Selection of surrogate bacteria in place of E. coli O157:H7 and Salmonella Typhimurium for pulsed electric field treatment of orange juice

International Journal of Food Microbiology

Volumn 139, Issue 1-2, 2010, Pages 1-8

  Gurtler, Joshua B ^a   Rivera, Rebecca B ^a   Zhang, Howard Q ^a   Geveke, David J ^a  

^a EASTERN REGIONAL RESEARCH CENTER   (United States)

Author keywords

E. coli O157:H7; Non pathogenic surrogate bacteria; Orange juice; Pulsed electric field; Salmonella

Indexed keywords

ARTICLE; BACTERIAL STRAIN; COLONY FORMING UNIT; ESCHERICHIA COLI O157; FOOD PROCESSING; FOOD SAFETY; KINETICS; NONHUMAN; ORANGE JUICE; PASTEURIZATION; PULSED ELECTRIC FIELD; SALMONELLA; SALMONELLA TYPHIMURIUM; TEMPERATURE;

BEVERAGES; CITRUS SINENSIS; ELECTRICITY; ESCHERICHIA COLI; ESCHERICHIA COLI O157; FOOD MICROBIOLOGY; FOOD PRESERVATION; FRUIT; LACTOBACILLUS; MICROBIAL VIABILITY; SALMONELLA; SALMONELLA TYPHIMURIUM;

BACTERIA (MICROORGANISMS); SALMONELLA; SALMONELLA TYPHIMURIUM;

EID: 77949913158     PISSN: 01681605     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2010.02.023     Document Type: Article

References (55)

1. Alkhafaji S., Farid M. Modeling the inactivation of Escherichia coli ATCC 25922 using pulsed electric field. Innovative Food Science and Emerging Technologies 2008, 9:448-454.
2. American Type Culture Collection, Manassas, VA, website, available at Accessed on February 24, 2009. http://www.atcc.org.
3. Beck-Hansen T., Knochel S. Factors influencing resuscitation and growth of heat injured Listeria monocytogenes 13-249 in sous vide cooked beef. International Journal of Food Microbiology 2001, 63:135-147.
4. Borowski A.G., Ingham S.W., Ingham B.H. Validation of ground-and-formed beef jerky processes using commercial lactic acid bacteria starter cultures as pathogen surrogates. Journal of Food Protection 2009, 72:1234-1237.
5. Chapman B., Ross T. Escherichia coli and Salmonella enterica are protected against acetic acid, but not hydrochloric acid, by hypertonicity. Applied and Environmental Microbiology 2009, 75:3605-3610.
6. Cheng H.-Y., Yang H.-Y., Chou C.-C. Influence of acid adaptation on the tolerance of Escherichia coli O157:H7 to some subsequent stresses. Journal of Food Protection 2002, 65:260-265.
7. Cortés C., Esteve M.J., Frígola A. Color of orange juice treated by High Intensity Pulsed Electric Fields during refrigerated storage and comparison with pasteurized juice. Food Control 2008, 19:151-158.
8. Curtiss R., Hassan J.O. Nonrecombinant and recombinant avirulent salmonella vaccines for poultry. Veterinary Immunology and Immunopathology 1996, 54:365-372.
9. Curtiss R., Porter S.B., Munson M., Tinge S.A., Hassan J.O., Gentry-Weeks C., Kelly S.M. Nonrecombinant and recombinant avirulent Salmonella live vaccines for poultry. Colonization Control of Human Bacterial Enteropathogens in Poultry 1991, 169-198. Academic Press, Inc, New York, NY. L.C. Blankenship, J.S. Bailey, N.A. Cox, S.E. Craven, R.J. Meinersmann, N.J. Stern (Eds.).
10. Curtiss, R. III, Tung, K.S.K. Recombinant avirulent Salmonella antifertility vaccines. United States Patent No. 5, 656, 488. August 12, 1997.
11. Duffy G., Riordan D.C.R., Sheridan J.J., Eblen B.S., Whiting R.C., Blair I.S., McDowell D.A. Differences in thermotolerance of various Escherichia coli O157:H7 strains in a salami matrix. Food Microbiology 1999, 16:83-91.
12. Eblen D.R., Annous B.A., Sapers G.M. Studies to select an appropriate nonpathogenic surrogate Escherichia coli strain for potential use in place of Escherichia coli O157:H7 and Salmonella in pilot plant studies. Journal of Food Protection 2005, 68:282-291.
13. Fairchild T.M., Foegeding P.M. A proposed nonpathogenic biological indicator for thermal inactivation of Listeria monocytogenes. Applied and Environmental Microbiology 1993, 59:1247-1250.
14. Kinetics of microbial inactivation for alternative food processing technologies Food and Drug Administration, Available at:, Accessed on April 10, 2009. http://vm.cfsan.fda.gov/;comm/ift-glos.html.
15. Food and Drug Administration Title 21-food and drugs. Part 120-hazard analysis critical control point (HACCP) systems. Subpart 24-process controls. Code of Federal Regulations 2009, U.S. Government Printing Office, Washington, DC.
16. Gailunas K.M., Matak K.E., Boyer R.R., Alvarado C.Z., Williams R.C., Sumner S.S. Use of UV light for the inactivation of Listeria monocytogenes and lactic acid bacteria species in recirculated chill brines. Journal of Food Protection 2008, 71:629-633.
17. Garren M.G., Harrison M.A., Russell S.M. Retention of acid tolerance and acid shock responses of Escherichia coli O157:H7 and non-O157:H7 isolates. Journal of Food Protection 1997, 60:1478-1482.
18. Geveke D.J., Gurtler J.B., Zhang H.Q. Inactivation of Lactobacillus plantarum in apple cider, using radio frequency electric fields. Journal of Food Protection 2009, 72:656-661.
19. Guerrero-Beltrán J.A., Barboza-Cánovas G.V. Reduction of Saccharomyces cerevisiae, Escherichia coli and Listeria innocua in apple juice by ultraviolet light. Journal of Food Process Engineering 2005, 28:437-452.
20. Gunes G., Blum L.K., Hotchkiss J.H. Inactivation of Escherichia coli (ATCC 4157) in diluted apple cider by dense phase carbon dioxide. Journal of Food Protection 2006, 69:12-16.
21. Gupta B.S., Masterson F., Magee T.R.A. Inactivation of E. coli K12 in apple juice by high voltage pulsed electric field. European Food Research and Technology 2003, 217:434-437.
22. Gupta B.S., Masterson F., Magee T.R.A. Inactivation of E. coli in cranberry juice by a high voltage pulsed electric field. Engineering in Life Sciences 2005, 5:148-151.
23. Hassan J.O., Curtiss R.I.I.I. Control of colonization by virulent Salmonella typhimurium by oral immunization of chickens with avirulent Δcya Δcrp S. typhimurium. Research in Microbiology 1990, 141:839-850.
24. Hassan J.O., Curtiss R.I.I.I. Development and evaluation of an experimental vaccination program using a live avirulent Salmonella typhimurium strain to protect immunized chickens against challenge with homologous and heterologous Salmonella serotypes. Infection and Immunity 1994, 62:5519-5527.
25. Islam M., Morgan J., Doyle M.P., Phatak S.C., Millner P., Jiang X. Fate of Salmonella enterica Serovar Typhimurium on carrots and radishes grown in fields treated with contaminated manure composts or irrigation water. Applied and Environmental Microbiology 2004, 70:2497-2502.
26. Islam M., Morgan J., Doyle M.P., Phatak S.C., Millner P., Jiang X. Persistence of Salmonella enterica serovar typhimurium on lettuce and parsley and in soils on which they were grown in fields treated with contaminated manure composts or irrigation water. Foodborne Pathogens and Disease 2004, 1:27-35.
27. Iu J., Mittal G.S., Griffiths M.W. Reduction in levels of Escherichia coli O157:H7 in apple cider by pulsed electric fields. Journal of Food Protection 2001, 64:964-969.
28. Jia M., Zhang H.Q., Min D.B. Pulsed electric field processing effects on flavor compounds and microorganisms of orange juice. Food Chemistry 1999, 65:445-451.
29. Jordan S.L., Pascual C., Bracey E., Mackey B.M. Inactivation and injury of pressure-resistant strains of Escherichia coli O157 and Listeria monocytogenes in fruit juices. Journal of Applied Microbiology 2001, 91:463-469.
30. Kaniga K., Compton M.S., Curtiss R., Sundaram P. Molecular and functional characterization of Salmonella enterica serovar Typhimurium poxA gene: effect on attenuation of virulence and protection. Infection and Immunity 1998, 66:5599-5606.
31. Keeling C., Niebuhr S.E., Acuff G.R., Dickson J.S. Evaluation of Escherichia coli biotype I as a surrogate for Escherichia coli O157:H7 for cooking, fermentation, freezing, and refrigerated storage in meat processes. Journal of Food Protection 2009, 72:728-732.
32. Kornacki J.L., Gurtler J.B., Yan Z., Cooper C.M. Evaluation of several modifications of an ecometric technique for assessment of media performance. Journal of Food Protection 2003, 66:1727-1732.
33. Ma L., Kornacki J.L., Zhang G., Lin C.-M., Doyle M.P. Development of thermal surrogate microorganisms in ground beef for in-plant critical control point validation studies. Journal of Food Protection 2007, 70:952-957.
34. Mak P.P., Ingham B.H., Ingham S.C. Validation of apple cider pasteurization treatments against Escherichia coli O157:H7, Salmonella, and Listeria monocytogenes. Journal of Food Protection 2001, 64:1679-1689.
35. Marshall K.M., Niebuhr S.E., Acuff G.R., Lucia L.M., Dickson J.S. Identification of Escherichia coli O157:H7 meat processing indicators for fresh meat through comparison of the effects of selected antimicrobial interventions. Journal of Food Protection 2005, 68:2580-2586.
36. McDonald C.J., Lloyd S.W., Vitale M.A., Petersson K., Innings F. Effects of pulsed electric fields on microorganisms in orange juice using electric field strengths of 30 and 50kV/cm. Journal of Food Science 2000, 65:984-989.
37. Niebuhr S.E., Laury A., Acuff G.R., Dickson J.S. Evaluation of nonpathogenic surrogate bacteria as process validation indicators for Salmonella enterica for selected antimicrobial treatments, cold storage, and fermentation in meat. Journal of Food Protection 2008, 71:714-718.
38. Parameters for determining pack/challenge study protocols. Journal of Food Protection 2010, 73:140-202. National Advisory Committee on the Microbiological Criteria for Foods.
39. Niemira B.A., Sommers C.H., Boyd G. Effect of freezing, irradiation, and frozen storage on survival of Salmonella in concentrated orange juice. Journal of Food Protection 2003, 66:1916-1919.
40. Oteiza J.M., Peltzer M., Gannuzzi L., Zaritzky N. Antimicrobial efficacy of UV radiation on Escherichia coli O157:H7 (EDL 933) in fruit juices of different absorptivities. Journal of Food Protection 2005, 68:49-58.
41. Perni S., Chalise P.R., Shama G., Kong M.G. Bacterial cells exposed to nanosecond pulsed electric fields show lethal and sublethal effects. International Journal of Food Microbiology 2007, 120:311-314.
42. Quintavalla S., Larini S., Mutti P., Barbuti S. Evaluation of the thermal resistance of different Salmonella serotypes in pork meat containing curing additives. International Journal of Food Microbiology 2001, 67:107-114.
43. Sampedro F., Geveke D.J., Fan X., Rodrigo D., Zhang Q.H. Shelf-life study of an orange juice-milk based beverage after PEF and thermal processing. Journal of Food Science 2009, 74:S107-S112.
44. Sheehan V.M., Ross P., Fitzgerald G.F. Assessing the acid tolerance and the technological robustness of probiotic cultures for fortification in fruit juices. Innovative Food Science and Emerging Technologies 2007, 8:279-284.
45. Somolinos M., García D., Mañas P., Condón S., Pagán R. Effect of environmental factors and cell physiological state on pulsed electric fields resistance and repair capacity of various strains of Escherichia coli. International Journal of Food Microbiology 2008, 124:260-267.
46. Unal R., Kim J., Yousef A.E. Inactivation of Escherichia coli O157:H7, Listeria monocytogenes, and Lactobacillus leichmannii by combinations of ozone and pulsed electric field. Journal of Food Protection 2001, 64:777-782.
47. Ukuku D.O., Geveke D.J., Cooke P., Zhang H.Q. Membrane damage and viability loss of Escherichia coli K-12 in apple juice treated with radio frequency electric field. Journal of Food Protection 2008, 71:684-690.
48. Ukuku D.O., Jin T., Zhang H. Membrane damage and viability loss of Escherichia coli K-12 and Salmonella enteritidis in liquid egg by thermal death time disk treatment. Journal of Food Protection 2008, 71:1988-1995.
49. Walkling-Ribeiro M., Noci F., Cronin D.A., Lyng J.G., Morgan D.J. Inactivation of Escherichia coli in a tropical fruit smoothie by a combination of heat and pulsed electric fields. Journal of Food Science 2008, 73:M395-M399.
50. Wang G., Doyle M.P. Heat shock response enhances acid tolerance of Escherichia coli O157:H7. Letters in Applied Microbiology 1998, 26(1):31-34.
51. Warf, Jr., C., Hageman, S.D., Piazza, M.C., Richardson, T.G., 2002. Treatment fluid application apparatus for foodstuffs and methods related thereto. United States Patent Application 20, 020, 090, 428.
52. Wesche A.M., Gurtler J.B., Marks B.P., Ryser E.T. Stress, sublethal injury, resuscitation, and virulence of bacterial foodborne pathogens. Journal of Food Protection 2009, 72:1121-1138.
53. Wesierska E., Trziszka T. Evaluation of the use of pulsed electrical field as a factor with antimicrobial activity. Journal of Food Engineering 2007, 78:1320-1325.
54. Yu K., Newman M.C., Archbold D.D., Hamilton-Kemp T.R. Survival of Escherichia coli O157:H7 on strawberry fruit and reduction of the pathogen population by chemical agents. Journal of Food Protection 2001, 64:1334-1340.
55. Zhang X., Kelly S.M., Bollen W., Curtiss R. Protection and immune responses induced by attenuated Salmonella typhimurium UK-1 strains. Microbial Pathogenesis 1999, 26:121-130.