Research paper
Direct evidence of H7N7 avian influenza virus mutation from low to high virulence on a single poultry premises during an outbreak in free range chickens in the UK, 2008

https://doi.org/10.1016/j.meegid.2018.06.005Get rights and content

Highlights

  • •

    Direct evidence of influenza virus evolution on a single poultry outbreak premises

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    First detection of a rare di-basic cleavage site motif unique to galliformes

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    Reassortment events suggested likely incursion of a wild bird origin precursor.

Abstract

H5 and H7 subtypes of low pathogenicity avian influenza viruses (LPAIVs) have the potential to evolve into highly pathogenic avian influenza viruses (HPAIVs), causing high mortality in galliforme poultry with substantial economic losses for the poultry industry. This study provides direct evidence of H7N7 LPAIV mutation to HPAIV on a single poultry premises during an outbreak that occurred in June 2008 in free range laying hens in Oxfordshire, UK. We report the first detection of a rare di-basic cleavage site (CS) motif (PEIPKKRGLF), unique to galliformes, that has previously been associated with a LPAIV phenotype. Three distinct HPAIV CS sequences (PEIPKRKKRGLF, PEIPKKKKRGLF and PEIPKKKKKKRGLF) were identified in the infected sheds suggesting molecular evolution at the outbreak premises. Further evidence for H7N7 LPAIV preceding mutation to HPAIV was derived by examining clinical signs, epidemiological descriptions and analysing laboratory results on the timing and proportions of seroconversion and virus shedding at each infected shed on the premises. In addition to describing how the outbreak was diagnosed and managed via statutory laboratory testing, phylogenetic analysis revealed reassortant events during 2006–2008 that suggested likely incursion of a wild bird origin LPAIV precursor to the H7N7 HPAIV outbreak. Identifying a precursor LPAIV is important for understanding the molecular changes and mechanisms involved in the emergence of HPAIV. This information can lead to understanding how and why only some H7 LPAIVs appear to readily mutate to HPAIV.

Section snippets

Abbreviations used in this manuscript

AIavian influenza
AIVavian influenza virus
APHAanimal and plant health agency
BHIBbrain-heart infusion broth
Ccloacal swab
CScleavage site
DBCSdi-basic CS
EFEembryonated fowls' eggs
EPEFE passage
EUEuropean Union
GISAIDGlobal Initiative on Sharing Avian Influenza Data
HAhaemagglutinin
HIhaemagglutination inhibition
HPAIhighly pathogenic avian influenza
HPAIVhighly pathogenic avian influenza virus
IHCimmunohistochemistry
IPinfected premises
IVPIintravenous pathogenicity index
LPAIlow pathogenicity

Description of infected premises (IP) and hens

The IP was a free-range laying hen farm (607,000 m2 area) near Banbury, Oxfordshire, UK. Approximately 25,000 hens were kept in four groups, each with a poultry house (shed) with a dedicated surrounding paddock. Sheds 1, 2 and 3 each held 3000 hens, while shed 4 was a large barn holding 16,000 hens. The hens in sheds 1, 2 and 3 were acquired on 25/02/2008 at 16 weeks age (point of lay), and those in shed 4 on 06/03/2008 at the same age. Both consignments were obtained from the same supplier,

Clinical signs

Retrospective records showed a fall in egg production had begun after 21/05/2008 (12 days prior to confirmation of NAD on 02/06/2008) when hens were 28-weeks-old in sheds 1–3. This fall was most marked in sheds 1 and 3 (Fig. 1), increasing to 37% and 36% respectively by 02/06/2008 (Table 1). Low mortality was recorded in shed 1 over six successive days and peaked at 74 birds (2.5% of the population) on 25/05/2008 but declined to a single death on 01/06/2008, the hens appearing to recover after

Discussion

The H7N7 HPAI outbreak at Banbury, Oxfordshire, in June 2008 is important for several reasons. Firstly, it was the first recorded H7 HPAI outbreak in chickens in the UK as all earlier HPAI outbreaks due to H7 subtype viruses had occurred in turkeys (Alexander and Brown, 2009) and secondly the direct detection of LPAIV precursors to a HPAIV outbreak in the same premises is a rare event. The simultaneous detection of both pathotypes by molecular means has been observed in two subsequent H7N7

Acknowledgements

The authors wish to thank Dr. Sharon Brookes and Dr. Dennis Alexander for their comments on the manuscript. This work was supported financially by Defra, UK under contract C (SV3400).

Declarations of interest

None.

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