Top

Published in:

01-12-2007 | Review

The threat of avian influenza A (H5N1). Part I: epidemiologic concerns and virulence determinants

Authors: Jindrich Cinatl Jr, Martin Michaelis, Hans W. Doerr

Published in: Medical Microbiology and Immunology | Issue 4/2007

Abstract

Among emerging and re-emerging infectious diseases, influenza constitutes one of the major threats to mankind. In this review series epidemiologic, virologic and pathologic concerns raised by infections of humans with avian influenza virus A/H5N1 are discussed. This first part concentrates on epidemiologic concerns and virulence determinants. H5N1 spread over the world and caused a series of fowl pest outbreaks. Significant human-to-human transmissions have not been observed yet. Mutations that make the virus more compatible with human-to-human transmission may occur at any time. Nevertheless, no one can currently predict with certainty whether H5N1 will become a human pandemic virus.

Kurtz J, Manvell RJ, Banks J (1996) Avian influenza virus isolated from a woman with conjunctivitis. Lancet 348:901–902PubMedCrossRef

Banks J, Speidel E, Alexander DJ (1998) Characterisation of an avian influenza A virus isolated from a human—is an intermediate host necessary for the emergence of pandemic influenza viruses? Arch Virol 143:781–787PubMedCrossRef

Yuen KY, Chan PK, Peiris M, Tsang DN, Que TL, Shortridge KF, Cheung PT, To WK, Ho ET, Sung R, Cheng AF (1998) Clinical features and rapid viral diagnosis of human disease associated with avian influenza A H5N1 virus. Lancet 351:467–471PubMedCrossRef

Chan PK (2002) Outbreak of avian influenza A(H5N1) virus infection in Hong Kong in 1997. Clin Infect Dis 34 Suppl 2:S58–64CrossRef

Taubenberger JK, Reid AH, Lourens RM, Wang R, Jin G, Fanning TG (2005) Characterization of the 1918 influenza virus polymerase genes. Nature 437:889–893PubMedCrossRef

Chen H, Smith GJ, Zhang SY, Qin K, Wang J, Li KS, Webster RG, Peiris JS, Guan Y (2005) Avian flu: H5N1 virus outbreak in migratory waterfowl. Nature 436:191–192PubMedCrossRef

Liu W, Wang J, Gao GF (2005) Highly pathogenic H5N1 influenza virus infection in migratory birds. Science 309:1206PubMedCrossRef

Nakajima K, Desselberger U, Palese P (1978) Recent human influenza A (H1N1) viruses are closely related genetically to strains isolated in 1950. Nature 274:334–339PubMedCrossRef

Horimoto T, Kawaoka Y (2005) Influenza: lessons from past pandemics, warnings from current incidents. Nat Rev Microbiol 3:591–600PubMedCrossRef

10.

Alexander DJ (2007) An overview of the epidemiology of avian influenza. Vaccine; in press

11.

Fouchier RA, Schneeberger PM, Rozendaal FW, Broekman JM, Kemink SA, Munster V, Kuiken T, Rimmelzwaan GF, Schutten M, Van Doornum GJ, Koch G, Bosman A, Koopmans M, Osterhaus AD (2004) Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome. Proc Natl Acad Sci USA 101:1356–1361PubMedCrossRef

12.

Olofsson S, Kumlin U, Dimock K, Arnberg N (2005) Avian influenza and sialic acid receptors: more than meets the eye? Lancet 5:184–188

13.

Van Borm S, Thomas I, Hanquet G, Lambrecht B, Boschmans M, Dupont G, Decaestecker M, Snacken R, van den Berg T (2005) Highly pathogenic H5N1 influenza virus in smuggled Thai eagles, Belgium. Emerg Infect Dis 11:702–705PubMed

14.

Defra (2005) Epidemiology report on avian influenza in a quarantine premises in Essex. http://www.defraweb/animalh/disease/notifiable/disease/aiepidemicrep111105.pdf

15.

The Writing Committee of the World Health Organization (WHO) Consultation on human influenza A/H5 (2005) Avian influenza A (H5N1) infection in humans. N Engl J. Med 29:1374–1385

16.

Webster G (2006) H5 influenza viruses. In: Kawaoka Y (ed) Influenza viruses. Current topics. Caister Academic Press, Norfolk, pp 281–298

17.

Smith GJ, Naipospos TS, Nguyen TD, de Jong MD, Vijaykrishna D, Usman TB, Hassan SS, Nguyen TV, Dao TV, Bui NA, Leung YH, Cheung CL, Rayner JM, Zhang JX, Zhang LJ, Poon LL, Li KS, Nguyen VC, Hien TT, Farrar J, Webster RG, Chen H, Peiris JS, Guan Y (2006) Evolution and adaptation of H5N1 influenza virus in avian and human hosts in Indonesia and Vietnam. Virology 350:258–268PubMedCrossRef

18.

Bridges CB, Lim W, Hu-Primmer J, Sims L, Fukuda K, Mak KH, Rowe T, Thompson WW, Conn L, Lu X, Cox NJ, Katz JM (2002) Risk of influenza A (H5N1) infection among poultry workers, Hong Kong, 1997–1998. J Infect Dis 185:1005–1010PubMedCrossRef

19.

Mounts AW, Kwong H, Izurieta HS, Ho Y, Au T, Lee M, Buxton Bridges C, Williams SW, Mak KH, Katz JM, Thompson WW, Cox NJ, Fukuda K (1999) Case-control study of risk factors for avian influenza A (H5N1) disease, Hong Kong, 1997. J Infect Dis 180:505–508PubMedCrossRef

20.

Tran TH, Nguyen TL, Nguyen TD, Luong TS, Pham PM, Nguyen VC, Pham TS, Vo CD, Le TQ, Ngo TT, Dao BK, Le PP, Nguyen TT, Hoang TL, Cao VT, Le TG, Nguyen DT, Le HN, Nguyen KT, Le HS, Le VT, Christiane D, Tran TT, Menno de J, Schultsz C, Cheng P, Lim W, Horby P, Farrar J; World Health Organization International Avian Influenza Investigative Team (2004) Avian influenza A (H5N1) in 10 patients in Vietnam. N Engl J Med 350:1179–1188

21.

Chotpitayasunondh T, Ungchusak K, Hanshaoworakul W, Chunsuthiwat S,Sawanpanyalert P, Kijphati R, Lochindarat S, Srisan P, Suwan P, Osotthanakorn Y, Anantasetagoon T, Kanjanawasri S, Tanupattarachai S, Weerakul J, Chaiwirattana R, Maneerattanaporn M, Poolsavathitikool R, Chokephaibulkit K, Apisarnthanarak A, Dowell SF (2005) Human disease from influenza A (H5N1), Thailand, 2004. Emerg Infect Dis 11:201–209PubMed

22.

Oner AF, Bay A, Arslan S, Akdeniz H, Sahin HA, Cesur Y, Epcacan S, Yilmaz N, Deger I, Kizilyildiz B, Karsen H, Ceyhan M (2006) Avian influenza A (H5N1) infection in eastern Turkey in 2006. N Engl J Med 355:2179–2185PubMedCrossRef

23.

Kandun IN, Wibisono H, Sedyaningsih ER, Yusharmen, Hadisoedarsuno W, Purba W, Santoso H, Septiawati C, Tresnaningsih E, Heriyanto B, Yuwono D, Harun S, Soeroso S, Giriputra S, Blair PJ, Jeremijenko A, Kosasih H, Putnam SD, Samaan G, Silitonga M, Chan KH, Poon LL, Lim W, Klimov A, Lindstrom S, Guan Y, Donis R, Katz J, Cox N, Peiris M, Uyeki TM (2006) Three Indonesian clusters of H5N1 virus infection in 2005. N Engl J Med 355:2186–2194PubMedCrossRef

24.

Normile D (2007) Epidemiology: Indonesia taps village wisdom to fight bird flu. Science 315:30–33PubMedCrossRef

25.

Katz JM, Lim W, Bridges CB, Rowe T, Hu-Primmer J, Lu X, Abernathy RA, Clarke M, Conn L, Kwong H, Lee M, Au G, Ho YY, Mak KH, Cox NJ, Fukuda K (1999) Antibody response in individuals infected with avian influenza A (H5N1) viruses and detection of anti-H5 antibody among household and social contacts. J Infect Dis 180:1763–1770PubMedCrossRef

26.

Butler C (2006) Pandemic “dry run” is cause for concern. Nature 441:554–555PubMedCrossRef

27.

Koopmans M, Wilbrink B, Conyn M, Natrop G, van der Nat H, Vennema H, Meijer A,van Steenbergen J, Fouchier R, Osterhaus A, Bosman A (2004) Transmission of H7N7 avian influenza A virus to human beings during a large outbreak in commercial poultry farms in the Netherlands. Lancet 363:587–593PubMedCrossRef

28.

Ghedin E, Sengamalay NA, Shumway M, Zaborsky J, Feldblyum T, Subbu V, Spiro DJ, Sitz J, Koo H, Bolotov P, Dernovoy D, Tatusova T, Bao Y, St George K, Taylor J, Lipman DJ, Fraser CM, Taubenberger JK, Salzberg SL (2005) Large-scale sequencing of human influenza reveals the dynamic nature of viral genome evolution. Nature 437:1162–1166PubMedCrossRef

29.

Neumann G, Kawaoka Y (2006) Host range restriction and pathogenicity in the context of influenza pandemic. Emerg Infect Dis 12:881–886PubMed

30.

Nelson MI, Holmes EC (2007) The evolution of epidemic influenza. Nat Rev Genetic 2007 Epub 2007 Jan 30

31.

Matrosovich M, Tuzikov A, Bovin N, Gambaryan A, Klimov A, Castrucci MR, Donatelli I, Kawaoka Y (2000) Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals. J Virol 74:8502–8512PubMedCrossRef

32.

Matrosovich MN, Klenk HD, Kawaoka Y (2006) Receptor specificity, host range, and pathogenicity of influenza viruses. In: Kawaoka Y (ed) Influenza viruses. Current topics. Caister Academic Press, Norfolk, pp 95–137

33.

Ito T, Couceiro JN, Kelm S, Baum LG, Krauss S, Castrucci MR, Donatelli I, Kida H, Paulson JC, Webster RG, Kawaoka Y (1998) Molecular basis for the generation in pigs of influenza A viruses with pandemic potential. J Virol 72:7367–7373PubMed

34.

Ha Y, Stevens DJ, Skehel JJ, Wiley DC (2001) X-ray structures of H5 avian and H9 swine influenza virus hemagglutinins bound to avian and human receptor analogs. Proc Natl Acad Sci USA 98:11181–11186PubMedCrossRef

35.

Skehel JJ, Wiley DC (2000) Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu Rev Biochem 69:531–569PubMedCrossRef

36.

Gamblin SJ, Haire LF, Russell RJ, Stevens DJ, Xiao B, Ha Y, Vasisht N, Steinhauer DA, Daniels RS, Elliot A, Wiley DC, Skehel JJ (2004) The structure and receptor binding properties of the 1918 influenza hemagglutinin. Science 303:1838–1842PubMedCrossRef

37.

Stevens J, Corper AL, Basler CF, Taubenberger JK, Palese P, Wilson IA (2004) Structure of the uncleaved human H1 hemagglutinin from the extinct 1918 influenza virus. Science 303:1866–1870PubMedCrossRef

38.

Kobasa D, Takada A, Shinya K, Hatta M, Halfmann P, Theriault S, Suzuki H,Nishimura H, Mitamura K, Sugaya N, Usui T, Murata T, Maeda Y, Watanabe S, Suresh M, Suzuki T, Suzuki Y, Feldmann H, Kawaoka Y (2004) Enhanced virulence of influenza A viruses with the haemagglutinin of the 1918 pandemic virus. Nature 431:703–7PubMedCrossRef

39.

Glaser L, Stevens J, Zamarin D, Wilson IA, Garcia-Sastre A, Tumpey TM, Basler CF, Taubenberger JK, Palese P (2005) A single amino acid substitution in 1918 influenza virus hemagglutinin changes receptor binding specificity. J Virol 79:11533–11536PubMedCrossRef

40.

Stevens J, Blixt O, Glaser L, Taubenberger JK, Palese P, Paulson JC, Wilson IA (2006) Glycan microarray analysis of the hemagglutinins from modern and pandemic influenza viruses reveals different receptor specificities. J Mol Biol 355:1143–1155PubMedCrossRef

41.

Tumpey TM, Maines TR, Van Hoeven N, Glaser L, Solorzano A, Pappas C, Cox NJ, Swayne DE, Palese P, Katz JM, Garcia-Sastre A (2007) A two-amino acid change in the hemagglutinin of the 1918 influenza virus abolishes transmission. Science 315:655–659PubMedCrossRef

42.

White J, Kartenbeck J, Helenius A (1982) Membrane fusion activity of influenza virus. EMBO J 1:217–222PubMed

43.

Klenk HD, Rott R, Orlich M, Blodorn J (1975) Activation of influenza A viruses by trypsin treatment. Virology 68:426–439PubMedCrossRef

44.

Murakami M, Towatari T, Ohuchi M, Shiota M, Akao M, Okumura Y, Parry MA, Kido H (2001) Mini-plasmin found in the epithelial cells of bronchioles triggers infection by broad-spectrum influenza A viruses and Sendai virus. Eur J Biochem 268:2847–2855PubMedCrossRef

45.

Stieneke-Grober A, Vey M, Angliker H, Shaw E, Thomas G, Roberts C, Klenk HD, Garten W (1992) Influenza virus hemagglutinin with multibasic cleavage site is activated by furin, a subtilisin-like endoprotease. EMBO J 11:2407–2414PubMed

46.

Horimoto T, Nakayama K, Smeekens SP, Kawaoka Y (1994) Proprotein-processing endoproteases PC6 and furin both activate hemagglutinin of virulent avian influenza viruses. J Virol 68:6074–6078PubMed

47.

Kawaoka Y, Naeve CW, Webster RG (1984) Is virulence of H5N2 influenza viruses in chickens associated with loss of carbohydrate from the hemagglutinin? Virology 139:303–316PubMedCrossRef

48.

Hatta M, Gao P, Halfmann P, Kawaoka Y (2001) Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science 293:1840–1842PubMedCrossRef

49.

Tumpey TM, Basler CF, Aguilar PV, Zeng H, Solorzano A, Swayne DE, Cox NJ, Katz JM, Taubenberger JK, Palese P, Garcia-Sastre A (2005) Characterization of the reconstructed 1918 Spanish influenza pandemic virus. Science 310:77–80PubMedCrossRef

50.

Goto H, Kawaoka Y (1998) A novel mechanism for the acquisition of virulence by a human influenza A virus. Proc Natl Acad Sci USA 95:10224–10228PubMedCrossRef

51.

Li S, Schulman J, Itamura S, Palese P (1993) Glycosylation of neuraminidase determines the neurovirulence of influenza A/WSN/33 virus. J Virol 67:6667–6673PubMed

52.

Garcia-Sastre A, Egorov A, Matassov D, Brandt S, Levy DE, Durbin JE, Palese P, Muster T (1998) Influenza A virus lacking the NS1 gene replicates in interferon-deficient systems. Virology 252:324–330PubMedCrossRef

53.

Garcia-Sastre A (2001) Inhibition of interferon-mediated antiviral responses by influenza A viruses and other negative-strand RNA viruses. Virology 279:375–384PubMedCrossRef

54.

Krug RM, Yuan W, Noah DL, Latham AG (2003) Intracellular warfare between human influenza viruses and human cells: the roles of the viral NS1 protein. Virology 309:181–189PubMedCrossRef

55.

Min JY, Krug RM (2006) The primary function of RNA binding by the influenza A virus NS1 protein in infected cells: Inhibiting the 2'–5' oligo (A) synthetase/RNase L pathway. Proc Natl Acad Sci USA 103:7100–7105PubMedCrossRef

56.

Krug RM (2006) Clues to the virulence of H5N1 viruses in humans. Science 311:1562–1563PubMedCrossRef

57.

Geiss GK, Salvatore M, Tumpey TM, Carter VS, Wang X, Basler CF, Taubenberger JK, Bumgarner RE, Palese P, Katze MG, Garcia-Sastre A (2002) Cellular transcriptional profiling in influenza A virus-infected lung epithelial cells: the role of the nonstructural NS1 protein in the evasion of the host innate defense and its potential contribution to pandemic influenza. Proc Natl Acad Sci USA 99:10736–10741PubMedCrossRef

58.

García-Sastre A (2006) Antiviral response in pandemic influenza viruses. Emerg Infect Dis 12:44–49PubMed

59.

Seo SH, Hoffmann E, Webster RG (2002) Lethal H5N1 influenza viruses escape host anti-viral cytokine responses. Nat Med 8:950–954PubMedCrossRef

60.

Obenauer JC, Denson J, Mehta PK, Su X, Mukatira S, Finkelstein DB, Xu X, Wang J, Ma J, Fan Y, Rakestraw KM, Webster RG, Hoffmann E, Krauss S, Zheng J, Zhang Z, Naeve CW (2006) Large-scale sequence analysis of avian influenza isolates. Science 311:1576–1580PubMedCrossRef

61.

Govorkova EA, Rehg JE, Krauss S, Yen HL, Guan Y, Peiris M, Nguyen TD, Hanh TH, Puthavathana P, Long HT, Buranathai C, Lim W, Webster RG, Hoffmann E (2005) Lethality to ferrets of H5N1 influenza viruses isolated from humans and poultry in 2004. J Virol 79:2191–2198PubMedCrossRef

62.

Gabriel G, Dauber B, Wolff T, Planz O, Klenk HD, Stech J (2005) The viral polymerase mediates adaptation of an avian influenza virus to a mammalian host. Proc Natl Acad Sci USA 102:18590–18595PubMedCrossRef

63.

de Jong MD, Simmons CP, Thanh TT, Hien VM, Smith GJ, Chau TN, Hoang DM, Chau NV, Khanh TH, Dong VC, Qui PT, Cam BV, Ha do Q, Guan Y, Peiris JS, Chinh NT, Hien TT, Farrar J (2006) Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat Med 12:1203–1207PubMedCrossRef

64.

Mase M, Tanimura N, Imada T, Okamatsu M, Tsukamoto K, Yamaguchi S (2006) Recent H5N1 avian influenza A virus increases rapidly in virulence to mice after a single passage in mice. J Gen Virol 87:3655–3659PubMedCrossRef

65.

Salomon R, Franks J, Govorkova EA, Ilyushina NA, Yen HL, Hulse-Post DJ, Humberd J, Trichet M, Rehg JE, Webby RJ, Webster RG, Hoffmann E (2006) The polymerase complex genes contribute to the high virulence of the human H5N1 influenza virus isolate A/Vietnam/1203/04. J Exp Med 203:689–697PubMedCrossRef

66.

Kawaoka Y, Krauss S, Webster RG (1989) Avian-to-human transmission of the PB1 gene of influenza A viruses in the 1957 and 1968 pandemics. J Virol 63:4603–4608PubMed

67.

Russell CJ, Webster RG (2005) The genesis of a pandemic influenza virus. Cell 123:368–371PubMedCrossRef

68.

Scholtissek C (1994) Molecular biological background of the species and organ specifity of influenza A viruses. Angew Chem Int Ed 25:47–56

69.

Zamarin D, Ortigoza MB, Palese P (2006) Influenza A virus PB1-F2 protein contributes to viral pathogenesis in mice. J Virol 80:7976–7983PubMedCrossRef

70.

Chen W, Calvo PA, Malide D, Gibbs J, Schubert U, Bacik I, Basta S, O’Neill R, Schickli J, Palese P, Henklein P, Bennink JR, Yewdell JW (2001) A novel influenza A virus mitochondrial protein that induces cell death. Nat Med 7:1306–1312PubMedCrossRef

71.

Mills CE, Robins JM, Bergstrom CT, Lipsitch M (2006) Pandemic influenza: risk of multiple introductions and the need to prepare for them. PLoS Med 3:0001–0005CrossRef

72.

Doerr HW, Varwig D, Allwinn R, Cinatl J Jr (2006) Will the next human influenza pandemic be caused by the virus of the avian flu A/H5N1? Arguments pro and counter. Med Microbiol Immunol (Berl) 195:45–47CrossRef

Title: The threat of avian influenza A (H5N1). Part I: epidemiologic concerns and virulence determinants
Authors: Jindrich Cinatl Jr
Martin Michaelis
Hans W. Doerr
Publication date: 01-12-2007
Publisher: Springer-Verlag
Published in: Medical Microbiology and Immunology / Issue 4/2007
Print ISSN: 0300-8584
Electronic ISSN: 1432-1831
DOI: https://doi.org/10.1007/s00430-007-0042-5

ACC 2024 Congress Coverage

Heart Failure Video

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

The threat of avian influenza A (H5N1). Part I: epidemiologic concerns and virulence determinants

Abstract

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 4/2007

The threat of avian influenza A (H5N1). Part III: antiviral therapy

Hepatitis B virus genotype E surface antigen detection with different immunoassays and diagnostic impact of mutations in the preS/S gene

The threat of avian influenza A (H5N1). Part IV: development of vaccines

CCR5 and CCR3 expression on T CD3+ lymphocytes from HIV/Leishmania co-infected subjects

Generation of genetic engineering monoclonal antibodies against prion protein

The threat of avian influenza a (H5N1): part II: Clues to pathogenicity and pathology

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page