Comparison of desiccation tolerance among Listeria monocytogenes, Escherichia coli O157:H7, Salmonella enterica, and Cronobacter sakazakii in powdered infant formula

Journal of Food Protection

Volumn 78, Issue 1, 2015, Pages 104-110

  Koseki, Shigenobu ^a,b   Nakamura, Nobutaka ^b   Shiina, Takeo ^b  

^a HOKKAIDO UNIVERSITY   (Japan)

^b NATIONAL FOOD RESEARCH INSTITUTE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; LISTERIA MONOCYTOGENES; SALMONELLA; SALMONELLA ENTERICA;

ARTIFICIAL MILK; BACTERIAL PHENOMENA AND FUNCTIONS; CRONOBACTER SAKAZAKII; DESICCATION; ESCHERICHIA COLI O157; FOOD CONTROL; FOOD STORAGE; HUMAN; INFANT; LISTERIA MONOCYTOGENES; MICROBIAL VIABILITY; MONTE CARLO METHOD; PHYSIOLOGY; SALMONELLA ENTERICA; TEMPERATURE;

BACTERIAL PROCESSES; CRONOBACTER SAKAZAKII; DESICCATION; ESCHERICHIA COLI O157; FOOD MICROBIOLOGY; FOOD STORAGE; HUMANS; INFANT; INFANT FORMULA; LISTERIA MONOCYTOGENES; MICROBIAL VIABILITY; MONTE CARLO METHOD; SALMONELLA ENTERICA; TEMPERATURE;

EID: 84920903891     PISSN: 0362028X     EISSN: 19449097     Source Type: Journal    
DOI: 10.4315/0362-028X.JFP-14-249     Document Type: Article

References (38)

1. Archer, J., E. T. Jervis, J. Bird, and J. E. Gaze. 1998. Heat resistance of Salmonella weltevreden in low-moisture environments. J. Food Prot. 61:969-973.
2. Aurass, P., R. Prager, and A. Flieger. 2011. EHEC/EAEC O104:H4 strain linked with the 2011 German outbreak of haemolytic uremic syndrome enters into the viable but non-culturable state in response to various stresses and resuscitates upon stress relief. Environ. Microbiol. 13:3139-3148.
3. Beuchat, L. R., H. Kim, J. B. Gurtler, L.-C. Lin, J.-H. Ryu, and G. M. Richards. 2009. Cronobacter sakazakii in foods and factors affecting its survival, growth, and inactivation. Int. J. Food Microbiol. 136:204-213.
4. Beuchat, L. R., E. Komitopoulou, H. Beckers, R. P. Betts, F. Bourdichon, S. Fanning, H. M. Joosten, and B. H. Ter Kuile. 2013. Low-water activity foods: increased concern as vehicles of foodborne pathogens. J. Food Prot. 76:150-172.
5. Beutin, L., and A. Martin. 2012. Outbreak of shiga toxin-producing Escherichia coli (STEC) O104:H4 infection in Germany causes a paradigm shift with regard to human pathogenicity of STEC strains. J. Food Prot. 75:408-418.
6. Bowen, A. B., and C. R. Braden. 2006. Invasive Enterobacter sakazakii disease in infants. Emerg. Infect. Dis. 12:1185-1189.
7. Centers for Disease Control and Prevention. 2007. Multistate outbreak of Salmonella serotype Tennessee infections associated with peanut butter - United States, 2006-2007. Morb. Mortal. Wkly. Rep. 56:521-524.
8. Centers for Disease Control and Prevention. 2009. Multistate outbreak of Salmonella infections associated with peanut butter and peanut butter-containing products - United States, 2008-2009. Morb. Mortal. Wkly. Rep. 58:85-90.
9. Corradini, M. G., and M. Peleg. 2004. Demonstration of the applicability of the Weibull-log-logistic survival model to the isothermal and nonisothermal inactivation of Escherichia coli K-12 MG1655. J. Food Prot. 67:2617-2621.
10. Edelson-Mammel, S. G., M. K. Porteous, and R. L. Buchanan. 2005. Survival of Enterobacter sakazakii in a dehydrated powdered infant formula. J. Food Prot. 68:1900-1902.
11. Elmnasser, N., M. Ritz-Bricaud, S. Guillou, F. Leroi, N. Orange, A. Bakhrouf, and M. Federighi. 2006. Adaptative response of Listeria monocytogenes to osmotic and chill stress: consequences on food safety. Rev. Med. Vet. Toulouse 157:92-101.
12. Gill, O. N., P. N. Sockett, C. L. Bartlett, M. S. Vaile, B. Rowe, R. J. Gilbert, C. Dulake, H. C. Murrell, and S. Salmaso. 1983. Outbreak of Salmonella napoli infection caused by contaminated chocolate bars. Lancet 321:574-577.
13. Gurtler, J. B., and L. R. Beuchat. 2007. Survival of Enterobacter sakazakii in powdered infant formula as affected by composition, water activity, and temperature. J. Food Prot. 70:1579-1586.
14. Gurtler, J. B., J. L. Kornacki, and L. R. Beuchat. 2005. Enterobacter sakazakii: a coliform of increased concern to infant health. Int. J. Food Microbiol. 104:1-34.
15. Isaacs, S., J. Aramini, B. Ciebin, J. A. Farrar, R. Ahmed, D. Middleton, A. U. Chandran, L. J. Harris, M. Howes, E. Chan, A. S. Pichette, K. Campbell, A. Gupta, L. Y. Lior, M. Pearce, C. Clark, F. Rodgers, F. Jamieson, I. Brophy, A. Ellis, for the Salmonella Enteritidis PT30 Outbreak Investigation Working Group. 2005. An international outbreak of Salmonellosis associated with raw almonds contaminated with a rare phage type of Salmonella Enteritidis. J. Food Prot. 68:191-198.
16. Iversen, C., and S. Forsythe. 2003. Risk profile of Enterobacter sakazakii, an emergent pathogen associated with infant milk formula. Trends Food Sci. Technol. 14:443-454.
17. Kandhai, M. C., M. W. Reij, M. van Schothorst, L. G. M. Gorris, and M. H. Zwietering. 2010. Inactivation rates of Cronobacter spp. and selected other bacterial strains in powdered infant formulae stored at different temperatures. J. Food Prot. 73:839-848.
18. Kapperud, G., S. Gustavsen, I. Hellesnes, A. H. Hansen, J. Lassen, J. Hirn, M. Jahkola, M. A. Montenegro, and R. Helmuth. 1990. Outbreak of Salmonella typhimurium infection traced to contaminated chocolate and caused by a strain lacking the 60-megadalton virulence plasmid. J. Clin. Microbiol. 28:2597-2601.
19. Kenney, S. J., and L. R. Beuchat. 2004. Survival, growth, and thermal resistance of Listeria monocytogenes in products containing peanut and chocolate. J. Food Prot. 67:2205-2211.
20. Kimber, M. A., H. Kaur, L. Wang, M. D. Danyluk, and L. J. Harris. 2012. Survival of Salmonella, Escherichia coli O157:H7, and Listeria monocytogenes on inoculated almonds and pistachios stored at 219, 4, and 24°C. J. Food Prot. 75:1394-1403.
21. Koseki, S., and K. Yamamoto. 2007. Water activity of bacterial suspension media unable to account for the baroprotective effect of solute concentration on the inactivation of Listeria monocytogenes by high hydrostatic pressure. Int. J. Food Microbiol. 115:43-47.
22. Lehmacher, A., J. Bockemühl, and S. Aleksic. 1995. Nationwide outbreak of human salmonellosis in Germany due to contaminated paprika and paprika-powdered potato chips. Epidemiol. Infect. 115:501-511.
23. Lleo, M. M., B. Bonato, M. C. Tafi, C. Signoretto, M. Boaretti, and P. Canepari. 2001. Resuscitation rate in different enterococcal species in the viable but non-culturable state. J. Appl. Microbiol. 91:1095-1102.
24. Mafart, P., O. Couvert, S. Gaillard, and I. Leguerinel. 2002. On calculating sterility in thermal preservation methods: application of the Weibull frequency distribution model. Int. J. Food Microbiol. 72:107-113.
25. Mattick, K. L., F. Jorgensen, P. Wang, J. Pound, M. Vandeven, L. Ward, J. Legan, H. Lappin-Scott, and T. Humphrey. 2001. Effect of challenge temperature and solute type on heat tolerance of Salmonella serovars at low water activity. Appl. Environ.Microbiol. 67:4128-4136.
26. Mattick, K. L., J. D. Legan, T. J. Humphrey, and M. Peleg. 2001. Calculating Salmonella inactivation in nonisothermal heat treatments from isothermal nonlinear survival curves. J. Food Prot. 64:606-613.
27. Miller, B. D., C. E. Rigdon, J. Ball, J. M. Rounds, R. F. Klos, B. M. Brennan, K. D. Arends, P. Kennelly, C. Hedberg, and K. E. Smith. 2012. Use of traceback methods to confirm the source of a multistate Escherichia coli O157:H7 outbreak due to in-shell hazelnuts. J. Food Prot. 75:320-327.
28. Neil, K. P., G. Biggerstaff, J. K. MacDonald, E. Trees, C. Medus, K. A. Musser, S. G. Stroika, D. Zink, and M. J. Sotir. 2012. A novel vehicle for transmission of Escherichia coli O157:H7 to humans: multistate outbreak of E. coli O157:H7 infections associated with consumption of ready-to-bake commercial prepackaged cookie dough-United States, 2009. Clin. Infect. Dis. 54:511-518.
29. Peleg, M., and M. D. Normand. 2004. Calculating microbial survival parameters and predicting survival curves from non-isothermal inactivation data. Crit. Rev. Food Sci. 44:409-418.
30. Peleg, M., and C. M. Penchina. 2000. Modeling microbial survival during exposure to a lethal agent with varying intensity. Crit. Rev. Food Sci. 40:159-172.
31. Peleg, M., C. M. Penchina, and M. B. Cole. 2001. Estimation of the survival curve of Listeria monocytogenes during non-isothermal heat treatments. Food Res. Int. 34:383-388.
32. Pin, C., T. Hansen, M. Muñoz-Cuevas, R. de Jonge, J. T. Rosenkrantz, C. Löfström, H. Aarts, and J. E. Olsen. 2012. The transcriptional heat shock response of Salmonella Typhimurium shows hysteresis and heated cells show increased resistance to heat and acid stress. PLoS One 7:e51196.
33. Podolak, R., E. Enache, W. Stone, D. G. Black, and P. H. Elliott. 2010. Sources and risk factors for contamination, survival, persistence, and heat resistance of Salmonella in low-moisture foods. J. Food Prot. 73:1919-1936.
34. Rowan, N. J. 2004. Viable but non-culturable forms of food and waterborne bacteria: quo vadis? Trends Food Sci. Technol. 15:462-467.
35. Shachar, D., and S. Yaron. 2006. Heat tolerance of Salmonella enterica serovars Agona, Enteritidis, and Typhimurium in peanut butter. J. Food Prot. 69:2687-2691.
36. Spotts Whitney, E. A., M. E. Beatty, T. H. Taylor, R. Weyant, J. Sobel, M. J. Arduino, and D. A. Ashford. 2003. Inactivation of Bacillus anthracis Spores. Emerg. Infect. Dis. 9:623-627.
37. van Bokhorst-van de Veen, H., T. Abee, M. Tempelaars, P. A. Bron, M. Kleerebezem, and M. L. Marco. 2011. Short- and long-term adaptation to ethanol stress and its cross-protective consequences in Lactobacillus plantarum. Appl. Environ. Microbiol. 77:5247-5256.
38. Werber, D., J. Dreesman, F. Feil, U. van Treeck, G. Fell, S. Ethelberg, A. M. Hauri, P. Roggentin, R. Prager, I. S. T. Fisher, S. C. Behnke, E. Bartelt, E. Weise, A. Ellis, A. Siitonen, Y. Andersson, H. Tschäpe, M. H. Kramer, and A. Ammon. 2005. International outbreak of Salmonella Oranienburg due to German chocolate. BMC Infect. Dis. 5:7.