1887
Research article Open Access
Like 0

Abstract

Since November 2016, Europe witnesses another wave of incursion of highly pathogenic avian influenza (HPAI) A(H5) viruses of the Asian origin goose/Guangdong (gs/GD) lineage. Infections with H5 viruses of clade 2.3.4.4b affect wild bird and poultry populations. H5 viruses of clades 2.2, 2.3.1.2c and 2.3.4.4a were detected previously in Europe in 2006, 2010 and 2014. Clades 2.2.1.2 and 2.3.2.1.c are endemic in Egypt and Western Africa, respectively and have caused human fatalities. Evidence exists of their co-circulation in the Middle East. Subtype H5 viruses of low pathogenicity (LPAI) are endemic in migratory wild bird populations. They potentially mutate into highly pathogenic phenotypes following transmission into poultry holdings. However, to date only the gs/GD H5 lineage had an impact on human health. Rapid and specific diagnosis marks the cornerstone for control and eradication of HPAI virus incursions. We present the development and validation of five real-time RT-PCR assays (RT-qPCR) that allow sequencing-independent pathotype and clade-specific distinction of major gs/GD HPAI H5 virus clades and of Eurasian LPAI viruses currently circulating. Together with an influenza A virus-generic RT-qPCR, the assays significantly speed up time-to-diagnosis and reduce reaction times in a OneHealth approach of curbing the spread of gs/GD HPAI viruses.

Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2017.22.1.30435
2017-01-05
2017-10-20
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2017.22.1.30435
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/22/1/eurosurv-22-30435-2.html?itemId=/content/10.2807/1560-7917.ES.2017.22.1.30435&mimeType=html&fmt=ahah

References

  1. Cheung TK, Poon LL. Biology of influenza a virus. Ann N Y Acad Sci. 2007;1102(1):1-25.  https://doi.org/10.1196/annals.1408.001  PMID: 17470908 
  2. Webster RG, Govorkova EA. Continuing challenges in influenza. Ann N Y Acad Sci. 2014;1323(1):115-39.  https://doi.org/10.1111/nyas.12462  PMID: 24891213 
  3. França MS, Brown JD. Influenza pathobiology and pathogenesis in avian species. Curr Top Microbiol Immunol. 2014;385:221-42.  https://doi.org/10.1007/82_2014_385  PMID: 25015786 
  4. Wallace RG, Bergmann L, Kock R, Gilbert M, Hogerwerf L, Wallace R, et al. The dawn of Structural One Health: a new science tracking disease emergence along circuits of capital. Soc Sci Med. 2015;129:68-77.  https://doi.org/10.1016/j.socscimed.2014.09.047  PMID: 25311784 
  5. Malik Peiris JS. Avian influenza viruses in humans. Rev Sci Tech. 2009;28(1):161-73.  https://doi.org/10.20506/rst.28.1.1871  PMID: 19618624 
  6. Capua I, Munoz O. Emergence of influenza viruses with zoonotic potential: open issues which need to be addressed. A review. Vet Microbiol. 2013;165(1-2):7-12.  https://doi.org/10.1016/j.vetmic.2013.01.044  PMID: 23567150 
  7. Smith GJ, Donis RO. World Health Organization/World Organisation for Animal HF, Agriculture Organization HEWG. Nomenclature updates resulting from the evolution of avian influenza A(H5) virus clades 2.1.3.2a, 2.2.1, and 2.3.4 during 2013-2014. Influenza Other Respi Viruses. 2015;9(5):271-6.  https://doi.org/10.1111/irv.12324 
  8. Lycett S, Bodewes R, Pohlmann A, Banks J, Bányai K, Boni MF, et al. Global Consortium for H5N8 and Related Influenza Viruses. Role for migratory wild birds in the global spread of avian influenza H5N8. Science. 2016;354(6309):213-7.  https://doi.org/10.1126/science.aaf8852  PMID: 27738169 
  9. Adlhoch C, Gossner C, Koch G, Brown I, Bouwstra R, Verdonck F, et al. Comparing introduction to Europe of highly pathogenic avian influenza viruses A(H5N8) in 2014 and A(H5N1) in 2005. Euro Surveill. 2014;19(50):20996.  https://doi.org/10.2807/1560-7917.ES2014.19.50.20996  PMID: 25597538 
  10. Abdelwhab EM, Hassan MK, Abdel-Moneim AS, Naguib MM, Mostafa A, Hussein IT, et al. Introduction and enzootic of A/H5N1 in Egypt: Virus evolution, pathogenicity and vaccine efficacy ten years on. Infect Genet Evol. 2016;40:80-90.  https://doi.org/10.1016/j.meegid.2016.02.023  PMID: 26917362 
  11. World Health Organization (WHO). Cumulative number of confirmed human cases for avian influenza A(H5N1) reported to WHO, 2003-2016. Geneva: WHO; 2016. [Accessed 01 Jan 2017]. Available from: http://www.who.int/influenza/human_animal_interface/H5N1_cumulative_table_archives/en/.
  12. Arafa AS, Naguib MM, Luttermann C, Selim AA, Kilany WH, Hagag N, et al. Emergence of a novel cluster of influenza A(H5N1) virus clade 2.2.1.2 with putative human health impact in Egypt, 2014/15. Euro Surveill. 2015;20(13):2-8.  https://doi.org/10.2807/1560-7917.ES2015.20.13.21085  PMID: 25860390 
  13. Tosh C, Nagarajan S, Kumar M, Murugkar HV, Venkatesh G, Shukla S, et al. Multiple introductions of a reassortant H5N1 avian influenza virus of clade 2.3.2.1c with PB2 gene of H9N2 subtype into Indian poultry. Infect Genet Evol. 2016;43:173-8.  https://doi.org/10.1016/j.meegid.2016.05.012  PMID: 27174088 
  14. Bi Y, Chen J, Zhang Z, Li M, Cai T, Sharshov K, et al. Highly pathogenic avian influenza H5N1 Clade 2.3.2.1c virus in migratory birds, 2014-2015. Virol Sin. 2016;31(4):300-5.  https://doi.org/10.1007/s12250-016-3750-4  PMID: 27405930 
  15. Naguib MM, Kinne J, Chen H, Chan KH, Joseph S, Wong PC, et al. Outbreaks of highly pathogenic avian influenza H5N1 clade 2.3.2.1c in hunting falcons and kept wild birds in Dubai implicate intercontinental virus spread. J Gen Virol. 2015;96(11):3212-2.  https://doi.org/10.1099/jgv.0.000274  PMID: 26350163 
  16. Tassoni L, Fusaro A, Milani A, Lemey P, Awuni JA, Sedor VB, et al. Genetically Different Highly Pathogenic Avian Influenza A(H5N1) Viruses in West Africa, 2015. Emerg Infect Dis. 2016;22(12):2132-6.  https://doi.org/10.3201/eid2212.160578  PMID: 27389972 
  17. Claes F, Morzaria SP, Donis RO. Emergence and dissemination of clade 2.3.4.4 H5Nx influenza viruses-how is the Asian HPAI H5 lineage maintained. Curr Opin Virol. 2016;16:158-63.  https://doi.org/10.1016/j.coviro.2016.02.005  PMID: 26991931 
  18. Lee DH, Torchetti MK, Winker K, Ip HS, Song CS, Swayne DE. Intercontinental Spread of Asian-Origin H5N8 to North America through Beringia by Migratory Birds. J Virol. 2015;89(12):6521-4.  https://doi.org/10.1128/JVI.00728-15  PMID: 25855748 
  19. ProMED-mail. Avian influenza H5N8 Germany. Archive. 2016;4641281(: 20161119):19. Available from: http://www.promedmail.org/post/20161119.4641281
  20. ProMED-mail. Avian influenza H5N8 Israel. Archive. 2016;4628359(: 20161114):14. Available from: http://www.promedmail.org/post/4628359
  21. Munster VJ, Baas C, Lexmond P, Waldenström J, Wallensten A, Fransson T, et al. Spatial, temporal, and species variation in prevalence of influenza A viruses in wild migratory birds. PLoS Pathog. 2007;3(5):e61.  https://doi.org/10.1371/journal.ppat.0030061  PMID: 17500589 
  22. Peiris JS, Cowling BJ, Wu JT, Feng L, Guan Y, Yu H, et al. Interventions to reduce zoonotic and pandemic risks from avian influenza in Asia. Lancet Infect Dis. 2016;16(2):252-8.  https://doi.org/10.1016/S1473-3099(15)00502-2  PMID: 26654122 
  23. Sims LD. Intervention strategies to reduce the risk of zoonotic infection with avian influenza viruses: scientific basis, challenges and knowledge gaps. Influenza Other Respi Viruses. 2013;7(Suppl 2):15-25.  https://doi.org/10.1111/irv.12076  PMID: 24034479 
  24. Höper D, Hoffmann B, Beer M. Simple, sensitive, and swift sequencing of complete H5N1 avian influenza virus genomes. J Clin Microbiol. 2009;47(3):674-9.  https://doi.org/10.1128/JCM.01028-08  PMID: 19109473 
  25. European Commission (EC). 2006/437/EC: Commission Decision of 4 August 2006 approving a Diagnostic Manual for avian influenza as provided for in Council Directive 2005/94/EC (notified under document number C(2006) 3477) (Text with EEA relevance). OJ L 237, 31.8.2006, p. 1-27. Brussels: EC; 2006. Available from: http://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX%3A32006D0437
  26. World Organisation for Animal Health/Food and Agriculture Organization of the United Nations (OIE/FAO). Network of expertise on animal influenza. Influenza A Cleavage sites. Paris/Rome: OIE/FAO; 2015. [Accessed 01 Dec 2016] Available from: http://www.offlu.net/fileadmin/home/en/resource-centre/pdf/Influenza_A_Cleavage_Sites.pdf
  27. Influenza research database (IRD). [Internet]. Highly Pathogenic H5N1 Clade Classification Tool. [Accessed 21 Nov 2016]. Available from: https://www.fludb.org/brc/h5n1Classifier.spg?method=ShowCleanInputPage&decorator=influenza
  28. Hoffmann B, Harder T, Lange E, Kalthoff D, Reimann I, Grund C, et al. New real-time reverse transcriptase polymerase chain reactions facilitate detection and differentiation of novel A/H1N1 influenza virus in porcine and human samples. Berl Munch Tierarztl Wochenschr. 2010;123(7-8):286-92. PMID: 20690540 
  29. Spackman E, Senne DA, Bulaga LL, Myers TJ, Perdue ML, Garber LP, et al. Development of real-time RT-PCR for the detection of avian influenza virus. Avian Dis. 2003;47(3) Suppl;1079-82.  https://doi.org/10.1637/0005-2086-47.s3.1079  PMID: 14575115 
  30. Hoffmann B, Hoffmann D, Henritzi D, Beer M, Harder TC. Riems influenza a typing array (RITA): An RT-qPCR-based low density array for subtyping avian and mammalian influenza a viruses. Sci Rep. 2016;6:27211.  https://doi.org/10.1038/srep27211  PMID: 27256976 
  31. Hoffmann B, Harder T, Starick E, Depner K, Werner O, Beer M. Rapid and highly sensitive pathotyping of avian influenza A H5N1 virus by using real-time reverse transcription-PCR. J Clin Microbiol. 2007;45(2):600-3.  https://doi.org/10.1128/JCM.01681-06  PMID: 17182758 
  32. Ampofo WK, Azziz-Baumgartner E, Bashir U, Cox NJ, Fasce R, Giovanni M, et al. WHO Writing Group. Strengthening the influenza vaccine virus selection and development process: Report of the 3rd WHO Informal Consultation for Improving Influenza Vaccine Virus Selection held at WHO headquarters, Geneva, Switzerland, 1-3 April 2014. Vaccine. 2015;33(36):4368-82.  https://doi.org/10.1016/j.vaccine.2015.06.090  PMID: 26148877 
  33. Wong S-S, Webby RJ. Traditional and new influenza vaccines. Clin Microbiol Rev. 2013;26(3):476-92.  https://doi.org/10.1128/CMR.00097-12  PMID: 23824369 
  34. European Centre for Disease Prevention and Control (ECDC). Outbreak of highly pathogenic avian influenza. A(H5N8) in Europe – 18 November 2016. Stockholm: ECDC; 2016. [Accessed 21 Nov 2016] Available from: http://ecdc.europa.eu/en/publications/Publications/risk-assessment-avian-influenza-H5N8-europe.pdf
  35. Kis Z, Jones J, Creanga A, Ferdinand K, Inui K, Gerloff N, et al. Real-time RT-PCR assay to differentiate clades of H5N1 avian influenza viruses circulating in Vietnam. J Virol Methods. 2013;193(2):452-8.  https://doi.org/10.1016/j.jviromet.2013.06.023  PMID: 23850699 
  36. Abdelwhab SM, Erfan AM, Grund C, Ziller M, Arafa A-S, Beer M, et al. Simultaneous detection and differentiation by multiplex real time RT-PCR of highly pathogenic avian influenza subtype H5N1 classic (clade 2.2.1 proper) and escape mutant (clade 2.2.1 variant) lineages in Egypt. Virol J. 2010;7(1):260.  https://doi.org/10.1186/1743-422X-7-260  PMID: 20929539 
/content/10.2807/1560-7917.ES.2017.22.1.30435
Loading

Data & Media loading...

Comment has been disabled for this content
Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error