Pathogenicity of highly pathogenic avian influenza H5N8 subtype for herring gulls (Larus argentatus): impact of homo- and heterosubtypic immunity on the outcome of infection

Abstract

To improve understanding of the pathobiology of highly pathogenic avian influenza virus (HPAIV) infections in wild birds, pathogenicity and transmissibility of HPAIV H5N8 subtype clade 2.3.4.4b was evaluated in ~ 8-week-old herring gulls (Larus argentatus) divided into 3 groups: naïve birds (group A), birds previously exposed to low pathogenic avian influenza virus (LPAIV) H5N1 (group B) and LPAIV H13N6 (group C). The HPAIV H5N8 virus was highly virulent for naïve gulls, that showed early morbidity, high mortality, a broad spectrum of clinical signs, including violent neurological disorders, systemic distribution of the virus in organs accompanied by high level of shedding and transmission to contact birds. Pre-exposure to homologous and heterologous LPAIV subtypes conferred only partial protection: we observed increased survival rate (statistically significant only in group B), nervous signs, pantropic distribution of virus in organs, shedding (significantly reduced in gulls of group C in the early phase of disease and asymptomatic shedding in the late phase), transmission to contact gulls (more pronounced in group B) and near-complete seroconversion in survivors. Histopathological and immunohistochemical results indicate virus tropism for the neural, respiratory and myocardial tissues. In conclusion, we demonstrate that HPAIV H5N8 clade 2.3.4.4b is highly virulent and lethal for fully susceptible herring gulls and that pre-exposure to homo- and heterosubtypic LPAIV only partially modulates the disease outcome.

Pathology of naturally acquired high pathogenicity avian influenza virus H5N1 infection in seabirds

“…and this was observed in the outbreak in gannet colonies. Further, contact transmission between common gulls (Larus canus) and European herring gulls have been documented previously with experimental infection with HPAIV H5N1 clade 2.2 and H5N8 clade 2.3.4.4b 23,46. More recent HPAIV H5N1 outbreaks (June and August 2022) in wild bird rescue centres / hospitals in England (East Sussex and Cornwall) have been confirmed in herring gulls.…”

“…Such lesions are like those reported from experimentally challenged common gulls with H5N1, plus naturally infected black headed gulls and herring gulls, together with a recent report of naturally infected sandwich terns ( Thalasseus sandvicensis ). 9,23,43,44,46 Although RT-PCR was not conducted on tissues from the current investigation, the abundance of virus antigens in the heart, brain, kidney, spleen, lung, pancreas, and liver strongly suggests the utility of these organs for diagnostic evaluation.…”

“…Further, contact transmission between common gulls ( Larus canus ) and European herring gulls have been documented previously with experimental infection with HPAIV H5N1 clade 2.2 and H5N8 clade 2.3.4.4b. 23,46 More recent HPAIV H5N1 outbreaks (June and August 2022) in wild bird rescue centres / hospitals in England (East Sussex and Cornwall) have been confirmed in herring gulls. After epidemiological assessment, the most likely source of infection appeared to be the introduction within the premises of infected / diseased herring gulls which had then transmitted the disease to the resident gulls of the same species within and among enclosures (APHA, unpublished data).…”

“…18,20,24,32,50 However, a recent experimental model has demonstrated previous exposure of the European herring gulls with LPAIV H5N1 or H13N6 only confer partial protection to subsequent HPAIV H5N8 clade 2.3.4.4b challenge. 46…”

“…18,20,24,32,50 However, a recent experimental model has demonstrated previous exposure of the European herring gulls with LPAIV H5N1 or H13N6 only confer partial protection to subsequent HPAIV H5N8 clade 2.3.4.4b challenge. 46 Prior to the unusual increased in cases during summer 2022, HPAIV-associated disease in the Laridae has been sporadically reported in East Asia and Europe, often in small numbers. 1,2,12,15,34,36,37,39 More recently there has been an increased detection of HPAI positive seabirds or Charadriiformes, 16,27 and critically, mortality events in seabirds associated with HPAIV infection reported in the UK, Europe and North America.…”