The influence of attachment to beef surfaces on the survival of cells of Salmonella enterica serovar Typhimurium DT104, at different aw values and at low storage temperatures

K.J. Kinsella, T Rowe, Ian Blair, DA McDowell, J.J. Sheridan

    Research output: Contribution to journalArticle

    13 Citations (Scopus)

    Abstract

    This study investigated the influence of attachment to beef surfaces on the survival, injury and death of stationary phase cells ofSalmonella enterica serovar Typhimurium DT104, compared to cells free in solution. The effects on cells are considered at different aw values and low temperatures in relation to osmotic and cold temperature shock effects. Attachment of cells to meat surfaces prevented cell injury and death from hyperosmosis and low temperatures, compared to meat solutions. Storage of cells for 72 h resulted in higher levels of cell death on cells attached to meat surfaces. The improved survival of cells in solutions was considered to be related to adaptation to osmotic stress as a result of exposure to a previous hyperosmotic shock and the ability of the cells to produce cold shock proteins. Pathogen cell growth at low temperatures is discussed in relation to the presence of low levels of NaCl. Finally the data is discussed in relation to pathogen survival on beef carcass surfaces during refrigeration.
    LanguageEnglish
    Pages786-793
    JournalFood Microbiology
    Volume24
    Issue number7-8
    DOIs
    Publication statusPublished - 2007

    Fingerprint

    Salmonella enterica
    Salmonella Typhimurium
    storage temperature
    cell viability
    Cell Survival
    beef
    Temperature
    cells
    Meat
    meat
    Shock
    temperature
    Cell Death
    Cold Shock Proteins and Peptides
    death
    pathogen survival
    Refrigeration
    beef carcasses
    Serogroup
    Red Meat

    Cite this

    @article{710aa680221d4a4b8cd7d9c53f014331,
    title = "The influence of attachment to beef surfaces on the survival of cells of Salmonella enterica serovar Typhimurium DT104, at different aw values and at low storage temperatures",
    abstract = "This study investigated the influence of attachment to beef surfaces on the survival, injury and death of stationary phase cells ofSalmonella enterica serovar Typhimurium DT104, compared to cells free in solution. The effects on cells are considered at different aw values and low temperatures in relation to osmotic and cold temperature shock effects. Attachment of cells to meat surfaces prevented cell injury and death from hyperosmosis and low temperatures, compared to meat solutions. Storage of cells for 72 h resulted in higher levels of cell death on cells attached to meat surfaces. The improved survival of cells in solutions was considered to be related to adaptation to osmotic stress as a result of exposure to a previous hyperosmotic shock and the ability of the cells to produce cold shock proteins. Pathogen cell growth at low temperatures is discussed in relation to the presence of low levels of NaCl. Finally the data is discussed in relation to pathogen survival on beef carcass surfaces during refrigeration.",
    author = "K.J. Kinsella and T Rowe and Ian Blair and DA McDowell and J.J. Sheridan",
    note = "Reference text: Baker, R.C., Qureshi, R.A., Hotchkiss, J.H., 1986. Effect of an elevated level of carbon dioxide containing atmosphere on the growth of spoilage and pathogenic bacteria at 2, 7 and 13 1C. Poul. Sci. 65, 729–737. Beales, N., 2004. Adaptation of microorganisms to cold temperatures, weak acid preservatives, low pH and osmotic stress: a review. Compreh. Rev. Food Sci. Food Saf. 3, 1–20. Beney, L., Gervais, P., 2001. Influence of the fluidity of the membrane on the response of microorganisms to environmental stresses. Appl. Microbiol. Biotechnol. 57, 34–42. Beney, L., Martinez de Maran˜ o´ n, I., Marechal, P.A., Gervais, P., 2000. Influence of thermal and osmotic stresses on the viability of the yeast Saccharomyces cerevisiae. Int. J. Food Microbiol. 55, 275–279. Benito, Y., Pin, C., Marin, M.L., Garcia, M.L., Selgas, M.D., Casas, C., 1997. Cell surface hydrophobicity and attachment of pathogenic and spoilage bacteria to meat surfaces. Meat Sci. 45, 419–425. Butler, J.L., Stewart, J.C., Vanderzant, C., Carpenter, Z.L., Smith, G.C., 1979. Attachment of microorganisms to pork skin and surfaces of beef and lamb carcasses. J. Food Prot. 42, 401–406. Casey, P.G., Condon, S., 2002. Sodium chloride decreases the bactericidal effect of acid pH on Escherichia coli O157:H7:H45. Int. J. Food Microbiol. 76, 199–206. Catsaras, M., Grebot, D., 1984. Multiplication des Salmonella dans la viande hache´ e. Bull. Acad. Vet. France 57, 501–512. Costerton, J.W., Geesey, G.G., Cheng, K.-J., 1978. How bacteria stick. Scient. Am. 238, 86–95. Cronan, J.E., Rock, C.O., 1996. Biosynthesis of Membrane Lipids. In: Neidhardt, F.C. (Ed.), Escherichia coli and Salmonella—Cellular and Molecular Biology. second ed., vol. 1, pp. 612–628. D’Aoust, J.-Y., 1991. Psychrotrophy and foodborne Salmonella. Int. J. Food Microbiol. 13, 207–216. Deibel, V., Schoeni, J., 2003. The clean operation. Biofilms: forming a defence strategy for the food plant. Food Saf. Mag. December 2002/ January 2003. Doyle, M.E., Mazzotta, A.S., 2000. Review of studies on the thermal resistance of Salmonellae. J. Appl. Microbiol. 93, 689–696. Doyle, M.P., Schoeni, J.L., 1984. Survival and growth characteristics of Escherichia coli associated with hemorrhagic colitis. Appl. Environ. Microbiol. 48, 855–856. Duffy, G., Riordan, D.C.R., Sheridan, J.J., Eblen, B.S,Whiting, R.C., Blair, I.S., McDowell, D.A., 1999. Differences in thermotolerance of various Escherichia coli O157:H7 strains in a salami matrix. Food Microbiol. 16, 83–91. Gawande, P.V., Bhagwat, A.A., 2002. Protective effects of cold temperature and surface-contact on acid tolerance of Salmonella spp. J. Appl. Microbiol. 93, 689–696. Humphrey, T.J., 2001. Salmonella Typhimurium definitive type 104: a multi-resistant Salmonella. Int. J. Food Microbiol. 67, 173–186. Humphrey, T.J., Wilde, S.J., Rowbury, R.J., 1997. Heat tolerance of Salmonella Typhimurium DT104 isolates attached to muscle tissue. Lett. Appl. Microbiol. 25, 265–268. Jordan, K.N., Hall, S., McClure, P.J., 1999. Osmotic stress on dilution of acid injured Escherichia coli O157: H7. Lett. Appl. Microbiol. 28, 389–393. Kinsella, K.J., Sheridan, J.J., Rowe, T.A., Butler, F., Delgado, A., Quispe-Ramirez, A., Blair, I.S., McDowell, D.A., 2006. Impact of a novel spray-chilling system on surface microflora, water activity and weight loss during beef carcass chilling. Food Microbiol. 23, 483–490. 793 Matches, J.B., Liston, J., 1972. Effects of incubation temperature on the salt tolerance of Salmonella. J. Milk Food Technol. 35, 39–44. Mattick, K.L., J{\o}rgensen, F., Legan, J.D., Cole, M.B., Porter, J., Lappin-Scott, H.M., Humphrey, T.J., 2000. Survival and filamentation of Salmonella enterica serovar enteritidis PT4 and Salmonella enterica serovar Typhimurium. Appl. Environ. Microbiol., 1274–1279. Mattick, K.L., J{\o}rgensen, F., Legan, J.D., Lappin-Scott, H.M., Humphrey, T.J., 2001. Improving recovery of Salmonella enterica serovar Typhimurium DT104 cells injured by heating at different water activity values. J. Food Protect. 64, 1472–1476. Medina, M.B., 2001. Binding of collagen I to Escherichia coli O157:H7 and inhibition by carrageenans. Int. J. Food Microbiol. 69, 199–208. Monier, J.-M., Lindow, S.E., 2003. Differential survival of solitary and aggregated bacterial cells promotes aggregate formation on leaf surfaces. Pro. Natl. Acad. Sci. 100, 15977–15982. Mossel, D.A.A., Jansma, M., de Waart, J., 1981. Chapter 3: Growth potential of 114 strains of epidemiologically most common salmonellae and arizonae between 3 and 17 1C. In: Roberts, T.A., Hobbs, G., Christian, J.H.B., Skovgaard, N. (Eds.), Psychrotrophic Microorgan- isms in Spoilage and Pathogenicity. Academic Press, New York, pp. 275–278. O’Byrne, C., Booth, I.R., 2002. Osmoregulation and its importance to foodborne microorganisms. Int. J. Food Microbiol. 74, 203–216. Phillips, L.E., Humphrey, T.J., Lappin-Scott, H.M., 1998. Chilling invokes different morphologies in two Salmonella enteritidis PT4 strains. J. Appl. Microbiol. 84, 820–826. Poirier, I., Mare´ chal, P.-A., Gervais, P., 1997. Effects of the kinetics of water potential variation on bacteria viability. J. Appl. Microbiol. 82, 101–106. Potts, M., 1994. Desiccation tolerance of prokaryotes. Microbiol. Rev. 58, 755–805. Record, M.T., Courtenay, E.S., Scott Cayley, D., Guttman, H.J., 1998. Responses of Escherichia coli to osmotic stress: large changes in amounts of cytoplasmic solutes and water. Trends Biochem. Sci. 23, 121–156. Russell, N.J., 2002. Bacterial membranes: the effects of chill storage and food processing. An overview. Int. J. Food Microbiol. 79, 27–34. Scherer, S., Neuhaus, K., 2002. Life at Low Temperatures. In: Dworkin, M., et al. (Eds.), The Prokaryotes: An Evolving Electronic Resource for the Microbiological Community, third ed. Springer, New York release 3.9, April 1, 2001. /http://link.springer-ny.com/link/service/ books/10125/S. Schwach, T.S., Zottola, E.A., 1982. Use of scanning electron microscopy to demonstrate microbial attachment to beef and beef contact surfaces. J. Food Sci. 47, 1401–1405. Shadbolt, C.T., McMeekin, T.A., 1990. Non-thermal death of Escherichia coli. Int. J. Food Microbiol. 49, 129–138. Sheridan, J.J., McDowell, D.A., 1998. Factors affecting the emergence of pathogens on foods. Meat Sci. 49, S151–S167. Smith, J.J., Howington, J.P., McFeters, G.A., 1994. Survival, physiological response, and recovery of enteric bacteria exposed to a polar marine environment. Appl. Environ. Microbiol. 60, 2977–2984. Vila-Sanjurjo, A., Schuwirth, B.S., Hau, C.W., Cate, J.H.D., 2004. Structural basis for the control of translation initiation during stress. Nat. Struct. Mol. Biol. 11, 1054–1059. Walls, I., Sheridan, J.J., Levett, P.N., 1989. A rapid method of enumerating microorganisms from beef, using an acridine orange direct count technique. Irish J. Food Sci. Technol. 13, 23–31. Wilhelmsson, O., Miller, K.J., 2002. Humectant permeability influences growth and compatible solute uptake by Staphylococcus aureus subjected to osmotic stress. J. Food Prot. 65, 1008–1015. Yamanaka, K., 1999. Cold shock response in Escherichia coli. J. Mol. Microbiol. Biotechnol. 1, 193–202. Yu, S.-L., Cooke, P.H., Tu, S.-I., 2001. Effects of chilling on sampling of bacteria attached to swine carcasses. Lett. Appl. Microbiol. 32, 205–210.",
    year = "2007",
    doi = "10.1016/j.fm.2006.12.004",
    language = "English",
    volume = "24",
    pages = "786--793",
    number = "7-8",

    }

    The influence of attachment to beef surfaces on the survival of cells of Salmonella enterica serovar Typhimurium DT104, at different aw values and at low storage temperatures. / Kinsella, K.J.; Rowe, T; Blair, Ian; McDowell, DA; Sheridan, J.J.

    Vol. 24, No. 7-8, 2007, p. 786-793.

    Research output: Contribution to journalArticle

    TY - JOUR

    T1 - The influence of attachment to beef surfaces on the survival of cells of Salmonella enterica serovar Typhimurium DT104, at different aw values and at low storage temperatures

    AU - Kinsella, K.J.

    AU - Rowe, T

    AU - Blair, Ian

    AU - McDowell, DA

    AU - Sheridan, J.J.

    N1 - Reference text: Baker, R.C., Qureshi, R.A., Hotchkiss, J.H., 1986. Effect of an elevated level of carbon dioxide containing atmosphere on the growth of spoilage and pathogenic bacteria at 2, 7 and 13 1C. Poul. Sci. 65, 729–737. Beales, N., 2004. Adaptation of microorganisms to cold temperatures, weak acid preservatives, low pH and osmotic stress: a review. Compreh. Rev. Food Sci. Food Saf. 3, 1–20. Beney, L., Gervais, P., 2001. Influence of the fluidity of the membrane on the response of microorganisms to environmental stresses. Appl. Microbiol. Biotechnol. 57, 34–42. Beney, L., Martinez de Maran˜ o´ n, I., Marechal, P.A., Gervais, P., 2000. Influence of thermal and osmotic stresses on the viability of the yeast Saccharomyces cerevisiae. Int. J. Food Microbiol. 55, 275–279. Benito, Y., Pin, C., Marin, M.L., Garcia, M.L., Selgas, M.D., Casas, C., 1997. Cell surface hydrophobicity and attachment of pathogenic and spoilage bacteria to meat surfaces. Meat Sci. 45, 419–425. Butler, J.L., Stewart, J.C., Vanderzant, C., Carpenter, Z.L., Smith, G.C., 1979. Attachment of microorganisms to pork skin and surfaces of beef and lamb carcasses. J. Food Prot. 42, 401–406. Casey, P.G., Condon, S., 2002. Sodium chloride decreases the bactericidal effect of acid pH on Escherichia coli O157:H7:H45. Int. J. Food Microbiol. 76, 199–206. Catsaras, M., Grebot, D., 1984. Multiplication des Salmonella dans la viande hache´ e. Bull. Acad. Vet. France 57, 501–512. Costerton, J.W., Geesey, G.G., Cheng, K.-J., 1978. How bacteria stick. Scient. Am. 238, 86–95. Cronan, J.E., Rock, C.O., 1996. Biosynthesis of Membrane Lipids. In: Neidhardt, F.C. (Ed.), Escherichia coli and Salmonella—Cellular and Molecular Biology. second ed., vol. 1, pp. 612–628. D’Aoust, J.-Y., 1991. Psychrotrophy and foodborne Salmonella. Int. J. Food Microbiol. 13, 207–216. Deibel, V., Schoeni, J., 2003. The clean operation. Biofilms: forming a defence strategy for the food plant. Food Saf. Mag. December 2002/ January 2003. Doyle, M.E., Mazzotta, A.S., 2000. Review of studies on the thermal resistance of Salmonellae. J. Appl. Microbiol. 93, 689–696. Doyle, M.P., Schoeni, J.L., 1984. Survival and growth characteristics of Escherichia coli associated with hemorrhagic colitis. Appl. Environ. Microbiol. 48, 855–856. Duffy, G., Riordan, D.C.R., Sheridan, J.J., Eblen, B.S,Whiting, R.C., Blair, I.S., McDowell, D.A., 1999. Differences in thermotolerance of various Escherichia coli O157:H7 strains in a salami matrix. Food Microbiol. 16, 83–91. Gawande, P.V., Bhagwat, A.A., 2002. Protective effects of cold temperature and surface-contact on acid tolerance of Salmonella spp. J. Appl. Microbiol. 93, 689–696. Humphrey, T.J., 2001. Salmonella Typhimurium definitive type 104: a multi-resistant Salmonella. Int. J. Food Microbiol. 67, 173–186. Humphrey, T.J., Wilde, S.J., Rowbury, R.J., 1997. Heat tolerance of Salmonella Typhimurium DT104 isolates attached to muscle tissue. Lett. Appl. Microbiol. 25, 265–268. Jordan, K.N., Hall, S., McClure, P.J., 1999. Osmotic stress on dilution of acid injured Escherichia coli O157: H7. Lett. Appl. Microbiol. 28, 389–393. Kinsella, K.J., Sheridan, J.J., Rowe, T.A., Butler, F., Delgado, A., Quispe-Ramirez, A., Blair, I.S., McDowell, D.A., 2006. Impact of a novel spray-chilling system on surface microflora, water activity and weight loss during beef carcass chilling. Food Microbiol. 23, 483–490. 793 Matches, J.B., Liston, J., 1972. Effects of incubation temperature on the salt tolerance of Salmonella. J. Milk Food Technol. 35, 39–44. Mattick, K.L., Jørgensen, F., Legan, J.D., Cole, M.B., Porter, J., Lappin-Scott, H.M., Humphrey, T.J., 2000. Survival and filamentation of Salmonella enterica serovar enteritidis PT4 and Salmonella enterica serovar Typhimurium. Appl. Environ. Microbiol., 1274–1279. Mattick, K.L., Jørgensen, F., Legan, J.D., Lappin-Scott, H.M., Humphrey, T.J., 2001. Improving recovery of Salmonella enterica serovar Typhimurium DT104 cells injured by heating at different water activity values. J. Food Protect. 64, 1472–1476. Medina, M.B., 2001. Binding of collagen I to Escherichia coli O157:H7 and inhibition by carrageenans. Int. J. Food Microbiol. 69, 199–208. Monier, J.-M., Lindow, S.E., 2003. Differential survival of solitary and aggregated bacterial cells promotes aggregate formation on leaf surfaces. Pro. Natl. Acad. Sci. 100, 15977–15982. Mossel, D.A.A., Jansma, M., de Waart, J., 1981. Chapter 3: Growth potential of 114 strains of epidemiologically most common salmonellae and arizonae between 3 and 17 1C. In: Roberts, T.A., Hobbs, G., Christian, J.H.B., Skovgaard, N. (Eds.), Psychrotrophic Microorgan- isms in Spoilage and Pathogenicity. Academic Press, New York, pp. 275–278. O’Byrne, C., Booth, I.R., 2002. Osmoregulation and its importance to foodborne microorganisms. Int. J. Food Microbiol. 74, 203–216. Phillips, L.E., Humphrey, T.J., Lappin-Scott, H.M., 1998. Chilling invokes different morphologies in two Salmonella enteritidis PT4 strains. J. Appl. Microbiol. 84, 820–826. Poirier, I., Mare´ chal, P.-A., Gervais, P., 1997. Effects of the kinetics of water potential variation on bacteria viability. J. Appl. Microbiol. 82, 101–106. Potts, M., 1994. Desiccation tolerance of prokaryotes. Microbiol. Rev. 58, 755–805. Record, M.T., Courtenay, E.S., Scott Cayley, D., Guttman, H.J., 1998. Responses of Escherichia coli to osmotic stress: large changes in amounts of cytoplasmic solutes and water. Trends Biochem. Sci. 23, 121–156. Russell, N.J., 2002. Bacterial membranes: the effects of chill storage and food processing. An overview. Int. J. Food Microbiol. 79, 27–34. Scherer, S., Neuhaus, K., 2002. Life at Low Temperatures. In: Dworkin, M., et al. (Eds.), The Prokaryotes: An Evolving Electronic Resource for the Microbiological Community, third ed. Springer, New York release 3.9, April 1, 2001. /http://link.springer-ny.com/link/service/ books/10125/S. Schwach, T.S., Zottola, E.A., 1982. Use of scanning electron microscopy to demonstrate microbial attachment to beef and beef contact surfaces. J. Food Sci. 47, 1401–1405. Shadbolt, C.T., McMeekin, T.A., 1990. Non-thermal death of Escherichia coli. Int. J. Food Microbiol. 49, 129–138. Sheridan, J.J., McDowell, D.A., 1998. Factors affecting the emergence of pathogens on foods. Meat Sci. 49, S151–S167. Smith, J.J., Howington, J.P., McFeters, G.A., 1994. Survival, physiological response, and recovery of enteric bacteria exposed to a polar marine environment. Appl. Environ. Microbiol. 60, 2977–2984. Vila-Sanjurjo, A., Schuwirth, B.S., Hau, C.W., Cate, J.H.D., 2004. Structural basis for the control of translation initiation during stress. Nat. Struct. Mol. Biol. 11, 1054–1059. Walls, I., Sheridan, J.J., Levett, P.N., 1989. A rapid method of enumerating microorganisms from beef, using an acridine orange direct count technique. Irish J. Food Sci. Technol. 13, 23–31. Wilhelmsson, O., Miller, K.J., 2002. Humectant permeability influences growth and compatible solute uptake by Staphylococcus aureus subjected to osmotic stress. J. Food Prot. 65, 1008–1015. Yamanaka, K., 1999. Cold shock response in Escherichia coli. J. Mol. Microbiol. Biotechnol. 1, 193–202. Yu, S.-L., Cooke, P.H., Tu, S.-I., 2001. Effects of chilling on sampling of bacteria attached to swine carcasses. Lett. Appl. Microbiol. 32, 205–210.

    PY - 2007

    Y1 - 2007

    N2 - This study investigated the influence of attachment to beef surfaces on the survival, injury and death of stationary phase cells ofSalmonella enterica serovar Typhimurium DT104, compared to cells free in solution. The effects on cells are considered at different aw values and low temperatures in relation to osmotic and cold temperature shock effects. Attachment of cells to meat surfaces prevented cell injury and death from hyperosmosis and low temperatures, compared to meat solutions. Storage of cells for 72 h resulted in higher levels of cell death on cells attached to meat surfaces. The improved survival of cells in solutions was considered to be related to adaptation to osmotic stress as a result of exposure to a previous hyperosmotic shock and the ability of the cells to produce cold shock proteins. Pathogen cell growth at low temperatures is discussed in relation to the presence of low levels of NaCl. Finally the data is discussed in relation to pathogen survival on beef carcass surfaces during refrigeration.

    AB - This study investigated the influence of attachment to beef surfaces on the survival, injury and death of stationary phase cells ofSalmonella enterica serovar Typhimurium DT104, compared to cells free in solution. The effects on cells are considered at different aw values and low temperatures in relation to osmotic and cold temperature shock effects. Attachment of cells to meat surfaces prevented cell injury and death from hyperosmosis and low temperatures, compared to meat solutions. Storage of cells for 72 h resulted in higher levels of cell death on cells attached to meat surfaces. The improved survival of cells in solutions was considered to be related to adaptation to osmotic stress as a result of exposure to a previous hyperosmotic shock and the ability of the cells to produce cold shock proteins. Pathogen cell growth at low temperatures is discussed in relation to the presence of low levels of NaCl. Finally the data is discussed in relation to pathogen survival on beef carcass surfaces during refrigeration.

    U2 - 10.1016/j.fm.2006.12.004

    DO - 10.1016/j.fm.2006.12.004

    M3 - Article

    VL - 24

    SP - 786

    EP - 793

    IS - 7-8

    ER -