Survival of acid adapted and non-acid adapted Salmonella Typhimurium in pasteurized orange juice and yogurt under different storage temperatures

Food Science and Technology International

Volumn 19, Issue 5, 2013, Pages 407-414

  Álvarez Ordóñez, Avelino ^a   Valdés, Lorena ^a   Bernardo, Ana ^a   Prieto, Miguel ^a   López, Mercedes ^a  

^a UNIVERSITY OF LEÓN   (Spain)

Author keywords

food safety; Salmonella Typhimurium

Indexed keywords

ACID TOLERANCE RESPONSE; BACTERIAL INACTIVATION; BRAIN HEART INFUSIONS; FOOD COMPOSITIONS; REFRIGERATION TEMPERATURES; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SALMONELLA TYPHIMURIUM; STORAGE TEMPERATURES;

CELLS; DAIRY PRODUCTS; FOOD SAFETY; FRUIT JUICES; PASTEURIZATION; SALMONELLA;

CYTOLOGY;

YOGHURT;

ADAPTATION; ARTICLE; CHEMISTRY; FOOD SAFETY; FOOD STORAGE; METHODOLOGY; PASTEURIZATION; PH; PHYSIOLOGY; SALMONELLA TYPHIMURIUM; SWEET ORANGE; TEMPERATURE; PROCEDURES; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

FOOD SAFETY; SALMONELLA TYPHIMURIUM;

ADAPTATION, PHYSIOLOGICAL; CITRUS SINENSIS; FOOD STORAGE; HYDROGEN-ION CONCENTRATION; PASTEURIZATION; SALMONELLA TYPHIMURIUM; TEMPERATURE; YOGURT;

EID: 84884244449     PISSN: 10820132     EISSN: 15321738     Source Type: Journal    
DOI: 10.1177/1082013212455343     Document Type: Article

References (44)

1. Álvarez-Ordóñez A, Fernández A, Bernardo A, López M. Comparison of acids on the induction of an acid tolerance response in Salmonella Typhimurium, consequences for food safety. Meat Science. 2009a ; 81 (1). 65-70
2. Álvarez-Ordóñez A, Fernández A, Bernardo A, López M. A comparative study of thermal and acid inactivation kinetics in fruit juices of Salmonella enterica serovar Typhimurium and Salmonella enterica serovar Senftenberg grown at acidic conditions. Foodborne Pathogens and Disease. 2009b ; 6 (9). 1147-1155
3. Álvarez-Ordóñez A, Fernández A, López M, Bernardo A. Relationship between membrane fatty acid composition and heat resistance of acid and cold stressed Salmonella Senftenberg CECT 4384. Food Microbiology. 2009c ; 26 (3). 347-353
4. 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. 2010a ; 27 (1). 44-49
5. Álvarez-Ordóñez A, Fernández A, Bernardo A, López M. Arginine and lysine decarboxylases and the acid tolerance response of Salmonella Typhimurium. International Journal of Food Microbiology. 2010b ; 136 (3). 278-282
6. Álvarez-Ordóñez A, Fernández A, Bernardo A, López M. Acid adaptation sensitizes Salmonella enterica serovar Typhimurium to osmotic and oxidative stresses. Archiv fur Lebensmittelhygiene. 2010c ; 61 (4). 148-152
7. Chang JM, Fang TJ. Survival of Escherichia coli O157:H7 and Salmonella enterica serovars Typhimurium in iceberg lettuce and the antimicrobial effect of rice vinegar against E. coli O157:H7. Food Microbiology. 2007 ; 24 (7-8). 745-751
8. D'Aoust JY. Infective dose of Salmonella Typhimurium in cheddar cheese. American Journal of Epidemiology. 1985 ; 122 (4). 717-719
9. D'Aoust JY The Microbiological Safety and Quality of Foods. Lund BM Baird-Parker TC Gould GW, ed. Gaithersberg, MD: Aspen ; 2000: 1233-1299.
10. de Jonge R, Ritmeester WS, Leusden FM. Adaptive responses of Salmonella enterica serovar Typhimurium DT104 and other S. Typhimurium strains and Escherichia coli O157:H7 to low pH environments. Journal of Applied Microbiology. 2003 ; 94 (4). 625-632
11. Dourou D, Porto-Fett ACS, Shoyer B, Call JE, Nychas GJE, Illg EK, et al. Behavior of Escherichia coli O157:H7, Listeria monocytogenes, and Salmonella Typhimurium in teewurst, a raw spreadable sausage. International Journal of Food Microbiology. 2009 ; 130 (3). 245-250
12. Driessen AJM, van de Vossenberg JLCM, Konings WN. Membrane composition and ion-permeability in extremophiles. FEMS Microbiology Reviews. 1996 ; 18: 139-148
13. EFSA. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2009. EFSA Journal. 2011 ; 9 (3). 2090-2090
14. El-Gazzar FE, Marth EH. Salmonellae, salmonellosis and dairy foods: a review. Journal of Dairy Science. 1992 ; 75 (9). 2327-2343
15. Evans MR, Salmon RL, Nehaul L, Mably S, Wafford L, Nolan-Farrell MZ, et al. An outbreak of Salmonella Typhimurium DT170 associated with kebab meat and yogurt relish. Epidemiology and Infection. 1999 ; 122 (3). 377-383
16. Foster JW, Hall HK. Adaptive acidification tolerance response of Salmonella Typhimurium. Journal of Bacteriology. 1990 ; 172 (2). 771-778
17. Gounadaki AS, Skandamis PN, Drosinos EH, Nychas GJE. Effect of packaging and storage temperature on the survival of Listeria monocytogenes inoculated post-processing on sliced salami. Journal of Food Protection. 2007 ; 70 (10). 2313-2330
18. Graumann P, Marahiel MA. Some like it cold: response of microorganisms to cold shock. Archives of Microbiology. 1996 ; 166 (5). 293-300
19. Greenacre EJ, Brocklehurst TF, Waspe CR, Wilson DR, Wilson PDG. Salmonella enterica serovar Typhimurium and Listeria monocytogenes acid tolerance response induced by organic acids at 20 °C: optimization and modeling. Applied and Environmental Microbiology. 2003 ; 69 (7). 3945-3951
20. Hsin-Yi C, Chou CC. Acid adaptation and temperature effect on the survival of E. coli O157:H7 in acidic fruit juice and lactic fermented milk product. International Journal of Food Microbiology. 2001 ; 70 (1-2). 189-195
21. Ingham SC, Su YC, Spangenberg DS. Survival of Salmonella Typhimurium and Escherichia coli O157:H7 in cheese brines. International Journal of Food Microbiology. 2000 ; 61 (1). 73-79
22. Inhot AM, Roering AM, Wierzba RK, Faith NG, Luchansky JB. Behaviour of Salmonella Typhimurium DT104 during the manufacture and storage of pepperoni. International Journal of Food Microbiology. 1998 ; 40 (1-2). 117-121
23. Jain S, Bidol SA, Austin JL, Berl E, Elson F, Lemaile-Williams M, et al. Multistate outbreak of Salmonella Typhimurium and Saintpaul infections associated with unpasteurized orange juice - United States, 2005. Clinical Infectious Diseases. 2009 ; 48 (8). 1065-1071
24. Kieboom J, Abee T. Arginine-dependent acid resistance in Salmonella enterica serovar Typhimurium. Journal of Bacteriology. 2006 ; 188 (15). 5650-5653
25. Koutsoumanis KP, Kendall PA, Sofos JN. Effect of food processing-related stresses on acid tolerance of Listeria monocytogenes. Applied and Environmental Microbiology. 2003 ; 69 (12). 7514-7516
26. Koutsoumanis KP, Sofos JN. 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 (4). 321-326
27. Leuschner RG, Boughtflower MP. Standarized laboratory-scale preparation of mayonnaise containing low levels of Salmonella enterica serovar Enteritidis. Journal of Food Protection. 2001 ; 64 (5). 623-629
28. Leyer GJ, Johnson EA. Acid adaptation promotes survival of Salmonella spp. in cheese. Applied and Environmental Microbiology. 1992 ; 58 (6). 2075-2080
29. Nedwell DB, Rutter M. Influence of temperature on growth rate and composition between two psychrotolerant Antarctic bacteria: low temperature diminishes affinity for substrate uptake. Applied and Environmental Microbiology. 1994 ; 60 (6). 1984-1992
30. Oyarzábal OA, Nogueira MCL, Gombas DE. Survival of Escherichia coli O157:H7, Listeria monocytogenes and Salmonella in juice concentrates. Journal of Food Protection. 2003 ; 66 (9). 1595-1598
31. Parish ME. Public health and nonpasteurized fruit juices. Critical Reviews in Microbiology. 1997 ; 23 (2). 109-119
32. Parish ME. Coliforms, Escherichia coli and Salmonella serovars associated with a citrus-processing facility implicated in a salmonellosis outbreak. Journal of Food Protection. 1998 ; 61 (3). 280-284
33. Parish ME, Narciso JA, Friedrich LM. Survival of salmonellae in orange juice. Journal of Food Safety. 1997 ; 17 (4). 273-281
34. Park YK, Bearson B, Bang SH, Bang IS, Foster JW. Internal pH crisis, lysine decarboxylase and the acid tolerance response of Salmonella Typhimurium. Molecular Microbiology. 1996 ; 20 (3). 605-611
35. Porto-Fett ACS, Hwang CA, Call JE, Juneja VK, Ingham SC, Ingham BH, et al. Viability of multi-strain mixtures of Listeria monocytogenes, Salmonella Typhimurium, or Escherichia coli O157:H7 inoculated into the batter or onto the surface of a soudjouk-style fermented semi-dry sausage. Food Microbiology. 2008 ; 25 (6). 793-801
36. Real Decreto 179/2003 (2003, February 18). Por el que se aprueba la Norma de Calidad para el yogur o yoghourt. Boletín Oficial del Estado 42: 6448-6450. Available at: http://www.boe.es/boe/dias/2003/02/18/pdfs/A06448- 06450.pdf.
37. Shen HW, Yu RC, Chou CC. Acid adaptation affects the viability of Salmonella Typhimurium during the lactic fermentation of skim milk and product storage. International Journal of Food Microbiology. 2007 ; 114 (3). 380-385
38. Skandamis PN, Stopforth JD, Yoon Y, Kendall PA, Sofos JN. Heat and acid tolerance responses of Listeria monocytogenes as affected by sequential exposure to hurdles during growth. Journal of Food Protection. 2009 ; 72 (7). 1412-1418
39. Sospedra I, Rubert J, Soriano JM, Mañes J. Incidence of microorganisms from fresh orange juice processed by squeezing machines. Food Control. 2012 ; 23 (1). 282-285
40. Stopforth JD, Skandamis PN, Geornaras I, Sofos JN. Acid tolerance of acid-adapted and non-acid adapted Escherichia coli O157:H7 strains in beef decontamination runoff fluids or on beef tissue. Food Microbiology. 2007 ; 24 (5). 530-538
41. Tosun H, Gönül SA. Acid adaptation protects Salmonella Typhimurium from environmental stresses. Turkish Journal of Biology. 2003 ; 27: 31-36
42. Uljas HE, Ingham SC. Survival of Escherichia coli O157:H7 in synthetic gastric fluid after cold and acid habituation in apple juice or tripticase soy broth acidified with hydrochloric acid or organic acids. Journal of Food Protection. 1998 ; 61 (8). 939-947
43. Vojdani JD, Beuchat LR, Tauxe RV. Juice-associated outbreaks of human illness in the United States, 1995 through 2005. Journal of Food Protection. 2008 ; 71 (2). 356-364
44. Waterman SR, Small PLC. 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. 1998 ; 64 (10). 3882-3886