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      The mosquitoes of Armenia: review of knowledge and results of a field survey with first report of Aedes albopictus Translated title: Les moustiques d’Arménie : synthèse des connaissances et résultats d’une étude de terrain avec une première mention pour Aedes albopictus

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          Abstract

          Background: In 2016, a field study was implemented in all Armenian provinces in order to update knowledge on the presence and distribution of both native and invasive mosquito species. Larvae and adult mosquitoes were sampled and identified on the basis of their morphology. Supplementary field surveys were performed in 2017–2018. Results: Between June 20 and July 12, 2016, 117 localities were visited. A total number of 197 sampling units were checked, of which 143 (73%) were positive for mosquitoes (with 1–6 species per sampling unit). A total number of 4157 mosquito specimens were identified to species or species complex level. Ten species represent first records for Armenia: Aedes albopictus, Ae. annulipes, Ae. cataphylla, Ae. cinereus/geminus (probably Ae. cinereus) , Ae. flavescens, Anopheles plumbeus, Coquillettidia richiardii, Culex martinii, Cx. torrentium and Culiseta subochrea. The invasive species Ae. albopictus was recorded in a single locality (Bagratashen) at the border point with Georgia, along the main road Tbilisi-Yerevan. This species was further recorded in 2017 and 2018, demonstrating its establishment and spread in north Armenia. These surveys confirm the presence of vectors of malaria parasites (in particular An. sacharovi) and West Nile virus ( Cx. pipiens). Conclusion: The knowledge of the Armenian mosquito fauna is extended to a list of 28 species. The record of Aedes albopictus, an important potential vector of many arboviruses, has important implications for public health.

          Translated abstract

          Contexte : En 2016, nous avons réalisé une étude sur le terrain dans toutes les provinces du pays dans le but d’actualiser la présence et la distribution des espèces de moustiques aussi bien natives qu’invasives. Les moustiques récoltés aux stades larvaires et adultes ont été identifiés sur des critères morphologiques. Des suivis additionnels ont été réalisés en 2017 et 2018. Résultats : Entre le 20 juin et le 12 juillet 2016, 117 localités ont été visitées. Au total, 197 unités de collecte ont été prospectées dont 143 (73%) se sont révélées positives pour les moustiques (avec de 1 à 6 espèces par unité de collecte). Au total, 4157 spécimens ont été identifiés au niveau de l’espèce ou du complexe d’espèces. Dix espèces ont été observées pour la première fois en Arménie : Aedes albopictus, Ae. annulipes, Ae. cataphylla, Ae. cinereus/geminus (probablement Ae. cinereus) , Ae. flavescens, Anopheles plumbeus, Coquillettidia richiardii, Culex martinii, Cx. torrentium et Culiseta subochrea. L’espèce invasive Ae. albopictus a été observée dans une seule localité (Bagratashen) à la frontière avec la Géorgie, sur l’axe routier principal Tbilisi-Yerevan. Cette espèce a également été observée en 2017 et en 2018, faisant la preuve de son installation et de sa diffusion dans le nord de l’Arménie. Ces suivis confirment la présence des vecteurs de Plasmodium humains (en particulier An. sacharovi) et du virus West Nile ( Cx. pipiens). Conclusion : La connaissance de la faune culicidienne d’Arménie progresse, avec une liste actualisée à 28 espèces. L’observation d’ Aedes albopictus, un important vecteur potentiel de nombreux arbovirus, a d’importantes implications en termes de santé publique.

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          Most cited references 26

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          Spread of the Invasive Mosquitoes Aedes aegypti and Aedes albopictus in the Black Sea Region Increases Risk of Chikungunya, Dengue, and Zika Outbreaks in Europe

          The yellow fever and dengue mosquito Aedes aegypti previously flourished around the Mediterranean and Black Sea for decades until the 1950s, and was responsible of large outbreaks of both yellow fever and dengue [1]. The first well-described large dengue outbreak in Greece in 1927–28 caused more than 1 million cases (90% of the population in Athens) with 1000–1500 fatalities. The disappearance of Ae. aegypti from the European continent in Mediterranean, Black Sea, and Macaronesian biogeographical regions [2] is not well understood and its return in these regions raises concerns about a possible resurgence of the pathogens that can be transmitted by this vector species. Besides, the tiger mosquito Aedes albopictus is extending its distribution range worldwide, and it has already invaded large parts of the Mediterranean [1]. Dengue and chikungunya becoming endemic in Europe? Since 2010, sporadic cases of locally acquired dengue have been notified in Europe and an outbreak occurred on Madeira Island between the week 39 of 2012 and the week 9 of 2013. Important drivers of these events are viraemic travellers and the invasion of both vector mosquito species Ae. aegypti and Ae. albopictus [1]. Recently, new autochthonous dengue cases were reported in southern France in 2014 [3,4] and 2015 [5], demonstrating the vulnerability of Europe to dengue. Therefore it is crucial to extend and strengthen surveillance of the invasive Aedes mosquitoes and to address the need for the rapid suppression if not elimination of newly introduced Ae. aegypti populations in the European region. This is of particular importance in southern Europe and the Caucasus, where Ae. aegypti was historically present. Recently the European Centre for Disease Prevention and Control (ECDC) and the European Food Safety Agency (EFSA) have initiated the VectorNet scheme (as an extension of Vbornet scheme), a network that aims to support these agencies in their preparedness for vector-borne diseases in the framework of the One-Health concept. The network, among others, gathers distribution data of major arthropod vectors. Information collected from the Black Sea region has already revealed the presence of Aedes albopictus in western Turkey (Edirne province, bordering Greece), Bulgaria, Romania, southern Russia (Sochi region) and Abkhazia, as well as the occurrence of Ae. aegypti in these two last territories [1, 6]. In order to complete our knowledge on the geographical spread of these species, we have performed field work in September 2015 to collect data on the distribution of invasive Aedes mosquitoes in Georgia and north-eastern Turkey. Significant findings of these studies have been (1) the presence of both Ae. aegypti and Ae. albopictus over extended areas of Georgia including Ae. aegypti in the capital city Tbilisi, and (2) the spread of both species into north-eastern Turkey (Fig 1). Adult populations of these two invasive mosquitoes showed being anthropophagic and were found at several locations (e.g. Batumi and coastal Black Sea localities). Immature mosquito aquatic stages were found in particular in used tyres stored in outdoor conditions. Specimens were identified by morphology and some confirmed by molecular methods. These original observations are suggestive of a high probability of further spread of both invasive mosquito species in particular to ports of the Black Sea via ships and ferries, and via ground vehicles to places frequented by tourists and into major cities of Turkey including Istanbul. This might be the presages of re-colonisation of Mediterranean Europe by Ae. aegypti. 10.1371/journal.pntd.0004664.g001 Fig 1 Current known distribution of Aedes aegypti and Aedes albopictus in the Black Sea region. Presence of the mosquito species is shown at province/district level (except for Russia, where the colonised area is much undersized). Light colours: known distribution up to August 2015; Dark colours: surveillance results, September 2015; Yellow: presence of Aedes aegypti, the yellow fever mosquito, only; blue: presence of Aedes albopictus, the tiger mosquito, only; red, presence of both Ae. aegypti and Ae. albopictus. AM: Armenia; AZ: Azerbaijan; BG: Bulgaria; GE: Georgia; GR: Greece; IQ: Iraq; IR: Iran; RO: Romania; RU: Russia; SY: Syria; TR: Turkey; UA: Ukraine. Currently, infectious diseases caused by viruses transmitted by both Ae. aegypti and Ae. albopictus are a growing global health concern. Dengue has shown a 30-fold increase in global incidence during the past 50 years, affecting more than 100 countries throughout tropical and subtropical regions of the world [7]. Chikungunya was restricted to limited parts of Africa and Asia until 2005, when it spread for the first time to territories of the Indian Ocean, but is now occurring globally [8]. Also Zika virus has recently become a global player, after its emerging in the Pacific [9], and now in the Americas [10]. In a number of western European countries [1] preparedness plans including surveillance of invasive mosquito vectors, of which results are gathered quarterly on VectorNet maps [11], and in some cases regional or national integrated plans combining surveillance and control of both vectors and diseases are implemented or under development (e.g. France, Italy, Belgium, Switzerland). Surveillance of invasive vectors (presence, spread, activity, and abundance) and detection of dengue and chikungunya cases (both introduced and autochthonous) aim at collecting data to estimate the risk level. Furthermore, there are also prevention plans in place that categorise stakeholders, define information flows, and list measures that may be activated according to the faced risk level. These might include application of focal vector control measures around disease cases and in areas where a competent vector is established and active, and complementary measures such as informing the public about mosquito bite prevention. Such integrated plans support preparedness and allow rapid implementation of adapted responses. It is now crucial to rapidly define such plans in all countries where Ae. aegypti or Ae. albopictus are established. Local physicians’ capacities to rapidly identify and notify these arboviral infections should be enhanced. International collaboration, in particular around the Black Sea, is crucial in order to support local capacities and boost Europe’s preparedness, which is essential for planning adequate and efficient measures in both pre-emptive situations as well as in outbreak response (Box 1). WHO member states already agreed on an international strategy for surveillance and control of invasive mosquito vectors and re-emerging vector-borne diseases [12]. Box 1. Improve preparedness for dengue, chikungunya, and Zika infection in Europe. Public health authorities, physicians, and scientists should familiarise themselves with dengue, chikungunya, and Zika infections and prepare appropriately. As long as no dengue/chikungunya/Zika-specific prophylaxis or therapeutics are available, sustainable vector management is the only currently available approach for prevention and control. ECDC guidelines for the surveillance of mosquito vectors [13,14], can be applied to guide mosquito surveillance plans Integrated surveillance and control programmes should be generalised, at least in the Mediterranean and the Black Sea regions. Eliminating Aedes aegypti from Europe? It has been observed that the elimination of an invasive mosquito species such as Ae. albopictus is extremely difficult if not impossible [15,16]. Although elimination could be achieved during the last century at some places in Europe and the Americas for Ae. aegypti [1,17], recent eradication plans have failed in most cases (e.g. USA) [18,19]. In Europe, Ae. aegypti was successfully eliminated following its introduction into the Netherlands [20], but it is doubtful that the species would have managed to successfully overwinter under the local climatic conditions anyway. This is in contrast however to the situation in the Portuguese Autonomous Region of Madeira, where Ae. aegypti maintains its presence, with some signs of expansion throughout the Island of Madeira despite active control campaigns implemented in particular during the large dengue outbreak in 2012–13 [21]. Major challenges include the difficulties in implementing control measures on privately owned land, and the limited effectiveness of classical control methods [22]. Thus, novel methods are needed to complete the panel of measures for sustainable integrated vector management. At least, control measures aiming at slowing down the rate of mosquito spread and/or suppress the mosquito population during periods of elevated risk of pathogen transmission should be implemented rapidly. Otherwise, assuming that pathogens are imported via travellers, outbreaks of dengue or chikungunya might become more frequent and Zika could emerge in Europe.
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            Host preferences in host-seeking and blood-fed mosquitoes in Switzerland.

            The avian zoonotic agent for West Nile virus (WNV) can cause neuroinvasive disease in horses and humans and is expanding its range in Europe. Analyses of the risk for transmission to these hosts in non-endemic areas are necessary. Host preferences of mosquitoes (Diptera: Culicidae), the main vectors of WNV, were determined in Switzerland using animal-baited trap (horse, chickens) experiments at a natural and a periurban site. This was undertaken on four occasions during May-September 2014. In addition, the hosts of 505 blood-fed mosquitoes collected in a zoo and in the field were determined. Mosquito data obtained in the animal bait experiments were corrected for host weight and body surface area and by Kleiber's scaling factor. Collections of 11-14 different mosquito species were achieved with these approaches. Statistically significant host preferences were identified in three species in both approaches. The other species showed opportunistic feeding behaviours to varying extents. Specifically, the invasive species Hulecoeteomyia japonica (= Aedes japonicus) was identified for the first time as feeding on avians in nature. Abundance data, spatiotemporal activity and laboratory vector competence for WNV suggested that, in addition to the main WNV vector Culex pipiens, H. japonica and Aedimorphus vexans (= Aedes vexans) are the most likely candidate bridge vectors for WNV transmission in Switzerland.
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              Malaria in the WHO European Region (1971-1999).

              The number of autochthonous reported cases of malaria fell from 90 506 to 37 170 between 1996 and 1999 in the WHO European Region. There has been, however, an eight-fold increase in imported cases since the 1970s: 1500 cases were reported in 1972, 13 000 cases in 1999. France, Germany, Italy, and the United Kingdom are the west European countries with the largest numbers of cases.
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                Author and article information

                Journal
                Parasite
                Parasite
                parasite
                Parasite
                EDP Sciences
                1252-607X
                1776-1042
                2020
                08 June 2020
                : 27
                : ( publisher-idID: parasite/2020/01 )
                Affiliations
                [1 ] National Center of Disease Control and Prevention, Ministry of Health 25 Heratsi str. Yerevan 0025 Republic of Armenia
                [2 ] Francis Schaffner Consultancy Lörracherstrasse 50 4125 Riehen Switzerland
                [3 ] National Centre for Vector Entomology, Institute of Parasitology, Vetsuisse Faculty, University of Zurich Winterthurerstrasse 266a 8057 Zürich Switzerland
                [4 ] MIVEGEC Unit, IRD, CNRS, University of Montpellier 911, avenue Agropolis BP 64501 34394 Montpellier cedex 5 France
                Author notes
                [* ]Corresponding author: vincent.robert@ 123456ird.fr
                Article
                parasite190162 10.1051/parasite/2020039
                10.1051/parasite/2020039
                7278218
                32508303
                © L. Paronyan et al., published by EDP Sciences, 2020

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                Page count
                Figures: 3, Tables: 4, Equations: 0, References: 31, Pages: 10
                Categories
                Research Article

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