TY - JOUR

T1 - “Frozen evolution” of an RNA virus suggests accidental release as a potential cause of arbovirus re-emergence

AU - Pascall, David J.

AU - Nomikou, Kyriaki

AU - Bréard, Emmanuel

AU - Zientara, Stephan

AU - da Silva Filipe, Ana

AU - Hoffmann, Bernd

AU - Jacquot, Maude

AU - Singer, Joshua B.

AU - de Clercq, Kris

AU - Bøtner, Anette

AU - Sailleau, Corinne

AU - Viarouge, Cyril

AU - Batten, Carrie

AU - Puggioni, Giantonella

AU - Ligios, Ciriaco

AU - Savini, Giovanni

AU - van Rijn, Piet A.

AU - Mertens, Peter P.C.

AU - Biek, Roman

AU - Palmarini, Massimo

PY - 2020

Y1 - 2020

N2 - The mechanisms underlying virus emergence are rarely well understood, making the appearance of outbreaks largely unpredictable. Bluetongue virus serotype 8 (BTV-8), an arthropod-borne virus of ruminants, emerged in livestock in northern Europe in 2006, spreading to most European countries by 2009 and causing losses of billions of euros. Although the outbreak was successfully controlled through vaccination by early 2010, puzzlingly, a closely related BTV-8 strain re-emerged in France in 2015, triggering a second outbreak that is still ongoing. The origin of this virus and the mechanisms underlying its re-emergence are unknown. Here, we performed phylogenetic analyses of 164 whole BTV-8 genomes sampled throughout the two outbreaks. We demonstrate consistent clock-like virus evolution during both epizootics but found negligible evolutionary change between them. We estimate that the ancestor of the second outbreak dates from the height of the first outbreak in 2008. This implies that the virus had not been replicating for multiple years prior to its re-emergence in 2015. Given the absence of any known natural mechanism that could explain BTV-8 persistence over this long period without replication, we hypothesise that the second outbreak could have been initiated by accidental exposure of livestock to frozen material contaminated with virus from approximately 2008. Our work highlights new targets for pathogen surveillance programmes in livestock and illustrates the power of genomic epidemiology to identify pathways of infectious disease emergence.

AB - The mechanisms underlying virus emergence are rarely well understood, making the appearance of outbreaks largely unpredictable. Bluetongue virus serotype 8 (BTV-8), an arthropod-borne virus of ruminants, emerged in livestock in northern Europe in 2006, spreading to most European countries by 2009 and causing losses of billions of euros. Although the outbreak was successfully controlled through vaccination by early 2010, puzzlingly, a closely related BTV-8 strain re-emerged in France in 2015, triggering a second outbreak that is still ongoing. The origin of this virus and the mechanisms underlying its re-emergence are unknown. Here, we performed phylogenetic analyses of 164 whole BTV-8 genomes sampled throughout the two outbreaks. We demonstrate consistent clock-like virus evolution during both epizootics but found negligible evolutionary change between them. We estimate that the ancestor of the second outbreak dates from the height of the first outbreak in 2008. This implies that the virus had not been replicating for multiple years prior to its re-emergence in 2015. Given the absence of any known natural mechanism that could explain BTV-8 persistence over this long period without replication, we hypothesise that the second outbreak could have been initiated by accidental exposure of livestock to frozen material contaminated with virus from approximately 2008. Our work highlights new targets for pathogen surveillance programmes in livestock and illustrates the power of genomic epidemiology to identify pathways of infectious disease emergence.

U2 - 10.1371/journal.pbio.3000673

DO - 10.1371/journal.pbio.3000673

M3 - Journal article

C2 - 32343693

AN - SCOPUS:85084107182

VL - 18

JO - PLoS Biology

JF - PLoS Biology

SN - 1544-9173

IS - 4

M1 - e3000673

ER -