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.

Laure Bournez,Elsa Jourdain,Mathieu Sarasa,Sandrine A Lacour,Sara Moutailler,Gérald Umhang,Sylvie Lecollinet,Francisco Llorente,Jean-Marc Boucher,Eva Faure,Cécile Beck,Franck Boué,Miguel A Jiménez-Clavero

doi:10.3390/v12010010

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.

Highlights

The importance of the Flavivirus genus in terms of public and animal health has increased in Europe over the last few decades [1,2,3]
We considered a serum sample to be i) “flavivirus-negative” when the result of the pan-flavivirus competitive ELISA (cELISA) was negative or was doubtful and negative in micro-neutralization tests (MNTs) or microsphere immunoassays (MIAs); or ii) “flavivirus-positive” when flavivirus antibodies were detected by the pan-flavivirus cELISA
As MNTs and MIAs gave complementary and specific results and identified the same viruses, we considered that a serum sample was positive for a specific virus (i.e., Usutu virus (USUV), tick-borne encephalitis virus (TBEV), Louping ill virus (LIV), West Nile virus (WNV)- or Bagaza virus (BAGV)-positive) when antibodies towards this virus were detected by at least one of the methods, MNTs or MIAs, given the conditions described above

Summary

Introduction

The importance of the Flavivirus genus (family Flaviviridae) in terms of public and animal health has increased in Europe over the last few decades [1,2,3]. Many of these viruses, such as West Nile virus (WNV) or tick-borne encephalitis virus (TBEV), are major human pathogens. In nature, these viruses are maintained in an enzootic cycle involving ornithophilic mosquitoes (WNV, Usutu virus, and Bagaza virus) or ticks (TBEV and Louping ill virus) as competent vectors, and birds or small mammals as main reservoir hosts.

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