Detection and isolation of H5N1 clade 2.3.4.4b high pathogenicity avian influenza virus from ticks (Ornithodoros maritimus) recovered from a naturally infected slender-billed gull (Chroicocephalus genei)

Abstract

Laridae birds, such as gulls, are known reservoirs of H13 and H16 low pathogenicity avian influenza virus (LPAIV) subtypes. However, during the recent outbreaks linked to the reemergence of high pathogenicity avian influenza virus (HPAIV) H5N1 clade 2.3.4.4b of the Goose/Guangdong lineage, European populations of Laridae birds suffered significant losses. HPAI cases were reported not only along the coastlines but also inland areas, particularly in France and Central Europe. During a diagnostic investigation of a group of Laridae birds, part of a HPAIV outbreak reported in the South of France in 2023, larval stages of Ornithodoros maritimus, a nidicolous soft tick parasitizing seabirds, were recovered from a slender-billed gull (Chroicocephalus genei). Affected birds exhibited gross and histopathological lesions consistent with systemic HPAIV infection. Immunohistochemistry revealed marked neurotropism, oculotropism and multicentric epitheliotropism. Viral isolation and sequencing analysis confirmed the presence of HPAIV H5N1 clade 2.3.4.4b in both the gull and ectoparasites, showing from 99.64% to 100% nucleotide identity across five of eight RNA segments. While additional research is needed to properly assess the vector competence of O. maritimus for HPAIV, ticks may represent an interesting non-invasive surveillance tool for these viruses. This is the first time a HPAIV has been successfully isolated from tick larvae. These findings represent a first step toward understanding the potential role played by ticks in the spread of avian influenza viruses within marine bird colonies and among other ecosystems, considering the occurrence of specific behavioral traits, such as kleptoparasitim and the position of gulls at the interface between wild and domestic species.