Skip to main content
Log in

Quantitative Evaluation of Thermal Inactivation Kinetics of Free-Floating Versus Surface-Attached Listeria innocua Cells

  • Published:
Food and Bioprocess Technology Aims and scope Submit manuscript

Abstract

Surface pasteurization is one of the decontamination treatments that can contribute to better preservation of meat products retaining most of their quality characteristics relatively intact if compared with the raw products. The current research compares the kinetics of free-floating and surface attached Listeria innocua cells by using integrated microbial and heat transfer modelling approaches. Surface pasteurization treatments are applied on a (abiotic) Teflon® model system in a novel steam surface decontamination rig. The experimental set-up prevented following four technological aspects to occur, (1) cold purge migration to the surface during the heating process, (2) inactivation kinetics of a cocktail of microbes, (3) protective effect of food components, and (4) physical distribution of bacteria throughout the depth of the product skin. Microbial load predictions are performed based on the inactivation parameters obtained during free-floating cell experiments. These predictions, when compared with the microbial data of the surface treatments, prove that the surface attached cells were much more heat resistant, despite the experimental set-up preventing the aforementioned (technological) events to occur. Indeed, surface attached cells can have different physiological/phenotypical/genetical characteristics, such as cell aggregations, colony formations, presence of flagella. In a final step, three techniques are implemented to evaluate mathematically the kinetics of the surface attached cells. Overall, this research’s significance is lying in the quantitative assessment of microbial heat resistance. The technological reasons underlying the increased microbial heat resistance on biotic and abiotic surfaces should be reevaluated, taking into account possible physiological/phenotypical/genetical characteristics.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Avens, J. S., Albright, S. N., Morton, A. S., Prewitt, B. E., Kendall, P. A., & Sofos, J. N. (2002). Destruction of microorganisms on chicken carcasses by steam and boiling water immersion. Food Control, 13, 445–450.

    Article  Google Scholar 

  • Bernaerts, K., Dens, E., Vereecken, K., Geeraerd, A., Standaert, A. R., Devlieghere, F., et al. (2004). Concepts and tools for predictive modeling of microbial dynamics. Journal of Food Protection, 67, 2041–2052.

    Google Scholar 

  • Bigelow, W. D. (1921). The logarithmic nature of thermal death time curves. Journal of Infectious Diseases, 29, 528–536.

    Google Scholar 

  • Briandet, R., Herry, J.-M., Bellon-Fontaine, M.-N. (2001). Determination of the van der Waals, electron donor and electron acceptor surface tension components of static Gram-positive microbial biofilms. Colloids and Surfaces B, 21, 299–310.

    Article  CAS  Google Scholar 

  • Cunliffe, D., Smart, C. A., Alexander, C., & Vulfson, E. N. (1999). Bacterial adhesion at synthetic surfaces. Applied and Environmental Microbiology, 65, 4995–5002.

    CAS  Google Scholar 

  • Cygnarowicz-Provost, M., Whiting, R. C., & Craig, J. R. (1994). Steam surface pasteurization of beef Frankfurters. Journal of Food Science, 59, 1–5.

    Article  Google Scholar 

  • Doyle, M. E., Mazzotta, A. S., Wang, T., Wiseman, D. W., & Scott, V. (2001). Heat resistance of Listeria monocytogenes. Journal of Food Protection, 64, 410–429.

    CAS  Google Scholar 

  • Fairchild, T. M., Swartzel, K. R., & Foegeding, P. M. (1994). Inactivation kinetics of Listeria innocua in skim milk in a continuous flow processing system. Journal of Food Science, 59, 960–963.

    Article  CAS  Google Scholar 

  • Foong, S. C. C., & Dickson, J. S. (2004). Attachment of Listeria monocytogenes on ready-to-eat meats. Journal of Food Protection, 67, 456–462.

    Google Scholar 

  • Gaillard, S., Leguerinel, I., & Mafart, P. (1998). Model for the combined effects of temperature, pH and water activity on thermal inactivation of Bacillus cereus spores. Journal of Food Science, 63, 887–889.

    Article  CAS  Google Scholar 

  • Geeraerd, A. H., Herremans, C. H., & Van Impe, J. F. (2000). Structural model requirements to describe microbial inactivation during a mild heat treatment. International Journal of Food Microbiology, 59, 185–209.

    Article  CAS  Google Scholar 

  • Geeraerd, A. H., Valdramidis, V. P., & Van Impe, J. F. (2005). GinaFiT, a freeware tool to assess non-log-linear microbial survivor curves. International Journal of Food Microbiology, 102, 95–105.

    Article  CAS  Google Scholar 

  • Goulet, V., Rocourt, J., Rebiere, I., Jacquet, C., Moyse, C., Dehaumont, P., et al. (1998). Listeriosis outbreak associated with the consumption of rillettes in France in 1993. Journal of Infectious Diseases, 177, 155–160.

    Article  CAS  Google Scholar 

  • Goulet, V., de Valk, H., Pierre, O., Stainer, F., Rocourt, J., Vaillant, V., et al. (2001). Effect of prevention measures on incidence of human listeriosis, France, 1987–1997. Emerging Infectious Diseases, 7, 983–989.

    Article  CAS  Google Scholar 

  • Hopp, B., Kresz, N., Kokavecz, J., Smausz, T., Schieferdecker, H., Döring, A., et al. (2004). Adhesive and morphological characteristics of surface chemically modified polytetrafluoroethylene films. Applied Surface Science, 221, 437–443.

    Article  CAS  Google Scholar 

  • Houben, J., & Eckenhausen, F. (2006). Surface pasteurization of vacuum-sealed precooked ready-to-eat meat products. Journal of Food Protection, 69, 459–468.

    Google Scholar 

  • ICMSF. (1996). ICMSF: microorganisms in foods 5, characteristics of microbial pathogens. London, UK: Blackie Academic and Professional.

    Google Scholar 

  • Incropera, F. P., & De Witt, D. P. (2002). Fundamentals of heat and mass transfer. New York, USA: Wiley.

    Google Scholar 

  • James, C., & James, S. (1999). Meat decontamination the state of the art. Bristol, UK: MAFF Advanced Fellowship in Food Process Engineering.

  • James, C., Goksoy, E. O., Corry, J. E. L., & James, S. J. (2000). Surface pasteurisation of poultry meat using steam at atmospheric pressure. Journal of Food Engineering, 45, 111–117.

    Article  Google Scholar 

  • Juneja, V. K., Elben, B. S., & Marks, H. M. (2001). Modeling non-linear survival curves to calculate thermal inactivation of Salmonella in poultry of different fat levels. International Journal of Food Microbiology, 70, 37–51.

    Article  CAS  Google Scholar 

  • Klose, A. A., Kaufman, V. F., Bayne, H. G., & Pool, M. F. (1971). Pasteurization of poultry meat by steam under reduced pressure. Poultry Science, 50, 1156–1160.

    Google Scholar 

  • Kondjoyan, A., Rouaud, O., McCann, M. S., Havet, M., Foster, A., Swain, M., et al. (2006). Modelling coupled heat-water transfers during a decontamination treatment of the surface of solid products by a jet of hot air. I. Sensitivity analysis of the model and first validations of product surface temperature under constant air temperature conditions. Journal of Food Engineering, 76, 53–62.

    Article  Google Scholar 

  • Lejeune, P. (2003). Contamination of abiotic surfaces: what a colonizing bacterium sees and how to blur it. Trends in Microbiology, 11, 179–184.

    Article  CAS  Google Scholar 

  • Lundén, J. M., Miettinen, M. K., Autio, T. J., & Korkeala, H. J. (2000). Persistent Listeria monocytogenes strains show enhanced adherence to food contact surface after short contact times. Journal of Food Protection, 63, 1204–1207.

    Google Scholar 

  • McCann, M. S., Sheridan, J. J., McDowell, D. A., & Blair, I. S. (2006). Effects of steam pasteurisation on Salmonella Typhimurium DT104 and Escherichia coli O157:H7 surface inoculated onto beef, pork and chicken. Journal of Food Engineering, 76, 32–40.

    Article  Google Scholar 

  • McEvoy, J. M., Doherty, A. M., Sheridan, J. J., Blair, I. S., & McDowell, D. A. (2001). Use of steam condensing at subatmospheric pressures to reduce Escherichia coli O157:H7 numbers on bovine hide. Journal of Food Protection, 64, 1655–1660.

    CAS  Google Scholar 

  • Morgan, A. I., Radewonuk, E. R., & Scullen, O. J. (1996). Ultra high temperature, ultra short time surface pasteurization of meat. Journal of Food Science, 61, 1216–1218.

    Article  Google Scholar 

  • Muriana, P. M., Quiby, W., Davidson, C. A., & Grooms, J. (2002). Postpackage pasteurization of ready-to-eat deli meats by submersion heating for reduction of Listeria monocytogenes. Journal of Food Protection, 65, 936–969.

    Google Scholar 

  • Muriana, P. M., Gande, N., Robertson, W., Jordan, B., & Mitra, S. (2004). Effect of prepackage and postpackage pasteurization on postprocess elimination of Listeria monocytogenes on deli turkey products. Journal of Food Protection, 67, 2472–2479.

    Google Scholar 

  • Murphy, R. Y., Marks, B. P., Johnson, E. R., & Johnson, M. G. (2000). Thermal inactivation kinetics of Salmonella and Listeria in ground chicken breast meat and liquid medium. Journal of Food Science, 65, 706–710.

    Article  CAS  Google Scholar 

  • Murphy, R. Y., Dunca, L. K., Johnson, E. R., Davis, M. D., Wolfe, R. E., & Brown, H. G. (2001). Thermal lethality of Salmonella Senftenberg and Listeria innocua in fully cooked and packaged chicken breast strips via steam pasteurization. Journal of Food Protection, 60, 2083–2087.

    Google Scholar 

  • Neter, J., Kutner, M. H., Nachtsheim, C. J., & Wasserman, W. (1996). Applied linear statistical models. 4th edn. Chicago, USA: McGraw-Hill.

    Google Scholar 

  • Olsen, S. J., Patrick, M., Hunter, S. B., Reddy, V., Kornstein, L., MacKenzie, W. R., et al. (2005). Multistate outbreak of Listeria monocytogenes infection linked to delicatessen turkey meat. Clinical Infectious Diseases, 40, 962–967.

    Article  Google Scholar 

  • Orta-Ramirez, A., Marks, B. P., Warsow, C. R., Booren, A. M., & Ryser, E. T. (2005). Enhanced thermal resistance of Salmonella in whole muscle compared to ground beef. Journal of Food Science, 70, M359–M362.

    Article  CAS  Google Scholar 

  • Özisik, M. N. (2004). Finite difference methods in heat transfer. Florida, USA: CRC Press.

    Google Scholar 

  • Phebus, R., Nutsch, A., Schafer, D., Wilson, R., Riemann, M., Leising, J., et al. (1997). Comparison of steam pasteurization and other methods for reduction of pathogens on surfaces of freshly slaughtered beef. Journal of Food Protection, 60, 476–484.

    Google Scholar 

  • Poschet, F., Geeraerd, A. H., Van Loey, A. M., Ly Nguyen, B., Hendrickx, M. E., & Van Impe JF. (2004). Assessing the optimal experimental setup for first order kinetic studies by Monte Carlo analysis. Food Control, 16, 873–882.

    Article  Google Scholar 

  • Prigent-Combaret, C., Vidal, O., Dorel, C., & Lejeune, P. (1999). Abiotic surface sensing and biofilm-dependent regulation of gene expression in Escherichia coli. Journal of Bacteriology, 181, 5993–6002.

    CAS  Google Scholar 

  • Sofos, J. N., & Smith, G. C. (1998). Nonacid meat decontamination technologies: Model studies and commercial applications. International Journal of Food Microbiology, 44, 171–188.

    Article  CAS  Google Scholar 

  • Sofos, J. N., Keith, E. B., & Gary, C. S. (1999). Meat safety research summaries processes to reduce contamination with pathogenic microorganisms in meat. Fort Collins, USA: Center for Red Meat Safety, Department of Animal Sciences, Colorado State University.

  • Techasena, O., & Flick, D. (1995). Surface temperature estimation of solid foods during a surface sterilization. LWT-Food Science and Technology, 28, 419–424.

    CAS  Google Scholar 

  • Tresse, O., Lebret, V., Benezech, T., & Faille, C. (2006). Comparative evaluation of adhesion, surface properties, and surface protein composition of Listeria monocytogenes strains after cultivation at constant pH of 5 and 7. Journal of Applied Microbiology, 101, 53–62.

    Article  CAS  Google Scholar 

  • Uyttendaele, M., De Troy, P., & Debevere, J. (1999). Incidence of Listeria monocytogenes in different types of meat products on the Belgian retail market. International Journal of Food Microbiology, 53, 75–80.

    Article  CAS  Google Scholar 

  • Valdramidis, V. P., Belaubre, N., Zuniga, R., Foster, A. M., Havet, M., Geeraerd, A. H., et al. (2005a). Development of predictive modelling approaches for surface temperature and associated microbiological inactivation during hot air decontamination. International Journal of Food Microbiology, 100, 261–274.

    Article  CAS  Google Scholar 

  • Valdramidis, V. P., Bernaerts, K., Van Impe, J. F., & Geeraerd, A. H. (2005b). An alternative approach to non-log-linear thermal microbial inactivation: modelling the number of log cycles reduction with respect to temperature. Food Technology and Biotechnology, 43, 321–327.

    Google Scholar 

  • Valdramidis, V. P., Geeraerd, A. H., Gaze, J. E., Kondojoyan, A., Boyd, A. R., Shaw, H. L., et al. (2006). Quantitative description of Listeria monocytogenes inactivation kinetics with temperature and water activity as the influencing factors: model prediction and methodological validation on dynamic data. Journal of Food Engineering, 76, 79–88.

    Article  Google Scholar 

  • Vatanyoopaisarn, S., Nazli, A., Dodd, C. E. R., Reeds, C. E. D., & Waites, W. M. (2000). Effect of flagella on initial attachment of Listeria monocytogenes to stainless steel. Applied and Environmental Microbiology, 66, 860–863.

    Article  CAS  Google Scholar 

  • Welt, B. A., Teixeira, A. A., Balaban, M. O., Smerage, G. H., & Sage, D. S. (1997). Iterative method for kinetic parameter estimation from dynamic thermal treatments. Journal of Food Science, 62, 8–14.

    Article  CAS  Google Scholar 

Download references

Acknowledgement

The authors wish to thank Dr. Isabelle Lebert for scientific discussions and Laurent Saint-André for his technical assistance. This research was supported by the French government and INRA for the post Doctoral fellowship of Claudine Péroval, by the projects EF/05/006 (Center-of-Excellence Optimization in Engineering) and OT/03/30 of the Research Council of the Katholieke Universiteit Leuven and by the Belgian Federal Science Policy Office (IAP/PAI and PODO II).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Annemie H. Geeraerd.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Valdramidis, V.P., Péroval, C., Portanguen, S. et al. Quantitative Evaluation of Thermal Inactivation Kinetics of Free-Floating Versus Surface-Attached Listeria innocua Cells. Food Bioprocess Technol 1, 285–296 (2008). https://doi.org/10.1007/s11947-007-0010-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11947-007-0010-5

Keywords

Navigation