Bayesian inference reveals host-specific contributions to the epidemic expansion of influenza A H5N1

Molecular Biology and Evolution

Volumn 32, Issue 12, 2015, Pages 3264-3275

  Trovão, Nídia Sequeira ^a   Suchard, Marc A ^b,c   Baele, Guy ^a   Gilbert, Marius ^d,e   Lemey, Philippe ^a  

^a REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^e FNRS   (Belgium)

Author keywords

Bayesian inference; Disease ecology; H5N1; Phylogeography; Viral evolution

Indexed keywords

VIRUS HEMAGGLUTININ; VIRUS SIALIDASE;

ARTICLE; ASIA; BAYES THEOREM; CENTRAL ASIAN; CHINA; EPIDEMIC; GENE SEQUENCE; HOST PATHOGEN INTERACTION; HOST RANGE; INFLUENZA A (H5N1); INFLUENZA A VIRUS (H5N1); MIGRATION; MOLECULAR EVOLUTION; NONHUMAN; PERSISTENT VIRUS INFECTION; PHASIANIDAE; RUSSIAN FEDERATION; VIRUS TRANSMISSION; WATERFOWL; ANIMAL; BIRD; DNA SEQUENCE; EVOLUTION; GENETICS; INFLUENZA IN BIRDS; PATHOGENICITY; PATHOLOGY; PHYLOGEOGRAPHY; PHYSIOLOGY; POPULATION MIGRATION; PROCEDURES; VIROLOGY;

ANIMAL MIGRATION; ANIMALS; ASIA; BAYES THEOREM; BIOLOGICAL EVOLUTION; BIRDS; CHINA; DISEASE OUTBREAKS; HOST-PATHOGEN INTERACTIONS; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA IN BIRDS; PHYLOGEOGRAPHY; RUSSIA; SEQUENCE ANALYSIS, DNA;

EID: 84977958758     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msv185     Document Type: Article

References (65)

1. Ayres DL, Darling A, Zwickl DJ, Beerli P, Holder MT, Lewis PO, Huelsenbeck JP, Ronquist F, Swofford DL, Cummings MP, et al. 2012. Beagle: an application programming interface and highperformance computing library for statistical phylogenetics. Syst Biol. 61(1):170-173.
2. Baele G, Lemey P. 2013. Bayesian evolutionary model testing in the phylogenomics era: matching model complexity with computational efficiency. Bioinformatics 29(16):1970-1979.
3. Baele G, Lemey P, Bedford T, Rambaut A, SuchardMA, Alekseyenko AV. 2012. Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty. Mol Biol Evol. 29(9):2157-2167.
4. Baele G, Lemey P, Vansteelandt S. 2013. Make the most of your samples: Bayes factor estimators for high-dimensional models of sequence evolution. BMC Bioinformatics 14:85.
5. Bedford T, Suchard MA, Lemey P, Dudas G, Gregory V, Hay AJ, McCauley JW, Russell CA, Smith DJ, Rambaut A. 2014. Integrating influenza antigenic dynamics with molecular evolution. Elife 3:e01914.
6. Bett B, Henning J, Abdu P, Okike I, Poole J, Young J, Randolph TF, Perry BD. 2014. Transmission rate and reproductive number of the H5N1 highly pathogenic avian influenza virus during the December 2005-July 2008 epidemic in Nigeria. Transbound Emerg Dis. 61(1):60-68.
7. Bielejec F, Rambaut A, Suchard MA, Lemey P. 2011. SPREAD: spatial phylogenetic reconstruction of evolutionary dynamics. Bioinformatics 27(20):2910-2912.
8. Bloomquist EW, Lemey P, Suchard MA. 2010. Three roads diverged? Routes to phylogeographic inference. Trends Ecol Evol. 25(11):626-632.
9. Bouckaert R, Lemey P, Dunn M, Greenhill SJ, Alekseyenko AV, Drummond AJ, Gray RD, Suchard MA, Atkinson QD. 2012. Mapping the origins and expansion of the Indo-European language family. Science 337(6097):957-960.
10. Cappelle J, Zhao D, Gilbert M, Nelson MI, Newman SH, Takekawa JY, Gaidet N, Prosser DJ, Liu Y, Li P, et al. 2014. Risks of avian influenza transmission in areas of intensive free-ranging duck production with wild waterfowl. Ecohealth 11:109-119.
11. Chen H, Smith GJD, Li KS, Wang J, Fan XH, Rayner JM, Vijaykrishna D, Zhang JX, Zhang LJ, Guo CT, et al. 2006. Establishment of multiple sublineages of H5N1 influenza virus in Asia: implications for pandemic control. Proc Natl Acad Sci U S A. 103(8):2845-2850.
12. Cowling BJ, Jin L, Lau EHY, Liao Q, Wu P, Jiang H, Tsang TK, Zheng J, Fang VJ, Chang Z, et al. 2013. Comparative epidemiology of human infections with avian influenza A H7N9 and H5N1 viruses in China: a population-based study of laboratory-confirmed cases. Lancet 382(9887):129-137.
13. Edwards CJ, Suchard MA, Lemey P, Welch JJ, Barnes I, Fulton TL, Barnett R, O'Connell TC, Coxon P, Monaghan N, et al. 2011. Ancient hybridization and an Irish origin for the modern polar bear matriline. Curr Biol. 21(15):1251-1258.
14. Faria NR, Suchard MA, Rambaut A, Lemey P. 2011. Toward a quantitative understanding of viral phylogeography. Curr Opin Virol. 1(5):423-429.
15. Faria NR, Suchard MA, Rambaut A, Streicker DG, Lemey P. 2013. Simultaneously reconstructing viral cross-species transmission history and identifying the underlying constraints. Philos Trans R Soc Lond B Biol Sci. 368(1614):20120196.
16. Fouchier RAM, Munster V, Wallensten A, Bestebroer TM, Herfst S, Smith D, Rimmelzwaan GF, Olsen B, Osterhaus ADME. 2005. Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J Virol. 79(5):2814-2822.
17. Fournié G, Guitian J, Desvaux S, Cuong VC, Dung DH, Pfeiffer DU, Mangtani P, Ghani AC. 2013. Interventions for avian influenza A (H5N1) risk management in live bird market networks. Proc Natl Acad Sci U S A. 110(22):9177-9182.
18. GilbertM, Golding N, Zhou H, Wint GRW, Robinson TP, Tatem AJ, Lai S, Zhou S, Jiang H, Guo D, et al. 2014. Predicting the risk of avian influenza A H7N9 infection in live-poultry markets across Asia. Nat Commun. 5:4116.
19. Gilbert M, Jambal L, Karesh WB, Fine A, Shiilegdamba E, Dulam P, Sodnomdarjaa R, Ganzorig K, Batchuluun D, Tseveenmyadag N, et al. 2012. Highly pathogenic avian influenza virus among wild birds in Mongolia. PLoS One 7(9):e44097.
20. Gilbert M, Newman SH, Takekawa JY, Loth L, Biradar C, Prosser DJ, Balachandran S, SubbaRao MV, Mundkur T, Yan B, et al. 2010. Flying over an infected landscape: distribution of highly pathogenic avian influenza H5N1 risk in South Asia and satellite tracking of wild waterfowl. Ecohealth 7(4):448-458.
21. Gilbert M, Xiao X, Chaitaweesub P, Kalpravidh W, Premashthira S, Boles S, Slingenbergh J. 2007. Avian influenza, domestic ducks and rice agriculture in Thailand. Agric Ecosyst Environ. 119:409-415.
22. GilbertM, Xiao X, Domenech J, Lubroth J, Martin V, Slingenbergh J. 2006. Anatidae migration in the western Palearctic and spread of highly pathogenic avian influenza H5NI virus. Emerg Infect Dis. 12(11):1650-1656.
23. Han J, JinM, Zhang P, Liu J, Wang L, Wen D, Wu X, Liu G, Zou Y, Lv X, et al. 2013. Epidemiological link between exposure to poultry and all influenza A(H7N9) confirmed cases in Huzhou city, China, March to May 2013. Euro Surveill. 18(20).
24. Herfst S, Schrauwen EJA, Linster M, Chutinimitkul S, deWit E, Munster VJ, Sorrell EM, Bestebroer TM, Burke DF, Smith DJ, et al. 2012. Airborne transmission of influenza A/H5N1 virus between ferrets. Science 336(6088):1534-1541.
25. Hill NJ, Takekawa JY, Ackerman JT, Hobson KA, Herring G, Cardona CJ, Runstadler JA, Boyce WM. 2012. Migration strategy affects avian influenza dynamics in mallards (Anas platyrhynchos). Mol Ecol. 21(24):5986-5999.
26. Holmes EC. 2008. Evolutionary history and phylogeography of human viruses. Annu Rev Microbiol. 62:307-328.
27. Hulse-Post DJ, Sturm-Ramirez KM, Humberd J, Seiler P, Govorkova EA, Krauss S, Scholtissek C, Puthavathana P, Buranathai C, Nguyen TD, et al. 2005. Role of domestic ducks in the propagation and biological evolution of highly pathogenic H5N1 influenza viruses in Asia. Proc Natl Acad Sci U S A. 102(30):10682-10687.
28. Katoh K, Toh H. 2008. Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform. 9(4):286-298.
29. Keawcharoen J, van Riel D, van Amerongen G, Bestebroer T, Beyer WE, van Lavieren R, Osterhaus ADME, Fouchier RAM, Kuiken T. 2008. Wild ducks as long-distance vectors of highly pathogenic avian influenza virus (H5N1). Emerg Infect Dis. 14(4):600-607.
30. Kim J-K, Negovetich NJ, Forrest HL, Webster RG. 2009. Ducks: the "Trojan horses" of H5N1 influenza. Influenza Other Respir Viruses. 3(4):121-128.
31. Lam TT-Y, Wang J, Shen Y, Zhou B, Duan L, Cheung C-L, Ma C, Lycett SJ, Leung CY-H, Chen X, et al. 2013. The genesis and source of the H7N9 influenza viruses causing human infections in china. Nature 502(7470):241-244.
32. Lemey P, Rambaut A, Bedford T, Faria N, Bielejec F, Baele G, Russell CA, Smith DJ, Pybus OG, Brockmann D, et al. 2014. Unifying viral genetics and human transportation data to predict the global transmission dynamics of human influenza H3N2. PLoS Pathog. 10(2):e1003932.
33. Lemey P, Rambaut A, Drummond AJ, Suchard MA. 2009. Bayesian phylogeography finds its roots. PLoS Comput Biol. 5(9):e1000520.
34. Lemey P, Rambaut A, Welch JJ, SuchardMA. 2010. Phylogeography takes a relaxed random walk in continuous space and time. Mol Biol Evol. 27(8):1877-1885.
35. Li FCK, Choi BCK, Sly T, Pak AWP. 2008. Finding the real case-fatality rate of H5N1 avian influenza. J Epidemiol Community Health. 62(6): 555-559.
36. Li Q, Zhou L, Zhou M, Chen Z, Li F, Wu H, Xiang N, Chen E, Tang F, Wang D, et al. 2014. Epidemiology of human infections with avian influenza A(H7N9) virus in China. N Engl J Med. 370:520-532.
37. Mather AE, Reid SWJ, Maskell DJ, Parkhill J, Fookes MC, Harris SR, Brown DJ, Coia JE, Mulvey MR, Gilmour MW, et al. 2013. Distinguishable epidemics of multidrug-resistant Salmonella typhimurium dt104 in different hosts. Science 341(6153):1514-1517.
38. Minin VN, SuchardMA. 2008. Counting labeled transitions in continuoustime Markov models of evolution. J Math Biol. 56(3):391-412.
39. Nelson MI, Holmes EC. 2007. The evolution of epidemic influenza. Nat Rev Genet. 8(3):196-205.
40. Nylinder S, Lemey P, DeBruyn M, Suchard MA, Pfeil BE, Walsh N, Anderberg AA. 2014. On the biogeography of Centipeda: a species-tree diffusion approach. Syst Biol. 63(2):178-191.
41. Pagel M, Meade A, Barker D. 2004. Bayesian estimation of ancestral character states on phylogenies. Syst Biol. 53(5):673-684.
42. Pfeiffer DU, Otte MJ, Roland-Holst D, Zilberman D. 2013. A one health perspective on HPAI H5N1 in the Greater Mekong sub-region. Comp Immunol Microbiol Infect Dis. 36:309-319.
43. Poovorawan Y, Pyungporn S, Prachayangprecha S, Makkoch J. 2013.Global alert to avian influenza virus infection: from H5N1 to H7N9. Pathog Glob Health. 107(5):217-223.
44. Pybus OG, Rambaut A. 2009. Evolutionary analysis of the dynamics of viral infectious disease. Nat Rev Genet. 10(8):540-550.
45. Pybus OG, Suchard MA, Lemey P, Bernardin FJ, Rambaut A, Crawford FW, Gray RR, Arinaminpathy N, Stramer SL, Busch MP, et al. 2012. Unifying the spatial epidemiology and molecular evolution of emerging epidemics. Proc Natl Acad Sci U S A. 109(37):15066-15071.
46. Russell CA, Fonville JM, Brown AEX, Burke DF, Smith DL, James SL, Herfst S, van Boheemen S, Linster M, Schrauwen EJ, et al. 2012. The potential for respiratory droplet-transmissible A/H5N1 influenza virus to evolve in a mammalian host. Science 336(6088):1541-1547.
47. Songserm T, Jam-on R, Sae-Heng N, Meemak N, Hulse-Post DJ, Sturm-Ramirez KM, Webster RG. 2006. Domestic ducks and H5N1 influenza epidemic, Thailand. Emerg Infect Dis. 12(4):575-581.
48. Suchard MA, Rambaut A. 2009. Many-core algorithms for statistical phylogenetics. Bioinformatics 25(11):1370-1376.
49. Suchard MA, Weiss RE, Sinsheimer JS. 2005. Models for estimating Bayes factors with applications to phylogeny and tests of monophyly. Biometrics 61(3):665-673.
50. Tian G, Zhang S, Li Y, Bu Z, Liu P, Zhou J, Li C, Shi J, Yu K, Chen H. 2005. Protective efficacy in chickens, geese and ducks of an H5N1-inactivated vaccine developed by reverse genetics. Virology 341(1):153-162.
51. Tian H, Zhou S, Dong L, VanBoeckel TP, Cui Y, Wu Y, Cazelles B, Huang S, Yang R, Grenfell BT, et al. 2015. Avian influenza H5N1 viral and bird migration networks in Asia. Proc Natl Acad Sci U S A. 112(1):172-177.
52. To KKW, Chan JFW, Chen H, Li L, Yuen K-Y. 2013. The emergence of influenza A H7N9 in human beings 16 years after influenza A H5N1: a tale of two cities. Lancet Infect Dis. 13(9):809-821.
53. Tong S, Li Y, Rivailler P, Conrardy C, Castillo DAA, Chen L-M, Recuenco S, Ellison JA, Davis CT, York IA, et al. 2012. A distinct lineage of influenza A virus from bats. Proc Natl Acad Sci U S A. 109(11):4269-4274.
54. Tong S, Zhu X, Li Y, Shi M, Zhang J, Bourgeois M, Yang H, Chen X, Recuenco S, Gomez J, et al. 2013. New world bats harbor diverse influenza A viruses. PLoS Pathog. 9(10):e1003657.
55. Vrancken B, Rambaut A, Suchard MA, Drummond A, Baele G, Derdelinckx I, VanWijngaerden E, Vandamme A-M, VanLaethem K, Lemey P. 2014. The genealogical population dynamics of HIV-1 in a large transmission chain: bridging within and among host evolutionary rates. PLoS Comput Biol. 10(4):e1003505.
56. Wallace RG, Fitch WM. 2008. Influenza A H5N1 immigration is filtered out at some international borders. PLoS One 3(2):e1697.
57. Wallace RG, Hodac H, Lathrop RH, Fitch WM. 2007. A statistical phylogeography of influenza A H5N1. Proc Natl Acad Sci U S A. 104(11):4473-4478.
58. Wang C, Luo J, Wang J, SuW, Gao S, ZhangM, Xie L, Ding H, Liu S, Liu X, et al. 2014. Novel human H7N9 influenza virus in China. Integr Zool. 9(3):372-375.
59. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. 1992. Evolution and ecology of influenza A viruses. Microbiol Rev. 56(1):152-179.
60. Webster RG, Peiris M, Chen H, Guan Y. 2006. H5N1 outbreaks and enzootic influenza. Emerg Infect Dis. 12(1):3-8.
61. WHO. 2015. Cumulative number of confirmed human cases for avian influenza A(H5N1) reported to WHO. Geneva (Switzerland): World Health Organization.
62. Worobey M, Han G-Z, Rambaut A. 2014. A synchronized global sweep of the internal genes of modern avian influenza virus. Nature. 508:254-257.
63. Xiao X, Gilbert M, Slingenbergh J, Lei F, Boles S. 2007. Remote sensing, ecological variables, and wild bird migration related to outbreaks of highly pathogenic H5N1 avian influenza. J Wildl Dis. 43(1):40-47.
64. Xu X, Subbarao, Cox NJ, Guo Y. 1999. Genetic characterization of the pathogenic influenza A/Goose/Guangdong/1/96 (H5N1) virus: similarity of its hemagglutinin gene to those of H5N1 viruses from the 1997 outbreaks in Hong Kong. Virology 261(1):15-19.
65. Yee KS, Carpenter TE, Cardona CJ. 2009. Epidemiology of H5N1 avian influenza. Comp Immunol Microbiol Infect Dis. 32(4):325-340.