Abstract
BackgroundWith over 800 million cases globally, campylobacteriosis is a major cause of food borne disease. In temperate climates incidence is highly seasonal but the underlying mechanisms are poorly understood, making human disease control difficult. We hypothesised that observed disease patterns reflect complex interactions between weather, patterns of human risk behaviour, immune status and level of food contamination. Only by understanding these can we find effective interventions.MethodsWe analysed trends in human Campylobacter cases in NE England from 2004 to 2009, investigating the associations between different risk factors and disease using time-series models. We then developed an individual-based (IB) model of risk behaviour, human immunological responses to infection and environmental contamination driven by weather and land use. We parameterised the IB model for NE England and compared outputs to observed numbers of reported cases each month in the population in 2004–2009. Finally, we used it to investigate different community level disease reduction strategies.ResultsRisk behaviours like countryside visits (t = 3.665, P < 0.001 and t = − 2.187, P = 0.029 for temperature and rainfall respectively), and consumption of barbecued food were strongly associated with weather, (t = 3.219, P = 0.002 and t = 2.015, P = 0.045 for weekly average temperature and average maximum temperature respectively) and also rain (t = 2.254, P = 0.02527). This suggests that the effect of weather was indirect, acting through changes in risk behaviour. The seasonal pattern of cases predicted by the IB model was significantly related to observed patterns (r = 0.72, P < 0.001) indicating that simulating risk behaviour could produce the observed seasonal patterns of cases. A vaccination strategy providing short-term immunity was more effective than educational interventions to modify human risk behaviour. Extending immunity to 1 year from 20 days reduced disease burden by an order of magnitude (from 2412–2414 to 203–309 cases per 50,000 person-years).ConclusionsThis is the first interdisciplinary study to integrate environment, risk behaviour, socio-demographics and immunology to model Campylobacter infection, including pathways to mitigation. We conclude that vaccination is likely to be the best route for intervening against campylobacteriosis despite the technical problems associated with understanding both the underlying human immunology and genetic variation in the pathogen, and the likely cost of vaccine development.
Highlights
With over 800 million cases globally, campylobacteriosis is a major cause of food borne disease
Time‐series analyses of cases of disease, human risk behaviours and weather We investigated the effects of seasonality in temperature and rainfall on three human risk behaviours: visits to the countryside, potential barbecue activity and purchase of chicken products for barbecue
We modelled the illness response of humans to exposure using data derived from human dose response experiments [14] and assumed that cooking on a barbecue would result in a 2.5-fold reduction in the dose of colony forming units (CFU) [23]
Summary
With over 800 million cases globally, campylobacteriosis is a major cause of food borne disease. We hypothesised that observed disease patterns reflect complex interactions between weather, patterns of human risk behaviour, immune status and level of food contamination. By understanding these can we find effective interventions. Campylobacter species are the most important gut pathogens in developed countries. Campylobacter is found in many animal species and these along with environmental exposures have been suggested to explain 20–40% of disease burden [12]. The relative importance of different exposures to disease remains largely unquantified which renders effective intervention to reduce the disease burden difficult. There is a dose–response relationship for infection [14, 15], but not symptoms [16]
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