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The effect of temperature on different Salmonella serotypes during warm seasons in a Mediterranean climate city, Adelaide, Australia

  • A. MILAZZO (a1), L. C. GILES (a1), Y. ZHANG (a1) (a2), A. P. KOEHLER (a3), J. E. HILLER (a1) (a4) and P. BI (a1)...

Summary

Changing trends in foodborne disease are influenced by many factors, including temperature. Globally and in Australia, warmer ambient temperatures are projected to rise if climate change continues. Salmonella spp. are a temperature-sensitive pathogen and rising temperature can have a substantial effect on disease burden affecting human health. We examined the relationship between temperature and Salmonella spp. and serotype notifications in Adelaide, Australia. Time-series Poisson regression models were fit to estimate the effect of temperature during warmer months on Salmonella spp. and serotype cases notified from 1990 to 2012. Long-term trends, seasonality, autocorrelation and lagged effects were included in the statistical models. Daily Salmonella spp. counts increased by 1·3% [incidence rate ratio (IRR) 1·013, 95% confidence interval (CI) 1·008–1·019] per 1 °C rise in temperature in the warm season with greater increases observed in specific serotype and phage-type cases ranging from 3·4% (IRR 1·034, 95% CI 1·008–1·061) to 4·4% (IRR 1·044, 95% CI 1·024–1·064). We observed increased cases of S. Typhimurium PT9 and S. Typhimurium PT108 notifications above a threshold of 39 °C. This study has identified the impact of warm season temperature on different Salmonella spp. strains and confirms higher temperature has a greater effect on phage-type notifications. The findings will contribute targeted information for public health policy interventions, including food safety programmes during warmer weather.

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Copyright

Corresponding author

*Author for correspondence: Ms. A. Milazzo or Professor P. Bi, School of Public Health, Level 7, 178 North Terrace, Adelaide, SA 5000, Australia. (Email: adriana.milazzo@adelaide.edu.au) (Email: peng.bi@adelaide.edu.au)

References

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1. Hall, GV, D'Souza, RM, Kirk, MD. Foodborne disease in the new millennium: out of the frying pan and into the fire? Medical Journal of Australia 2002; 177: 614618.
2. Majowicz, SE, et al. The global burden of nontyphoidal Salmonella gastroenteritis. Clinical Infectious Diseases 2010; 50: 882889.
3. Kirk, M, et al. Foodborne illness, Australia, circa 2000 and circa 2010. Emerging Infectious Diseases 2014; 20: 18571864.
4. Lalor, K. Salmonella surveillance in Australia and Victoria. In: Proceedings of the Environmental Health Professionals Australia. Inaugural National Symposium. Melbourne, Victoria: Environmental Health Professionals Australia, 2012, pp. 2.
5. The OzFoodNet Working Group. Monitoring the incidence and causes of diseases potentially transmitted by food in Australia: Annual Report of the OzFoodNet Network, 2009. Communicable Diseases Intelligence 2010; 31: 345365.
6. Hall, G, et al. Estimating foodborne gastroenteritis, Australia. Emerging Infectious Diseases 2005; 11: 12571264.
7. Smith, K, et al. Human health: impacts, adaptation, and co-benefits. United Kingdom and New York, NY, USA: Intergovernmental Panel on Climate Change; 2014. Climate Change 2014: Impacts, Adaptation, and Vulnerability Part A: Global and Sectoral Aspects Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change.
8. Department of Environment and Natural Resources. Regional climate change projections: Adelaide and Mount Lofty Ranges, South Australia; 2010.
9. Deo, RC, et al. On Australian heat waves: time series analysis of extreme temperature events in Australia, 1950–2005. In: MODSIM 2007 International Congress on Modelling and Simulation. New Zealand: The Modelling and Simulation Society of Australia and NZ Inc., 2007, p. 10.
10. Miraglia, M, et al. Climate change and food safety: an emerging issue with special focus on Europe. Food and Chemical Toxicology 2009; 47: 10091021.
11. Britton, E, et al. Positive association between ambient temperature and salmonellosis notifications in New Zealand, 1965–2006. Australian and New Zealand Journal of Public Health 2010; 34: 126129.
12. D'Souza, RM, et al. Does ambient temperature affect foodborne disease? Epidemiology 2004; 15: 8692.
13. Fleury, M, et al. A time series analysis of the relationship of ambient temperature and common bacterial enteric infections in two Canadian provinces. International Journal of Biometeorology 2006; 50: 385391.
14. Grjibovski, AM, et al. Climate variations and salmonellosis in northwest Russia: a time-series analysis. Epidemiology and Infection 2013; 141: 269276.
15. Grjibovski, AM, Kosbayeva, A, Menne, B. The effect of ambient air temperature and precipitation on monthly counts of salmonellosis in four regions of Kazakhstan, Central Asia, in 2000–2010. Epidemiology and Infection 2014; 142: 608615.
16. Lal, A, et al. Climate variability, weather and enteric disease incidence in New Zealand: time series analysis. PLoS ONE 2013; 8: e83484.
17. Naumova, EN, et al. Seasonality in six enterically transmitted diseases and ambient temperature. Epidemiology and Infection 2007; 135: 281292.
18. Zhang, Y, Bi, P, Hiller, J. Climate variations and salmonellosis transmission in Adelaide, South Australia: A comparison between regression models. International Journal of Biometeorology 2008; 52: 179187.
19. Zhang, Y, Bi, P, Hiller, JE. Climate variations and Salmonella infection in Australian subtropical and tropical regions. Science of the Total Environment 2010; 408: 524530.
20. Kovats, RS, et al. The effect of temperature on food poisoning: a time-series analysis of salmonellosis in ten European countries. Epidemiology and Infection 2004; 132: 443453.
21. Lake, IR, et al. A re-evaluation of the impact of temperature and climate change on foodborne illness. Epidemiology and Infection 2009; 137: 15381547.
22. Ravel, A, et al. Seasonality in human salmonellosis: assessment of human activities and chicken contamination as driving factors. Foodborne Pathogens and Disease 2010; 7: 785794.
23. Rabsch, W. Salmonella Typhimurium phage typing for pathogens. In: Schatten, H, Eisenstark, A, eds. Salmonella: Totowa, NJ: Humana Press, 2007, pp. 177211.
24. Craig, D, Batholomaeus, A. Agents of foodborne illness. A technical series summarising key information on microorganisms associated with foodborne illness. Canberra: Food Standards Australia New Zealand; 2011.
25. Strawn, LK, et al. Distributions of salmonella subtypes differ between two U.S. produce-growing regions. Applied and Environmental Microbiology 2014; 80: 39823991.
26. Ashbolt, R, Kirk, MD. Salmonella Mississippi infections in Tasmania: the role of native Australian animals and untreated drinking water. Epidemiology and Infection 2006; 134: 12571265.
27. Xiang, J, et al. Association between high temperature and work-related injuries in Adelaide, South Australia, 2001–2010. Journal of Occupational and Environmental Medicine 2014; 71: 246252.
28. Hansen, A, et al. The effect of heat waves on mental health in a temperate Australian city. Environmental Health Perspectives 2008; 116: 13691375.
29. Pang, S, et al. Genomic diversity and adaptation of Salmonella enterica serovar Typhimurium from analysis of six genomes of different phage types. BMC Genomics 2013; 14: 718.
30. Bi, P, et al. Weather and notified Campylobacter infections in temperate and sub-tropical regions of Australia: an ecological study. Journal of Infection 2008; 57: 317323.
31. Lim, JA, Lee, DH, Heu, S. The interaction of human enteric pathogens with plants. Plant Pathology 2014; 30: 109116.
32. Naumova, EN, MacNeill, IB. Time-distributed effect of exposure and infectious outbreaks. Environmetrics 2009; 20: 235248.
33. Vally, H, et al. Proportion of illness acquired by foodborne transmission for nine enteric pathogens in Australia: an expert elicitation. Foodborne Pathogens and Disease 2014; 11: 727733.
34. Edwards, F, et al. Climate change adaptation at the intersection of food and health. Asia-Pacific Journal of Public Health 2011; 23: 91S104.
35. Microbiological Diagnostic Unit. National Enteric Pathogens Surveillance Scheme Non-Human Annual Report 2012: Microbiological Diagnostic Unit, The University of Melbourne, 2012.
36. Denehy, EJ, et al. Outbreak of Salmonella typhimurium phage type 44 infection among attendees of a wedding reception, April 2009. Communicable Diseases Intelligence 2011; 35: 192196.
37. Fearnley, E, et al. Salmonella in chicken meat, eggs and humans; Adelaide, South Australia, 2008. International Journal of Food Microbiology 2011; 146: 219227.
38. Gole, VC, et al. Effect of egg washing and correlation between eggshell characteristics and egg penetration by various Salmonella Typhimurium strains. PLoS ONE 2014; 9: e90987.
39. Najjar, Z, et al. An outbreak of Salmonella Infantis gastroenteritis in a residential aged care facility associated with thickened fluids. Epidemiology and Infection 2012; 140: 22642272.
40. Stephens, N, Coleman, D, Shaw, K. Recurring outbreaks of Salmonella typhimurium phage type 135 associated with the consumption of products containing raw egg in Tasmania. Communicable Diseases Intelligence 2008; 32: 466468.
41. Bambrick, HJ, et al. Climate change and health in the urban environment: adaptation opportunities in Australian cities. Asia-Pacific Journal of Public Health 2011; 23: 67S79.

Keywords

The effect of temperature on different Salmonella serotypes during warm seasons in a Mediterranean climate city, Adelaide, Australia

  • A. MILAZZO (a1), L. C. GILES (a1), Y. ZHANG (a1) (a2), A. P. KOEHLER (a3), J. E. HILLER (a1) (a4) and P. BI (a1)...

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