acid stress response of Listeria monocytogenes, Escherichia coli O157:H7 and Salmonella typhimurium after habituation at different pH conditions. Letters in Applied Microbiology 2004, 38:321-326.
32. Koutsoumanis K.P., Kendall P.A., Sofos J.N. Effect of food processing-related stresses on acid tolerance of Listeria monocytogenes. Applied and Environmental Microbiology 2003, 69:7514-7516.
33. S (RpoS) ir required for a sustained acid tolerant respomse in virulent Salmonella Typhimurium. Molecular Microbiology 1995, 17:155-167.
34. Leverentz B., Conway W.S., Janisiewiez W., Abadias M., Kurtzman C.P., Camp M.J. Biocontrol of the food-borne pathogens Listeria monocytogenes and Salmonella enterica serovar Poona on fresh-cut apples with naturally occurring bacterial and yeast antagonists. Applied and Environmental Microbiology 2006, 72:1135-1140.
35. 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 2000, 63:876-883.
36. Lou Y.Q., Yousef A.E. Adaptation to sublethal environmental stresses protects Listeria monocytogenes against lethal preservation factors. Applied and Environmental Microbiology 1997, 63:1252-1255.
37. Luo Y., Barbosa-Canovas G.V. Preservation of apple slices using ascorbic acid and 4-hexylresorcinol. Food Science and Technology International 1996, 2:315-321.
38. Molnar-Perl I., Friedman M. Inhibition of browning by sulfur amino-acids. 3. Apples and potatoes. Journal of Agricultural and Food Chemistry 1990, 38:1652-1656.
39. Nguyen-The C., Carlin F. The microbiology of minimally processed fresh fruits and vegetables. Critical Reviews in Food Science and Nutrition 1994, 34:371-401.
40. Oms-Oliu G., Aguiló-Aguayo I., Martín-Belloso O. Inhibition of browning on fresh-cut pear wedges by natural compounds. Journal of Food Science 2006, 71:S216-S224.
41. Park C.-M., Hung Y.-C., Doyle M.P., Ezeike G.O.I., Kim C. Pathogen reduction and quality of lettuce treated with electrolyzed oxidizing and acidified chlorinated water. Journal of Food Science 2001, 66:1368-1372.
42. Phan-Thanh L., Montagne A. Physiological and biochemical aspects of the acid survival of Listeria monocytogenes. Journal of General and Applied Microbiology 1998, 44:183-191.
43. Phan-Thanh L., Mahouin F., Alige S. Acid responses of Listeria monocytogenes. International Journal of Food Microbiology 2000, 55:121-126.
44. Pizzocaro F., Torreggiani D., Gilardi G. Inhibition of apple polyphenoloxidase (PPO) by ascorbic acid, citric acid and sodium chloride. Journal of Food Processing and Preservation 1993, 17:21-30.
45. Raybaudi-Massilia R.M., Mosqueda-Melgar J., Sobrino-López A., Soliva-Fortuny R., Martín-Belloso O. Use of malic acid and other quality stabilizing compounds to assure the safety of fresh-cut 'Fuji' apples by inactivation of Listeria monocytogenes, Salmonella Enteritidis and Escherichia coli O157:H7. Journal of Food Safety 2009, 29:236-252.
46. Rico D., Martín-Diana A.B., Frías J.M., Barat J.M., Henehan G.T.M., Barry-Ryan C. Improvement in texture using calcium lactate and heat-shock treatments for stored ready-to-eat carrots. Journal of Engineering 2007, 79:1196-1206.
47. Rojas-Grau M.A., Sobrino-Lopez A., Tapia M.S., Martin-Belloso O. Browning inhibition in fresh-cut 'fuji' apple slices by natural antibrowning agents. Journal of Food Science 2006, 71:S59-S65.
48. Roller S., Lusengo J. Developments in natural food preservatives. Agro Food Industry Hi-Tech 1997, 8:22-25.
49. ® AS1 browning inhibitor in fresh-cut fruit salads applications, with emphasis on apple wedges. Journal of Horticultural Science & Biotechnology 2009, 62-67.
50. Rupasinghe H.P.V., Murr D.P., DeEll J.R., Odumeru J. Influence of 1-methylcyclopropene and NatureSeal on the quality of fresh-cut "Empire" and "Crispin" apples. Journal of Food Quality 2005, 28:289-307.
51. Samelis J., Ikeda J.S., Sofos J.N. Evaluation of the pH-dependent, stationary-phase acid tolerance in Listeria monocytogenes and Salmonella typhimurium DT104 induced by culturing in media with 1% glucose: a comparative study with Escherichia coli O157:H7. Journal of Applied Microbiology 2003, 95:563-575.
52. Sapers G.M., Hicks K.B., Phillips J.G., Garzarella L., Pondish D.L., Matulaitis R.M., McCormack T.J., Sondey S.M., Seib P.A., Elatawy Y.S. Control of enzymatic browning in apple with ascorbic acid derivatives, polyphenol oxidase-inhibitors, and complexing agents. Journal of Food Science 1989, 54:997-1002.
53. Sapers G.M., Miller R.L., Pilizota V., Mattrazzo A.M. Antimicrobial treatments for minimally processed cantaloupe melon. Journal of Food Science 2001, 65:529-532.
54. Soliva-Fortuny R.C., Grigelmo-Miguel N., Odriozola-Serrano I., Gorinstein S., Martín-Belloso O. Browning evaluation of ready-to-eat apples as affected by modified atmosphere packaging. Journal of Agricultural and Food Chemistry 2001, 49:3685-3690.
55. Soliva-Fortuny R.C., Oms-Oliu G., Martín-Belloso O. Effects of ripeness stages on the storage atmosphere, color, and textural properties of minimally processed apple slices. Journal of Food Science 2002, 67:1958-1963.
56. Son S.M., Moon K.D., Lee C.Y. Inhibitory effects of various antibrowning agents on apple slices. Food Chemistry 2001, 73:23-30.
57. 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 2001, 64:147-151.
58. Toivonen P.M.A. Influence of harvest maturity on cut-edge browning of 'Granny Smith' fresh apple slices treated with anti-browning solution after cutting. Lwt-Food Science and Technology 2008, 41:1607-1609.
59. 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.