Browse > Article
http://dx.doi.org/10.7845/kjm.2018.8044

Inferring transmission routes of avian influenza during the H5N8 outbreak of South Korea in 2014 using epidemiological and genetic data  

Choi, Sang Chul (Department of Biotechnology, Sungshin Women's University)
Publication Information
Korean Journal of Microbiology / v.54, no.3, 2018 , pp. 254-265 More about this Journal
Abstract
Avian influenza recently damaged the poultry industry, which suffered a huge economic loss reaching billions of U.S. dollars in South Korea. Transmission routes of the pathogens would help plan to control and limit the spread of the devastating biological tragedy. Phylogenetic analyses of pathogen's DNA sequences could sketch transmission trees relating hosts with directed edges. The last decade has seen the methodological development of inferring transmission trees using epidemiological as well as genetic data. Here, I reanalyzed the DNA sequence data that had originated in the highly pathogenic avian influenza H5N8 outbreak of South Korea in 2014. The H5N8 viruses spread geographically contiguously from the origin of the outbreak, Jeonbuk. The Jeonbuk origin viruses were known to spread to four provinces neighboring Jeonbuk. I estimated the transmission tree of the host domestic and migratory wild birds after combining multiple runs of Markov chain Monte Carlo using a Bayesian method for inferring transmission trees. The estimated transmission tree, albeit with a rather large uncertainty in the directed edges, showed that the viruses spread from Jeonbuk through Chungnam to Gyeonggi. Domestic birds of breeder or broiler ducks were estimated to appear to be at the terminal nodes of the transmission tree. This observation confirmed that migratory wild birds played an important role as one of the main infection mediators in the avian influenza H5N8 outbreak of South Korea in 2014.
Keywords
genomic epidemiology; influenza virus; Markov chain Monte Carlo; transmission tree;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Drummond AJ, Suchard MA, Xie D, and Rambaut A. 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969-1973.   DOI
2 Edgar RC. 2004. MUSCLE - a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5, 113.   DOI
3 Fouchier RAM, Munster V, Wallensten A, Bestebroer TM, Herfst S, Smith D, Rimmelzwaan GF, Olsen B, and Osterhaus ADME. 2005. Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J. Virol. 79, 2814-2822.   DOI
4 Hall M, Woolhouse M, and Rambaut A. 2015. Epidemic reconstruction in a phylogenetics framework: transmission trees as partitions of the node set. PLoS Comput. Biol. 11, e1004613.   DOI
5 Hill SC, Lee YJ, Song BM, Kang HM, Lee EK, Hanna A, Gilbert M, Brown IH, and Pybus OG. 2015. Wild waterfowl migration and domestic duck density shape the epidemiology of highly pathogenic H5N8 influenza in the Republic of Korea. Infect. Genet. Evol. 34, 267-277.   DOI
6 Hinshaw VS, Webster RG, and Rodriguez RJ. 1979. Influenza A viruses: combinations of hemagglutinin and neuraminidase subtypes isolated from animals and other sources. Arch. Virol. 62, 281-290.   DOI
7 Janies D, Hill AW, Guralnick R, Habib F, Waltari E, and Wheeler WC. 2007. Genomic analysis and geographic visualization of the spread of avian influenza (H5N1). Syst. Biol. 56, 321-329.   DOI
8 Jeong J, Kang HM, Lee EK, Song BM, Kwon YK, Kim HR, Choi KS, Kim JY, Lee HJ, Moon OK, et al. 2014. Highly pathogenic avian influenza virus (H5N8) in domestic poultry and its relationship with migratory birds in South Korea during 2014. Vet. Microbiol. 173, 249-257.   DOI
9 Kim HK, Jeong DG, and Yoon SW. 2017a. Recent outbreaks of highly pathogenic avian influenza viruses in South Korea. Clin. Exp. Vaccine Res. 6, 95-103.   DOI
10 Kang HM, Jeong OM, Kim MC, Kwon JS, Paek MR, Choi JG, Lee EK, Kim YJ, Kwon JH, and Lee YJ. 2010. Surveillance of avian influenza virus in wild bird fecal samples from South Korea, 2003-2008. J. Wildl. Dis. 46, 878-888.   DOI
11 Kim HR, Lee YJ, Park CK, Oem JK, Lee OS, Kang HM, Choi JG, and Bae YC. 2012. Highly pathogenic avian influenza (H5N1) outbreaks in wild birds and poultry, South Korea. Emerg. Infect. Dis. 18, 480-483.   DOI
12 Kim YI, Park SJ, Kwon HI, Kim EH, Si YJ, Jeong JH, Lee IW, Nguyen HD, Kwon JJ, Choi WS, et al. 2017b. Genetic and phylogenetic characterizations of a novel genotype of highly pathogenic avian influenza (HPAI) H5N8 viruses in 2016/2017 in South Korea. Infect. Genet. Evol. 53, 56-67.   DOI
13 Ku KB, Park EH, Yum J, Kim JA, Oh SK, and Seo SH. 2014. Highly pathogenic avian influenza A(H5N8) virus from waterfowl, South Korea, 2014. Emerg. Infect. Dis. 20, 1587-1588.   DOI
14 Kwon HI, Song MS, Pascua PNQ, Baek YH, Lee JH, Hong SP, Rho JB, Kim JK, Poo H, Kim CJ, et al. 2011. Genetic characterization and pathogenicity assessment of highly pathogenic H5N1 avian influenza viruses isolated from migratory wild birds in 2011, South Korea. Virus Res. 160, 305-315.   DOI
15 Nagy A, Vostinakova V, Pindova Z, Hornickova J, Cernikova L, Sedlak K, Mojzis M, Dirbakova Z, and Machova J. 2009. Molecular and phylogenetic analysis of the H5N1 avian influenza virus caused the first highly pathogenic avian influenza outbreak in poultry in the Czech Republic in 2007. Vet. Microbiol. 133, 257-263.   DOI
16 Lee DH, Lee HJ, Lee YN, Park JK, Lim TH, Kim MS, Youn HN, Lee JB, Park SY, Choi IS, et al. 2011. Evidence of intercontinental transfer of North American lineage avian influenza virus into Korea. Infect. Genet. Evol. 11, 232-236.   DOI
17 Li KS, Guan Y, Wang J, Smith GJD, Xu KM, Duan L, Rahardjo AP, Puthavathana P, Buranathai C, Nguyen TD, et al. 2004. Genesis of a highly pathogenic and potentially pandemic H5N1 influenza virus in eastern Asia. Nature 430, 209-213.   DOI
18 Liu J, Xiao H, Lei F, Zhu Q, Qin K, Zhang XW, Zhang XL, Zhao D, Wang G, Feng Y, et al. 2005. Highly pathogenic H5N1 influenza virus infection in migratory birds. Science 309, 1206-1206.   DOI
19 Mahardika GN, Jonas M, Murwijati T, Fitria N, Suartha IN, Suartini IGAA, and Wibawan IWT. 2016. Molecular analysis of hemagglutinin-1 fragment of avian influenza H5N1 viruses isolated from chicken farms in Indonesia from 2008 to 2010. Vet. Microbiol. 186, 52-58.   DOI
20 Morelli MJ, Thebaud G, Chadoeuf J, King DP, Haydon DT, and Soubeyrand S. 2012. A Bayesian inference framework to reconstruct transmission trees using epidemiological and genetic data. PLoS Comput. Biol. 8, e1002768.   DOI
21 Nair H, Brooks WA, Katz M, Roca A, Berkley JA, Madhi SA, Simmerman JM, Gordon A, Sato M, Howie S, et al. 2011. Global burden of respiratory infections due to seasonal influenza in young children: a systematic review and meta-analysis. Lancet 378, 1917-1930.   DOI
22 Shin JH, Woo C, Wang SJ, Jeong J, An IJ, Hwang JK, Jo SD, Yu SD, Choi K, Chung HM, et al. 2015. Prevalence of avian influenza virus in wild birds before and after the HPAI H5N8 outbreak in 2014 in South Korea. J. Microbiol. 53, 475-480.   DOI
23 Nguyen T, Rivailler P, Davis CT, Thi Hoa D, Balish A, Hoang Dang N, Jones J, Thi Vui D, Simpson N, Thu Huong N, et al. 2012. Evolution of highly pathogenic avian influenza (H5N1) virus populations in Vietnam between 2007 and 2010. Virology 432, 405-416.   DOI
24 Olsen B, Munster VJ, Wallensten A, Waldenstrom J, Osterhaus ADME, and Fouchier RAM. 2006. Global patterns of influenza a virus in wild birds. Science 312, 384-388.   DOI
25 Osmani MG, Ward MP, Giasuddin M, Islam MR, and Kalam A. 2014. The spread of highly pathogenic avian influenza (subtype H5N1) clades in Bangladesh, 2010 and 2011. Prev. Vet. Med. 114, 21-27.   DOI
26 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. USA 109, 15066-15071.   DOI
27 Reperant LA, Kuiken T, and Osterhaus ADME. 2012. Influenza viruses: from birds to humans. Hum. Vaccin Immunother. 8, 7-16.   DOI
28 Sakoda Y, Ito H, Uchida Y, Okamatsu M, Yamamoto N, Soda K, Nomura N, Kuribayashi S, Shichinohe S, Sunden Y, et al. 2012. Reintroduction of H5N1 highly pathogenic avian influenza virus by migratory water birds, causing poultry outbreaks in the 2010-2011 winter season in Japan. J. Gen. Virol. 93, 541-550.   DOI
29 Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, and Ideker T. 2003. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504.   DOI
30 Shu Y and McCauley J. 2017. GISAID: Global initiative on sharing all influenza data - from vision to reality. Euro Surveill. 22, 1-3.
31 Sonnberg S, Webby RJ, and Webster RG. 2013. Natural history of highly pathogenic avian influenza H5N1. Virus Res. 178, 63-77.   DOI
32 Theary R, San S, Davun H, Allal L, and Lu H. 2012. New outbreaks of H5N1 highly pathogenic avian influenza in domestic poultry and wild birds in Cambodia in 2011. Avian Dis. 56, 861-864.   DOI
33 Tian H, Zhou S, Dong L, Van Boeckel TP, Cui Y, Newman SH, Takekawa JY, Prosser DJ, Xiao X, Wu Y, et al. 2015. Avian influenza H5N1 viral and bird migration networks in Asia. Proc. Natl. Acad. Sci. USA 112, 172-177.   DOI
34 Bouckaert R, Heled J, Kuhnert D, Vaughan T, Wu CH, Xie D, Suchard MA, Rambaut A, and Drummond AJ. 2014. BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 10, e1003537.   DOI
35 World Health Organization. 1971. A revised system of nomenclature for influenza viruses. Bull. World Health Organ. 45, 119-124.
36 Ypma RJF, van Ballegooijen WM, and Wallinga J. 2013. Relating phylogenetic trees to transmission trees of infectious disease outbreaks. Genetics 195, 1055-1062.   DOI
37 Uchida Y, Suzuki Y, Shirakura M, Kawaguchi A, Nobusawa E, Tanikawa T, Hikono H, Takemae N, Mase M, Kanehira K, et al. 2012. Genetics and infectivity of H5N1 highly pathogenic avian influenza viruses isolated from chickens and wild birds in Japan during 2010-11. Virus Res. 170, 109-117.   DOI
38 Alexander DJ. 2007. An overview of the epidemiology of avian influenza. Vaccine 25, 5637-5644.   DOI
39 Alkhamis MA, Moore BR, and Perez AM. 2015. Phylodynamics of H5N1 highly pathogenic avian influenza in Europe, 2005-2010: potential for molecular surveillance of new outbreaks. Viruses 7, 3310-3328.   DOI
40 Baek YH, Pascua PNQ, Song MS, Park KJ, Kwon HI, Lee JH, Kim SY, Moon HJ, Kim CJ, and Choi YK. 2010. Surveillance and characterization of low pathogenic H5 avian influenza viruses isolated from wild migratory birds in Korea. Virus Res. 150, 119-128.   DOI
41 Chanock RH, Cockburn WC, Davenport FM, Dowdle WR, de St Groth SF, Fukumi H, Kilbourne ED, Schild GC, Schulman JL, Sohier R, et al. 1972. A revised system of influenza virus nomenclature: A report of the WHO study group on classification. Virology 47, 854-856.   DOI
42 Cottam EM, Thebaud G, Wadsworth J, Gloster J, Mansley L, Paton DJ, King DP, and Haydon DT. 2008. Integrating genetic and epidemiological data to determine transmission pathways of foot-and-mouth disease virus. Proc. R Soc. B 275, 887-895.   DOI
43 de Jong JC, Claas ECJ, Osterhaus ADME, Webster RG, and Lim WL. 1997. A pandemic warning? Nature 389, 554.
44 Didelot X, Fraser C, Gardy J, and Colijn C. 2017. Genomic infectious disease epidemiology in partially sampled and ongoing outbreaks. Mol. Biol. Evol. 34, 997-1007.
45 Didelot X, Gardy J, and Colijn C. 2014. Bayesian inference of infectious disease transmission from whole-genome sequence data. Mol. Biol. Evol. 31, 1869-1879.   DOI