A G1-lineage H9N2 virus with oviduct tropism causes chronic pathological changes in the infundibulum and a long-lasting drop in egg production

Abstract

Since 1997, G1-lineage H9N2 avian influenza viruses have been circulating in Asia and later on in the Middle East, and they have been associated to mild respiratory disease, drops in egg production and moderate mortality in chickens, in particular in the presence of concurrent infections. In this study, we investigated the importance of the G1-lineage H9N2 A/chicken/Israel/1163/2011 virus as a primary pathogen in layers, analyzing its tropism and binding affinity for the oviduct tissues, and investigating the long-term impact on egg production. Besides causing a mild respiratory infection, the virus replicated in the oviduct of 60% of the hens causing different degrees of salpingitis throughout the organ, in particular at the level of the infundibulum, where the detection of the virus was associated with severe heterophilic infiltrate, and necrosis of the epithelium. Binding affinity assays confirmed that the infundibulum was the most receptive region of the oviduct. The drop in egg production was at its peek at 2 weeks post-infection (pi) (60% decrease) and continued up to 80 days pi (35% decrease). On day 80 pi, non-laying birds showed egg yolk peritonitis, and histopathological analyses described profound alteration of the infundibulum architecture, duct ectasia and thinning of the epithelium, while the rest of the oviduct and ovary appeared normal. Our results show that this H9N2 virus is a primary pathogen in layer hens, and that its replication in the infundibulum is responsible for acute and chronic lesions that limits the effective functionality of the oviduct, compromising the commercial life of birds.Electronic supplementary materialThe online version of this article (10.1186/s13567-018-0575-1) contains supplementary material, which is available to authorized users.

H9 Influenza Viruses: An Emerging Challenge

“…Y439-like viruses were initially identified from disease outbreaks in chickens in South Korea and from domestic ducks in Hong Kong in the mid-1990s. Since then, Y439-h9.2-like viruses have been isolated sporadically from wild birds and have been associated with outbreaks in domestic birds in Europe, Indonesia, Southeast Asia, Southeast Russia, Oceania, South Africa, Zambia, and Malawi (Abolnik et al 2006;Bonfante et al 2018;Peacock et al 2019). In Europe, vaccination has been adopted to prevent reoccurrences especially in turkeys in Germany and Italy (Capua and Alexander 2009).…”

“…Common respiratory signs include swelling of the sinuses and discharge from the eyes, nares, and mouth. In more severe cases, birds have severe dyspnea and difficulty breathing (Guo et al 2000;Nili et al 2013;Wang et al 2015aWang et al , 2016aBonfante et al 2018). H9N2 infections occur throughout the year, with lower morbidity in the summer (Xu et al 2007b).…”

Avian influenza overview August – November 2018

“…In an experiment in laying hens, it was demonstrated that a G1 lineage of A(H9N2) virus spread beyond respiratory and digestive tract, replicated in the infundibulum and caused lesions in the oviduct resulting in a long-term drop in egg production (Bonfante et al, 2018).…”

“…Domestic and wild birdsDetectionAs mentioned in previous reports(EFSA et al, 2018b;EFSA et al, 2018c), A(H9N2) is the most commonly detected non-notifiable subtype of influenza viruses in poultry in Asia, the Middle East and North Africa(Bonfante et al, 2018;Chrzastek et al, 2018;Xu et al, 2018; Zhu et al, 2018). This has also reduced the human exposure to the virus and no human cases have been reported since March 2018 (Zeng et al, 2018).4.4.5.…”

Avian influenza overview February– August 2019

“…Domestic and wild birdsDetectionAs mentioned in previous EFSA reports, A(H9N2) is the most commonly detected non-notifiable subtype of influenza viruses in poultry in Asia, the Middle East and North Africa(Bonfante et al, 2018;Chrzastek et al, 2018; Xu et al, 2018; Zhu et al, 2018). LPAI A(H9N2) 4.4.6.1.…”