The Evolution of Highly Pathogenic Avian Influenza A (H5) in Poultry in Nigeria, 2021–2022

In 2021, amidst the COVID-19 pandemic and global food insecurity, the Nigerian poultry sector was exposed to the highly pathogenic avian influenza (HPAI) virus and its economic challenges. Between 2021 and 2022, HPAI caused 467 outbreaks reported in 31 of the 37 administrative regions in Nigeria. In this study, we characterized the genomes of 97 influenza A viruses of the subtypes H5N1, H5N2, and H5N8, which were identified in different agro-ecological zones and farms during the 2021–2022 epidemic. The phylogenetic analysis of the HA genes showed a widespread distribution of the H5Nx clade 2.3.4.4b and similarity with the HPAI H5Nx viruses that have been detected in Europe since late 2020. The topology of the phylogenetic trees indicated the occurrence of several independent introductions of the virus into the country, followed by a regional evolution of the virus that was most probably linked to its persistent circulation in West African territories. Additional evidence of the evolutionary potential of the HPAI viruses circulating in this region is the identification in this study of a putative H5N1/H9N2 reassortant virus in a mixed-species commercial poultry farm. Our data confirm Nigeria as a crucial hotspot for HPAI virus introduction from the Eurasian territories and reveal a dynamic pattern of avian influenza virus evolution within the Nigerian poultry population.

[1]  T. Kuiken,et al.  Avian influenza overview December 2022 – March 2023 , 2023, EFSA journal. European Food Safety Authority.

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

[3]  I. Monne,et al.  Emergence of a Reassortant 2.3.4.4b Highly Pathogenic H5N1 Avian Influenza Virus Containing H9N2 PA Gene in Burkina Faso, West Africa, in 2021 , 2022, Viruses.

[4]  H. Yao,et al.  Rapid emergence of a PB2 D701N substitution during adaptation of an H9N2 avian influenza virus in mice , 2022, Archives of Virology.

[5]  M. Liao,et al.  Novel Reassortant Avian Influenza A(H5N6) Virus, China, 2021 , 2022, Emerging infectious diseases.

[6]  A. Gultyaev,et al.  Hemagglutinin Subtype Specificity and Mechanisms of Highly Pathogenic Avian Influenza Virus Genesis , 2022, Viruses.

[7]  J. Hughes,et al.  Zoonotic avian influenza viruses evade human BTN3A3 restriction , 2022, bioRxiv.

[8]  G. Gao,et al.  N-linked glycosylation enhances hemagglutinin stability in avian H5N6 influenza virus to promote adaptation in mammals , 2022, PNAS nexus.

[9]  M. Steensels,et al.  Redesign and Validation of a Real-Time RT-PCR to Improve Surveillance for Avian Influenza Viruses of the H9 Subtype , 2022, Viruses.

[10]  A. Omotayo,et al.  Rising Food Prices and Farming Households Food Insecurity during the COVID-19 Pandemic: Policy Implications from SouthWest Nigeria , 2022, Agriculture.

[11]  Hualan Chen,et al.  SUMOylation of Matrix Protein M1 and Filamentous Morphology Collectively Contribute to the Replication and Virulence of Highly Pathogenic H5N1 Avian Influenza Viruses in Mammals , 2021, Journal of virology.

[12]  I. Monne,et al.  Live Bird Markets in Nigeria: A Potential Reservoir for H9N2 Avian Influenza Viruses , 2021, Viruses.

[13]  I. Monne,et al.  Genetic characterization of Highly Pathogenic Avian Influenza H5Nx clade 2.3.4.4b reveals independent introductions in Nigeria. , 2021, Transboundary and emerging diseases.

[14]  M. Beer,et al.  Genotyping and reassortment analysis of highly pathogenic avian influenza viruses H5N8 and H5N2 from Egypt reveals successive annual replacement of genotypes. , 2020, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[15]  T. Takimoto,et al.  Key Role of the Influenza A Virus PA Gene Segment in the Emergence of Pandemic Viruses , 2020, Viruses.

[16]  A. Fusaro,et al.  First detection of highly pathogenic H5N6 avian influenza virus on the African continent , 2020, Emerging microbes & infections.

[17]  P. Lemey,et al.  Disentangling the role of Africa in the global spread of H5 highly pathogenic avian influenza , 2019, Nature Communications.

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

[19]  Clement A Meseko,et al.  Migratory waterfowls from Europe as potential source of highly pathogenic avian influenza infection to Nigeria poultry , 2018, Nigerian Veterinary Journal.

[20]  M. Beer,et al.  Evidence of exposure of domestic pigs to Highly Pathogenic Avian Influenza H5N1 in Nigeria , 2018, Scientific Reports.

[21]  M. Kiso,et al.  Enhanced Replication of Highly Pathogenic Influenza A(H7N9) Virus in Humans , 2018, Emerging infectious diseases.

[22]  Juan Li,et al.  T160A mutation-induced deglycosylation at site 158 in hemagglutinin is a critical determinant of the dual receptor binding properties of clade 2.3.4.4 H5NX subtype avian influenza viruses. , 2018, Veterinary microbiology.

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

[24]  P. Lemey,et al.  Genetically Different Highly Pathogenic Avian Influenza A(H5N1) Viruses in West Africa, 2015 , 2016, Emerging infectious diseases.

[25]  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.

[26]  I. Monne,et al.  Highly Pathogenic Avian Influenza A(H5N1) Virus in Poultry, Nigeria, 2015. , 2015, Emerging infectious diseases.

[27]  Tiago J. S. Lopes,et al.  Identification of mammalian-adapting mutations in the polymerase complex of an avian H5N1 influenza virus , 2015, Nature Communications.

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

[29]  Clement A Meseko,et al.  Circulation of the low pathogenic avian influenza subtype H5N2 virus in ducks at a live bird market in Ibadan, Nigeria , 2014, Infectious Diseases of Poverty.

[30]  Björn Usadel,et al.  Trimmomatic: a flexible trimmer for Illumina sequence data , 2014, Bioinform..

[31]  Mauricio O. Carneiro,et al.  From FastQ Data to High‐Confidence Variant Calls: The Genome Analysis Toolkit Best Practices Pipeline , 2013, Current protocols in bioinformatics.

[32]  K. Katoh,et al.  MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability , 2013, Molecular biology and evolution.

[33]  P. Daszak,et al.  Prediction and prevention of the next pandemic zoonosis , 2012, The Lancet.

[34]  A. Wilm,et al.  LoFreq: a sequence-quality aware, ultra-sensitive variant caller for uncovering cell-population heterogeneity from high-throughput sequencing datasets , 2012, Nucleic acids research.

[35]  P. S. Ekong,et al.  Effect of intervention on the control of Highly Pathogenic Avian Influenza in Nigeria , 2012, The Pan African medical journal.

[36]  O. Bouchez,et al.  Field Monitoring of Avian Influenza Viruses: Whole-Genome Sequencing and Tracking of Neuraminidase Evolution Using 454 Pyrosequencing , 2012, Journal of Clinical Microbiology.

[37]  W. Hagemeijer,et al.  Reassortant low-pathogenic avian influenza H5N2 viruses in African wild birds. , 2011, The Journal of general virology.

[38]  T. Carpenter,et al.  Emergence and Genetic Variation of Neuraminidase Stalk Deletions in Avian Influenza Viruses , 2011, PloS one.

[39]  Ryo Takano,et al.  The HA and NS Genes of Human H5N1 Influenza A Virus Contribute to High Virulence in Ferrets , 2010, PLoS pathogens.

[40]  Wei Wang,et al.  A Comprehensive Surveillance of Adamantane Resistance among Human Influenza a Virus Isolated from Mainland China between 1956 and 2009 , 2010, Antiviral therapy.

[41]  Zejun Li,et al.  Identification of Amino Acids in HA and PB2 Critical for the Transmission of H5N1 Avian Influenza Viruses in a Mammalian Host , 2009, PLoS pathogens.

[42]  D. Marc,et al.  A Genetically Engineered Waterfowl Influenza Virus with a Deletion in the Stalk of the Neuraminidase Has Increased Virulence for Chickens , 2009, Journal of Virology.

[43]  Jonathan E. Allen,et al.  Conserved amino acid markers from past influenza pandemic strains , 2009, BMC Microbiology.

[44]  Y. Kawaoka,et al.  Selection of H5N1 Influenza Virus PB2 during Replication in Humans , 2009, Journal of Virology.

[45]  I. Monne,et al.  Introduction into Nigeria of a Distinct Genotype of Avian Influenza Virus (H5N1) , 2009, Emerging infectious diseases.

[46]  Y. Kawaoka,et al.  Two amino acid residues in the matrix protein M1 contribute to the virulence difference of H5N1 avian influenza viruses in mice. , 2009, Virology.

[47]  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.

[48]  R. Krug,et al.  Influenza A Virus Polymerase Is an Integral Component of the CPSF30-NS1A Protein Complex in Infected Cells , 2008, Journal of Virology.

[49]  F. Fasina,et al.  Serologic and virologic surveillance of avian influenza in Nigeria, 2006-7. , 2008, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[50]  Y. Choi,et al.  Emergence of Amantadine-Resistant H3N2 Avian Influenza A Virus in South Korea , 2008, Journal of Clinical Microbiology.

[51]  W. Hagemeijer,et al.  Evidence of Infection by H5N2 Highly Pathogenic Avian Influenza Viruses in Healthy Wild Waterfowl , 2008, PLoS pathogens.

[52]  I. Monne,et al.  Development and Validation of a One-Step Real-Time PCR Assay for Simultaneous Detection of Subtype H5, H7, and H9 Avian Influenza Viruses , 2008, Journal of Clinical Microbiology.

[53]  R. Wagner,et al.  Avian and 1918 Spanish Influenza A Virus NS1 Proteins Bind to Crk/CrkL Src Homology 3 Domains to Activate Host Cell Signaling* , 2008, Journal of Biological Chemistry.

[54]  Tin Wee Tan,et al.  Identification of human-to-human transmissibility factors in PB2 proteins of influenza A by large-scale mutual information analysis , 2008, BMC Bioinformatics.

[55]  Guohua Deng,et al.  A Single-Amino-Acid Substitution in the NS1 Protein Changes the Pathogenicity of H5N1 Avian Influenza Viruses in Mice , 2007, Journal of Virology.

[56]  Chih-Jen Wei,et al.  Immunization by Avian H5 Influenza Hemagglutinin Mutants with Altered Receptor Binding Specificity , 2007, Science.

[57]  David B. Finkelstein,et al.  Persistent Host Markers in Pandemic and H5N1 Influenza Viruses , 2007, Journal of Virology.

[58]  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.

[59]  Gavin J. D. Smith,et al.  Distribution of amantadine-resistant H5N1 avian influenza variants in Asia. , 2006, The Journal of infectious diseases.

[60]  R. Webster,et al.  Molecular Basis of Replication of Duck H5N1 Influenza Viruses in a Mammalian Mouse Model , 2005, Journal of Virology.

[61]  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.

[62]  W. J. Bean,et al.  Evolution and ecology of influenza A viruses , 1992, Microbiological reviews.

[63]  I. Capua,et al.  Changes in the haemagglutinin and the neuraminidase genes prior to the emergence of highly pathogenic H7N1 avian influenza viruses in Italy , 2001, Archives of Virology.