Detection of non-notifiable H4N6 avian influenza virus in poultry in Great Britain

• Published in: Veterinary microbiology 2018-10, Vol.224, p.107-115
• Main Authors: Reid, Scott M., Brookes, Sharon M., Núñez, Alejandro, Banks, Jill, Parker, C. Daniel, Ceeraz, Vanessa, Russell, Christine, Seekings, Amanda, Thomas, Saumya S., Puranik, Anita, Brown, Ian H.
• Format: Article
• Language: English
• Subjects: Animals; Animals, Wild - virology; Aquatic birds; Avian flu; Avian influenza A virus; Birds; Broiler breeders; Chickens; Chickens - virology; Commercial layer chickens; Diagnosis, Differential; Differential diagnosis; Disease control; Disease Outbreaks - prevention & control; Disease Outbreaks - veterinary; Egg production; Eggs; Epidemiological Monitoring; Exo-a-sialidase; Gene deletion; Genomes; Hemagglutinins; Hemagglutinins - genetics; High-Throughput Nucleotide Sequencing; Infections; Influenza; Influenza A virus - genetics; Influenza A virus - growth & development; Influenza A virus - isolation & purification; Influenza A virus - pathogenicity; Influenza in Birds - epidemiology; Influenza in Birds - virology; Intravenous administration; Legislation; NAD; Neuraminidase - genetics; Non-notifiable avian influenza virus; Notifiable avian disease ‘testing to exclude’ scheme; Pathogenesis; Pathogenicity; Pathogens; Phylogeny; Pilot Projects; Polymerase chain reaction; Poultry; Poultry - virology; Poultry Diseases - diagnosis; Poultry Diseases - epidemiology; Poultry Diseases - virology; Real-Time Polymerase Chain Reaction; Reverse transcription; Serology; Specific pathogen free; Stalk deletion; Surveillance for avian influenza; Turkeys - virology; Viruses
• ISSN: 0378-1135; 1873-2542
• DOI: 10.1016/j.vetmic.2018.08.026

•H4N6 LPAIV isolated from broiler breeder chickens from the first submission to the NAD ‘testing to exclude’ (TTE) scheme.•A second H4N6 LPAIV case in June 2014 affected free-range laying chickens in GB, reflecting a different clinical presentation.•The two H4N6 LPAIVs were genetically very similar but not identical (overall ≥ 99.7% identity).•Stalk deletion in the neuraminidase sequence indicated viral adaptation to poultry.•Viral genome analyses implied that the virus had not recently transferred from wild birds, indicating spread within the poultry sector. A 12-month pilot project for notifiable avian disease (NAD) exclusion testing in chicken and turkey flocks in Great Britain (GB) offered, in partnership with industry, opportunities to carry out differential diagnosis in flocks where NAD was not suspected, and to identify undetected or undiagnosed infections. In May 2014, clinical samples received from a broiler breeder chicken premises that had been experiencing health and production problems for approximately one week tested positive by avian influenza (AI) real-time reverse transcription polymerase chain reaction (RRT-PCR). Following immediate escalation to an official, statutory investigation to rule out the presence of notifiable AI virus (AIV; H5 or H7 subtypes), a non-notifiable H4N6 low pathogenicity (LP) AIV was detected through virus isolation in embryonated specific pathogen free (SPF) fowls’ eggs, neuraminidase inhibition test, cleavage site sequencing and AIV subtype H4-specific serology. Premises movement restrictions were lifted, and no further disease control measures were implemented as per the United Kingdom (UK) legislation. Phylogenetic analysis of the haemagglutinin and neuraminidase genes of the virus revealed closest relationships to viruses from Mallard ducks in Sweden during 2007 and 2009. In June 2014, clinical suspicion of NAD was reported in a flock of free-range laying chickens elsewhere in GB, due to increasing daily mortality and reduced egg production over a five-day period. An H4N6 LPAIV with an intravenous pathogenicity index of 0.50 was isolated. This virus was genetically highly similar, but not identical, to the virus detected during May 2014. Full viral genome analyses showed characteristics of a strain that had not recently transferred from wild birds, implying spread within the poultry sector had occurred. A stalk deletion in the neuraminidase gene sequence indicated an adaptation of the virus to poultry. Furthe