#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Evolutionary Analysis of Inter-Farm Transmission Dynamics in a Highly Pathogenic Avian Influenza Epidemic


Phylogenetic studies have largely contributed to better understand the emergence, spread and evolution of highly pathogenic avian influenza during epidemics, but sampling of genetic data has never been detailed enough to allow mapping of the spatiotemporal spread of avian influenza viruses during a single epidemic. Here, we present genetic data of H7N7 viruses produced from 72% of the poultry farms infected during the 2003 epidemic in the Netherlands. We use phylogenetic analyses to unravel the pathways of virus transmission between farms and between infected areas. In addition, we investigated the evolutionary processes shaping viral genetic diversity, and assess how they could have affected our phylogenetic analyses. Our results show that the H7N7 virus was characterized by a high level of genetic diversity driven mainly by a high neutral substitution rate, purifying selection and limited positive selection. We also identified potential reassortment in the three genes that we have tested, but they had only a limited effect on the resolution of the inter-farm transmission network. Clonal sequencing analyses performed on six farm samples showed that at least one farm sample presented very complex virus diversity and was probably at the origin of chronological anomalies in the transmission network. However, most virus sequences could be grouped within clearly defined and chronologically sound clusters of infection and some likely transmission events between farms located 0.8–13 Km apart were identified. In addition, three farms were found as most likely source of virus introduction in distantly located new areas. These long distance transmission events were likely facilitated by human-mediated transport, underlining the need for strict enforcement of biosafety measures during outbreaks. This study shows that in-depth genetic analysis of virus outbreaks at multiple scales can provide critical information on virus transmission dynamics and can be used to increase our capacity to efficiently control epidemics.


Vyšlo v časopise: Evolutionary Analysis of Inter-Farm Transmission Dynamics in a Highly Pathogenic Avian Influenza Epidemic. PLoS Pathog 7(6): e32767. doi:10.1371/journal.ppat.1002094
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002094

Souhrn

Phylogenetic studies have largely contributed to better understand the emergence, spread and evolution of highly pathogenic avian influenza during epidemics, but sampling of genetic data has never been detailed enough to allow mapping of the spatiotemporal spread of avian influenza viruses during a single epidemic. Here, we present genetic data of H7N7 viruses produced from 72% of the poultry farms infected during the 2003 epidemic in the Netherlands. We use phylogenetic analyses to unravel the pathways of virus transmission between farms and between infected areas. In addition, we investigated the evolutionary processes shaping viral genetic diversity, and assess how they could have affected our phylogenetic analyses. Our results show that the H7N7 virus was characterized by a high level of genetic diversity driven mainly by a high neutral substitution rate, purifying selection and limited positive selection. We also identified potential reassortment in the three genes that we have tested, but they had only a limited effect on the resolution of the inter-farm transmission network. Clonal sequencing analyses performed on six farm samples showed that at least one farm sample presented very complex virus diversity and was probably at the origin of chronological anomalies in the transmission network. However, most virus sequences could be grouped within clearly defined and chronologically sound clusters of infection and some likely transmission events between farms located 0.8–13 Km apart were identified. In addition, three farms were found as most likely source of virus introduction in distantly located new areas. These long distance transmission events were likely facilitated by human-mediated transport, underlining the need for strict enforcement of biosafety measures during outbreaks. This study shows that in-depth genetic analysis of virus outbreaks at multiple scales can provide critical information on virus transmission dynamics and can be used to increase our capacity to efficiently control epidemics.


Zdroje

1. CattoliGMonneIFusaroAJoannisTMLombinLH 2009 Highly pathogenic avian influenza virus subtype H5N1 in Africa: a comprehensive phylogenetic analysis and molecular characterization of isolates. PLoS ONE 4 e4842

2. LamTT-YHonC-CPybusOGKosakovsky PondSLWongRT-Y 2008 Evolutionary and transmission dynamics of reassortant H5N1 influenza virus in Indonesia. PLoS Pathog 4 e1000130

3. LemeyPRambautADrummondAJSuchardMA 2009 Bayesian phylogeography finds its roots. PLoS Comput Biol 5 e1000520

4. HolmesECGrenfellBT 2009 Discovering the phylodynamics of RNA viruses. PLoS Comput Biol 5 e1000505

5. CottamEMThebaudGWadsworthJGlosterJMansleyL 2008 Integrating genetic and epidemiological data to determine transmission pathways of foot-and-mouth disease virus. Proc Biol Sci 275 887 895

6. StegemanABoumaAElbersARWde JongMCMNodelijkG 2004 Avian influenza A virus (H7N7) epidemic in the Netherlands in 2003: course of the epidemic and effectiveness of control measures. J Infect Dis 190 2088 2095

7. KoopmansMWilbrinkBConynMNatropGvan der NatH 2004 Transmission of H7N7 avian influenza A virus to human beings during a large outbreak in commercial poultry farms in the Netherlands. Lancet 363 587 593

8. FouchierRAMSchneebergerPMRozendaalFWBroekmanJMKeminkSAG 2004 Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome. Proc Natl Acad Sci U S A 101 1356 1361

9. BoenderGJHagenaarsTJBoumaANodelijkGElbersARW 2007 Risk maps for the spread of highly pathogenic avian influenza in poultry. PLoS Comput Biol 3 e71

10. de WitEMunsterVJvan RielDBeyerWEPRimmelzwaanGF 2010 Molecular determinants of adaptation of highly pathogenic avian influenza H7N7 viruses to efficient replication in the human host. J Virol 84 1597 1606

11. HeathLvan der WaltEVarsiniAMartinDP 2006 Recombination patterns in aphthoviruses mirror those found in other picornaviruses. J Virol 80 11827 11832

12. DrummondAJNichollsGKRodrigoAGSolomonW 2002 Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. Genetics 161 1307 1320

13. DrummondAJRambautA 2007 BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7 214

14. SuchardMAWeissRESinsheimerJS 2001 Bayesian selection of continuous-time Markov Chain evolutionary models. Mol Biol Evol 18 1001 1013

15. DrummondAJHoSYWPhillipsMJRambautA 2006 Relaxed phylogenetics and dating with confidence. PLoS Biol 4 e88

16. BandeltHJForsterPRohlA 1999 Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16 37 48

17. Network 4.516: Free phylogenetic network software. Available: http://www.fluxus-engineering.com. Accessed on 11 August 2010.

18. YangZ 1997 PAML: a program package for phylogenetic analysis by maximum likelihood. Comp Appl Biosci 13 555 556

19. YangZWongWSWNielsenR 2005 Bayes Empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 22 1107 1118

20. Kosakovsky PondSLFrostSDW 2005 Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 22 1208 1222

21. PerdueMLLatimerJWCrawfordJM 1995 A novel carbohydrate addition site on the hemagglutinin protein of a highly pathogenic H7 subtype avian influenza virus. Virology 213 276 281

22. SalimenMOCarrJKBurkeDSMcCutchanFE 1995 Identification of breakpoints in intergenotypic recombinants of HIV type 1 by bootscanning. AIDS Res Hum Retroviruses 11 1423 1425

23. ChenRHolmesEC 2006 Avian influenza virus exhibits rapid evolutionary dynamics. Mol Biol Evol 23 2336 2341

24. BosMEHVan BovenMNielenMBoumaAElbersARW 2007 Estimating the day of highly pathogenic avian influenza (H7N7) virus introduction into a poultry flock based on mortality data. Vet Res 38 493 504

25. IqbalMXiaoHBaillieGWarryAEssenSC 2009 Within-host variation of avian influenza viruses. Phil Trans R Soc Lond B Biol Sci 364 2739 2747

26. WangGPSherrill-MixSAChangKQuinceCBushmanFD 2010 Hepatitis C virus transmission bottlenecks analyzed by deep sequencing. J Virol 84 6218 6228

27. ErikssonNPachterLMitsuyaYRheeSWangC 2008 Viral population estimation using pyrosequencing. PLoS Comput Biol 4 e1000074

28. CilloniFToffanAGiannecchiniSClausiVAzziA 2010 Increased pathogenicity and shedding in chickens of a wild bird-origin low pathogenicity avian influenza virus of the H7N3 subtype following multiple in vivo passages in quail and turkey. Avian Dis 54 555 557

29. PillaiSPSPantin-JackwoodMYassineHMSaifYMLeeCW 2010 The high susceptibility of turkeys to influenza viruses of different origins implies their importance as potential intermediate hosts. Avian Dis 54 522 526

30. LebarbenchonCFeareCJRenaudFThomasFGauthier-ClercM 2010 Persistence of highly pathogenic avian influenza viruses in natural ecosystems. Emerg Infect Dis 16 1057 1062

31. YamamotoYNakamuraKYamadaMMaseM 2010 Persistence of avian influenza virus (H5N1) in feathers detached from bodies of infected domestic ducks. Appl Environ Microbiol 76 5496 5499

32. Domanska-BlicharzKMintaZSmietankaKMarcheSvan den BergT 2010 H5N1 high pathogenicity avian influenza virus survival in different types of water. Avian Dis 54 734 737

33. ThomasMEBoumaAEkkerHMFonkenAJMStegemanJA 2005 Risk factors for the introduction of high pathogenicity avian influenza virus into poultry farms during the epidemic in the Netherlands in 2003. Prev Vet Med 69 1 11

34. Bos MarianEHte BeestDEvan BovenMRobert-Du Ry van Beest HolleMMeijerA 2010 High probability of avian influenza virus (H7N7) transmission from poultry to humans active in disease control on infected farms. J Infect Dis 201 1390 1396

35. BavinckVBoumaAvan BovenMBosMEHStassenE 2009 The role of backyard poultry flocks in the epidemic of highly pathogenic avian influenza virus (H7N7) in the Netherlands in 2003. Prev Vet Med 88 247 254

36. HallTA 1999 BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Res 41 95 98

37. Kosakovsky PondSLFrostSDW 2005 Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21 2531 2533

38. SmithGJDVijaykrishnaDBahlJLycettSJWorobeyM 2009 Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459 1122 1125

39. RambautADrummondAJ 2007 Tracer v1.5.: MCMC trace analyses tool. Available: http://beast.bio.ed.ac.uk/Tracer. Accessed 11 August 2010

40. RambautA 2008 FigTree v.1.3.1.: Tree figure drawing tool. Available: http://tree.bio.ed.ac.uk/software/figtree. Accessed 11 August 2010

41. HuelsenbeckJPRonquistF 2001 MrBayes: bayesian inference of phylogeny. Bioinformatics 17 754 755

42. GuindonSGascuelO 2003 A Simple, fast, and accurate algorithm to estimate large phylogenies by Maximum Likelihood. Syst Biol 52 696 704

43. KumarSDudleyJNeiMTamuraK 2008 MEGA: A biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinformatics 9 299 306

44. LoleKSBollingerRCParanjapeRSGadkariDKulkarniSS 1999 Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol 73 152 160

45. YangZNielsenRGoldmanNPedersenA-MK 2000 Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155 431 449

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2011 Číslo 6
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#