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      Epidemiology of Usutu Virus: The European Scenario

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          Abstract

          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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          Emergence of Usutu virus, an African Mosquito-Borne Flavivirus of the Japanese Encephalitis Virus Group, Central Europe

          During late summer 2001 in Austria, a series of deaths in several species of birds occurred, similar to the beginning of the West Nile virus (WNV) epidemic in the United States. We necropsied the dead birds and examined them by various methods; pathologic and immunohistologic investigations suggested a WNV infection. Subsequently, the virus was isolated, identified, partially sequenced, and subjected to phylogenetic analysis. The isolates exhibited 97% identity to Usutu virus (USUV), a mosquito-borne Flavivirus of the Japanese encephalitis virus group; USUV has never previously been observed outside Africa nor associated with fatal disease in animals or humans. If established in central Europe, this virus may have considerable effects on avian populations; whether USUV has the potential to cause severe human disease is unknown.
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            Usutu Virus, Italy, 1996

            Retrospective analysis of archived tissue samples from bird deaths in the Tuscany region of Italy in 1996 identified Usutu virus. Partial sequencing confirmed identity with the 2001 Vienna strain and provided evidence for a much earlier introduction of this virus into Europe than previously assumed.
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              European Surveillance for West Nile Virus in Mosquito Populations

              A wide range of arthropod-borne viruses threaten both human and animal health either through their presence in Europe or through risk of introduction. Prominent among these is West Nile virus (WNV), primarily an avian virus, which has caused multiple outbreaks associated with human and equine mortality. Endemic outbreaks of West Nile fever have been reported in Italy, Greece, France, Romania, Hungary, Russia and Spain, with further spread expected. Most outbreaks in Western Europe have been due to infection with WNV Lineage 1. In Eastern Europe WNV Lineage 2 has been responsible for human and bird mortality, particularly in Greece, which has experienced extensive outbreaks over three consecutive years. Italy has experienced co-circulation with both virus lineages. The ability to manage this threat in a cost-effective way is dependent on early detection. Targeted surveillance for pathogens within mosquito populations offers the ability to detect viruses prior to their emergence in livestock, equine species or human populations. In addition, it can establish a baseline of mosquito-borne virus activity and allow monitoring of change to this over time. Early detection offers the opportunity to raise disease awareness, initiate vector control and preventative vaccination, now available for horses, and encourage personal protection against mosquito bites. This would have major benefits through financial savings and reduction in equid morbidity/mortality. However, effective surveillance that predicts virus outbreaks is challenged by a range of factors including limited resources, variation in mosquito capture rates (too few or too many), difficulties in mosquito identification, often reliant on specialist entomologists, and the sensitive, rapid detection of viruses in mosquito pools. Surveillance for WNV and other arboviruses within mosquito populations varies between European countries in the extent and focus of the surveillance. This study reviews the current status of WNV in mosquito populations across Europe and how this is informing our understanding of virus epidemiology. Key findings such as detection of virus, presence of vector species and invasive mosquito species are summarized, and some of the difficulties encountered when applying a cost-effective surveillance programme are highlighted.
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                Author and article information

                Journal
                Pathogens
                Pathogens
                pathogens
                Pathogens
                MDPI
                2076-0817
                26 August 2020
                September 2020
                : 9
                : 9
                : 699
                Affiliations
                [1 ]Department of Virology, Croatian Institute of Public Health, 10000 Zagreb, Croatia; irena.tabain@ 123456hzjz.hr (I.T.); maja.bogdanic11@ 123456gmail.com (M.B.)
                [2 ]School of Medicine, University of Zagreb, 10000 Zagreb, Croatia; anna.mrzljak@ 123456gmail.com
                [3 ]Department for Virology, Scientific Veterinary Institute, 21000 Novi Sad, Serbia; tomy@ 123456niv.ns.ac.rs
                [4 ]Poultry Center, Croatian Veterinary Institute, 10000 Zagreb, Croatia; v_savic@ 123456veinst.hr
                [5 ]Department of Microbiology and Infectious Diseases with Clinic, Faculty of Veterinary Medicine, University of Zagreb, 10000 Zagreb, Croatia; ljubo.barbic@ 123456vef.hr (L.B.); vladimir.stevanovic@ 123456vef.hr (V.S.); ibenvin@ 123456vef.hr (I.B.)
                [6 ]Department of Epidemiology, Andrija Stampar Teaching Institute of Public Health, 10000 Zagreb, Croatia; ana.klobucar@ 123456stampar.hr
                [7 ]Department of Medicine, Merkur University Hospital, 10000 Zagreb, Croatia
                [8 ]Department of Epidemiology, Croatian Institute of Public Health, 10000 Zagreb, Croatia; maja.ilic@ 123456hzjz.hr
                [9 ]Department for Intensive Care Medicine and Neuroinfectology, University Hospital for Infectious Diseases “Dr Fran Mihaljevic”, 10000 Zagreb, Croatia; marijasantini.ms@ 123456gmail.com
                [10 ]Environmental Health Department, Croatian Institute of Public Health, 10000 Zagreb, Croatia; kcapak@ 123456hzjz.hr
                [11 ]OIE Reference Center for West Nile Disease, Istituto Zooprofilattico Sperimentale “G. Caporale”, 64100 Teramo, Italy; f.monaco@ 123456izs.it (F.M.); g.savini@ 123456izs.it (G.S.)
                [12 ]Laboratory for Diagnostics, Croatian Veterinary Institute, Regional Institute Split, 21000 Split, Croatia; e.listes.vzs@ 123456veinst.hr
                Author notes
                [* ]Correspondence: tatjana.vilibic-cavlek@ 123456hzjz.hr ; Tel.: +385-1-4863-238
                Author information
                https://orcid.org/0000-0002-1877-5547
                https://orcid.org/0000-0002-9164-3356
                https://orcid.org/0000-0003-0398-5346
                https://orcid.org/0000-0003-3464-6830
                https://orcid.org/0000-0001-6270-2305
                Article
                pathogens-09-00699
                10.3390/pathogens9090699
                7560012
                32858963
                02996c13-77e8-4ea8-a834-ea2aff84eecf
                © 2020 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 19 July 2020
                : 24 August 2020
                Categories
                Review

                usutu virus,epidemiology,europe,“one health”
                usutu virus, epidemiology, europe, “one health”

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