Red deer (Cervus elaphus) Did Not Play the Role of Maintenance Host for Bluetongue Virus in France: The Burden of Proof by Long-Term Wildlife Monitoring and Culicoides Snapshots

Sophie Rossi,Damien Vitour,Bruno Mathieu,Gina Zanella,Camille Ninio,Corinne Novella,Emmanuel Bréard,Eva Faure,Maryline Pellerin,Etienne Guillaumat,Stevan Mondoloni,Cyril Viarouge,Claire Garros,Stéphan Zientara,Agnès Ariston,Corinne Sailleau,Stéphane Barbier,Aurélie Barboiron,Thomas Balenghien,Laëtitia Gardès,Christophe Tholoniat,Jean Claude Delécolle ,P Gibert ,D Gauthier

doi:10.3390/v11100903

Abstract

Bluetongue virus (BTV) is a Culicoides-borne pathogen infecting both domestic and wild ruminants. In Europe, the Red Deer (Cervus elaphus) (RD) is considered a potential BTV reservoir, but persistent sylvatic cycle has not yet been demonstrated. In this paper, we explored the dynamics of BTV1 and BTV8 serotypes in the RD in France, and the potential role of that species in the re-emergence of BTV8 in livestock by 2015 (i.e., 5 years after the former last domestic cases). We performed 8 years of longitudinal monitoring (2008–2015) among 15 RD populations and 3065 individuals. We compared Culicoides communities and feeding habits within domestic and wild animal environments (51,380 samples). Culicoides diversity (>30 species) varied between them, but bridge-species able to feed on both wild and domestic hosts were abundant in both situations. Despite the presence of competent vectors in natural environments, BTV1 and BTV8 strains never spread in RD along the green corridors out of the domestic outbreak range. Decreasing antibody trends with no PCR results two years after the last domestic outbreak suggests that seropositive young RD were not recently infected but carried maternal antibodies. We conclude that RD did not play a role in spreading or maintaining BTV in France.

Highlights

Bluetongue virus (BTV) is a Culicoides-borne pathogen that may infect several ruminant species, including both domestic and wild animals [1,2]
This study highlights the interest of long-term wildlife surveillance and the appropriate storage of sera/organ banks at a national level, which requires a sound collaboration between national agencies, laboratories, researchers, biologists, farmers, and hunting organizations
The absence of RNA detection more than 1 year after the last domestic outbreak, and the decrease of seroprevalence and NA titers in all sampled RD populations over time, suggest that no persistent sylvatic cycle could settle after the fade out of BTV1 or BTV serotype 8 (BTV8) in livestock

Summary

Introduction

Bluetongue virus (BTV) is a Culicoides-borne pathogen that may infect several ruminant species, including both domestic and wild animals [1,2]. This raises the question of the possible maintenance of BTV in sylvatic cycle, which is well known in Northern American wildlife but not yet demonstrated in Europe [3,4]. The maintenance of sylvatic cycle requires: (i) Wild ruminants as amplificatory hosts, i.e., able to develop a sufficiently long and high viremia to infect Culicoides females; (ii) competent. Culicoides vector species able to bite them; and (iii) sufficient interactions between the infected wild ruminants and sylvatic-associated Culicoides vector species to ensure epidemiological cycles in natural environments. In Spain, the species composition seems more influenced by the climate

Results

Discussion

Conclusion