Predicting the spatio-temporal spread of West Nile virus in Europe.
Abstract: West Nile virus is a widely spread arthropod-born virus, which has mosquitoes as vectors and birds as reservoirs. Humans, as dead-end hosts of the virus, may suffer West Nile Fever (WNF), which sometimes leads to death. In Europe, the first large-scale epidemic of WNF occurred in 1996 in Romania. Since then, human cases have increased in the continent, where the highest number of cases occurred in 2018. Using the location of WNF cases in 2017 and favorability models, we developed two risk models, one environmental and the other spatio-environmental, and tested their capacity to predict in 2018: 1) the location of WNF; 2) the intensity of the outbreaks (i.e. the number of confirmed human cases); and 3) the imminence of the cases (i.e. the Julian week in which the first case occurred). We found that climatic variables (the maximum temperature of the warmest month and the annual temperature range), human-related variables (rain-fed agriculture, the density of poultry and horses), and topo-hydrographic variables (the presence of rivers and altitude) were the best environmental predictors of WNF outbreaks in Europe. The spatio-environmental model was the most useful in predicting the location of WNF outbreaks, which suggests that a spatial structure, probably related to bird migration routes, has a role in the geographical pattern of WNF in Europe. Both the intensity of cases and their imminence were best predicted using the environmental model, suggesting that these features of the disease are linked to the environmental characteristics of the areas. We highlight the relevance of river basins in the propagation dynamics of the disease, as outbreaks started in the lower parts of the river basins, from where WNF spread towards the upper parts. Therefore, river basins should be considered as operational geographic units for the public health management of the disease.
Publication Date: 2021-01-07 PubMed ID: 33411739PubMed Central: PMC7790247DOI: 10.1371/journal.pntd.0009022Google Scholar: Lookup
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- Journal Article
- Research Support
- Non-U.S. Gov't
- Climate
- Disease control
- Disease Outbreaks
- Disease Prevalence
- Disease Surveillance
- Disease Transmission
- Ecology
- Environment
- Epidemiology
- Equine Health
- Geographical Differences
- Horses
- Migration
- Mosquito-borne Diseases
- Predictive Model
- Public Health
- Vector-borne disease
- Veterinary Research
- Veterinary Science
- West Nile Virus
Summary
This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.
This research focuses on predicting the spread and impact of West Nile fever (WNF) in Europe, based on environmental factors and geographic patterns tied to bird migration routes. It puts forward two potential predictive models – an environmental one and a spatio-environmental one – and explores their effectiveness.
Overview of Research Methodology
- The researchers have created two predictive models to forecast the spread of WNF in Europe. These models are termed as ‘environmental’ and ‘spatio-environmental’ models.
- The data input for these models was derived from the location of WNF cases in 2017.
- The models were then tested for their prediction accuracy for 2018 on three different aspects: 1) the location of WNF cases; 2) the intensity of outbreaks, that is, the number of confirmed human cases of the disease; 3) the imminence of the cases, meaning the Julian week during which the first case of WNF occurred.
Key Findings
- The study revealed that certain climatic variables, such as the maximum temperature of the warmest month and the annual temperature range, had significant predictive power.
- Additionally, it was found that human-related variables, such as rain-fed agriculture, the density of poultry, and horses also played an important role in predicting WNF outbreaks.
- The features of the topo-hydrographic environment, specifically the presence of rivers and altitude, were among the best predictors of WNF outbreaks in Europe.
- Overall, the spatio-environmental model was the most useful in predicting the location of WNF outbreaks. This suggested that a spatial structure, which is likely related to bird migration routes, has a significant role in the geographical pattern of WNF in Europe.
- The intensity of cases and their imminence were best predicted using the environmental model, indicating that these features of the disease are intrinsically linked to the environmental characteristics of certain areas.
Implications and Recommendations
- The study found a notable role of river basins in the propagation dynamics of the disease. Outbreaks typically started in the lower parts of the river basins and spread towards the upper parts.
- Given this finding, the researchers recommend that these river basins should be considered as operational geographic units for the public health management of the disease.
Cite This Article
APA
García-Carrasco JM, Muñoz AR, Olivero J, Segura M, Real R.
(2021).
Predicting the spatio-temporal spread of West Nile virus in Europe.
PLoS Negl Trop Dis, 15(1), e0009022.
https://doi.org/10.1371/journal.pntd.0009022 Publication
Researcher Affiliations
- Biogeography, Diversity and Conservation Lab, Department of Animal Biology, Faculty of Sciences, University of Málaga, Málaga, Spain.
- Biogeography, Diversity and Conservation Lab, Department of Animal Biology, Faculty of Sciences, University of Málaga, Málaga, Spain.
- Biogeography, Diversity and Conservation Lab, Department of Animal Biology, Faculty of Sciences, University of Málaga, Málaga, Spain.
- International Vaccination Center of Malaga, Maritime Port of Malaga, Ministry of Health, Consumption and Social Welfare, Government of Spain, Málaga, Spain.
- Biogeography, Diversity and Conservation Lab, Department of Animal Biology, Faculty of Sciences, University of Málaga, Málaga, Spain.
MeSH Terms
- Climate
- Disease Outbreaks
- Environment
- Europe / epidemiology
- Humans
- Rivers
- West Nile Fever / epidemiology
- West Nile Fever / transmission
Conflict of Interest Statement
The authors have declared that no competing interests exist.
References
This article includes 64 references
- Chancey C, Grinev A, Volkova E, Rios M. The global ecology and epidemiology of West Nile virus.. Biomed Res Int 2015;2015:376230.
- Balenghien T, Vazeille M, Grandadam M, Schaffner F, Zeller H, Reiter P, Sabatier P, Fouque F, Bicout DJ. Vector competence of some French Culex and Aedes mosquitoes for West Nile virus.. Vector Borne Zoonotic Dis 2008 Oct;8(5):589-95.
- Petersen LR, Brault AC, Nasci RS. West Nile virus: review of the literature.. JAMA 2013 Jul 17;310(3):308-15.
- Durand B, Tran A, Balança G, Chevalier V. Geographic variations of the bird-borne structural risk of West Nile virus circulation in Europe.. PLoS One 2017;12(10):e0185962.
- Young JJ, Coulombier D, Domanović D, Zeller H, Gossner CM. One Health approach for West Nile virus surveillance in the European Union: relevance of equine data for blood safety.. Euro Surveill 2019 Apr;24(16).
- Kramer LD, Li J, Shi P. West Nile virus. Lancet Neurol 2007;6: 1999–2005.
- Ulbert S. West Nile virus vaccines - current situation and future directions.. Hum Vaccin Immunother 2019;15(10):2337-2342.
- Calistri P, Giovannini A, Hubalek Z, Ionescu A, Monaco F, Savini G, Lelli R. Epidemiology of west nile in europe and in the mediterranean basin.. Open Virol J 2010 Apr 22;4:29-37.
- Smithburn KC, Hughes TP, Burke AW, Paul JH. A Neurotropic Virus Isolated from the Blood of a Native of Uganda. Am J Trop Med Hyg 1940;s1-20: 471–492.
- Joubert L, Oudar J, Hannoun C, Beytout D, Corniou B, Guillon JC, Panthier R. [Epidemiology of the West Nile virus: study of a focus in Camargue. IV. Meningo-encephalomyelitis of the horse].. Ann Inst Pasteur (Paris) 1970 Feb;118(2):239-47.
- Tsai TF, Popovici F, Cernescu C, Campbell GL, Nedelcu NI. West Nile encephalitis epidemic in southeastern Romania.. Lancet 1998 Sep 5;352(9130):767-71.
- Chirico F, Magnavita N. West Nile virus infection in Europe: need for an integration of occupational health practice and public health activities. Commentary.. Ann Ist Super Sanita 2019 Jan-Mar;55(1):3-5.
- European Centre for Disease Prevention and Control. West Nile virus. 2019.
- Ziegler U, Lühken R, Keller M, Cadar D, van der Grinten E, Michel F, Albrecht K, Eiden M, Rinder M, Lachmann L, Höper D, Vina-Rodriguez A, Gaede W, Pohl A, Schmidt-Chanasit J, Groschup MH. West Nile virus epizootic in Germany, 2018.. Antiviral Res 2019 Feb;162:39-43.
- Murray KA, Olivero J, Roche B, Tiedt S, Guégan JF. Pathogeography: leveraging the biogeography of human infectious diseases for global health management.. Ecography 2018 Sep;41(9):1411-1427.
- Olivero J, Fa JE, Real R, Farfán MÁ, Márquez AL, Vargas JM. Mammalian biogeography and the Ebola virus in Africa. Mammal Review 2017. pp. 24–37.
- Barker CM. Models and Surveillance Systems to Detect and Predict West Nile Virus Outbreaks.. J Med Entomol 2019 Oct 28;56(6):1508-1515.
- Romero D, Olivero J, Real R, Guerrero JC. Applying fuzzy logic to assess the biogeographical risk of dengue in South America.. Parasit Vectors 2019 Sep 5;12(1):428.
- Zadeh LA. Fuzzy sets. Inf Control 1965;8: 338–353.
- Solanki P, Dhawan S, Kabra B. A Fuzzy Model for Minining Amino Acid Assosiations In Peptide Sequences of Flavivirus Sub Families. Biosci Biotechnol Res Commun 2019;12: 1047–1062.
- Real R, Barbosa AM, Vargas JM. Obtaining environmental favourability functions from logistic regression. Environ Ecol Stat 2006;13: 237–245.
- European Commission. Eurostat, NUTS- Nomenclature of Territorial Units for Statistics. Luxemburg: Eurostat; 2003.
- Crovello TJ. Quantitative biogeography: an overview. Taxon 1981;30: 563–575.
- European Commission. Commission implementing decision 2018/945 of 22 June 2018 on the communicable diseases and related special health issues to be covered by epidemiological surveillance as well as relevant case definitions. Luxembourg; 2018.
- Rao CR. Large sample tests of statistical hypotheses concerning several parameters with applications to problems of estimation. Math Proc Cambridge Philos Soc 1948;44: 50–57.
- Benjamini Y, Hochberg Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing Yoav Benjamini; Yosef Hochberg. Journal of the Royal Statistical Society. Series B (Methodological) 1995;57: 289–300.
- Legendre P. Spatial Autocorrelation: Trouble or New Paradigm?. Ecology 1993;74: 1659–1673.
- Legendre P, Legendre L. Numerical Ecology. Elsevier Science, editor. Amsterdam (The Netherlands); 1998.
- Lobo JM, Jiménez-valverde A, Real R. AUC: A misleading measure of the performance of predictive distribution models. Glob Ecol Biogeogr 2008;17: 145–151.
- Fielding AH, Bell JF. A review of methods for the assessment of prediction errors in conservation presence/absence models. Environ Conserv 1997;24: 38–49.
- Barbosa AM, Real R, Muñoz AR, Brown JA. New measures for assessing model equilibrium and prediction mismatch in species distribution models. Divers Distrib 2013;19: 1333–1338.
- Hosmer DW, Lemeshow S. Goodness of fit tests for the multiple logistic regression model. Commun Stat—Theory Methods 1980; 1043–4069.
- Miller ME, Hui SL, Tierney WM. Validation techniques for logistic regression models.. Stat Med 1991 Aug;10(8):1213-26.
- Muñoz AR, Jiménez-Valverde A, Márquez AL, Moleón M, Real R. Environmental favourability as a cost-efficient tool to estimate carrying capacity. Divers Distrib 2015;21: 1388–1400.
- Olivero J, Real R, Vargas JM. Distribution of breeding, wintering, and resident waterbirds in Europe: Biotic regions and the macroclimate. Ornis Fenn 1998;75: 153–175.
- Bárcena S, Real R, Olivero J, Mario Vargas J. Latitudinal trends in breeding waterbird species richness in Europe and their environmental correlates. Biodivers Conserv 2004;13: 1997–2014.
- Márquez AL, Real R, Vargas JM. Dependence of broad-scale geographical variation in fleshy-fruited plant species richness on disperser bird species richness. Glob Ecol Biogeogr 2004;13: 295–304.
- Hosmer DW, Lemeshow S, Sturdivant RX. Applied Logistic Regression. 3rd ed. Hoboken: Wiley; 2013.
- Crowder DW, Dykstra EA, Brauner JM, Duffy A, Reed C, Martin E, Peterson W, Carrière Y, Dutilleul P, Owen JP. West nile virus prevalence across landscapes is mediated by local effects of agriculture on vector and host communities.. PLoS One 2013;8(1):e55006.
- Bowden SE, Magori K, Drake JM. Regional differences in the association between land cover and West Nile virus disease incidence in humans in the United States.. Am J Trop Med Hyg 2011 Feb;84(2):234-8.
- Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, Holt RD, Hudson P, Jolles A, Jones KE, Mitchell CE, Myers SS, Bogich T, Ostfeld RS. Impacts of biodiversity on the emergence and transmission of infectious diseases.. Nature 2010 Dec 2;468(7324):647-52.
- Ezenwa VO, Godsey MS, King RJ, Guptill SC. Avian diversity and West Nile virus: testing associations between biodiversity and infectious disease risk.. Proc Biol Sci 2006 Jan 7;273(1582):109-17.
- Wilson JD, Evans AD, Grice P V. Bird conservation and agriculture. Cambridge University Press; 2009.
- Donal PF, Gree RE, Heath MF. Agricultural intensification and the collapse of Europe's farmland bird populations.. Proc Biol Sci 2001 Jan 7;268(1462):25-9.
- Tolsá MJ, García-Peña GE, Rico-Chávez O, Roche B, Suzán G. Macroecology of birds potentially susceptible to West Nile virus.. Proc Biol Sci 2018 Dec 19;285(1893):20182178.
- Boukraa S, de La Grandiere MA, Bawin T, Raharimalala FN, Zimmer JY, Haubruge E, Thiry E, Francis F. Diversity and ecology survey of mosquitoes potential vectors in Belgian equestrian farms: A threat prevention of mosquito-borne equine arboviruses.. Prev Vet Med 2016 Feb 1;124:58-68.
- Wang G, Minnis RB, Belant JL, Wax CL. Dry weather induces outbreaks of human West Nile virus infections.. BMC Infect Dis 2010 Feb 24;10:38.
- Vogels CBF, Hartemink N, Koenraadt CJM. Modelling West Nile virus transmission risk in Europe: effect of temperature and mosquito biotypes on the basic reproduction number.. Sci Rep 2017 Jul 10;7(1):5022.
- Reisen WK, Fang Y, Martinez VM. Effects of temperature on the transmission of west nile virus by Culex tarsalis (Diptera: Culicidae).. J Med Entomol 2006 Mar;43(2):309-17.
- Hartley DM, Barker CM, Le Menach A, Niu T, Gaff HD, Reisen WK. Effects of temperature on emergence and seasonality of West Nile virus in California.. Am J Trop Med Hyg 2012 May;86(5):884-94.
- Semenza JC, Suk JE. Vector-borne diseases and climate change: a European perspective.. FEMS Microbiol Lett 2018 Feb 1;365(2).
- Paz S. Effects of climate change on vector-borne diseases: an updated focus on West Nile virus in humans. Emerg Top Life Sci 2019;3: 143–152.
- Valiakos G, Papaspyropoulos K, Giannakopoulos A, Birtsas P, Tsiodras S, Hutchings MR, Spyrou V, Pervanidou D, Athanasiou LV, Papadopoulos N, Tsokana C, Baka A, Manolakou K, Chatzopoulos D, Artois M, Yon L, Hannant D, Petrovska L, Hadjichristodoulou C, Billinis C. Use of wild bird surveillance, human case data and GIS spatial analysis for predicting spatial distributions of West Nile virus in Greece.. PLoS One 2014;9(5):e96935.
- Getachew D, Balkew M, Tekie H. Anopheles larval species composition and characterization of breeding habitats in two localities in the Ghibe River Basin, southwestern Ethiopia.. Malar J 2020 Feb 11;19(1):65.
- Moirano G, Richiardi L, Calzolari M, Merletti F, Maule M. Recent rapid changes in the spatio-temporal distribution of West Nile Neuro-invasive Disease in Italy.. Zoonoses Public Health 2020 Feb;67(1):54-61.
- Sándor AD, Mărcuţan DI, D'Amico G, Gherman CM, Dumitrache MO, Mihalca AD. Do the ticks of birds at an important migratory hotspot reflect the seasonal dynamics of Ixodes ricinus at the migration initiation site? A case study in the Danube Delta.. PLoS One 2014;9(2):e89378.
- Koleček J, Procházka P, El-Arabany N, Tarka M, Ilieva M, Hahn S. Cross-continental migratory connectivity and spatiotemporal migratory patterns in the great reed warbler. J Avian Biol 2016;47: 756–767.
- Smart M, Azafzaf H, Dlensi H. The “eurasian” spoonbill (platalea leucorodia) in Africa. Ostrich 2007;78: 495–500.
- Briedis M, Bauer S, Adamík P, Alves JA, Costa JS, Emmenegger T. Broad-scale patterns of the Afro-Palaearctic landbird migration. Glob Ecol Biogeogr 2020; 1–14.
- Youssef SR, Eissa DG, Abo-Shady RA, Aly Fouad NT, Kattab DK, Fathey H, Abdullaha Elewa AA, Reda DM. Seroprevalence of anti-WNV IgG antibodies and WNV-RNA in Egyptian blood donors.. J Med Virol 2017 Aug;89(8):1323-1329.
- Soliman A, Mohareb E, Salman D, Saad M, Salama S, Fayez C, Hanafi H, Medhat I, Labib E, Rakha M, El-Sayed N, Yingst S, Tjaden J, Earhart K. Studies on West Nile virus infection in Egypt.. J Infect Public Health 2010;3(2):54-9.
- Chianese A, Stelitano D, Astorri R, Serretiello E, Teresa M, Rocca D. West Nile virus: an overview of current information. Transl Med Rep 2019;3: 8145.
- Burki T. Increase of West Nile virus cases in Europe for 2018.. Lancet 2018 Sep 22;392(10152):1000.
- European Centre for Disease Prevention and Control. Weekly updates: 2020 West Nile virus transmission season. 2020.
Citations
This article has been cited 16 times.- McCarter MSJ, Self S, Dye-Braumuller KC, Lee C, Li H, Nolan MS. The utility of a Bayesian predictive model to forecast neuroinvasive West Nile virus disease in the United States of America, 2022.. PLoS One 2023;18(9):e0290873.
- Giatropoulos A, Koliopoulos G, Pantelakis PN, Papachristos D, Michaelakis A. Evaluating the Sublethal Effects of Origanum vulgare Essential Oil and Carvacrol on the Biological Characteristics of Culex pipiens biotype molestus (Diptera: Culicidae).. Insects 2023 Apr 20;14(4).
- Albrecht L, Kaufeld KA. Investigating the impact of environmental factors on West Nile virus human case prediction in Ontario, Canada.. Front Public Health 2023;11:1100543.
- Mencattelli G, Silverj A, Iapaolo F, Ippoliti C, Teodori L, Di Gennaro A, Curini V, Candeloro L, Conte A, Polci A, Morelli D, Perrotta MG, Marini G, Rosà R, Monaco F, Segata N, Rizzoli A, Rota-Stabelli O, Savini G, West Nile Working Group. Epidemiological and Evolutionary Analysis of West Nile Virus Lineage 2 in Italy.. Viruses 2022 Dec 22;15(1).
- Amin YES, Ahmed-Abakur EH. West Nile virus IgG antibodies among blood donors in Sudan: a cross-sectional study.. New Microbes New Infect 2022 Nov-Dec;49-50:101062.
- Riccò M, Zaniboni A, Satta E, Ranzieri S, Cerviere MP, Marchesi F, Peruzzi S. West Nile Virus Infection: A Cross-Sectional Study on Italian Medical Professionals during Summer Season 2022.. Trop Med Infect Dis 2022 Nov 28;7(12).
- Marini G, Pugliese A, Wint W, Alexander NS, Rizzoli A, Rosà R. Modelling the West Nile virus force of infection in the European human population.. One Health 2022 Dec;15:100462.
- Giatropoulos A, Bellini R, Pavlopoulos DT, Balatsos G, Karras V, Mourafetis F, Papachristos DP, Karamaouna F, Carrieri M, Veronesi R, Haroutounian SA, Michaelakis A. Efficacy Evaluation of Oregano Essential Oil Mixed with Bacillus thuringiensis israelensis and Diflubenzuron against Culex pipiens and Aedes albopictus in Road Drains of Italy.. Insects 2022 Oct 25;13(11).
- Ganzenberg S, Sieg M, Ziegler U, Pfeffer M, Vahlenkamp TW, Hörügel U, Groschup MH, Lohmann KL. Seroprevalence and Risk Factors for Equine West Nile Virus Infections in Eastern Germany, 2020.. Viruses 2022 May 30;14(6).
- Ramzi A, El Ouali Lalami A, Ez Zoubi Y, Assouguem A, Almeer R, Najda A, Ullah R, Ercisli S, Farah A. Insecticidal Effect of Wild-Grown Mentha pulegium and Rosmarinus officinalis Essential Oils and Their Main Monoterpenes against Culex pipiens (Diptera: Culicidae).. Plants (Basel) 2022 Apr 28;11(9).
- Defilippo F, Dottori M, Lelli D, Chiari M, Cereda D, Farioli M, Chianese R, Cerioli MP, Faccin F, Canziani S, Trogu T, Sozzi E, Moreno A, Lavazza A, Restelli U. Assessment of the Costs Related to West Nile Virus Monitoring in Lombardy Region (Italy) between 2014 and 2018.. Int J Environ Res Public Health 2022 May 3;19(9).
- Farooq Z, Rocklöv J, Wallin J, Abiri N, Sewe MO, Sjödin H, Semenza JC. Artificial intelligence to predict West Nile virus outbreaks with eco-climatic drivers.. Lancet Reg Health Eur 2022 Jun;17:100370.
- García-Carrasco JM, Muñoz AR, Olivero J, Segura M, Real R. Mapping the Risk for West Nile Virus Transmission, Africa.. Emerg Infect Dis 2022 Apr;28(4):777-785.
- Lourenço J, Barros SC, Zé-Zé L, Damineli DSC, Giovanetti M, Osório HC, Amaro F, Henriques AM, Ramos F, Luís T, Duarte MD, Fagulha T, Alves MJ, Obolski U. West Nile virus transmission potential in Portugal.. Commun Biol 2022 Jan 10;5(1):6.
- Riccò M, Peruzzi S, Balzarini F. Public Perceptions on Non-Pharmaceutical Interventions for West Nile Virus Infections: A Survey from an Endemic Area in Northern Italy.. Trop Med Infect Dis 2021 Jun 29;6(3).
- Riccò M, Peruzzi S, Balzarini F. Epidemiology of West Nile Virus Infections in Humans, Italy, 2012-2020: A Summary of Available Evidences.. Trop Med Infect Dis 2021 Apr 24;6(2).
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