Effects of storage and the presence of a beef microflora on the thermal resistance of Salmonella Typhimurium DT104 in beef and broth systems

M.S. McCann, A.C. McGovern, D.A. McDowell, I.S. Blair, J.J. Sheridan

    Research output: Contribution to journalArticle

    3 Citations (Scopus)
    LanguageEnglish
    Pages1561
    JournalJournal of Applied Microbiology
    Volume102
    Issue number6
    DOIs
    Publication statusPublished - 2007

    Keywords

    • beef
    • beef microflora
    • broth
    • Salmonella Typhimurium DT104
    • thermal resistance

    Cite this

    McCann, M.S. ; McGovern, A.C. ; McDowell, D.A. ; Blair, I.S. ; Sheridan, J.J. / Effects of storage and the presence of a beef microflora on the thermal resistance of Salmonella Typhimurium DT104 in beef and broth systems. In: Journal of Applied Microbiology. 2007 ; Vol. 102, No. 6. pp. 1561.
    @article{3b25814394ed45688066b9909de88e51,
    title = "Effects of storage and the presence of a beef microflora on the thermal resistance of Salmonella Typhimurium DT104 in beef and broth systems",
    keywords = "beef, beef microflora, broth, Salmonella Typhimurium DT104, thermal resistance",
    author = "M.S. McCann and A.C. McGovern and D.A. McDowell and I.S. Blair and J.J. Sheridan",
    note = "Reference text: Aldsworth, T.G., Sharman, R.L., Dodd, C.E.R. and Stewart, G.S.A.B. (1998) A competitive microflora increases the resistance of Salmonella Typhimurium to inimical processes: evidence for a suicide response. Appl Environ Microbiol64, 1323–1327. Anon (2004) Microbiology of food and animal feeding stuffs – horizontal methods for the detection of Salmonella spp. In 2002-07-15, 2004 Amendment, 4th edn. pp. 1–19. Switzerland: International Organisation of Standards [ISO 6579:2000 (E)]. Bacon, R.T., Ransom, J.R., Sofos, J.N., Kendall, P.A., Belk, K.E. and Smith, G.C. (2003) Thermal inactivation of susceptible and multiantimicrobial resistant Salmonella strains grown in the absence or presence of glucose. Appl Environ Microbiol 69, 4123–4128. Bayles, D.O., Tunick, M.H., Foglia, T.A. and Miller, A.J. (2000) Cold shock and its effect on ribosomes and thermal tolerance in Listeria monocytogenes. Appl Environ Microbiol 66, 4351–4355. Berry, E.D. and Koohmaraie, M. (2001) Effect of different levels of beef bacterial microflora on the growth and survival of Escherichia coli O157:H7 on beef carcass tissue. J Food Prot64, 1138–1144. Blackburn, C., Curtis, L.M., Humpheson, L., Billon, C. and McClure, P.J. (1997) Development of thermal inactivation models for Salmonella Enteritidis and Escherichia coli O157:H7 with temperature, pH and NaCl as controlling factors. Int J Food Microbiol 38, 31–44. Byrne, C.M., Bolton, D.J., Sheridan, J.J., Blair, I.S. and McDowell, D.A. (2002) The effect of commercial production and product formulation stresses on the heat resistance of Escherichia coli O157:H7 (NCTC 12900) in beef burgers. Int J Food Microbiol 79, 183–192. Davies, A., O'Neill, P., Towers, L. and Cooke, M. (1996) An outbreak of Salmonella Typhimurium DT104 food poisoning associated with eating beef. Commun Dis Rep11, R159–R162. Doyle, M.E. and Mazzotta, A.S. (2000) Review of studies on the thermal resistance of Salmonellae. J Food Prot63, 779–795. Doyle, M.P. and Schoeni, J.L. (1984) Survival and growth characteristics of Escherichia coli associated with hemorrhagic colitis. Appl Environ Microbiol48, 855–856. Duffy, G., Ellison, A., Anderson, W., Cole, M.B. and Stewart, G.S.A.B. (1995) Use of bioluminescence to model the thermal inactivation of Salmonella Typhimurium in the presence of a competitive microflora. Appl Environ Microbiol61, 3463–3465. Duffy, G., Riordain, D.C.R., Sheridan, J.J., Eblen, B.S., Whiting, R.C., Blair, I.S. and McDowell, D.A. (1999a) Differences in thermotolerance of various Escherichia coli O157:H7 strains in a salami matrix. Food Microbiol 16, 83–91. Duffy, G., Whiting, R.C. and Sheridan, J.J. (1999b) The effect of a competitive microflora, pH and temperature on the growth kinetics of Escherichia coli O157:H7. Food Microbiol 16, 299–307. Ethelberg, S. (2005) Salmonellosis outbreak linked to carpaccio made from imported raw beef, Denmark, June–August 2005. Euro Surveill10, E050922.3. Available from: http://www.eurosurveillance.org/ew/2005/050922.asp#3. Humphrey, T.J. (1990) Heat resistance in Salmonella Enteriditis phage type 4: the influence of storage temperatures before heating. J Appl Bacteriol69, 493–497. Humphrey, T.J. (1998) Pathogenity in isolates of Salmonella enterica serotype Enteritidis PT4 which differ in RpoS expression: effects of growth phase and low temperature. Epidemiol Infect 121, 295–301. Humphrey, T.J (2001) Salmonella Typhimurium definitive type 104. A multi-resistant Salmonella. Int J Food Microbiol67, 173–186. Humphrey, T.J., Wilde, S.J. and Rowbury, R.J. (1997) Heat tolerance of Salmonella Typhimurium DT104 isolates attached to muscle tissue. Lett Appl Microbiol 25, 265–268. Jackson, T.C., Hardin, M.D. and Acuff, G.R. (1995) Heat resistance of Escherichia coli O157:H7 in a nutrient medium and in ground beef patties as influenced by storage and holding temperatures. J Food Prot 59, 230–237. Katsui, N., Tsuchido, T., Takano, M. and Shibasaki, I. (1982) Viability of heat-stressed cells of micro-organisms as influenced by pre-incubation and post-incubation temperatures. J Appl Bacteriol53, 103–108. Kerr, M. and Sheridan, J.J. (2002) Hygiene and safety of Irish beef carcasses. Natl Food Centre Res Rep 57, 1–16. Miller, A.J., Bayles, D.O. and Eblen, B.S. (2000) Cold shock induction of thermal sensitivity in Listeria monocytogenes. Appl Environ Microbiol66, 4345–4350. McMahon, C.M.M., Byrne, C.M., Sheridan, J.J., McDowell, D.A., Blair, I.S. and Hegarty, T. (2000) The effect of culture growth phase on induction of the heat shock response in Yersinia enterocolitica and Listeria monocytogenes. J Appl Microbiol 89, 198–206. O'Hare, C.O., Doran, G., Delappe, N., Morris, D., Buckley, V., Corbett-Fenney, G., McKeown, P., Anderson, W.et al. (2004) Antimicrobial resistance and phage types of human and non-human Salmonella enterica in Ireland, 1998–2003. Commun Dis Pub Health7, 193–199. Panoff, J.-M., Thammavongs, B., Gueguen, M. and Boutibonnes, P. (1998) Cold stress responses in mesophilic bacteria. Cryobiology36, 75–83. Phadtare, S., Alsina, J. and Inouye, M. (1999) Cold-shock responses and cold shock proteins. Curr Opin Microbiol2, 175–180. Quintavalla, S., Larini, S., Mutti, P. and Barbuti, S. (2001) Evaluation of the thermal resistance of different Salmonella serotypes in pork meat containing curing additives. Int J Food Microbiol67, 107–114. Rowbury, R.J. (2003) Temperature effects on biological systems: introduction. Sci Prog86, 1–8. Samelis, J. and Sofos, J.N. (2001) Influence of the natural microflora flora on the acid tolerance response of Listeria monocytogenes in a model system of fresh meat decontamination fluids. Appl Environ Microbiol67, 2410–2420. Scherer, S. and Neuhaus, K. (2005) Life at low temperatures. Available from: http://141.150.157.117:8080/prokPUB/chaptm/418/01_00.htm. Tamplin, M.L. (2002) Growth of Escherichia coli O157:H7 in raw ground beef stored at 10 °C and the influence of competitive bacterial flora, strain variation, and fat level. J Food Prot65, 1535–1540. Vold, L., Holck, A., Wasteson, Y. and Nissen, H. (2000) High levels of background flora inhibits growth of Escherichia coli O157:H7 in ground beef. Int J Food Microbiol 56, 219–225. Wall, P.G., Lamden, K., Ryan, M., Griffin, M., Therelfall, E.J., Ward, L.R. and Rowe, B. (1994) A case control study of infection with the epidemic strain of multiresistant Salmonella. Typhimurium DT104CDR 4, R130–R135. Walsh, C., Duffy, G., Sheridan, J.J., Fanning, S., Blair, I.S. and McDowell, D.A. (2005) Thermal resistance of antibiotic resistant and antibiotic sensitive Salmonella spp. on chicken meat. J Food Safety25, 288–302. Wesche, A.M., Marks, B.P. and Ryser, E.T. (2005) Thermal resistance of heat-, cold and starvation-injured Salmonella in irradiated comminuted turkey. J Food Prot 68, 942–948. Whiting, R.C. and Golden, M.H. (2002) Variation among Escherichia coli O157:H7 strains relative to their growth, survival, thermal inactivation, and toxin production in broth. Int J Food Microbiol 75, 127–133. Wilson, D.N. and Nierhaus, K.H. (2004) The how and Y of cold shock. Nat Struct Mol Biol11, 1026–1028.",
    year = "2007",
    doi = "10.1111/j.1365-2672.2006.03223.x",
    language = "English",
    volume = "102",
    pages = "1561",
    journal = "Journal of Applied Microbiology",
    issn = "1364-5072",
    number = "6",

    }

    Effects of storage and the presence of a beef microflora on the thermal resistance of Salmonella Typhimurium DT104 in beef and broth systems. / McCann, M.S.; McGovern, A.C.; McDowell, D.A.; Blair, I.S.; Sheridan, J.J.

    In: Journal of Applied Microbiology, Vol. 102, No. 6, 2007, p. 1561.

    Research output: Contribution to journalArticle

    TY - JOUR

    T1 - Effects of storage and the presence of a beef microflora on the thermal resistance of Salmonella Typhimurium DT104 in beef and broth systems

    AU - McCann, M.S.

    AU - McGovern, A.C.

    AU - McDowell, D.A.

    AU - Blair, I.S.

    AU - Sheridan, J.J.

    N1 - Reference text: Aldsworth, T.G., Sharman, R.L., Dodd, C.E.R. and Stewart, G.S.A.B. (1998) A competitive microflora increases the resistance of Salmonella Typhimurium to inimical processes: evidence for a suicide response. Appl Environ Microbiol64, 1323–1327. Anon (2004) Microbiology of food and animal feeding stuffs – horizontal methods for the detection of Salmonella spp. In 2002-07-15, 2004 Amendment, 4th edn. pp. 1–19. Switzerland: International Organisation of Standards [ISO 6579:2000 (E)]. Bacon, R.T., Ransom, J.R., Sofos, J.N., Kendall, P.A., Belk, K.E. and Smith, G.C. (2003) Thermal inactivation of susceptible and multiantimicrobial resistant Salmonella strains grown in the absence or presence of glucose. Appl Environ Microbiol 69, 4123–4128. Bayles, D.O., Tunick, M.H., Foglia, T.A. and Miller, A.J. (2000) Cold shock and its effect on ribosomes and thermal tolerance in Listeria monocytogenes. Appl Environ Microbiol 66, 4351–4355. Berry, E.D. and Koohmaraie, M. (2001) Effect of different levels of beef bacterial microflora on the growth and survival of Escherichia coli O157:H7 on beef carcass tissue. J Food Prot64, 1138–1144. Blackburn, C., Curtis, L.M., Humpheson, L., Billon, C. and McClure, P.J. (1997) Development of thermal inactivation models for Salmonella Enteritidis and Escherichia coli O157:H7 with temperature, pH and NaCl as controlling factors. Int J Food Microbiol 38, 31–44. Byrne, C.M., Bolton, D.J., Sheridan, J.J., Blair, I.S. and McDowell, D.A. (2002) The effect of commercial production and product formulation stresses on the heat resistance of Escherichia coli O157:H7 (NCTC 12900) in beef burgers. Int J Food Microbiol 79, 183–192. Davies, A., O'Neill, P., Towers, L. and Cooke, M. (1996) An outbreak of Salmonella Typhimurium DT104 food poisoning associated with eating beef. Commun Dis Rep11, R159–R162. Doyle, M.E. and Mazzotta, A.S. (2000) Review of studies on the thermal resistance of Salmonellae. J Food Prot63, 779–795. Doyle, M.P. and Schoeni, J.L. (1984) Survival and growth characteristics of Escherichia coli associated with hemorrhagic colitis. Appl Environ Microbiol48, 855–856. Duffy, G., Ellison, A., Anderson, W., Cole, M.B. and Stewart, G.S.A.B. (1995) Use of bioluminescence to model the thermal inactivation of Salmonella Typhimurium in the presence of a competitive microflora. Appl Environ Microbiol61, 3463–3465. Duffy, G., Riordain, D.C.R., Sheridan, J.J., Eblen, B.S., Whiting, R.C., Blair, I.S. and McDowell, D.A. (1999a) Differences in thermotolerance of various Escherichia coli O157:H7 strains in a salami matrix. Food Microbiol 16, 83–91. Duffy, G., Whiting, R.C. and Sheridan, J.J. (1999b) The effect of a competitive microflora, pH and temperature on the growth kinetics of Escherichia coli O157:H7. Food Microbiol 16, 299–307. Ethelberg, S. (2005) Salmonellosis outbreak linked to carpaccio made from imported raw beef, Denmark, June–August 2005. Euro Surveill10, E050922.3. Available from: http://www.eurosurveillance.org/ew/2005/050922.asp#3. Humphrey, T.J. (1990) Heat resistance in Salmonella Enteriditis phage type 4: the influence of storage temperatures before heating. J Appl Bacteriol69, 493–497. Humphrey, T.J. (1998) Pathogenity in isolates of Salmonella enterica serotype Enteritidis PT4 which differ in RpoS expression: effects of growth phase and low temperature. Epidemiol Infect 121, 295–301. Humphrey, T.J (2001) Salmonella Typhimurium definitive type 104. A multi-resistant Salmonella. Int J Food Microbiol67, 173–186. Humphrey, T.J., Wilde, S.J. and Rowbury, R.J. (1997) Heat tolerance of Salmonella Typhimurium DT104 isolates attached to muscle tissue. Lett Appl Microbiol 25, 265–268. Jackson, T.C., Hardin, M.D. and Acuff, G.R. (1995) Heat resistance of Escherichia coli O157:H7 in a nutrient medium and in ground beef patties as influenced by storage and holding temperatures. J Food Prot 59, 230–237. Katsui, N., Tsuchido, T., Takano, M. and Shibasaki, I. (1982) Viability of heat-stressed cells of micro-organisms as influenced by pre-incubation and post-incubation temperatures. J Appl Bacteriol53, 103–108. Kerr, M. and Sheridan, J.J. (2002) Hygiene and safety of Irish beef carcasses. Natl Food Centre Res Rep 57, 1–16. Miller, A.J., Bayles, D.O. and Eblen, B.S. (2000) Cold shock induction of thermal sensitivity in Listeria monocytogenes. Appl Environ Microbiol66, 4345–4350. McMahon, C.M.M., Byrne, C.M., Sheridan, J.J., McDowell, D.A., Blair, I.S. and Hegarty, T. (2000) The effect of culture growth phase on induction of the heat shock response in Yersinia enterocolitica and Listeria monocytogenes. J Appl Microbiol 89, 198–206. O'Hare, C.O., Doran, G., Delappe, N., Morris, D., Buckley, V., Corbett-Fenney, G., McKeown, P., Anderson, W.et al. (2004) Antimicrobial resistance and phage types of human and non-human Salmonella enterica in Ireland, 1998–2003. Commun Dis Pub Health7, 193–199. Panoff, J.-M., Thammavongs, B., Gueguen, M. and Boutibonnes, P. (1998) Cold stress responses in mesophilic bacteria. Cryobiology36, 75–83. Phadtare, S., Alsina, J. and Inouye, M. (1999) Cold-shock responses and cold shock proteins. Curr Opin Microbiol2, 175–180. Quintavalla, S., Larini, S., Mutti, P. and Barbuti, S. (2001) Evaluation of the thermal resistance of different Salmonella serotypes in pork meat containing curing additives. Int J Food Microbiol67, 107–114. Rowbury, R.J. (2003) Temperature effects on biological systems: introduction. Sci Prog86, 1–8. Samelis, J. and Sofos, J.N. (2001) Influence of the natural microflora flora on the acid tolerance response of Listeria monocytogenes in a model system of fresh meat decontamination fluids. Appl Environ Microbiol67, 2410–2420. Scherer, S. and Neuhaus, K. (2005) Life at low temperatures. Available from: http://141.150.157.117:8080/prokPUB/chaptm/418/01_00.htm. Tamplin, M.L. (2002) Growth of Escherichia coli O157:H7 in raw ground beef stored at 10 °C and the influence of competitive bacterial flora, strain variation, and fat level. J Food Prot65, 1535–1540. Vold, L., Holck, A., Wasteson, Y. and Nissen, H. (2000) High levels of background flora inhibits growth of Escherichia coli O157:H7 in ground beef. Int J Food Microbiol 56, 219–225. Wall, P.G., Lamden, K., Ryan, M., Griffin, M., Therelfall, E.J., Ward, L.R. and Rowe, B. (1994) A case control study of infection with the epidemic strain of multiresistant Salmonella. Typhimurium DT104CDR 4, R130–R135. Walsh, C., Duffy, G., Sheridan, J.J., Fanning, S., Blair, I.S. and McDowell, D.A. (2005) Thermal resistance of antibiotic resistant and antibiotic sensitive Salmonella spp. on chicken meat. J Food Safety25, 288–302. Wesche, A.M., Marks, B.P. and Ryser, E.T. (2005) Thermal resistance of heat-, cold and starvation-injured Salmonella in irradiated comminuted turkey. J Food Prot 68, 942–948. Whiting, R.C. and Golden, M.H. (2002) Variation among Escherichia coli O157:H7 strains relative to their growth, survival, thermal inactivation, and toxin production in broth. Int J Food Microbiol 75, 127–133. Wilson, D.N. and Nierhaus, K.H. (2004) The how and Y of cold shock. Nat Struct Mol Biol11, 1026–1028.

    PY - 2007

    Y1 - 2007

    KW - beef

    KW - beef microflora

    KW - broth

    KW - Salmonella Typhimurium DT104

    KW - thermal resistance

    U2 - 10.1111/j.1365-2672.2006.03223.x

    DO - 10.1111/j.1365-2672.2006.03223.x

    M3 - Article

    VL - 102

    SP - 1561

    JO - Journal of Applied Microbiology

    T2 - Journal of Applied Microbiology

    JF - Journal of Applied Microbiology

    SN - 1364-5072

    IS - 6

    ER -