Outbreak of highly pathogenic avian influenza A(H5N1) clade 2.3.4.4b virus in cats, Poland, June to July 2023

Background Over a 3-week period in late June/early July 2023, Poland experienced an outbreak caused by highly pathogenic avian influenza (HPAI) A(H5N1) virus in cats. Aim This study aimed to characterise the identified virus and investigate possible sources of infection. Methods We performed next generation sequencing and phylogenetic analysis of detected viruses in cats. Results We sampled 46 cats, and 25 tested positive for avian influenza virus. The identified viruses belong to clade 2.3.4.4b, genotype CH (H5N1 A/Eurasian wigeon/Netherlands/3/2022-like). In Poland, this genotype was responsible for several poultry outbreaks between December 2022 and January 2023 and has been identified only sporadically since February 2023. Viruses from cats were very similar to each other, indicating one common source of infection. In addition, the most closely related virus was detected in a dead white stork in early June. Influenza A(H5N1) viruses from cats possessed two amino acid substitutions in the PB2 protein (526R and 627K) which are two molecular markers of virus adaptation in mammals. The virus detected in the white stork presented one of those mutations (627K), which suggests that the virus that had spilled over to cats was already partially adapted to mammalian species. Conclusion The scale of HPAI H5N1 virus infection in cats in Poland is worrying. One of the possible sources seems to be poultry meat, but to date no such meat has been identified with certainty. Surveillance should be stepped up on poultry, but also on certain species of farmed mammals kept close to infected poultry farms.

[1]  T. Kuiken,et al.  Avian influenza overview April – June 2023 , 2023, EFSA journal. European Food Safety Authority.

[2]  T. Kuiken,et al.  Avian influenza overview March – April 2023 , 2023, EFSA journal. European Food Safety Authority.

[3]  Thomas P. Fabrizio,et al.  Rapid evolution of A(H5N1) influenza viruses after intercontinental spread to North America , 2023, Nature communications.

[4]  W. Courtens,et al.  Highly pathogenic avian influenza causes mass mortality in Sandwich tern (Thalasseus sandvicensis) breeding colonies across northwestern Europe , 2023, bioRxiv.

[5]  T. Kuiken,et al.  Avian influenza overview June – September 2022 , 2022, EFSA journal. European Food Safety Authority.

[6]  C. Terregino,et al.  Silent Infection of Highly Pathogenic Avian Influenza Virus (H5N1) Clade 2.3.4.4b in a Commercial Chicken Broiler Flock in Italy , 2022, Viruses.

[7]  A. Fusaro,et al.  Avian influenza, a new threat to public health in Europe? , 2021, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[8]  K. Wyrostek,et al.  Highly Pathogenic Avian Influenza H5N8 in Poland in 2019–2020 , 2020, Journal of veterinary research.

[9]  Yi-Mo Deng,et al.  Inventory of molecular markers affecting biological characteristics of avian influenza A viruses , 2019, Virus Genes.

[10]  A. von Haeseler,et al.  UFBoot2: Improving the Ultrafast Bootstrap Approximation , 2017, bioRxiv.

[11]  F. Velkers,et al.  The role of rodents in avian influenza outbreaks in poultry farms: a review , 2017, The Veterinary quarterly.

[12]  M. Beer,et al.  Riems influenza a typing array (RITA): An RT-qPCR-based low density array for subtyping avian and mammalian influenza a viruses , 2016, Scientific Reports.

[13]  G. Cattoli,et al.  Susceptibility to and transmission of H5N1 and H7N1 highly pathogenic avian influenza viruses in bank voles (Myodes glareolus) , 2015, Veterinary Research.

[14]  A. von Haeseler,et al.  IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies , 2014, Molecular biology and evolution.

[15]  A. Franklin,et al.  Low-Pathogenic Avian Influenza Viruses in Wild House Mice , 2012, PloS one.

[16]  D. Guo,et al.  Single mutation at the amino acid position 627 of PB2 that leads to increased virulence of an H5N1 avian influenza virus during adaptation in mice can be compensated by multiple mutations at other sites of PB2. , 2009, Virus research.

[17]  Michael G. Katze,et al.  A Single-Amino-Acid Substitution in a Polymerase Protein of an H5N1 Influenza Virus Is Associated with Systemic Infection and Impaired T-Cell Activation in Mice , 2009, Journal of Virology.

[18]  John Steel,et al.  Transmission of Influenza Virus in a Mammalian Host Is Increased by PB2 Amino Acids 627K or 627E/701N , 2009, PLoS pathogens.

[19]  A. Tomoiu,et al.  Avian Influenza A Virus Polymerase Association with Nucleoprotein, but Not Polymerase Assembly, Is Impaired in Human Cells during the Course of Infection , 2008, Journal of Virology.

[20]  J. Doudna,et al.  An inhibitory activity in human cells restricts the function of an avian-like influenza virus polymerase. , 2008, Cell host & microbe.

[21]  Jin Hyun Kim,et al.  Growth of H5N1 Influenza A Viruses in the Upper Respiratory Tracts of Mice , 2007, PLoS pathogens.

[22]  K. Labadie,et al.  Host-range determinants on the PB2 protein of influenza A viruses control the interaction between the viral polymerase and nucleoprotein in human cells. , 2007, Virology.

[23]  I. Brown,et al.  Validated H5 Eurasian Real-Time Reverse Transcriptase–Polymerase Chain Reaction and Its Application in H5N1 Outbreaks in 2005–2006 , 2007, Avian diseases.

[24]  R. Webster,et al.  The polymerase complex genes contribute to the high virulence of the human H5N1 influenza virus isolate A/Vietnam/1203/04 , 2006, The Journal of experimental medicine.

[25]  Yoshihiro Kawaoka,et al.  PB2 amino acid at position 627 affects replicative efficiency, but not cell tropism, of Hong Kong H5N1 influenza A viruses in mice. , 2004, Virology.

[26]  K. Lohman,et al.  Development of a Real-Time Reverse Transcriptase PCR Assay for Type A Influenza Virus and the Avian H5 and H7 Hemagglutinin Subtypes , 2002, Journal of Clinical Microbiology.

[27]  Yoshihiro Kawaoka,et al.  Molecular Basis for High Virulence of Hong Kong H5N1 Influenza A Viruses , 2001, Science.

[28]  B. Murphy,et al.  A single amino acid in the PB2 gene of influenza A virus is a determinant of host range , 1993, Journal of virology.

[29]  H. Bandelt,et al.  Median-joining networks for inferring intraspecific phylogenies. , 1999, Molecular biology and evolution.