Climate, human behaviour or environment: individual-based modelling of Campylobacter seasonality and strategies to reduce disease burden

Stephen P Rushton, Roy A. Sanderson (Corresponding Author), Peter J Diggle, Mark D F Shirley, Alasdair P Blain, Iain Lake, James A Maas, William D K Reid, Jo Hardstaff, Nicola Williams, Natalia R Jones, Daniel Rigby, Norval J C Strachan, Ken J Forbes, Paul R Hunter, Thomas J Humphrey, Sarah J O'Brien

Research output: Contribution to journalArticle

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Abstract

BACKGROUND: With 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.

METHODS: We 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.

RESULTS: Risk 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).

CONCLUSIONS: This 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.

Original languageEnglish
Article number34
Number of pages13
JournalJournal of translational medicine
Volume17
Issue number1
DOIs
Publication statusPublished - 21 Jan 2019

Fingerprint

Campylobacter
Risk-Taking
Climate
Weather
Immunology
Allergy and Immunology
England
Temperature
Immunity
Vaccination
Rain
Interdisciplinary Studies
Contamination
Campylobacter Infections
Food Contamination
Disease control
Foodborne Diseases
Medical Genetics
Pathogens
Land use

Keywords

  • Campylobacter
  • Individual-based modelling
  • Risk behaviours
  • food
  • weather
  • vaccination
  • Weather
  • Vaccination
  • Food

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)

Cite this

Climate, human behaviour or environment : individual-based modelling of Campylobacter seasonality and strategies to reduce disease burden. / Rushton, Stephen P; Sanderson, Roy A. (Corresponding Author); Diggle, Peter J; Shirley, Mark D F; Blain, Alasdair P; Lake, Iain; Maas, James A; Reid, William D K; Hardstaff, Jo; Williams, Nicola; Jones, Natalia R; Rigby, Daniel; Strachan, Norval J C; Forbes, Ken J; Hunter, Paul R; Humphrey, Thomas J; O'Brien, Sarah J.

In: Journal of translational medicine, Vol. 17, No. 1, 34, 21.01.2019.

Research output: Contribution to journalArticle

Rushton, SP, Sanderson, RA, Diggle, PJ, Shirley, MDF, Blain, AP, Lake, I, Maas, JA, Reid, WDK, Hardstaff, J, Williams, N, Jones, NR, Rigby, D, Strachan, NJC, Forbes, KJ, Hunter, PR, Humphrey, TJ & O'Brien, SJ 2019, 'Climate, human behaviour or environment: individual-based modelling of Campylobacter seasonality and strategies to reduce disease burden' Journal of translational medicine, vol. 17, no. 1, 34. https://doi.org/10.1186/s12967-019-1781-y
Rushton, Stephen P ; Sanderson, Roy A. ; Diggle, Peter J ; Shirley, Mark D F ; Blain, Alasdair P ; Lake, Iain ; Maas, James A ; Reid, William D K ; Hardstaff, Jo ; Williams, Nicola ; Jones, Natalia R ; Rigby, Daniel ; Strachan, Norval J C ; Forbes, Ken J ; Hunter, Paul R ; Humphrey, Thomas J ; O'Brien, Sarah J. / Climate, human behaviour or environment : individual-based modelling of Campylobacter seasonality and strategies to reduce disease burden. In: Journal of translational medicine. 2019 ; Vol. 17, No. 1.
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abstract = "BACKGROUND: With 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.METHODS: We 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.RESULTS: Risk 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).CONCLUSIONS: This 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.",
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author = "Rushton, {Stephen P} and Sanderson, {Roy A.} and Diggle, {Peter J} and Shirley, {Mark D F} and Blain, {Alasdair P} and Iain Lake and Maas, {James A} and Reid, {William D K} and Jo Hardstaff and Nicola Williams and Jones, {Natalia R} and Daniel Rigby and Strachan, {Norval J C} and Forbes, {Ken J} and Hunter, {Paul R} and Humphrey, {Thomas J} and O'Brien, {Sarah J}",
note = "Acknowledgements: We thank colleagues within the Modelling, Evidence and Policy Research Group for useful feedback on this manuscript. Competing interests: The authors declare that they have no competing interests. Availability of data and materials: The R code used in this research is available at https://gitlab.com/rasanderson/campylobacter-microsimulation; it is platform independent, R version 3.3.0 and above. Funding: This research was funded by Medical Research Council Grant, Natural Environment Research Council, Economic and Social Research Council, Biotechnology and Biological Sciences Research Council, and the Food Standards Agency through the Environmental and Social Ecology of Human Infectious Diseases Initiative (Sources, seasonality, transmission and control: Campylobacter and human behaviour in a changing environment (ENIGMA); Grant Reference G1100799-1). PRH, SJO’B, and IRL are funded in part by the NIHR Health Protection Research Unit in Gastrointestinal Infection, at the University of Liverpool. PRH and IRL are also funded in part by the NIHR Health Protection Research Unit in Emergency Preparedness and Response, at King’s College London. The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR, the Department of Health or Public Health England.",
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TY - JOUR

T1 - Climate, human behaviour or environment

T2 - individual-based modelling of Campylobacter seasonality and strategies to reduce disease burden

AU - Rushton, Stephen P

AU - Sanderson, Roy A.

AU - Diggle, Peter J

AU - Shirley, Mark D F

AU - Blain, Alasdair P

AU - Lake, Iain

AU - Maas, James A

AU - Reid, William D K

AU - Hardstaff, Jo

AU - Williams, Nicola

AU - Jones, Natalia R

AU - Rigby, Daniel

AU - Strachan, Norval J C

AU - Forbes, Ken J

AU - Hunter, Paul R

AU - Humphrey, Thomas J

AU - O'Brien, Sarah J

N1 - Acknowledgements: We thank colleagues within the Modelling, Evidence and Policy Research Group for useful feedback on this manuscript. Competing interests: The authors declare that they have no competing interests. Availability of data and materials: The R code used in this research is available at https://gitlab.com/rasanderson/campylobacter-microsimulation; it is platform independent, R version 3.3.0 and above. Funding: This research was funded by Medical Research Council Grant, Natural Environment Research Council, Economic and Social Research Council, Biotechnology and Biological Sciences Research Council, and the Food Standards Agency through the Environmental and Social Ecology of Human Infectious Diseases Initiative (Sources, seasonality, transmission and control: Campylobacter and human behaviour in a changing environment (ENIGMA); Grant Reference G1100799-1). PRH, SJO’B, and IRL are funded in part by the NIHR Health Protection Research Unit in Gastrointestinal Infection, at the University of Liverpool. PRH and IRL are also funded in part by the NIHR Health Protection Research Unit in Emergency Preparedness and Response, at King’s College London. The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR, the Department of Health or Public Health England.

PY - 2019/1/21

Y1 - 2019/1/21

N2 - BACKGROUND: With 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.METHODS: We 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.RESULTS: Risk 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).CONCLUSIONS: This 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.

AB - BACKGROUND: With 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.METHODS: We 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.RESULTS: Risk 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).CONCLUSIONS: This 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.

KW - Campylobacter

KW - Individual-based modelling

KW - Risk behaviours

KW - food

KW - weather

KW - vaccination

KW - Weather

KW - Vaccination

KW - Food

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