Exposure of Wild Ungulates to the Usutu and Tick-Borne Encephalitis Viruses in France in 2009–2014: Evidence of Undetected Flavivirus Circulation a Decade Ago

Abstract

Flaviviruses have become increasingly important pathogens in Europe over the past few decades. A better understanding of the spatiotemporal distribution of flaviviruses in France is needed to better define risk areas and to gain knowledge of the dynamics of virus transmission cycles. Serum samples from 1014 wild boar and 758 roe deer from 16 departments (administrative units) in France collected from 2009 to 2014 were screened for flavivirus antibodies using a competitive ELISA (cELISA) technique. Serum samples found to be positive or doubtful by cELISA were then tested for antibodies directed against West Nile virus (WNV), Usutu virus (USUV), Bagaza virus (BAGV), and tick-borne encephalitis/Louping ill viruses (TBEV/LIV) by microsphere immunoassays (except BAGV) and micro-neutralization tests. USUV antibodies were detected only in southeastern and southwestern areas. TBEV/LIV antibodies were detected in serum samples from eastern, southwestern and northern departments. The results indicate continuous circulation of USUV in southern France from 2009 to 2014, which was unnoticed by the French monitoring system for bird mortality. The findings also confirm wider distribution of TBEV in the eastern part of the country than of human clinical cases. However, further studies are needed to determine the tick-borne flavivirus responsible for the seroconversion in southwestern and northern France.

West Nile Virus and Related Flavivirus in European Wild Boar (Sus scrofa), Latium Region, Italy: A Retrospective Study

“…Comparing to the prevalence found in other European countries, the values obtained in the wild boar in the present study are higher than those reported in the Czech Republic (4.1% ) [17], similar to that reported in France in 2009-2014 (5.6% for Flavivirus and 3.4% for USUV) [26][27][28][29][30][31][32][33][34], but are lower than those reported in Spain, with a mean prevalence of 12.6% but with a significantly higher seroprevalence (27%) in wetland habitats during 2006-2010 [19], and in Serbia by [34] (17.6% WNV prevalence). In this study, only four wild boar sera showed USUV specificity.…”

“…The presence of antibodies against WNV and closely related Flaviviruses, like USUV, was analyzed using a commercial competitive enzyme-linked-immunosorbent assay (ELISA ID Screen West Nile Competition Multi-Species (Innovative Diagnostics, Montpelier, France),) for detection of West Nile virus antibodies against the pr-E and pr-M envelope proteins containing an epitope common to all Flaviviruses according to the manufacturer's protocol [24][25][26]. This Elisa test has a high cross-reactivity, thus it is suitable for the detection of a wide range of flaviviruses, although it has been designed for the diagnosis of WNV infection.…”

Epidemiology of Usutu Virus: The European Scenario

“…These data reported, for the first time, detection of USUV in mosquitoes that concurrently accompanied the emergence of USUV in blackbirds and a human case during the period 2015–2016 [ 44 ]. A serological study conducted among wild ungulates (2009–2014) indicated the continuous circulation of USUV in southern France with seropositivity of 8.0% in wild boar and 1.0% in roe deer [ 26 ]. In addition, a serological survey conducted in 2009–2019 found low titers of USUV neutralizing antibodies in sentinel wild birds (magpie; Pica pica ) in the Camargue area [ 82 ].…”

“…USUV RNA was also found in bats ( Pipistrellus pipistrellus ) in Germany and Belgium [ 19 , 20 ]. Moreover, USUV antibodies were sporadically detected in horses [ 21 , 22 , 23 ], dogs [ 24 ], squirrels [ 25 ], wild boar, roe deer [ 26 ] and lizards [ 27 ] ( Figure 1 ), expanding the USUV host range ( Figure 1 ), however these species are considered incidental hosts.…”

A Duplex Quantitative Real-Time Reverse Transcription-PCR for Simultaneous Detection and Differentiation of Flaviviruses of the Japanese Encephalitis and Ntaya Serocomplexes in Birds

“…The recent emergence of different flaviviruses in wide regions of the world makes co-circulation of these pathogens in same geographic areas more likely (12,13,39). Furthermore, there is a range of flavivirus species sharing vectors and hosts, producing similar disease pattern in susceptible animals.…”