{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,21]],"date-time":"2026-02-21T08:40:07Z","timestamp":1771663207566,"version":"3.50.1"},"reference-count":46,"publisher":"Public Library of Science (PLoS)","issue":"1","license":[{"start":{"date-parts":[[2024,1,18]],"date-time":"2024-01-18T00:00:00Z","timestamp":1705536000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000270","name":"Natural Environment Research Council","doi-asserted-by":"publisher","award":["MR\/K019341\/1"],"award-info":[{"award-number":["MR\/K019341\/1"]}],"id":[{"id":"10.13039\/501100000270","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100010661","name":"Horizon 2020 Framework Programme","doi-asserted-by":"publisher","award":["773830"],"award-info":[{"award-number":["773830"]}],"id":[{"id":"10.13039\/100010661","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100018336","name":"National Institute for Health Research Health Protection Research Unit","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100018336","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Natural Environmental Council","award":["NE\/R01440X\/1"],"award-info":[{"award-number":["NE\/R01440X\/1"]}]},{"name":"Wellcome Trust HEROIC project","award":["216035\/Z\/19\/Z"],"award-info":[{"award-number":["216035\/Z\/19\/Z"]}]}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"abstract":"<jats:p>Disentangling the impact of the weather on transmission of infectious diseases is crucial for health protection, preparedness and prevention. Because weather factors are co-incidental and partly correlated, we have used geography to separate out the impact of individual weather parameters on other seasonal variables using campylobacteriosis as a case study. Campylobacter infections are found worldwide and are the most common bacterial food-borne disease in developed countries, where they exhibit consistent but country specific seasonality. We developed a novel conditional incidence method, based on classical stratification, exploiting the long term, high-resolution, linkage of approximately one-million campylobacteriosis cases over 20 years in England and Wales with local meteorological datasets from diagnostic laboratory locations. The predicted incidence of campylobacteriosis increased by 1 case per million people for every 5\u00b0 (Celsius) increase in temperature within the range of 8\u00b0\u201315\u00b0. Limited association was observed outside that range. There were strong associations with day-length. Cases tended to increase with relative humidity in the region of 75\u201380%, while the associations with rainfall and wind-speed were weaker.<\/jats:p>\n<jats:p>The approach is able to examine multiple factors and model how complex trends arise, <jats:italic>e.g<\/jats:italic>. the consistent steep increase in campylobacteriosis in England and Wales in May-June and its spatial variability. This transparent and straightforward approach leads to accurate predictions without relying on regression models and\/or postulating specific parameterisations. A key output of the analysis is a thoroughly phenomenological description of the incidence of the disease conditional on specific local weather factors. The study can be crucially important to infer the elusive mechanism of transmission of campylobacteriosis; for instance, by simulating the conditional incidence for a postulated mechanism and compare it with the phenomenological patterns as benchmark. The findings challenge the assumption, commonly made in statistical models, that the transformed mean rate of infection for diseases like campylobacteriosis is a mere additive and combination of the environmental variables.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1011714","type":"journal-article","created":{"date-parts":[[2024,1,18]],"date-time":"2024-01-18T18:24:42Z","timestamp":1705602282000},"page":"e1011714","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":10,"title":["A mathematical, classical stratification modeling approach to disentangling the impact of weather on infectious diseases: A case study using spatio-temporally disaggregated Campylobacter surveillance data for England and Wales"],"prefix":"10.1371","volume":"20","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-6150-2843","authenticated-orcid":true,"given":"Giovanni","family":"Lo Iacono","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Alasdair J. C.","family":"Cook","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Gianne","family":"Derks","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Lora E.","family":"Fleming","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Nigel","family":"French","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Emma L.","family":"Gillingham","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4150-9375","authenticated-orcid":true,"given":"Laura C.","family":"Gonzalez Villeta","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Clare","family":"Heaviside","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Roberto M.","family":"La Ragione","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Giovanni","family":"Leonardi","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Christophe E.","family":"Sarran","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sotiris","family":"Vardoulakis","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Francis","family":"Senyah","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Arnoud H. M.","family":"van Vliet","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Gordon","family":"Nichols","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2024,1,18]]},"reference":[{"issue":"2","key":"pcbi.1011714.ref001","first-page":"1","article-title":"Economic cost of campylobacter, norovirus and rotavirus disease in the United Kingdom","volume":"11","author":"CC Tam","year":"2016","journal-title":"PLoS ONE"},{"issue":"10063","key":"pcbi.1011714.ref002","doi-asserted-by":"crossref","first-page":"3027","DOI":"10.1016\/S0140-6736(16)31593-8","article-title":"Global, regional, and national causes of under-5 mortality in 2000\u201315: an updated systematic analysis with implications for the Sustainable Development Goals","volume":"388","author":"L Liu","year":"2016","journal-title":"The Lancet"},{"issue":"10303","key":"pcbi.1011714.ref003","doi-asserted-by":"crossref","first-page":"870","DOI":"10.1016\/S0140-6736(21)01207-1","article-title":"Global, regional, and national progress towards Sustainable Development Goal 3.2 for neonatal and child health: all-cause and cause-specific mortality findings from the Global Burden of Disease Study 2019","volume":"398","author":"KR Paulson","year":"2021","journal-title":"The Lancet"},{"issue":"10239","key":"pcbi.1011714.ref004","doi-asserted-by":"crossref","first-page":"1779","DOI":"10.1016\/S0140-6736(20)30114-8","article-title":"Mapping geographical inequalities in childhood diarrhoeal morbidity and mortality in low-income and middle-income countries, 2000-17: Analysis for the Global Burden of Disease Study 2017","volume":"395","author":"RC Reiner","year":"2020","journal-title":"The Lancet"},{"issue":"9","key":"pcbi.1011714.ref005","doi-asserted-by":"crossref","first-page":"909","DOI":"10.1016\/S1473-3099(17)30276-1","article-title":"Estimates of global, regional, and national morbidity, mortality, and aetiologies of diarrhoeal diseases: a systematic analysis for the Global Burden of Disease Study 2015","volume":"17","author":"C Troeger","year":"2017","journal-title":"The Lancet Infectious Diseases"},{"issue":"1645","key":"pcbi.1011714.ref006","doi-asserted-by":"crossref","first-page":"20130426","DOI":"10.1098\/rstb.2013.0426","article-title":"After 2015: infectious diseases in a new era of health and development","volume":"369","author":"C Dye","year":"2014","journal-title":"Philosophical transactions of the Royal Society of London Series B, Biological sciences"},{"key":"pcbi.1011714.ref007","doi-asserted-by":"crossref","DOI":"10.1201\/b13390","volume-title":"Environmental Medicine","author":"JG Ayres","year":"2010"},{"key":"pcbi.1011714.ref008","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1146\/annurev.publhealth.28.021406.144128","article-title":"Seasonality of infectious diseases","volume":"28","author":"DN Fisman","year":"2007","journal-title":"Annual review of public health"},{"issue":"September","key":"pcbi.1011714.ref009","article-title":"Over half of known human pathogenic diseases can be aggravated by climate change","volume":"12","author":"C Mora","year":"2022","journal-title":"Nature Climate Change"},{"issue":"1","key":"pcbi.1011714.ref010","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1029\/2021GH000452","article-title":"Associations Between Eight Earth Observation-Derived Climate Variables and Enteropathogen Infection: An Independent Participant Data Meta-Analysis of Surveillance Studies With Broad Spectrum Nucleic Acid Diagnostics","volume":"6","author":"JM Colston","year":"2022","journal-title":"GeoHealth"},{"issue":"6","key":"pcbi.1011714.ref011","doi-asserted-by":"crossref","first-page":"e0005659","DOI":"10.1371\/journal.pntd.0005659","article-title":"Challenges in developing methods for quantifying the effects of weather and climate on water-associated diseases: A systematic review","volume":"11","author":"G Lo Iacono","year":"2017","journal-title":"PLOS Neglected Tropical Diseases"},{"issue":"12","key":"pcbi.1011714.ref012","doi-asserted-by":"crossref","first-page":"e1001921","DOI":"10.1371\/journal.pmed.1001921","article-title":"World Health Organization Estimates of the Global and Regional Disease Burden of 22 Foodborne Bacterial, Protozoal, and Viral Diseases, 2010: A Data Synthesis","volume":"12","author":"MD Kirk","year":"2015","journal-title":"PLOS Medicine"},{"key":"pcbi.1011714.ref013","unstructured":"WHO. Campylobacteriosis Report of an Expert Consultation. July; 2012. Available from: http:\/\/apps.who.int\/iris\/bitstream\/10665\/80751\/1\/9789241564601{_}eng.pdf."},{"issue":"1","key":"pcbi.1011714.ref014","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1136\/gut.2011.238386","article-title":"Longitudinal study of infectious intestinal disease in the UK (IID2 study): incidence in the community and presenting to general practice","volume":"61","author":"CC Tam","year":"2012","journal-title":"Gut"},{"issue":"1977","key":"pcbi.1011714.ref015","article-title":"A restatement of the natural science evidence base regarding the source, spread and control of Campylobacter species causing human disease","volume":"289","author":"MR Goddard","year":"2022","journal-title":"Proceedings of the Royal Society B: Biological Sciences"},{"key":"pcbi.1011714.ref016","first-page":"1","article-title":"Advisory Committee on the Microbiological Safety of Food Second Report on Campylobacter","author":"ACMSF","year":"2005","journal-title":"Advisory Committee on the Microbiological Safety of Food"},{"key":"pcbi.1011714.ref017","article-title":"Year 4 Report. A microbiological survey of Campylobacter contamination in fresh whole UK-produced chilled chickens at retail sale","author":"F Jorgensen","year":"2019","journal-title":"Public Health England"},{"key":"pcbi.1011714.ref018","doi-asserted-by":"crossref","first-page":"2526","DOI":"10.1017\/S0950268813000356","article-title":"Increased risk for Campylobacter jejuni and C. coli infection of pet origin in dog owners and evidence for genetic association between strains causing infection in humans and their pets","volume":"141","author":"LM Gras","year":"2013","journal-title":"Epidemiology and infection"},{"issue":"3","key":"pcbi.1011714.ref019","doi-asserted-by":"crossref","first-page":"361","DOI":"10.3201\/eid1103.040460","article-title":"Fly transmission of Campylobacter","volume":"11","author":"GL Nichols","year":"2005","journal-title":"Emerging infectious diseases"},{"issue":"4","key":"pcbi.1011714.ref020","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1136\/bmjopen-2012-001179","article-title":"Campylobacter epidemiology: a descriptive study reviewing 1 million cases in England and Wales between 1989 and 2011","volume":"2","author":"GL Nichols","year":"2012","journal-title":"BMJ open"},{"issue":"1","key":"pcbi.1011714.ref021","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1186\/s12879-019-3840-7","article-title":"Seasonality and the effects of weather on Campylobacter infections","volume":"19","author":"A Djennad","year":"2019","journal-title":"BMC Infectious Diseases"},{"issue":"2","key":"pcbi.1011714.ref022","doi-asserted-by":"crossref","first-page":"256","DOI":"10.1046\/j.1365-2672.2001.01239.x","article-title":"The effects of UVB and temperature on the survival of natural populations and pure cultures of Campylobacter jejuni, Camp. coli, Camp. lari and urease-positive thermophilic campylobacters (UPTC) in surface waters","volume":"90","author":"K Obiri-Danso","year":"2001","journal-title":"Journal of Applied Microbiology"},{"issue":"S6","key":"pcbi.1011714.ref023","doi-asserted-by":"crossref","first-page":"68S","DOI":"10.1046\/j.1365-2672.2001.01355.x","article-title":"Campylobacters in water, sewage and the environment","volume":"90","author":"K Jones","year":"2003","journal-title":"Journal of Applied Microbiology"},{"issue":"1","key":"pcbi.1011714.ref024","doi-asserted-by":"crossref","first-page":"1067","DOI":"10.1186\/s12889-018-5931-6","article-title":"Pathogen seasonality and links with weather in England and Wales: a big data time series analysis","volume":"18","author":"MPC Cherrie","year":"2018","journal-title":"BMC Public Health"},{"key":"pcbi.1011714.ref025","unstructured":"Anonymous. Medical & Environmental Data Mash-up Infrastructure; Retrieved 27\/02\/2019. Available at: https:\/\/www.ecehh.org\/research\/medmi\/."},{"issue":"2","key":"pcbi.1011714.ref026","doi-asserted-by":"crossref","first-page":"1725","DOI":"10.3390\/ijerph110201725","article-title":"Data mashups: Potential contribution to decision support on climate change and health","volume":"11","author":"LE Fleming","year":"2014","journal-title":"International Journal of Environmental Research and Public Health"},{"issue":"1","key":"pcbi.1011714.ref027","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1186\/s12879-018-3106-9","article-title":"A comparison of weather variables linked to infectious disease patterns using laboratory addresses and patient residence addresses","volume":"18","author":"A Djennad","year":"2018","journal-title":"BMC Infectious Diseases"},{"key":"pcbi.1011714.ref028","unstructured":"Public Health England. PHE centres: local authority lookup; 2014. Available from: https:\/\/www.gov.uk\/government\/publications\/phe-centres-local-authority-lookup."},{"issue":"1","key":"pcbi.1011714.ref029","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/0304-3800(94)00034-F","article-title":"A model comparison for daylength as a function of latitude and day of year","volume":"80","author":"WC Forsythe","year":"1995","journal-title":"Ecological Modelling"},{"issue":"5","key":"pcbi.1011714.ref030","doi-asserted-by":"crossref","first-page":"386","DOI":"10.1093\/oxfordjournals.aje.a117440","article-title":"The distribution of incubation periods of infectious disease. 1949","volume":"141","author":"PE Sartwell","year":"1995","journal-title":"American journal of epidemiology"},{"issue":"2","key":"pcbi.1011714.ref031","doi-asserted-by":"crossref","first-page":"209","DOI":"10.3201\/eid2102.130504","article-title":"Quantifying reporting timeliness to improve outbreak control","volume":"21","author":"AB Marinovi\u0107","year":"2015","journal-title":"Emerging infectious diseases"},{"key":"pcbi.1011714.ref032","volume-title":"Probability and its Applications","author":"D J V Daley","year":"2003"},{"issue":"8","key":"pcbi.1011714.ref033","doi-asserted-by":"crossref","first-page":"972","DOI":"10.1017\/S0950268818000894","article-title":"Weather correlates of Campylobacter prevalence in broilers at slaughter under tropical conditions in Sri Lanka","volume":"146","author":"RS Kalupahana","year":"2018","journal-title":"Epidemiology and Infection"},{"issue":"1","key":"pcbi.1011714.ref034","doi-asserted-by":"crossref","DOI":"10.1111\/j.1936-704X.2019.03324.x","article-title":"Investigating Relationship Between Soil Moisture and Precipitation Globally Using Remote Sensing Observations","volume":"168","author":"R Sehler","year":"2019","journal-title":"Journal of Contemporary Water Research & Education"},{"issue":"5","key":"pcbi.1011714.ref035","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1016\/0531-5565(75)90005-4","article-title":"Ambient temperature, physical activity and aging in the housefly, Musca domestica","volume":"10","author":"S Ragland","year":"1975","journal-title":"Experimental gerontology"},{"issue":"4","key":"pcbi.1011714.ref036","doi-asserted-by":"crossref","first-page":"802","DOI":"10.1111\/j.1365-2656.2008.01390.x","article-title":"A working guide to boosted regression trees","volume":"77","author":"J Elith","year":"2008","journal-title":"Journal of Animal Ecology"},{"issue":"4","key":"pcbi.1011714.ref037","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1007\/s00484-004-0241-3","article-title":"Climate variability and campylobacter infection: An international study","volume":"49","author":"R Sari Kovats","year":"2005","journal-title":"International Journal of Biometeorology"},{"key":"pcbi.1011714.ref038","article-title":"A microbiological survey of campylobacter contamination in fresh whole UK-produced chilled chickens at retail sale (Y5)","author":"F Jorgensen","year":"2021","journal-title":"Public Health England"},{"issue":"9","key":"pcbi.1011714.ref039","doi-asserted-by":"crossref","first-page":"1663","DOI":"10.1017\/S0950268811002159","article-title":"The spatial and temporal determinants of campylobacteriosis notifications in New Zealand, 2001-2007","volume":"140","author":"SEF Spencer","year":"2012","journal-title":"Epidemiology and Infection"},{"issue":"150","key":"pcbi.1011714.ref040","doi-asserted-by":"crossref","first-page":"20180534","DOI":"10.1098\/rsif.2018.0534","article-title":"Extending statistical models for source attribution of zoonotic diseases: a study of campylobacteriosis","volume":"16","author":"SJ Liao","year":"2019","journal-title":"Journal of The Royal Society Interface"},{"issue":"1","key":"pcbi.1011714.ref041","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s12967-019-1781-y","article-title":"Climate, human behaviour or environment: Individual-based modelling of Campylobacter seasonality and strategies to reduce disease burden","volume":"17","author":"SP Rushton","year":"2019","journal-title":"Journal of Translational Medicine"},{"key":"pcbi.1011714.ref042","unstructured":"Gonzalez Villeta L. Modelling the influence of weather and climate in human disease: salmonellosis today and tomorrow (submitted). PhD thesis; University of Surrey; 2023."},{"issue":"9","key":"pcbi.1011714.ref043","doi-asserted-by":"crossref","first-page":"e0004957","DOI":"10.1371\/journal.pntd.0004957","article-title":"A Unified Framework for the Infection Dynamics of Zoonotic Spillover and Spread","volume":"10","author":"G Lo Iacono","year":"2016","journal-title":"PLOS Neglected Tropical Diseases"},{"issue":"6","key":"pcbi.1011714.ref044","doi-asserted-by":"crossref","first-page":"e236","DOI":"10.1016\/S2542-5196(19)30093-2","article-title":"Examining the influence of weather on rotavirus infection","volume":"3","author":"GL Nichols","year":"2019","journal-title":"The Lancet Planetary Health"},{"key":"pcbi.1011714.ref045","unstructured":"R Core Team. R: A Language and Environment for Statistical Computing; 2021. Available from: https:\/\/www.R-project.org\/."},{"key":"pcbi.1011714.ref046","unstructured":"Great Britain shapefile;. Available from: https:\/\/www.eea.europa.eu\/data-and-maps\/data\/eea-reference-grids-2\/gis-files\/great-britain-shapefile."}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1011714","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,1,18]],"date-time":"2024-01-18T18:25:10Z","timestamp":1705602310000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1011714"}},"subtitle":[],"editor":[{"given":"Nic","family":"Vega","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2024,1,18]]},"references-count":46,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2024,1,18]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1011714","relation":{},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,1,18]]}}}