Individual and combined application of dry heat with high hydrostatic pressure to inactivate Salmonella and Escherichia coli O157:H7 on alfalfa seeds

Food Microbiology

Volumn 28, Issue 1, 2011, Pages 119-127

  Neetoo, Hudaa ^a   Chen, Haiqiang ^a  

^a UNIVERSITY OF DELAWARE   (United States)

Author keywords

Dry heat; Escherichia coli O157:H7; High pressure; Salmonella; Seeds

Indexed keywords

ALFALFA; ARTICLE; BACTERIAL COUNT; DESICCATION; ESCHERICHIA COLI O157; FOOD CONTROL; FOOD HANDLING; GERMINATION; GROWTH, DEVELOPMENT AND AGING; HEAT; HYDROSTATIC PRESSURE; METHODOLOGY; MICROBIOLOGY; PLANT SEED; PRODUCT SAFETY; SALMONELLA; WASTE MANAGEMENT;

COLONY COUNT, MICROBIAL; CONSUMER PRODUCT SAFETY; DECONTAMINATION; DESICCATION; ESCHERICHIA COLI O157; FOOD HANDLING; FOOD MICROBIOLOGY; GERMINATION; HOT TEMPERATURE; HYDROSTATIC PRESSURE; MEDICAGO SATIVA; SALMONELLA; SEEDS;

ESCHERICHIA COLI; MEDICAGO SATIVA; SALMONELLA;

EID: 78149376868     PISSN: 07400020     EISSN: 10959998     Source Type: Journal    
DOI: 10.1016/j.fm.2010.09.004     Document Type: Article

References (59)

1. Baird-Parker A.C., Boothroyd M., Jones E. The effect of water activity on the heat resistance of heat sensitive and heat resistant strains of Salmonella. J. Appl. Bacteriol. 1970, 33:515-522.
2. Balasubramaniam V.M., Ting E.Y., Stewart C.M., Robbins J.A. Recommended laboratory practices for conducting high-pressure microbial experiments. Innov. Food Sci. Emerg. Technol. 2004, 5:299-306.
3. Barak J.D., Whitehand L.C., Charkowski A.O. Differences in attachment of Salmonella Enterica serovars and Escherichia coli O157:H7 to alfalfa sprouts. Appl. Environ. Microbiol. 2002, 68:4758-4763.
4. Barak J.D., Delwiche M.J., Sananikone K. Comparison of primers for the detection of pathogenic Escherichia coli using real-time PCR. Lett. Appl. Microbiol. 2005, 41:112-118.
5. Bari M.L., Nazuka E., Sabina Y., Todoriki S., Isshiki K. Chemical and irradiation treatments for killing Escherichia coli O157:H7 on alfalfa, radish, and mung bean seeds. J. Food Prot. 2003, 66:767-774.
6. Bari M.L., Todoriki S., Kawamoto S., Nei D., Enomoto K. Combination treatments for killing Escherichia coli O157:H7 on alfalfa, radish, broccoli, and mung bean seeds. J. Food Prot. 2009, 72:631-636.
7. Bari M.L., Kawamoto S., Sugiyama J. Repeated quick hot-and-chilling treatments for the inactivation of Escherichia coli O157:H7 in mung bean and radish seeds. Foodborne Pathog. Dis. 2009, 6:137-143.
8. Basavarajappa B.S., Shetty S.H., Prakash H.S. Membrane deterioration and other biochemical changes associated with accelerated ageing of maize seeds. Seed Sci. Technol. 1991, 19:279-286.
9. Betts, R., 2007. Water, water, everywhere nor any drop to drink - The problem of Salmonella in low-moisture foods. IAFP Special Interest Session on Salmonella growth, persistence and survival in low-moisture foods and their environment - strategies for control. IAFP annual meeting, July 8-11, Buena Vista, Florida.
10. Beuchat L.R., Scouten A.J. Combined effects of water activity, temperature and chemical treatments on the survival of Salmonella and Escherichia coli O157:H7 on alfalfa seeds. J. Appl. Microbiol. 2002, 92:382-395.
11. Bhagwat A.A., Chan L., Han R., Tan J., Kothary M., Jean-Gilles J., Tall B.D. Characterization of enterohemorrhagic Escherichia coli strains based on acid resistance phenotypes. Infect. Immun. 2005, 73:4993-5003.
12. Centers for Disease Control and Prevention Annual Listing of Foodborne Disease Outbreaks 2008, Available at:, CDC, Atlanta, GA. http://www.cdc.gov/foodborneoutbraks/outbreak_data.htm.
13. Chapman B. Sprouts Associated Outbreaks in North America, 1990-2009. Accessed on from Ben Chapman Bites 2009, Food Safety Network, (accessed 05.14.09.). http://foodsafety.k-state.edu/en/article-details.php%3Fa_2%26c_6%26sc_36%26id_865.
14. Chen H., Hoover D.G., Kingsley D.H. Temperature and treatment time influence high hydrostatic pressure inactivation of feline calicivirus, a norovirus surrogate. J. Food Prot. 2005, 68:2389-2394.
15. Chen H., Guan D., Hoover D.G. Sensitivities of food-borne pathogens to pressure changes. J. Food Prot. 2006, 69:130-136.
16. Chen H. Temperature-assisted pressure inactivation of Listeria monocytogenes in turkey breast meat. Int. J. Food Microbiol. 2007, 117:55-60.
17. Cotterill O.J., Glauert J. Thermal resistance of salmonellae in egg yolk containing 10% sugar or salt after storage at various temperatures. Poult. Sci. 1971, 50:109-115.
18. Doyle M.E., Mazzotta A.S. Review of studies on the thermal resistance of salmonellae. J. Food Prot. 2000, 63:779-795.
19. Farooq M., Basra S.M.A., Hafeez K., Warriach E.A. Influence of high- and low-temperature treatments on seed germination and seedling vigor of coarse and fine rice. Int. Rice Res. Notes 2004, 29:75-77.
20. Feng G., Churey J.J., Worobo R.W. Thermal Inactivation of Salmonella and Escherichia coli O157:H7 on alfalfa seeds. J. Food Prot. 2007, 70:1698-1703.
21. Fett W.F., Cooke P.H. A survey of native microbial aggregates on alfalfa, clover and mung bean sprout cotyledons for thickness as determined by confocal scanning laser microscopy. Food Microbiol. 2005, 22:253-259.
22. Fett W.F., Tortorello M., Fu T. Seed sprouts: the state of microbiological safety. Microbiology of Fresh Produce 2005, 167-219. ASM Press, Washington, D.C. K.R. Matthews (Ed.).
23. Goepfert J.M., Biggie R.A. Heat resistance of Salmonella Typhimurium and Salmonella Senftenberg 775W in milk chocolate. Appl. Microbiol. 1968, 16:1939-1940.
24. Gutierrez E. Japan prepares as O157 strikes again. Lancet 1997, 349:1156.
25. Hansen N.H., Riemann H. Factors affecting the heat resistance of non-sporing organisms. J. Appl. Bacteriol. 1963, 26:314-333.
26. Hogan E., Kelly A., Sun D.W. High pressure processing of foods: an overview. Emerging Technologies for Food Processing 2005, 3-32. Elsevier Academic Press, London. D.W. Sun (Ed.).
27. Hora R., Kumar M., Kostrzynska M., Dixon M.A., Warriner K. Inactivation of Escherichia coli O157:H7 and Salmonella on artificially or naturally contaminated mung beans (Vigna radiata L) using a stabilized oxychloro-based sanitizer. Lett. Appl. Microbiol. 2007, 44:188-193.
28. Hu H., Churey J.J., Worobo R.W. Heat treatments to enhance the safety of mung bean seeds. J. Food Prot. 2004, 67:1257-1260.
29. Humphrey T. Salmonella Typhimurium definitive type 104: a multi-resistant Salmonella. Int. J. Food Microbiol. 2001, 67:173-186.
30. Ibrahim S.A., Salameh M.M., Phetsomphou S., Yang H., Seo C.W. Application of caffeine, 1,3,7-trimethylxanthine, to control Escherichia coli O157:H7. Food Chem. 2006, 99:645-650.
31. Jaquette C.B., Beuchat L.R., Mahon B.E. Efficacy of chlorine and heat treatment in killing Salmonella Stanley inoculated onto alfalfa seeds and growth and survival of the pathogen during sprouting and storage. Appl. Environ. Microbiol. 1996, 62:2212-2215.
32. Kingsley D.H., Guan D., Hoover D.G., Chen H. Inactivation of hepatitis A virus by high pressure processing: the role of temperature and pressure oscillation. J. Food Prot. 2006, 69:2454-2459.
33. Kirby R.M., Davies R. Survival of dehydrated cells of Salmonella Typhimurium LT2 at high temperatures. J. Appl. Bacteriol. 1990, 68:241-246.
34. Kural A.G., Chen H. Conditions for a 5-log reduction of Vibrio vulnificus in oysters through high hydrostatic pressure treatment. Int. J. Food Microbiol. 2008, 122:180-187.
35. Kural A.G., Kingsley D.H., Shearer A.E.H., Chen H. Conditions for high pressure inactivation of Vibrio parahaemolyticus in oysters. Int. J. Food Microbiol. 2008, 127:1-5.
36. Liu T.S., Snoeyenbos G.H., Carlson V.L. Thermal resistance of Salmonella Senftenberg 775W in dry animal feeds. Avian Dis. 1969, 13(6):611-631.
37. Martin R.E., Cushwa C.T. Effects of heat and moisture on leguminous seed. Proc. Annu. Tall Timbers Fire Ecol. Conf. 1966, 5:159-175.
38. Mattick K.L., Jorgensen F., Legan J.D., Lappin-Scott H., Humphrey T.J. Habituation of Salmonella spp. at reduced water activity and its effect on heat tolerance. Appl. Environ. Microbiol. 2000, 66:4921-4925.
39. Meyerowitz S. Sprouts: The Miracle Food 1999, Sproutman Publications, Massachusetts, 57-79.
40. Neetoo H., Ye M., Chen H. Potential application of high hydrostatic pressure to eliminate Escherichia coli O157:H7 on alfalfa sprouted seeds. Int. J. Food Microbiol. 2008, 128:348-353.
41. Neetoo H., Chen H., Pizzolato T. Elimination of Escherichia coli O157:H7 from alfalfa seeds through a combination of high hydrostatic pressure and mild heat. Appl. Environ. Microbiol. 2009, 75:1901-1907.
42. Neetoo H., Chen H. Inactivation of Salmonella and Escherichia coli O157:H7 on artificially contaminated alfalfa seeds using high hydrostatic pressure. Food Microbiol. 2010, 27:332-338.
43. Ng H., Bayne H.G., Garibaldi J.A. Heat resistance of Salmonella: the uniqueness of Salmonella Seftenberg775W. Appl. Microbiol. 1969, 17:78-82.
44. O'Mahony M., Cowden J., Smyth B., Lynch D., Hall M., Rowe B., Tearle E.L., Tettmar R.E., Rampling A.S., Coles M., Gilbert R.J., Kingcott R.J., Barlett C.L.R. An outbreak of Salmonella Saintpaul infection associated with bean sprouts. Epidemiol. Infect. 1990, 104:229-235.
45. Ponce E., Pla R., Capellas M., Guamis B., Mor-Mur M. Inactivation of Escherichia coli inoculated in liquid whole egg by high hydrostatic pressure. Food Microbiol. 1998, 15:265-272.
46. Ponce E., Pla R., Sendra E., Guamis B., Mor-Mur M. Destruction of Salmonella enteritidis inoculated in liquid whole egg by high hydrostatic pressure: comparative study in selective and non-selective media. Food Microbiol. 1999, 16:357-365.
47. Ponka A., Anderson Y., Sitonen A., DeJong B., Jahkola M., Haikala O., Kuhmonen A., Pakkala P. Salmonella in alfalfa sprouts. Lancet 1995, 345:462-463.
48. Proctor M.E., Hamacher M., Tortorello M.L., Archer J.R., Davis J.P. Multistate outbreak of Salmonella serovar Muenchen infections associated with alfalfa sprouts grown from seeds pretreated with calcium hypochlorite. J. Clin. Microbiol. 2001, 39:3461-3465.
49. Puohiniemi R., Heiskanen T., Sitonen A. Molecular epidemiology of two international sprout-borne Salmonella outbreaks. J. Clin. Microbiol. 1997, 35:2487-2491.
50. Rajkowski K.T., Thayer D.W. Alfalfa seed germination and yield ratio and alfalfa sprout microbial keeping quality following irradiation of seeds and sprouts. J. Food Prot. 2001, 64:1988-1995.
51. Riemann H. Effect of water activity on the heat resistance of Salmonella in 'dry' materials. Appl. Microbiol. 1968, 16:1621-1622.
52. Romling U., Bian Z., Hammar M., Sierralta W.D., Normark S. Curli fibers are highly conserved between Salmonella Typhimurium and Escherichia coli with respect to operon structure and regulation. J. Bacteriol. 1998, 180:722-731.
53. Staker E.V. The effect of dry heat on alfalfa and its adulterants. J. Am. Soc. Agron. 1925, 17:32-40.
54. Stewart G. Effect of color of seed, of scarification, and of dry heat on the germination of alfalfa seed and some of its impurities. J. Am. Soc. Agron. 1926, 18:743-761.
55. Sumner S.S., Sandros T.M., Harmon M.C., Scott V.N., Bernard D.T. Heat resistance of Salmonella Typhimurium and Listeria monocytogenes in sucrose solutions of various water activities. J. Food Sci. 1991, 56:1741-1743.
56. Taormina P.J., Beuchat L.R., Slutsker L. Infections associated with eating seed sprouts: an international concern. Emerg. Infect. Dis. 1999, 5:626-634.
57. Van Beneden C.A., Keene W.E., Stang R.A., Werker D.H., King A.S., Mahon B., Hedberg K., Bell A., Kelly M.T., Balan V.K., MacKenzie W.R., Fleming D. Multinational outbreak of Salmonella Enterica serotype Newport infections due to contaminated alfalfa sprouts. J. Am. Med. Assoc. 1999, 281:158-162.
58. Wang B.S.P., Berjak P. Beneficial effects of moist chilling on the seeds of black spruce (Picea mariana [Mill.] B.S.P.). Ann. Bot. 2000, 86:29-36.
59. Zink, D., 2007. The return of Salmonella. IAFP Special Interest Session on Salmonella growth, persistence and survival in low-moisture foods and their environment - strategies for control. IAFP annual meeting, July 8-11, Buena Vista, Florida.