Assessment of Influenza D Virus in Domestic Pigs and Wild Boars in France: Apparent Limited Spread within Swine Populations Despite Serological Evidence of Breeding Sow Exposure

Abstract

In order to assess influenza D virus (IDV) infections in swine in France, reference reagents were produced in specific pathogen free pigs to ensure serological and virological analyses. Hemagglutination inhibition (HI) assays were carried out on 2090 domestic pig sera collected in 2012–2018 in 102 farms. Only 31 sera from breeding sows sampled in 2014–2015 in six farrow-to-finish herds with respiratory disorders contained IDV-specific antibodies. In two of them, within-herd percentage of positive samples (73.3% and 13.3%, respectively) and HI titers (20–160) suggested IDV infections, but virus persistence was not confirmed following new sampling in 2017. All growing pigs tested seronegative, whatever their age and the sampling year. Moreover, PB1-gene RT-qPCR performed on 452 nasal swabs taken in 2015–2018 on pigs with acute respiratory syndrome (137 farms) gave negative results. In Corse, a Mediterranean island where pigs are mainly bred free-range, 2.3% of sera (n = 177) sampled on adult pigs in 2013–2014 obtained low HI titers. Finally, 0.5% of sera from wild boars hunted in 2009–2016 (n = 644) tested positive with low HI titers. These results provide the first serological evidence that sows were exposed to IDV in France but with a limited spread within the swine population.

Emerging Influenza D virus infection in European livestock as determined in serology studies: Are we underestimating its spread over the continent?

“…Available serological results in cattle in Europe are summarized in Table 1. (Gorin et al 2019). Herds were mostly located in Brittany region, known to have the highest pig density in France.…”

“…A different scenario emerged from serological studies conducted on serum samples collected in swine farms. A serosurvey across France was conducted on 2090 sera collected from 102 different farms between 2012 and 2018 (Gorin et al., 2019). Herds were mostly located in Brittany region, known to have the highest pig density in France.…”

“…Indeed, various studies report a high prevalence of IDV in this species (Luo et al., 2017; O’Donovan, Donohoe, Ducatez, Meyer, & Ryan, 2019; Oliva et al., 2019; Rosignoli et al., 2017) whereas historically cattle had never been considered a potential reservoir of influenza A viruses (Sreenivasan, Thomas, Kaushik, Wang, & Li, 2019). Currently, the list of susceptible species include cattle, swine (Foni et al., 2017; Gorin et al., 2019), small ruminants (O’Donovan et al., 2019; Oliva et al., 2019; Quast et al., 2015), camelids (Murakami et al., 2019; Salem et al., 2017), feral swine (Ferguson et al., 2018) and horses (Nedland et al., 2018). The emergence of the novel IDV in pigs initially raised public health concerns, as swine is a well‐known host of other zoonotic Influenza viruses.…”

Epidemiology and Clinical Characteristics of Influenza C Virus

“…The recent development of RT-PCR for ICV detection has resulted in expanded understanding of ICV clinical characteristics, seasonality, and molecular epidemiology. A related novel influenza D virus (IDV), was discovered in swine in Oklahoma in 2011 and has been detected in other mammals [15][16][17][18][19]; however, while cattle workers exhibit seropositivity, no definitive evidence of productive human infection with IDV has been reported [20,21]. In this review, we discuss the epidemiology and clinical characteristics of ICV.…”

The first decade of research advances in influenza D virus

“…Following this initial report, IDV was subsequently found to be widespread throughout other European countries, including Italy, Luxembourg, Ireland and the UK () [34–37]. The prevalence of IDV in Europe was similar to that in North America, in which the virus and/or its specific antibodies were detected in multiple animal species, including cattle, swine, wild boar, sheep and goats, while the highest prevalence of IDV was observed in cattle () [36, 38–41]. Serosurveys in Italy, Luxembourg and Ireland revealed extremely high IDV-seropositive rates in cattle (92.4, 80.2 and 94.6 %, respectively) () [36, 39, 41].…”