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  Previous issue date: 2014Fundação Oswaldo Cruz. Instituto de Comunicação e Informação Científica e Tecnológica em Saúde. RIo de Janeiro, RJ, Brasil.Institut Català de Ciències del Clima. Barcelona, Catalonia, Spain

Barcellos, Christovam

Lowe, Rachel

PLoS Neglected Tropical Diseases

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Barcellos, C; Lowe, R (2014) Dengue and the world football cup: amatter of timing. PLoS neglected tropical diseases, 8 (7). e3022.ISSN 1935-2727 DOI: 10.1371/journal.pntd.0003022Downloaded from: http://researchonline.lshtm.ac.uk/3515707/DOI: 10.1371/journal.pntd.0003022Usage GuidelinesPlease refer to usage guidelines at http://researchonline.lshtm.ac.uk/policies.html or alterna-tively contact researchonline@lshtm.ac.uk.Available under license: http://creativecommons.org/licenses/by/2.5/ViewpointsDengue and the World Football Cup: A Matter of TimingChristovam Barcellos1*, Rachel Lowe21Health Communication and Information Institute, Fundac¸a˜o Oswaldo Cruz (ICICT/FIOCRUZ), Manguinhos, Rio de Janeiro, Brazil, 2 Institut Catala` de Cie`ncies del Clima(IC3), Barcelona, Catalonia, SpainThe possibility of a dengue feveroutbreak during the FIFA Football WorldCup raised controversies about the use ofhealth data and the impact of climate ondengue dynamics. One example of thisdebate is the article ‘‘Football fever couldbe a dose of dengue’’ recently published inNature by Simon Hay and its repercussionin media and scientific forums. The riskmap presented by Hay appears to be froma previously published global dengue riskassessment, but zoomed into the Brazilianterritory. It is important to distinguishbetween downscale and zoom. The envi-ronmental spatial covariates used to pro-duce the map may be relevant for theglobal perspective, but in Brazil, otherspatiotemporal variables influence trans-mission intensity and permanence. Forinstance, dengue vectors are well adaptedto urban and peri-urban environmentsand infest even dry regions. However,small, cold, and remote cities are virtuallypreserved from prolonged transmission.We provide a nationwide risk map,averaging June dengue incidence ratesfor 2001–2012. The areas along theAmazonian rivers and in the inner por-tions of southernmost states are actuallylow-risk areas, while elevated dengue riskis found in the central Brazilian plateau.During austral summer, high incidence isobserved in all central regions, while inwinter, transmission is restricted to narrowareas along the northern coast and centralregions. Among the cities where footballgames will take place, Porto Alegre,Curitiba, and Sa˜o Paulo are located inyear-round low-transmission areas. Dur-ing the winter, only Fortaleza, Natal,Recife, Salvador (along the northeastcoast), and Cuiaba´ remain in active, albeitlow, transmission areas. The differencebetween these maps relates to the consid-eration of seasonality, timing, and scale.Dengue and the World Cup: AMatter of TimingThere has been a growing interest indisease modelling in recent years. This hasbenefited from the computational devel-opment of mathematical formulations andthe increasing availability of environmen-tal and health data. We acknowledge therecent initiative in mapping the globaldistribution and magnitude of denguefever [1]. However, the application ofthese results to country-specific scenariosshould be handled with care, especiallywith reference to Brazil, in the context ofthe 2014 FIFA World Cup [2].The dengue risk map (http:\\go.nature.com/8g1io5), presented by Hay [2] appearsto be from a previously published globaldengue risk assessment, but zoomed into theBrazilian territory [1]. It is important todistinguish between downscale and zoom.The model in Bhatt et al. [1] was built usingprecipitation, temperature, vegetation/mois-ture, urbanisation, accessibility, and povertyas spatial covariates. These factors may berelevant for the global perspective, but inBrazil, other climatic and spatiotemporalvariables influence transmission intensity andpermanence. For instance, dengue vectors(Aedes aegypti and Aedes albopictus) are welladapted to urban and peri-urban environ-ments and infest even dry regions. However,small, cold, and remote cities are virtuallypreserved from prolonged transmission [3].Here we provide nationwide risk maps,averaging dengue incidence rates from 2001to 2012, for February (the peak of transmis-sion) and June (the start of the World Cup).The maps were produced by smoothingmean dengue incidence rates during Febru-ary and June, respectively, between 2001and 2012. Dengue data was obtained fromthe Notifiable Diseases Information System(SINAN), organised by the Brazilian Minis-try of Health and freely available via theHealth Information Department (DATA-SUS). All confirmed cases of dengue fever(DF) were considered in the analysis, from2001 to 2012. Incidence rates were calcu-lated for the 553 microregions in mainlandBrazil, and ordinary kriging was applied tospatially interpolate point values. The per-manent transmission area was calculated asthe proportion of years with reporteddengue cases above the high dengue riskthreshold, defined by the Ministry of Health(300 cases per 100,000 inhabitants) [3]. Thisprocedure allows the identification of citieswith suitable climatic and socio-demograph-ic conditions to sustain long-term transmis-sion and separates permanent transmissionfrom areas experiencing isolated outbreaks[3].The June dengue risk map differsconsiderably from that previously pub-lished [2]. For example, the areas alongthe Amazonian rivers and in the innerportions of southernmost states are actuallylow-risk areas, while the central Brazilianplateau is an elevated dengue risk area.There are notable differences betweenspatial incidence patterns in summer andwinter (Figure 1). During austral summer,high incidence is observed in all centralregions, while in winter, transmission isrestricted to narrow areas along thenorthern coast and central regions.Among the cities where football gameswill take place, Porto Alegre, Curitiba, andSa˜o Paulo are located in year-round low-transmission areas. During the winter,only Fortaleza, Natal, Recife, Salvador(along the northeast coast), and Cuiaba´remain in active, albeit low, transmissionareas. Other host cities, such as Rio deJaneiro, Manaus, Brası´lia, and Belo Hor-izonte, are within the permanent trans-Citation: Barcellos C, Lowe R (2014) Dengue and the World Football Cup: A Matter of Timing. PLoS Negl TropDis 8(7): e3022. doi:10.1371/journal.pntd.0003022Editor: Duane J. Gubler, Duke-NUS, SingaporePublished July 24, 2014Copyright:  2014 Barcellos, Lowe. This is an open-access article distributed under the terms of the CreativeCommons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium,provided the original author and source are credited.Funding: The dengue and climate research has received funding from the DENFREE project (grant agreementnu282378) and Climate and Health Observatory (CNPq process 552746/2011-8). This article is a contribution ofthe Brazilian National Institute of Science and Technology (INCT) for Climate Change funded by CNPq Processnumber 573797/2008-0. The funders had no role in study design, data collection and analysis, decision topublish, or preparation of the manuscript.Competing Interests: The authors have declared that no competing interests exist.* Email: xris@fiocruz.brPLOS Neglected Tropical Diseases | www.plosntds.org 1 July 2014 | Volume 8 | Issue 7 | e3022mission area but present lower risk duringthe World Cup season.The difference between the map pub-lished by Hay and those presented hererelates to the consideration of seasonality,timing, and scale.Brazilian health information is freelyavailable for a variety of health events.However, use of this data must be carefullyconsidered as it is produced within acomplex and unequal public health service.For instance, Hay [2] states that denguenotification data were not ‘‘enough’’ foranalysis in Curitiba and Porto Alegre in thesouthern region. This is due to the virtualabsence of dengue cases in these cities.Assigning state level registers to these citiesis unsuitable for incidence estimates.At present, all four dengue virus sero-types circulate in Brazil [4] and there isalready a large internal flux of travellersconnecting large cities in the country. Thearrival of a massive influx of tourists for theWorld Cup may produce two outcomes ofdengue transmission dynamics. If suscepti-ble individuals reach cities, even during anoutbreak, only a small fraction of infectedpeople may present symptoms, dependingon age, collective and individual immunitystatus, and virus serotype. Massad andWilder-Smith [5] calculated the risk ofinfection for travellers visiting an endemiccountry for one month as 0.01% and 0.4%during the low and high transmissionperiods, respectively. Considering the spe-cific climatic and demographic conditionsin which the World Cup will occur, only avery small fraction of cases are expectedamong visitors [6]. The lag between virusintrinsic and extrinsic reproduction canextend from two to three weeks [7]. Thisprocess may be longer during winter, whenthe FIFA World Cup will occur. Connect-ing the arrival of a susceptible population,exposure to the virus, and spread of thedisease is a matter of timing.Modelling tools to predict dengue riskin space and time have been developedfor Brazil, driven by climate and non-climate information [8,9]. A recentstudy produced a dengue early warningthree months ahead of the 2014 WorldCup [10], driven by seasonal climateforecasts and the epidemiological situa-tion at the time of forecast, with a riskmap and uncertainty estimates for the553 microregions of Brazil. The modelresults showed a low probability ofdengue outbreaks for cities located inthe south and central regions (Brası´lia,Cuiaba´, Curitiba, Porto Alegre, and Sa˜oPaulo), moderate risk in Rio de Janeiro,Belo Horizonte, Salvador, and Manaus,and a higher probability of exceeding300 cases per 100,000 inhabitants inFortaleza, Natal, and Recife. Therefore,efforts to reduce dengue incidence andseverity should be concentrated in thesecities.References1. Bhatt S, Gething PW, Brady OJ, Messina JP,Farlow AW, et al. (2013) The global distributionand burden of dengue. Nature 496: 504–507.2. Hay S (2013) Football fever could be a dose ofdengue. Nature 503: 439.3. Barcellos C, Lowe R (2014) Expansion of thedengue transmission area in Brazil: the role ofclimate and cities. Trop Med Int Health 19: 159–168.4. Villabona-Arenas CJ, de Oliveira JL, CapraCdS, Balarini K, Loureiro M, et al. (2014)Detection of four dengue serotypes suggests risein hyperendemicity in urban centers of Brazil.PLoS Negl Trop Dis 8: e2620. doi:10.1371/journal.pntd.00026205. Massad E, Wilder-Smith A (2009) Risk estimatesof dengue in travelers to dengue endemic areasusing mathematical models. J Travel Med 16:191–193.6. Massad E, Wilder-Smith A, Ximenes R, AmakuM, Lopez LF, et al. (2014) Risk of symptomaticdengue for foreign visitors to the 2014 FIFAWorld Cup in Brazil. Mem Inst Oswaldo Cruz109: 394–397.7. Chan M, Johansson MA (2012) The IncubationPeriods of Dengue Viruses. PLoS ONE 7:e50972. doi:10.1371/journal.pone.00509728. Lowe R, Bailey TC, Stephenson DB, GrahamRJ, Coelho CAS, et al. (2011) Spatio-temporalmodelling of climate-sensitive disease risk:Towards an early warning system for dengueinBrazil. Comput Geosci. 37: 371–381.9. Lowe R, Bailey TC, Stephenson DB, Jupp TE,Graham RJ, et al. (2013) The developmentof an early warning system for climate-sensitive disease risk with a focus on dengueepidemics in Southeast Brazil. Statist Med 32:864–883.10. Lowe R, Barcellos C, Coelho CA, Bailey TC,Coelho GE, et al. (2014) Dengue outlook forthe World Cup in Brazil: an early warningmodel framework driven by real-time seasonalclimate forecasts. Lancet Infect Dis. E-puba h e a d o f p r i n t . d o i : 1 0 . 1 0 1 6 / S 1 4 7 3 -3099(14)70781-9Figure 1. Average dengue incidence rates (per 100,000 inhabitants) for February (left) and June (right) 2001–2012.doi:10.1371/journal.pntd.0003022.g001PLOS Neglected Tropical Diseases | www.plosntds.org 2 July 2014 | Volume 8 | Issue 7 | e3022

Dengue and the world football cup: a matter of timing.

Institut Català de Ciències del Clima. Barcelona, Catalonia, Spain.Fundação Oswaldo Cruz. Instituto de Comunicação e Informação Científica e Tecnológica em Saúde. RIo de Janeiro, RJ, Brasil

Dengue and the world football cup: a matter of timing.

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