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      West Nile virus keeps on moving up in Europe

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          Abstract

          The 2020 arthropod vector season in Europe is approaching its end. Data from indicator-based surveillance on vector-borne diseases in 2020 will be reported to the European Centre for Disease Prevention and Control (ECDC) only in 2021, but we are already able to draw a preliminary picture from data obtained via event-based surveillance and weekly reporting of West Nile virus (WNV) infections. In 2020, WNV caused remarkable outbreaks in certain areas in Europe, such as Spain and the Netherlands. However, the largest outbreak of human WNV infections in European Union/European Economic Area (EU/EEA) countries was recorded in 2018, when 11 countries reported 1,548 locally acquired mosquito-borne infections [1]. The number of WNV infections in 2018 exceeded the cumulative number of all reported infections between 2010 and 2017, and the highest number of newly affected areas (n = 45) was reported [2]. Even though in 2019, the number of reported locally acquired human WNV infections dropped by 73% compared with 2018, the total numbers were still the second highest ever recorded. Most countries reported numbers of infections similar to before 2018, while Greece continued to report a high number of infections [1]. Since the start of the 2020 transmission season on 1 June, and as at 12 November, EU/EEA countries have reported 315 human cases of WNV infection with known place of infection through the European Surveillance System (TESSy): Greece (n = 143), Spain (n = 77), Italy (n = 66), Germany (n = 13), Romania (n = 6), the Netherlands (n = 6), Hungary (n = 3) and Bulgaria (n = 1) [3] (Figure). It is noteworthy that some countries reporting very low numbers of infections in 2020, ranging from none to six, had previously detected higher numbers of human WNV infections (e.g. Austria, Hungary, Serbia, Romania). Additionally, in other endemic countries reporting a large number of cases (i.e. Greece and Italy), the proportion of the more severe manifestation of the infection, West Nile neuroinvasive disease (WNND), was higher than the average of the previous 5 years. Figure Distribution of locally acquired human West Nile virus infections by affected areas and transmission seasons, EU/EEA countries and EU neighbouring countries, 2011–2020a (n = 3,876) ECDC: European Centre for Disease Prevention and Control; EEA: European Economic Area; EU: European Union. a Data last updated on 16 November 2020. Source: ECDC. Within the last decade, the geographical spread of a genetic WNV lineage 2 strain has been observed in Central Europe and in the Mediterranean region [4]. In Germany, this EU-dominant strain was first detected in 2018 in resident birds and horses. The first five locally acquired vector-borne human cases were reported in 2019 in the country. In the current issue of Eurosurveillance, Pietsch et al. report an outbreak of nine locally acquired cases of West Nile fever (WNF) and WNND in Leipzig, Germany, in August and September 2020 [5]. The authors hypothesise endemic seasonal circulation of WNV lineage 2 in the city of Leipzig in 2020 and also in the coming years; therefore, they suggest population’s and healthcare workers’ WNV awareness should be further increased as well as the surveillance in animals. WNV lineage 2 was also reported in bird and mosquito samples in the Netherlands, for the first time, at the end of August 2020 [6]. Hereafter, the first locally acquired human WNV infections were diagnosed, in the region of Utrecht, in September and October [3,7]. Since 2017, WNV lineage 2 has been spreading further west in the Mediterranean region, via the south of France, reaching Catalonia in north-eastern Spain, where it only caused sporadic cases in birds [8]. However, an unprecedented outbreak of WNV infections occurred in the southern Spanish provinces of Seville, Cádiz and Badajoz, between July and September 2020, comprising 77 infections diagnosed in humans and 137 documented outbreaks among equids [3]. A lineage 1 WNV strain was detected in both humans and animals, hence this outbreak has no epidemiological link to other concurrent WNV outbreaks in Europe [8]. Of note, Spain did not report locally acquired WNV infections in humans from 2017 to 2019. Albeit numbers of human WNV infections in 2020 were lower than in previous years, the geographic expansion of WNV has continued in Europe. The environmental and ecological drivers of WNV are complex and not known in detail, yet. Nevertheless, ambient temperature is known as one important determinant through its effect on mosquito reproduction rates and the extrinsic virus period in mosquitoes [9]. According to the monthly climate bulletins of the Copernicus Climate Change Service [10], positive surface air anomalies were recorded in the southern regions of the Iberian Peninsula from July to August, as well as in north-west Europe from August to October. The temporospatial overlap with the WNV outbreaks might be a mere coincidence, but in the long term, the environmental conditions tend to become more favourable for WNV establishment and seasonal circulation in many European regions [9]. The European spread of another flavivirus, closely related to WNV, the Usutu virus (USUV), may be regarded as an example [11,12]. The first cases of USUV-associated wild bird mortality events were described in Italy in 1996 and in Austria in 2001. Within two decades, USUV has spread all over Europe, except for the Baltic countries and Scandinavia, and in 2020, USUV emerged in the United Kingdom [13]. Although the ecology and epizootiology of USUV and WNV differ in several points (e.g. higher genetic diversity of USUV in Europe indicates various, recent introductions from Africa), the two viruses share mosquito vectors and avian hosts; therefore, the environmental and ecological conditions suitable for USUV may indicate the same for WNV (e.g. vector competences [14]). Most of the diagnosed human WNV infections in 2020 were reported from areas with virus activities already recorded in the previous years. This, together with genetic data, indicates overwintering and local circulation of the virus. Therefore, once established, the likelihood of maintenance and the risk of re-emergence of WNV infections in the affected European areas are high. The geographical spread after recent WNV lineage 2 introduction may be limited e.g. as it was seen in the eastern federal states of Germany, since 2018, but a massive geographical spread has been observed 4 to 5 years after its first emergence in Europe [4]. The annual fluctuations in WNV activity can be influenced by several factors. In the current issue of Eurosurveillance, Lourenço et al. have analysed West Nile virus epidemiology in Israel [15]. WNV infections caused by diverse strains have been diagnosed in the country in the past decade. In 2020, Israel reported 17 human cases as at 12 November. Authors adapted a suitability index to WNV and found that it confirmed the geotemporal estimation of transmission potential of WNV in the country. Several further studies have been and are investigating the ecological and environmental drivers of WNV [16,17]. Factors associated to national health systems, such as diagnostic awareness and vigilance, diagnostic capabilities and capacities, surveillance and reporting accuracies could also contribute to the annual variations of diagnosed and reported cases in a country. In 2020, the extraordinary and unprecedented burden on national health diagnostic systems caused by the coronavirus disease (COVID-19) pandemic might have had an influence on WNV surveillance in some countries. The maintenance of national preparedness for seasonal WNV outbreaks in the forthcoming years is particularly important in countries where – even if sporadic – cases have been reported previously, as well as in countries where the ecological conditions are suitable for WNV emergence and establishment. The risk and public health impact of human WNV infections in the different European countries clearly and significantly varies. In certain countries, surveillance of human WNV infections might be challenging or of low priority. The natural cycle of WNV involves avian hosts and mosquito vectors, while – besides humans – equids are also frequent, incidental hosts of the virus. Therefore, integrated animal-human WNV surveillance with systematic response and control measures e.g. for blood donation safety, vector control, awareness and information campaigns, might allow a more efficient utilisation of national resources and capacities. Animal WNV infections should be diagnosed timely and EU/EEA countries are encouraged to report infections via the Animal Disease Notification System of the European Commission. These data are visualised together with the TESSy data on human cases in ECDC’s weekly updated maps on WNV infections in Europe [1]. The joint animal-human surveillance data can provide more accurate information on WNV activity within the transmission season than solely data from human infections. Joint efforts on WNV surveillance and control could be one of the good examples for a One Health approach towards zoonotic diseases.

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          Most cited references13

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          Explosive spread of a neuroinvasive lineage 2 West Nile virus in Central Europe, 2008/2009.

          For the first time outside sub-Saharan Africa, a lineage 2 West Nile virus (WNV) emerged in Hungary in 2004. It caused sporadic cases of encephalitis in goshawks (Accipiter gentilis), other predatory birds, and in mammals. As a consequence, a surveillance program was initiated in Hungary and in Austria, which included virological, molecular, serological and epidemiological investigations in human beings, birds, horses, and mosquitoes. The virus strain became endemic to Hungary, however only sporadic cases of infections were observed between 2004 and 2007. Unexpectedly, explosive spread of the virus was noted in 2008, when neuroinvasive West Nile disease (WND) was diagnosed all over Hungary in dead goshawks and other birds of prey (n=25), in horses (n=12), and humans (n=22). At the same time this virus also spread to the eastern part of Austria, where it was detected in dead wild birds (n=8). In 2009, recurrent WND outbreaks were observed in Hungary and Austria, in wild birds, horses, and humans in the same areas. Virus isolates of both years exhibited closest genetic relationship to the lineage 2 WNV strain which emerged in 2004. As we know today, the explosive spread of the lineage 2 WNV in 2008 described here remained not restricted to Hungary and Austria, but this virus dispersed further to the south to various Balkan states and reached northern Greece, where it caused the devastating neuroinvasive WND outbreak in humans in 2010. Copyright © 2013 Elsevier B.V. All rights reserved.
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            Usutu virus: A new threat?

            Usutu virus (USUV) is an emerging arbovirus that was first isolated in South Africa in 1959. This Flavivirus is maintained in the environment through a typical enzootic cycle involving mosquitoes and birds. USUV has spread to a large part of the European continent over the two decades mainly leading to substantial avian mortalities with a significant recrudescence of bird infections recorded throughout Europe within the few last years. USUV infection in humans is considered to be most often asymptomatic or to cause mild clinical signs. Nonetheless, a few cases of neurological complications such as encephalitis or meningoencephalitis have been reported. USUV and West Nile virus (WNV) share many features, like a close phylogenetic relatedness and a similar ecology, with co-circulation frequently observed in nature. However, USUV has been much less studied and in-depth comparisons of the biology of these viruses are yet rare. In this review, we discuss the main body of knowledge regarding USUV and compare it with the literature on WNV, addressing in particular virological and clinical aspects, and pointing data gaps.
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              Epidemiology of Usutu Virus: The European Scenario

              Usutu virus (USUV) is an emerging arbovirus isolated in 1959 (Usutu River, Swaziland). Previously restricted to sub-Saharan Africa, the virus was introduced in Europe in 1996. While the USUV has received little attention in Africa, the virus emergence has prompted numerous studies with robust epidemiological surveillance programs in Europe. The natural transmission cycle of USUV involves mosquitoes (vectors) and birds (amplifying hosts) with humans and other mammals considered incidental (“dead-end”) hosts. In Africa, the virus was isolated in mosquitoes, rodents and birds and serologically detected in horses and dogs. In Europe, USUV was detected in bats, whereas antibodies were found in different animal species (horses, dogs, squirrels, wild boar, deer and lizards). While bird mortalities were not reported in Africa, in Europe USUV was shown to be highly pathogenic for several bird species, especially blackbirds (Turdus merula) and great gray owls (Strix nebulosa). Furthermore, neurotropism of USUV for humans was reported for the first time in both immunocompromised and immunocompetent patients. Epizootics and genetic diversity of USUV in different bird species as well as detection of the virus in mosquitoes suggest repeated USUV introductions into Europe with endemization in some countries. The zoonotic potential of USUV has been reported in a growing number of human cases. Clinical cases of neuroinvasive disease and USUV fever, as well as seroconversion in blood donors were reported in Europe since 2009. While most USUV strains detected in humans, birds and mosquitoes belong to European USUV lineages, several reports indicate the presence of African lineages as well. Since spreading trends of USUV are likely to continue, continuous multidisciplinary interventions (“One Health” concept) should be conducted for monitoring and prevention of this emerging arboviral infection.
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                Author and article information

                Journal
                Euro Surveill
                Euro Surveill
                eurosurveillance
                Eurosurveillance
                European Centre for Disease Prevention and Control (ECDC)
                1025-496X
                1560-7917
                19 November 2020
                : 25
                : 46
                : 2001938
                Affiliations
                [1 ]European Centre for Disease Prevention and Control (ECDC), Stockholm, Sweden
                Author notes

                Correspondence: Tamás Bakonyi ( Tamas.Bakonyi@ 123456ecdc.europa.eu )

                Article
                2001938 2001938
                10.2807/1560-7917.ES.2020.25.46.2001938
                7678036
                33213684
                3070f3de-eda5-46f4-81b4-9b18b808bfe7
                This article is copyright of the authors or their affiliated institutions, 2020.

                This is an open-access article distributed under the terms of the Creative Commons Attribution (CC BY 4.0) Licence. You may share and adapt the material, but must give appropriate credit to the source, provide a link to the licence, and indicate if changes were made.

                History
                : 13 November 2020
                : 18 November 2020
                Categories
                Editorial
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                europe,west nile fever,west nile virus,climate change,outbreaks,surveillance,travel,epidemiology

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