The relationship between warm season temperatures and heatwaves on the incidence of Salmonella and Campylobacter cases in Adelaide, South Australia

Abstract

Background Salmonella and Campylobacter spp. are the most common foodborne disease pathogens reported worldwide. Changes in climate observed through increasing warmer ambient temperature and heatwaves are considered to be contributing factors to the emergence and re-emergence of foodborne diseases. Warmer ambient temperature enhances the survival of pathogens in the environment, leading to increased contamination of food and water directly impacting on human health when resulting in diarrhoeal illness. Indirectly, social and behavioural factors may also have an impact on foodborne disease as a consequence of climate change. Warmer weather may bring about a change in people’s eating behaviour, food preferences, and behaviour related to unsafe food practices potentially increasing the risk of foodborne illness. However, evidence concerning the effects of warmer temperature and heatwaves on Salmonella and Campylobacter infection is still relatively scarce, and little is known about human behaviour related to food safety practices in response to warmer weather. Aim This thesis is divided into four studies each with specific aims. In broad terms, these were: study 1) to assess food safety practices, food shopping preferences and eating behaviours of people diagnosed with Salmonella or Campylobacter infection and resident of South Australia in the warm season months (January to March 2013), and to identify if socioeconomic status is associated with their behaviour and practices; study 2) to examine the relationship between warmer ambient temperature and the incidence of Salmonella and serotypes; study 3) to examine the relationship between heatwaves and the incidence of Salmonella and serotypes; and study 4) to examine the relationship between warmer ambient temperature, and heatwaves and the incidence of Campylobacter infection in Adelaide, capital city of South Australia from 1990 to 2012. An overall aim was to provide scientific evidence for public health policy making and practical guideline development for foodborne disease control and prevention in the context of climate change. Methods Disease notification data for all studies were obtained from the South Australian state’s health department notifiable disease surveillance system. Climate data for studies 2 to 4 were sourced from the Bureau of Meteorology. Logistic regression was the analytic approach used in study 1, a cross-sectional survey using a questionnaire to examine knowledge, behaviour and perceptions related to food safety. In addition, information about behaviour and preferences related to shopping and dining out, consumption of foods on warm days, preferences for receiving food safety information on warm days and perceived probability of heat as a risk factor for infectious gastroenteritis was also collected. Time-series analysis was the overarching framework used in the analyses for studies 2 through 4 to quantify the effects of temperature and heatwaves on Salmonella disease notifications (overall and the five common serotypes), and Campylobacter disease notifications in the warm season months (October to March). Specific approaches within these studies included Poisson regression analysis with Generalized Estimating Equations and Distributed Lag Non-Linear Models. Results In study 1, Salmonella and Campylobacter cases generally engaged in unsafe personal and food hygiene practices. Participants had poor knowledge of food safety and they were not aware of high-risk foods associated with an increased risk of foodborne illness. Survey responses specifically related to warm weather found that certain food safety practices, and participants’ eating behaviours and food preferences were influenced by temperature, but that generally socioeconomic status did not influence food safety practices. In study 2, daily Salmonella notifications were positively associated with temperature, such that cases increased by 1.3% per 1oC rise in temperature in the warm season. However, greater increases in incidence of Salmonella notifications were observed among specific serotypes and phage types. A temperature threshold of 38oC was detected at which notifications for certain Salmonella phage types increased in Adelaide. In study 3, heatwave intensity had a significant effect on daily counts of overall salmonellosis with a 34% increase in risk of infection. Specific Salmonella serotypes and phage types were sensitive to the effects of heatwaves. Further, the effects of temperature during heatwaves on the number of Salmonella cases and serotypes were found at lags of up to 14 days. In study 4, there was little evidence of an increase in risk of Campylobacter cases associated with either temperature or heatwaves in the warm seasons. During a heatwave, Campylobacter notifications decreased by 19% within a temperature range of 39-40.9oC. Conclusion This thesis presents the first detailed examination of the effects of warm season temperature and heatwaves on Salmonella and Campylobacter notifications. Furthermore, this is the first research reported to assess the effects of ambient temperature and heatwaves on Salmonella serotypes and their phage types. Overall, these findings demonstrate an increased incidence of Salmonella notifications in the warm seasons associated with higher temperature, and more pronounced effects during heatwaves. The findings have also highlighted that human behaviour and food safety practices are influenced by temperature in the warm season months. These results provide important evidence for policy makers and stakeholders to develop and recommend early warning systems about foodborne disease prevention during heatwaves. In addition, the results highlight the need for targeted public health interventions at a household and population-level in raising awareness and providing education about the importance of food safety in warmer weather.