Highly Pathogenic Avian Influenza A(H5N8) Virus Spread by Short- and Long-Range Transmission, France, 2016–17

Abstract

I nfluenza A viruses are enveloped viruses of the Alphainfluenzavirus genus in the Orthomyxoviridae family. Their negative-stranded RNA genome consists of 8 segments encoding a total of 10-14 proteins. Avian influenza viruses (AIVs) are classified on the basis of antigenic differences in their surface glycoproteins, hemagglutinin (H1-H16) and neuraminidase (N1-N9) (1). H5 and H7 subtypes can become highly pathogenic avian influenza (HPAI) viruses after the evolution of multiple basic amino acids in the cleavage site of hemagglutinin protein (2,3). This mutation enables the virus to replicate efficiently in all organs, causing a severe and often fatal systemic disease. In contrast, the cleavage site of hemagglutinin in low pathogenicity AIVs lacks these multiple amino acids, restricting viral replication to the respiratory and digestive tracts. Low pathogenicity AIVs cause subclinical or mild disease that can be aggravated by secondary infections (4,5). Because H5 and H7 AIVs can evolve to be highly pathogenic, the diseases caused by these subtypes are notifiable to national and international bodies (6). Since 1996, highly pathogenic H5 viruses of the A/goose/Guangdong/1/96 (Gs/GD/96) lineage have caused recurrent outbreaks with high death rates in birds. These HPAIs are categorized into 10 distinct clades (0-9) on the basis of hemagglutinin sequences (7). These clades are found in Asia; a few have spread to Africa, Europe, and North America (8-10). Europe experienced major introductions of H5N1 of clade 2.2 during 2005-2007 and H5N8 of clade 2.3.4.4 during 2014-2020 (11-14). Many reassortments were observed on Gs/Gd/1/96-like viruses, especially within clade 2.3.4.4. The reassortments generated several subtypes including H5N1, H5N2, H5N5, H5N6, and H5N8 (11,15-17). During winter 2016-17, twenty-nine countries in Europe reported 1,576 cases of Gs/Gd/1/96like H5N8 infections in wild birds and 1,134 in poultry, especially domestic ducks (18). During this outbreak, researchers identified 6 HPAI A(H5N8) genotypes in Europe; 2 of these genotypes were identified using 6 sequences from infected birds in France (19). France had 539 cases of HPAI A(H5N8) infections, 51 in wild birds and 488 in poultry flocks, most of which occurred at duck farms producing foie gras (18). A previous study used spatiotemporal analysis of clinical cases comprising 2 distinct epizootic periods in southwestern France (20). The first period spanned November 28, 2016-February 2, 2017 and comprised 4 spatiotemporal clusters (20). The second period spanned February 3-March 23, 2017 and comprised a single spatiotemporal cluster (20).

Serological Evidence of Backyard Pig Exposure to Highly Pathogenic Avian Influenza H5N8 Virus during 2016–2017 Epizootic in France

“…Even if some cross-reaction exists between H1 av and H1pdm, both viruses were assumed having circulated in this farm based on individual HI titers, which is consistent with data from the swIAV surveillance conducted at that time in this region [ 36 ]. This is also in accordance with the fact that no HPAI-H5 outbreak was reported in wild birds or poultry farms in this département during the epizootic [ 26 ].…”

“…The serum taken in May 2017 on the remaining pig gave negative HI results with all antigens, probably because of low levels of anti-IAV antibodies following natural decrease, as suggested by the S/P value obtained in ELISA, which was close to the method threshold for this sample. Thus, analyses conducted in herd #2 led to hypothesize that pig #1 had been most probably infected with an H5Nx virus from clade 2.3.4.4b a few weeks before sampling on 23 December, e.g., possibly the epizootic HPAI-H5N8 responsible for the outbreak that was confirmed in ducks in this farm #2 on 1 December [ 25 , 26 ]. Virus transmission could have happened through direct contact between species and/or exposure to fomites, since ducks and backyard pigs would have shared the same outdoor route on the farm.…”

“…In autumn/winter 2016–2017, HPAI-H5N8 viruses from A/goose/Guandong/1/1996 (Gs/Gd) lineage, clade 2.3.4.4b, were responsible for outbreaks in domestic poultry in Europe [ 22 , 23 , 24 , 25 , 26 , 27 ]. Death rate was lower than for previous 2005–2006 and 2014–2015 HPAI-H5 epizootics, but the magnitude of the 2016–2017 epizootic, considering the numbers of affected farms, and countries and the diversity of infected wild bird species, was unprecedented with a huge economic impact [ 23 ].…”

“…Death rate was lower than for previous 2005–2006 and 2014–2015 HPAI-H5 epizootics, but the magnitude of the 2016–2017 epizootic, considering the numbers of affected farms, and countries and the diversity of infected wild bird species, was unprecedented with a huge economic impact [ 23 ]. In France, 538 cases, i.e., 52 wild birds and 486 poultry flocks, of HPAI-H5N8 infections were reported from November 2016 to June 2017 [ 23 , 25 , 26 ]. The duck production sector located in the southwestern part of the country was the most affected, first with local farm-to-farm spreading of the disease, then with an increased average distance between affected farms as it extended westwards.…”

Phylodynamic assessment of control measures for highly pathogenic avian influenza epidemics in France

“…It remains critically important to learn as much as possible from this devastating epidemic, particularly as France once again experienced an HPAI outbreak in December 2020 [2]. The 2016-17 epidemic was caused by an H5N8 virus of the lineage 2.3.4.4b (A/Gs/Gd/1/96 clade) of Asian origin that was likely introduced by migratory birds [3]. The epidemic was largely concentrated in southwest France, encompassing the Occitanie and the Nouvelle-Aquitaine régions (the largest French territorial administrative division) [4].…”