Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Science and Society
  • Published:

Salmonella, stress responses and food safety

Nature Reviews Microbiology volume 2, pages 504–509 (2004)Cite this article

Abstract

The ability of Salmonella to survive in the food chain is due, in part, to its ability to respond effectively to environmental changes. It is unlikely that Salmonella will ever be eradicated from the food chain — the results from laboratory research, such as investigations of the response of Salmonella to different stresses, must therefore be translated into improved intervention strategies for food producers and consumers.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: The effects of transfer from 20°C to 45°C on the heat and acid tolerance of Salmonella Enteritidis PT4.
Figure 2: Salmonella infections in England and Wales, 1982–2003.

References

  1. Pang, T., Bhutta, Z. A., Finlay, B. B. & Altwegg, M. Typhoid fever and other salmonellosis: a continuing challenge. Trends Microbiol. 3, 253–255 (1995).

    Article  CAS  Google Scholar 

  2. Helms, M., Vastrup, P., Gerner–Schmidt, P. & Mølbak, K. Short and long term mortality associated with foodborne bacterial gastrointestinal infections: registry based study. BMJ 326, 357–361 (2003).

    Article  Google Scholar 

  3. McClelland, M. et al. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413, 852–856 (2001).

    Article  CAS  Google Scholar 

  4. Bearson, B. L., Wilson, L. & Foster, J. W. A low pH-inducible, PhoPQ-dependent acid tolerance response protects Salmonella typhimurium against inorganic acid stress. J. Bacteriol. 180, 2409–2417 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Corry, J. E. L. & Roberts, T. A. A note on the development of resistance to heat and gamma radiation in Salmonella. J. Appl. Bacteriol. 33, 733–737 (1970).

    Article  CAS  Google Scholar 

  6. D'Aoust, J. Y. Salmonella and the international food trade. Int. J. Food Microbiol. 24, 11–31 (1994).

    Article  CAS  Google Scholar 

  7. Loewen, P. C., Hu, B., Strutinsky, J. & Sparling, R. Regulation in the rpoS regulon of Escherichia coli. Can. J. Microbiol. 44, 707–717 (1998).

    Article  CAS  Google Scholar 

  8. El-Gedaily, A., Paesold, G., Chen, C. Y., Guiney, D. G. & Krause, M. Plasmid virulence gene expression induced by short-chain fatty acids in Salmonella dublin: identification of rpoS-dependent and rpoS-independent mechanisms. J. Bacteriol. 179, 1409–1412 (1997).

    Article  CAS  Google Scholar 

  9. PHLS Communicable Disease Surveillance Centre. Salmonella enteritidis outbreaks in England and Wales, September to November 2002. Commun. Disease Rep. Weekly [online], <http://www.hpa.org.uk/cdr/PDFfiles/2002/cdr4902.pdf> (2002).

  10. Health Protection Agency. Salmonella enteritidis outbreak in central London linked to Spanish eggs. Commun. Disease Rep. Weekly [online], <http://www.hpa.org.uk/cdr/PDFfiles/2004/cdr0304.pdf> (2004).

  11. Crook, P. D. A European outbreak of Salmonella enterica serotype Typhimurium definitive phage type 204b in 2000. Clin. Microbiol. Infect. 9, 839–845 (2003).

    Article  CAS  Google Scholar 

  12. Horby, P. W. et al. A national outbreak of multi-resistant Salmonella enterica serovar Typhimurium definitive phage type (DT) 104 associated with consumption of lettuce. Epidemiol. Infect. 130, 169–178 (2003).

    Article  CAS  Google Scholar 

  13. Humphrey, T. J. Salmonella Typhimurium definitive type (DT) 104: a multi-resistant Salmonella. [online], <http://europe.ilsi.org/file/ILSISalm.pdf> (International Life Sciences Institute, 2000).

  14. LeClerc, J. E., Li, B., Payne, W. L. & Cebula, T. A. High mutation frequencies among Escherichia coli and Salmonella pathogens. Science 274, 1208–1211 (1996).

    Article  CAS  Google Scholar 

  15. Ivanova, A., Renshaw, M., Guntaka, R. V. & Eisenstark A. DNA base sequence variability in katF (putative sigma factor) gene of Escherichia coli. Nucleic Acids Res. 20, 5479–5480 (1992).

    Article  CAS  Google Scholar 

  16. Waterman, S. R. & Small, P. L. C. Characterization of the acid-resistance phenotype and rpoS alleles of shiga-like toxin-producing Escherichia coli. Infect. Immun. 64, 2808–2811 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Jørgensen, F. et al. Invasiveness in chickens, stress resistance and RpoS status of wild-type Salmonella enterica subsp. enterica serovar Typhimurium definitive type 104 and serovar Enteritidis phage type 4 isolates. Microbiology 146, 3227–3235 (2000).

    Article  Google Scholar 

  18. Robbe-Saule, V., Algorta, G., Rouilhac, I. & Norel, F. Characterization of the RpoS status of clinical isolates of Salmonella enterica. Appl. Environ. Microbiol. 69, 4352–4358 (2003).

    Article  CAS  Google Scholar 

  19. Ferenci, T. What is driving the acquisition of mutS and rpoS polymorphisms in Escherichia coli? Trends Microbiol. 11, 457–461 (2003).

    Article  CAS  Google Scholar 

  20. Russell, J. B., Diez-Gonzalez, F. & Jarvis, G. N. Effects of diet shifts on Escherichia coli in cattle. J. Dairy Sci. 83, 863–873 (2000).

    Article  CAS  Google Scholar 

  21. Humphrey, T. J., Richardson, N. P., Statton, K. M. & Rowbury, R. J. Effects of temperature shift on acid and heat tolerance in Salmonella enteritidis phage type 4. Appl. Environ. Microbiol. 59, 3120–3122 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Banatvala, N., Cramp, A., Jones, I. R. & Feldman, R. A. Salmonellosis in north Thames (East), UK: associated risk factors. Epidemiol. Infect. 122 201–207 (1999).

    Article  CAS  Google Scholar 

  23. Smith, J. L. The role of gastric acid in preventing foodborne disease and how bacteria overcome acid conditions. J. Food Prot. 66 1292–1303 (2003).

    Article  Google Scholar 

  24. Berends, B. R., Van Knapen, F., Mossel, D. A., Burt, S. A. & Snijders, J. M. Impact on human health of Salmonella spp. on pork in The Netherlands and the anticipated effects of some currently proposed control strategies. Int. J. Food Microbiol. 44 219–229 (1998).

    Article  CAS  Google Scholar 

  25. Lee, Y. K., Puong, K. Y., Ouwehand, A. C. & Salminen, S. Displacement of bacterial pathogens from mucus and Caco-2 cell surface by lactobacilli. J. Med. Microbiol. 52, 925–930 (2003).

    Article  Google Scholar 

  26. Asahara, T., Nomoto, K., Shimizu, K., Watanuki, M. & Tanaka, R. Increased resistance of mice to Salmonella enterica serovar Typhimurium infection by synbiotic administration of Bifidobacteria and transgalactosylated oligosaccharides. J. Appl. Microbiol. 91, 985–996 (2001).

    Article  CAS  Google Scholar 

  27. St Louis, M. E. et al. The emergence of grade A eggs as a major source of Salmonella Enteritidis infections: new implications for the control of salmonellosis. JAMA 259, 2103–2107 (1988).

    Article  CAS  Google Scholar 

  28. Poppe, C. in Salmonella Enterica Serovar Enteritidis in Humans and Animals: Epidemiology, Pathogenesis, and Control (eds Saeed, A. M., Gast, R. K., Potter, M. E. & Wall, P. G.) (Iowa State Univ. Press, Ames, Iowa, 1999).

    Google Scholar 

  29. Advisory Committee on the Microbiological Safety of Food. Second report on Salmonella in eggs. [online], <http://archive.food.gov.uk/committees/acmsf/acmsf010509.pdf> (2001).

  30. Humphrey, T. J. et al. Isolates of Salmonella enterica Enteritidis PT4 with enhanced heat and acid tolerance are more virulent in mice and more invasive in chickens. Epidemiol. Infect. 117, 79–88 (1996).

    Article  CAS  Google Scholar 

  31. De Buck, J., Van Immerseel, F., Meulemans, G., Haesebrouck, F. & Ducatelle, R. Adhesion of Salmonella enterica serotype Enteritidis isolates to chicken isthmal glandular secretions. Vet. Microbiol. 29, 223–233 (2003).

    Article  Google Scholar 

  32. Guard-Petter, J. in Salmonella Enterica Serovar Enteritidis in Humans and Animals: Epidemiology, Pathogenesis, and Control (eds Saeed, A. M., Gast, R. K., Potter, M. E. & Wall, P. G.) (Iowa State Univ. Press, Ames, Iowa, 1999).

    Google Scholar 

  33. Keller, L. H., Schifferli, D. M., Benson, C. E., Aslam, S. & Eckroade, R. J. Invasion of chicken reproductive tissues and forming eggs is not unique to Salmonella Enteritidis. Avian Dis. 41, 535–539 (1997).

    Article  CAS  Google Scholar 

  34. Guard-Petter, J. The chicken, the egg and Salmonella Enteritidis. Environ. Microbiol. 3, 421–430 (2001).

    Article  CAS  Google Scholar 

  35. Advisory Committee on the Microbiological Safety of Food. First Report on Salmonella in eggs. (Food Standards Agency, The Stationery Office, London, 1993).

  36. Lu, S., Killoran, P. B. & Riley, L. W. Association of Salmonella enterica serovar Enteritidis yafD with resistance to chicken egg albumen. Infect. Immun. 71, 6734–6741 (2003).

    Article  CAS  Google Scholar 

  37. Health Protection Agency. LACORS/HPA collaborative study of raw shell eggs and their use in catering premises. Commun. Dis. Rep. Weekly [online], <http://www.hpa.org.uk/cdr/pdffiles/2004/cdr1204.pdf> (2004).

  38. Humphrey, T. J., Baskerville, A., Chart, H. & Rowe, B. Infection of egg-laying hens with Salmonella Enteritidis PT4 by oral inoculation. Vet. Rec. 125, 531–532 (1989).

    Article  CAS  Google Scholar 

  39. Burton, C. L. et al. The growth response of Escherichia coli to neurotransmitters and related catecholamine drugs requires a functional enterobactin biosynthesis and uptake system. Infect. Immun. 70, 5913–5923 (2002).

    Article  CAS  Google Scholar 

  40. Gruenewald, R. et al. in Salmonella Enterica Serovar Enteritidis in Humans and Animals: Epidemiology, Pathogenesis, and Control (eds Saeed, A. M., Gast, R. K., Potter, M. E. & Wall, P. G.) (Iowa State Univ. Press, Ames, Iowa, 1999).

    Google Scholar 

  41. Senhaji, A. F. The protective effect of fat on the heat resistance of bacteria. J. Food Technol. 12, 203–216 (1977).

    Article  Google Scholar 

  42. Mattick, K. L., Humphrey, T. J. & Rowbury, R. Morphological changes of Escherichia coli O157, E. coli and Salmonella in response to marginal growth conditions common in foods. Sci. Prog. (New Haven) 86, 103–113 (2003).

    Article  Google Scholar 

  43. Mattick, K. The survival of Salmonella spp. at high temperature and low water activity. Thesis, Univ. Exeter (2001).

  44. Hecker, M., Heim, C., Volker, U. & Wolfel, L. Induction of stress proteins by sodium chloride treatment in Bacillus subtilis. Arch. Microbiol. 150, 564–566 (1988).

    Article  CAS  Google Scholar 

  45. Levy, S. B. Active efflux, a common mechanism for biocide and antibiotic resistance. Symp. Ser. Soc. Appl. Microbiol. 31, 65S–71S (2002).

    Article  CAS  Google Scholar 

  46. De Wit, J. C., Brockhuizen, G. & Kampelmacher, E. H. Cross-contamination during the preparation of frozen chickens in the kitchen. J. Hyg. 83, 27–32 (1979).

    Article  CAS  Google Scholar 

  47. Humphrey, T. J., Martin, K. W. & Whitehead, A. Contamination of hands and work surfaces with Salmonella Enteritidis PT4 during the preparation of egg dishes. Epidemiol. Infect. 113, 403–409 (1994).

    Article  CAS  Google Scholar 

  48. Humphrey, T. J., Slater, E., McAlpine, K., Rowbury, R. J. & Gilbert, R. J. Salmonella Enteritidis phage type 4 isolates more tolerant of heat, acid, or hydrogen peroxide also survive longer on surfaces. Appl. Environ. Microbiol. 61, 3161–3164 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

I would like to acknowledge the work of the staff in the Bristol Food Safety Group, who undertook much of the work reported here.

Author information

Authors and Affiliations

  1. School of Clinical Veterinary Science, University of Bristol, Langford, Bristol, BS40 5DU, UK

    Tom Humphrey

Authors
  1. Tom Humphrey
    View author publications

    You can also search for this author in PubMed Google Scholar

Ethics declarations

Competing interests

The author provides occasional consultancy to the British Egg Industry Council and Marks & Spencer.

Related links

Related links

DATABASES

Entrez

E. coli K12

E. coli O157

Salmonella enterica serovar Enteritidis

Salmonella enterica serovar Typhi

Salmonella enterica serovar Typhimurium

SwissProt

RpoS

FURTHER INFORMATION

Tom Humphrey's laboratory

CDC Food-borne diseases

Health Protection Agency

Salmonellosis disease information

WHO Food-borne diseases

British Egg Information Service

Rights and permissions

Reprints and permissions

About this article

Cite this article

Humphrey, T. Salmonella, stress responses and food safety. Nat Rev Microbiol 2, 504–509 (2004). https://doi.org/10.1038/nrmicro907

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrmicro907

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing