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2</a>a and b&#41;&#46; The worldwide distribution of <span class="elsevierStyleItalic">Aedes</span> raises fears that ZIKV infection can spread to other geographical locations where the disease is currently not present&#46; A similar situation has already occurred with other arboviruses transported by <span class="elsevierStyleItalic">Aedes</span>&#44; such as the case of the native transmission of the chikungunya and dengue viruses in Italy and France&#46;<a class="elsevierStyleCrossRefs" href="#bib0280"><span class="elsevierStyleSup">16&#44;17</span></a></p><elsevierMultimedia ident="fig0010"></elsevierMultimedia></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Risk of Zika virus disease during the Olympic Games</span><p id="par0020" class="elsevierStylePara elsevierViewall">From an epidemiological point of view&#44; it is well known that the congregation of individuals who attend multitudinous events puts thousands of international travelers at risk of acquiring infectious diseases&#44; with the subsequent possibility of importing the diseases to the travelers&#8217; places of origin&#44; where a competent vector might be present for transmitting the diseases&#46; Numerous studies have described infectious disease outbreaks following large human gatherings&#44; such as religious events &#40;annual pilgrimage to Mecca&#44; World Youth Day&#41;&#44; open-air festivals &#40;concerts&#44; carnivals&#41; and sporting events &#40;Olympics&#44; international soccer competitions&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0290"><span class="elsevierStyleSup">18</span></a> The possible explosive dissemination of the disease by ZIKV represented a public health challenge in terms of the preparation and surveillance for the Olympic and Paralympic Games&#44; which took place from August 5th to September 18 in Brazil&#46;</p><p id="par0025" class="elsevierStylePara elsevierViewall">Faced with this scenario&#44; a hundred physicians and scientists from various countries&#44; including Brazil&#44; issued an open letter in May 20&#44; 2016&#44; to Margaret Chan&#44; the Director-General of WHO&#44; to reconsider delaying or changing the location of the Olympic and Paralympic Games in Brazil&#44; due to the public health risk for athletes and the general public in terms of acquiring ZIKV&#46; After assessing the situation&#44; the WHO issued a press release on May 28&#44; 2016&#44; stating that &#8220;canceling or changing the location of the 2016 Olympics will not significantly alter the international spread of the Zika virus&#46;&#8221;<a class="elsevierStyleCrossRef" href="#bib0295"><span class="elsevierStyleSup">19</span></a> The evidence supporting this decision is presented below&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">The concern for the health of athletes and spectators who attend a sports event taking place in regions with communicable infections is not new&#46; A similar situation occurred for the risk of dengue for tourists and athletes who traveled to Brazil in 2014 for the World Cup&#46; For this sports event&#44; which was held between June and July 2014&#44; 400&#44;000 international visitors and more than 600&#44;000 Brazilian visitors were expected&#46;<a class="elsevierStyleCrossRef" href="#bib0300"><span class="elsevierStyleSup">20</span></a> A mathematical model was developed for this context&#44; in which the individual risk of dengue for tourists was estimated to be between 6<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">&#8722;5</span> and 4<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">&#8722;4</span>&#44; which represents an expected risk of infection among tourists of 3 to 59 cases of symptomatic dengue&#46;<a class="elsevierStyleCrossRef" href="#bib0305"><span class="elsevierStyleSup">21</span></a> Fortunately&#44; 2014 had an unusually low incidence of dengue in the cities where the soccer competitions were held&#46; Ultimately&#44; the Brazilian authorities documented only 3 cases of dengue among tourists&#46;<a class="elsevierStyleCrossRef" href="#bib0310"><span class="elsevierStyleSup">22</span></a></p><p id="par0035" class="elsevierStylePara elsevierViewall">Although the <span class="elsevierStyleItalic">Ae&#46; aegypti</span> mosquito is present year round&#44; the vector transmission ability is significantly reduced when the minimum temperature is below 22<span class="elsevierStyleHsp" style=""></span>&#176;C&#46;<a class="elsevierStyleCrossRefs" href="#bib0315"><span class="elsevierStyleSup">23&#44;24</span></a> In these conditions&#44; the extrinsic incubation period&#44; defined as the time during which the mosquito can transmit the disease&#44; is extended to more than 2 weeks&#46;<a class="elsevierStyleCrossRef" href="#bib0325"><span class="elsevierStyleSup">25</span></a> Minimum temperatures above 22<span class="elsevierStyleHsp" style=""></span>&#176;C are predicted only for the middle of November&#46; Therefore&#44; diseases transmitted by this vector are less common during winter months&#46;</p><p id="par0040" class="elsevierStylePara elsevierViewall">The <span class="elsevierStyleItalic">Ae&#46; aegypti</span> mosquito therefore has a seasonal distribution&#44; given that it is more abundant in the austral summer months &#40;January to February in Rio de Janeiro&#41; and less so in winter &#40;between July and August&#41;&#44; when temperatures are somewhat warmer &#40;between 19<span class="elsevierStyleHsp" style=""></span>&#176;C and 26<span class="elsevierStyleHsp" style=""></span>&#176;C&#41; and precipitation decreases significantly&#46; It has been estimated that the individual risk of being bitten by an <span class="elsevierStyleItalic">Ae&#46; aegypti</span> mosquito in Rio de Janeiro during the 3 weeks in which the Olympics were held was 3&#46;5<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">&#8722;2</span>&#46;<a class="elsevierStyleCrossRef" href="#bib0330"><span class="elsevierStyleSup">26</span></a> The individual risk of symptomatic dengue virus infection for tourists during this period was estimated at 5<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">&#8722;4</span>&#46;<a class="elsevierStyleCrossRef" href="#bib0335"><span class="elsevierStyleSup">27</span></a> Taking into account the arrival of between 350&#44;000 and 500&#44;000 tourists&#44; according to the mathematical models&#44; this would represent a total of 4 &#40;1&#8211;36&#41; cases of symptomatic dengue&#46; This estimate was performed assuming that the tourist population has a similar level of exposure as that of residents&#46; However&#44; it is very likely that visitors are more protected due to the greater use of barrier methods against mosquito bites &#40;repellents&#44; insect screens&#44; hotel air conditioning&#44; etc&#46;&#41;&#46; It was also predicted that tourists would limit their visits to areas where the Games were being held and to other eminently touristic areas of the city&#44; which would have better control of the vector density &#40;fumigation&#44; elimination of larval breeding sites&#44; etc&#46;&#41;&#44; and avoid peripheral areas of the city where the risk is greater&#46; The area more to the north of Rio&#44; where the incidence of dengue &#40;and that of ZIKV&#41; has been reported as historically higher&#44; was not the epicenter of the various Olympic events&#46;<a class="elsevierStyleCrossRef" href="#bib0340"><span class="elsevierStyleSup">28</span></a></p><p id="par0045" class="elsevierStylePara elsevierViewall">Estimates regarding ZIKV infection are more complicated&#44; because its actual incidence rate is unknown&#46; This is mainly due to the lack of available rapid diagnostic tests&#44; to the need for expensive and specialized laboratory resources&#44; to the presence of mild and nonspecific symptoms and&#44; more commonly&#44; to the complete lack of symptoms&#46; It is estimated that in 2015 there were between 500&#44;000 and 1&#44;500&#44;000 infections &#40;both symptomatic and asymptomatic&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0345"><span class="elsevierStyleSup">29</span></a> Based on this datum&#44; a number of authors have postulated that the risk of ZIKV infection in August would be between 9<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">&#8722;6</span> and 3<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>10<span class="elsevierStyleSup">&#8722;5</span>&#46;<a class="elsevierStyleCrossRef" href="#bib0305"><span class="elsevierStyleSup">21</span></a> This would represent a 15-fold lower risk of ZIKV infection than by dengue&#44; according to the proposed model&#46;<a class="elsevierStyleCrossRef" href="#bib0350"><span class="elsevierStyleSup">30</span></a> Entomological studies have suggested that <span class="elsevierStyleItalic">Ae&#46; aegypti</span> of Rio de Janeiro is less efficient in transmitting ZIKV than dengue&#46;<a class="elsevierStyleCrossRef" href="#bib0260"><span class="elsevierStyleSup">12</span></a> The previous risk assessments could therefore be overestimated&#46;</p><p id="par0050" class="elsevierStylePara elsevierViewall">In terms of the risk of increasing the number of cases of imported ZIKV&#44; there are models that have calculated that 508&#8211;1779 cases of ZIKV infections imported to Europe could occur throughout 2016&#44; of which 116&#8211;355 would be symptomatic&#46; The estimates indicate that the countries that would receive the highest number of cases of imported ZIKV would be France&#44; Portugal and Italy &#40;between 54 and 189 cases would be diagnosed in Spain&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0305"><span class="elsevierStyleSup">21</span></a> According to the latest update from the European Centre for Disease Prevention and Control &#40;August 2&#41;&#44; 1136 cases of imported ZIKV have been recorded in Europe&#46;<a class="elsevierStyleCrossRef" href="#bib0355"><span class="elsevierStyleSup">31</span></a> As of August 8&#44; 2016&#44; 219 cases of imported ZIKV have been reported in Spain&#46;<a class="elsevierStyleCrossRef" href="#bib0360"><span class="elsevierStyleSup">32</span></a></p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Risk of exporting ZIKV disease to Europe and Spain</span><p id="par0055" class="elsevierStylePara elsevierViewall">The explosive spread of the disease throughout Central and South America has raised fears that ZIKV could reach other more distant areas of the planet and continue its spread toward areas of the world that have a competent vector and an infection-naive population&#46; The first native cases of ZIKV infection in the United States of America have already been recorded&#44;<a class="elsevierStyleCrossRef" href="#bib0365"><span class="elsevierStyleSup">33</span></a> and the fear that attendees at the Olympics could export the disease to Europe is worth considering&#46;</p><p id="par0060" class="elsevierStylePara elsevierViewall">The arrival of summer in Europe&#44; when the <span class="elsevierStyleItalic">Aedes</span> mosquito population is at its peak and the vector&#39;s viral replication is at its most efficient&#44; could facilitate the onset of native cases&#44; as has already happened with dengue and chikungunya&#44; with minor disease outbreaks of native transmission in France or Italy&#46;<a class="elsevierStyleCrossRefs" href="#bib0280"><span class="elsevierStyleSup">16&#44;17</span></a></p><p id="par0065" class="elsevierStylePara elsevierViewall">The WHO classifies the risk of ZIKV transmission to Europe in summer as low to moderate&#46; The Portuguese island of Madeira&#44; Georgia and the southern part of the Russian Federation are areas of greater risk&#44; given that their territories have the primary vector of transmission &#40;<span class="elsevierStyleItalic">Ae&#46; aegypti</span>&#41;&#46; However&#44; the WHO also warns of the more moderate risk in 18 mainly Mediterranean countries where the secondary vector is present &#40;<span class="elsevierStyleItalic">Ae&#46; albopictus</span>&#41;&#44; including France&#44; Greece&#44; Italy&#44; Turkey and Spain&#46;<a class="elsevierStyleCrossRef" href="#bib0370"><span class="elsevierStyleSup">34</span></a></p><p id="par0070" class="elsevierStylePara elsevierViewall">We also need to mention sexual transmission as a potential source of contagion&#44; which increases the risk of exporting the disease to areas far from where the disease was acquired&#46; This transmission pathway is already perfectly documented&#44; both for a man infecting a woman&#44;<a class="elsevierStyleCrossRef" href="#bib0375"><span class="elsevierStyleSup">35</span></a> a man infecting another man<a class="elsevierStyleCrossRef" href="#bib0380"><span class="elsevierStyleSup">36</span></a> and a woman infecting a man&#46;<a class="elsevierStyleCrossRef" href="#bib0385"><span class="elsevierStyleSup">37</span></a> This scenario represents a new public health challenge&#46;</p><p id="par0075" class="elsevierStylePara elsevierViewall">Considering all this&#44; measures aimed at controlling the vector &#40;selective fumigation&#44; elimination of breeding sites&#44; etc&#46;&#41; should be reinforced to prevent individuals who might arrive in the viremic phase from starting the chain of native transmission in Spain&#46;</p><p id="par0080" class="elsevierStylePara elsevierViewall">In terms of the specific risk of ZIKV transmission from Brazil in 2016&#44; it is worth noting that the greatest risk of dissemination &#40;and thereby exporting the disease&#41; took place during this year&#39;s Carnival in Rio&#44; when ZIKV activity was at its maximum level&#46; In February 2016&#44; more than 1 million tourists visited Rio de Janeiro&#44; which represents approximately double the tourist population estimated for the Olympic Games&#46; During this time&#44; not only was ZIKV infection at its maximum incidence peak but also most of the carnival activities were open air&#44; increasing the tourists&#8217; exposure to the vector&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Other potential health risks during the Olympic Games</span><p id="par0085" class="elsevierStylePara elsevierViewall">We need to consider that arboviruses are not the only health risk for athletes and other travelers&#46; An analysis of diseases imported by travelers to Brazil performed by the Geosentinel network between 1997 and 2013 showed that skin disease was the most prevalent among returning travelers &#40;especially <span class="elsevierStyleItalic">larva migrans</span> and insect bites&#41;&#44; followed by gastrointestinal disease &#40;acute and subacute diarrhea&#41; and febrile syndrome &#40;mainly nonspecific febrile illness&#44; followed by dengue&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0390"><span class="elsevierStyleSup">38</span></a></p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Conclusions</span><p id="par0090" class="elsevierStylePara elsevierViewall">The best measure for preventing the acquisition of ZIKV is to provide accurate and reliable information on the disease&#44; emphasizing individual protection measures against mosquito bites&#46; We need to stress the need to use condoms to prevent this and other sexually transmitted diseases<a class="elsevierStyleCrossRef" href="#bib0395"><span class="elsevierStyleSup">39</span></a> and for pregnant women to follow the international recommendations to avoid traveling to these endemic areas&#46;<a class="elsevierStyleCrossRef" href="#bib0400"><span class="elsevierStyleSup">40</span></a> For their part&#44; the healthcare authorities of the endemic countries should increase efforts to minimize the presence of <span class="elsevierStyleItalic">Ae&#46; aegypti</span>&#44; such as selective fumigation and the elimination of breeding sites&#46;</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Conflicts of interest</span><p id="par0095" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflicts of interest&#46;</p></span></span>"
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        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">The recent outbreak of Zika virus infection in Brazil has aroused considerable media interest due to its association with neurological malformations in children born from mothers infected by the virus and to its association with Guillain&#8211;Barr&#233; syndrome in adults&#46; This relationship has led to the World Health Organisation declaring the current epidemic as a &#8220;<span class="elsevierStyleItalic">Public Health Emergency of International Concern</span>&#8221;&#46; Controversy also emerged on the advisability of delaying or changing the location of the Olympic and Paralympic Games&#44; which were held in August at various locations in Brazil&#46; In this article&#44; we review the available evidence on the risk of Zika and dengue virus infection in individuals who travel to endemic countries&#44; especially for multitudinous events&#46;</p></span>"
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        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">El brote reciente de infecci&#243;n por virus Zika en Brasil ha despertado gran inter&#233;s medi&#225;tico por su asociaci&#243;n a malformaciones neurol&#243;gicas en ni&#241;os nacidos de madres infectadas y a s&#237;ndrome de Guillain-Barr&#233; en el adulto&#46; Esta relaci&#243;n ha llevado a la Organizaci&#243;n Mundial de la Salud a declarar la actual epidemia como &#171;<span class="elsevierStyleItalic">Emergencia de Salud P&#250;blica de Inter&#233;s Internacional</span>&#187;&#46; Incluso surgi&#243; la pol&#233;mica sobre la conveniencia de retrasar o cambiar de ubicaci&#243;n los Juegos Ol&#237;mpicos y Paral&#237;mpicos que se celebraron en el pasado mes de agosto en distintas ubicaciones de Brasil&#46; En el presente art&#237;culo se revisa la evidencia disponible sobre el riesgo que existe de infecci&#243;n por virus Zika y Dengue en personas que viajen a pa&#237;ses end&#233;micos&#44; especialmente por eventos multitudinarios&#46;</p></span>"
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        "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Please cite this article as&#58; D&#237;az-Men&#233;ndez M&#44; Trigo E&#44; de la Calle-Prieto F&#44; Arsuaga M&#46; Infecci&#243;n por virus Zika durante los Juegos Ol&#237;mpicos de R&#237;o&#58; &#191;alarma o riesgo real&#63; Rev Clin Esp&#46; 2017&#59;217&#58;155&#8211;160&#46;</p>"
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                          "etal" => true
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                            2 => "A&#46; Iamarino"
                            3 => "O&#46; Faye"
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                            5 => "M&#46; Diallo"
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                      "doi" => "10.1371/journal.pntd.0002636"
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Review
Zika virus infection during the Olympic Games in Rio: A fear or an actual risk?
Infección por virus Zika durante los Juegos Olímpicos de Río: ¿alarma o riesgo real?
M. Díaz-Menéndez
Corresponding author
marta.diaz@salud.madrid.org

Corresponding author.
, E. Trigo, F. de la Calle-Prieto, M. Arsuaga
Unidad de Medicina Tropical y del Viajero, Hospital Universitario La Paz-Carlos III, Madrid, Spain

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