The Role of Human Transportation Networks in Mediating the Genetic Structure of Seasonal Influenza in the United States
The rapid, long-distance spread of human pathogens such as seasonal influenza A across modern transportation networks presents a tremendous challenge for public health. Previous work based on influenza-like illness reports has demonstrated that commuters play an important role in the transmission of influenza across the United States. However, genetic structuring of influenza populations within a single season has not previously been detected. Here, we use sequence data collected over multiple seasons to investigate how human movement along the aviation and commuter networks in the United States contributes to influenza transmission at the regional scale. We confirm that commuters can play an integral role in interstate influenza transmission, but found that this pattern was specific to the influenza A subtype under investigation. We additionally show that strong county-to-county commuter flows do not necessarily fall within state boundaries, emphasizing the need for more precise spatial data to be associated with publically available sequences. Our results demonstrate that genetic structure does exist for influenza populations during the course of a single season at the regional scale and highlight the need to incorporate host movement patterns when studying spatial population structure.
Vyšlo v časopise:
The Role of Human Transportation Networks in Mediating the Genetic Structure of Seasonal Influenza in the United States. PLoS Pathog 11(6): e32767. doi:10.1371/journal.ppat.1004898
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1004898
Souhrn
The rapid, long-distance spread of human pathogens such as seasonal influenza A across modern transportation networks presents a tremendous challenge for public health. Previous work based on influenza-like illness reports has demonstrated that commuters play an important role in the transmission of influenza across the United States. However, genetic structuring of influenza populations within a single season has not previously been detected. Here, we use sequence data collected over multiple seasons to investigate how human movement along the aviation and commuter networks in the United States contributes to influenza transmission at the regional scale. We confirm that commuters can play an integral role in interstate influenza transmission, but found that this pattern was specific to the influenza A subtype under investigation. We additionally show that strong county-to-county commuter flows do not necessarily fall within state boundaries, emphasizing the need for more precise spatial data to be associated with publically available sequences. Our results demonstrate that genetic structure does exist for influenza populations during the course of a single season at the regional scale and highlight the need to incorporate host movement patterns when studying spatial population structure.
Zdroje
1. Biek R, Henderson JC, Waller LA, Rupprecht CE, Real LA. A high-resolution genetic signature of demographic and spatial expansion in epizootic rabies virus. Proc Natl Acad Sci U S A. 2007;104(19):7993–8. 17470818
2. Real LA, Henderson JC, Biek R, Snaman J, Jack TL, Childs JE, et al. Unifying the spatial population dynamics and molecular evolution of epidemic rabies virus. P Natl Acad Sci USA. 2005;102(34):12107–11. 16103358
3. Walsh PD, Biek R, Real LA. Wave-like spread of Ebola Zaire. Plos Biol. 2005;3(11):1946–53.
4. Epperson BK. Geographical Genetics. Princeton: Princeton University Press; 2003.
5. Wright S. Isolation by distance. Genetics. 1943;28(2):114–38. 17247074
6. Brockmann D, Helbing D. The hidden geometry of complex, network-driven contagion phenomena. Science. 2013;342(6164):1337–42. doi: 10.1126/science.1245200 24337289
7. Rvachev LA, Longini IM. A mathematical model for the global spread of influenza. Math Biosci. 1985;75(1):3–22.
8. Hufnagel L, Brockmann D, Geisel T. Forecast and control of epidemics in a globalized world. P Natl Acad Sci USA. 2004;101(42):15124–9. 15477600
9. Colizza V, Barrat A, Barthelemy M, Vespignani A. The modeling of global epidemics: stochastic dynamics and predictability. Bulletin of mathematical biology. 2006;68(8):1893–921. 17086489
10. Colizza V, Barrat A, Barthelemy M, Vespignani A. The role of the airline transportation network in the prediction and predictability of global epidemics. P Natl Acad Sci USA. 2006;103(7):2015–20. 16461461
11. Tatem AJ, Rogers DJ, Hay SI. Global transport networks and infectious disease spread. In: Simon I. Hay AG, David JR, editors. Advances in Parasitology: Academic Press; 2006. p. 293–343. 16647974
12. Gomes MFC, Pastore y Piontti A, Rossi L, Chao D, Longini I, Halloran ME, et al. Assessing the International Spreading Risk Associated with the 2014 West African Ebola Outbreak. PLoS Currents. 2014;6:ecurrents.outbreaks.cd818f63d40e24aef769dda7df9e0da5.
13. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, et al. Global trends in emerging infectious diseases. Nature. 2008;451(7181):990–3. doi: 10.1038/nature06536 18288193
14. Smith KF, Guegan JF. Changing Geographic Distributions of Human Pathogens. Annu Rev Ecol Evol S. 2010;41:231–50.
15. Balcan D, Colizza V, Goncalves B, Hu H, Ramasco JJ, Vespignani A. Multiscale mobility networks and the spatial spreading of infectious diseases. P Natl Acad Sci USA. 2009;106(51):21484–9. doi: 10.1073/pnas.0906910106 20018697
16. Simonsen L. The global impact of influenza on morbidity and mortality. Vaccine. 1999;17:S3–S10. 10471173
17. Russell CA, Jones TC, Barr IG, Cox NJ, Garten RJ, Gregory V, et al. The global circulation of seasonal influenza A (H3N2) viruses. Science. 2008;320(5874):340–6. doi: 10.1126/science.1154137 18420927
18. Bahl J, Nelson MI, Chan KH, Chen RB, Vijaykrishna D, Halpin RA, et al. Temporally structured metapopulation dynamics and persistence of influenza A H3N2 virus in humans. P Natl Acad Sci USA. 2011;108(48):19359–64. doi: 10.1073/pnas.1109314108 22084096
19. Nelson MI, Edelman L, Spiro DJ, Boyne AR, Bera J, Halpin R, et al. Molecular epidemiology of A/H3N2 and A/H1N1 influenza virus during a single epidemic season in the United States. Plos Pathog. 2008;4(8).
20. Viboud C, Bjornstad ON, Smith DL, Simonsen L, Miller MA, Grenfell BT. Synchrony, waves, and spatial hierarchies in the spread of influenza. Science. 2006;312(5772):447–51. 16574822
21. Centers for Disease Control and Prevention. FluView: A Weekly Influenza Surveillance Report Prepared by the Influenza Division. Atlanta [Accessed 2014 May]; http://www.cdc.gov/flu/weekly/pastreports.htm.
22. Ferguson NM, Galvani AP, Bush RM. Ecological and immunological determinants of influenza evolution. Nature. 2003;422(6930):428–33. 12660783
23. Rambaut A, Pybus OG, Nelson MI, Viboud C, Taubenberger JK, Holmes EC. The genomic and epidemiological dynamics of human influenza A virus. Nature. 2008;453(7195):615–9. doi: 10.1038/nature06945 18418375
24. Simonsen L, Viboud C, Taylor R, Miller M. The Epidemiology of Influenza and Its Control. In: Rappuoli R, Del Giudice G, editors. Influenza Vaccines for the Future: Springer Basel; 2011. p. 27–54.
25. Lemey P, Rambaut A, Bedford T, Faria N, Bielejec F, Baele G, et al. Unifying Viral Genetics and Human Transportation Data to Predict the Global Transmission Dynamics of Human Influenza H3N2. Plos Pathog. 2014;10(2):e1003932. doi: 10.1371/journal.ppat.1003932 24586153
26. Brownstein JS, Wolfe CJ, Mandl KD. Empirical evidence for the effect of airline travel on inter-regional influenza spread in the United States. PLoS medicine. 2006;3(10):e401. 16968115
27. Ratmann O, Donker G, Meijer A, Fraser C, Koelle K. Phylodynamic inference and model assessment with approximate bayesian computation: influenza as a case study. Plos Comput Biol. 2012;8(12).
28. Koelle K, Cobey S, Grenfell B, Pascual M. Epochal evolution shapes the phylodynamics of interpandemic influenza A (H3N2) in humans. Science. 2006;314(5807):1898–903. 17185596
29. Koelle K, Khatri P, Kamradt M, Kepler TB. A two-tiered model for simulating the ecological and evolutionary dynamics of rapidly evolving viruses, with an application to influenza. J R Soc Interface. 2010;7(50):1257–74. doi: 10.1098/rsif.2010.0007 20335193
30. Bedford T, Rambaut A, Pascual M. Canalization of the evolutionary trajectory of the human influenza virus. Bmc Biol. 2012;10. doi: 10.1186/1741-7007-10-10 22348706
31. Atkinson W, Wolfe S, Hamborsky J, editors. Epidemiology and Prevention of Vaccine-Preventable Diseases. 12 ed. Washington DC: Public Health Foundation; 2012.
32. Association of Public Health Laboratories, Centers for Disease Control and Prevention. Influenza Virologic Surveillance Right Size Roadmap. 2013. http://www.aphl.org/aphlprograms/infectious/influenza/Pages/Influenza-Virologic-Surveillance-Right-Size-Roadmap.aspx
33. Centers for Disease Control and Prevention. FluView Web Portal: National and Regional Level Outpatient Illness and Viral Surveillance. [Accessed 2014 Feb]; http://gis.cdc.gov/grasp/fluview/fluportaldashboard.html.
34. Simonsen L, Reichert TA, Viboud C, Blackwelder WC, Taylor RJ, Miller MA. Impact of influenza vaccination on seasonal mortality in the US elderly population. Arch Intern Med. 2005;165(3):265–72. 15710788
35. Legendre P, Fortin MJ. Comparison of the Mantel test and alternative approaches for detecting complex multivariate relationships in the spatial analysis of genetic data. Molecular ecology resources. 2010;10(5):831–44. doi: 10.1111/j.1755-0998.2010.02866.x 21565094
36. Thiemann C, Theis F, Grady D, Brune R, Brockmann D. The structure of borders in a small world. PloS one. 2010;5(11):e15422. doi: 10.1371/journal.pone.0015422 21124970
37. Medlock J, Galvani AP. Optimizing influenza vaccine distribution. Science. 2009;325(5948):1705–8. doi: 10.1126/science.1175570 19696313
38. Bao Y, Bolotov P, Dernovoy D, Kiryutin B, Zaslavsky L, Tatusova T, et al. The Influenza Virus Resource at the National Center for Biotechnology Information. Journal of Virology. 2008;82(2):596–601. 17942553
39. Biomatters. Geneious version 5.6.2.
40. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A. Relaxed phylogenetics and dating with confidence. Plos Biology. 2006;4(5):699–710.
41. Drummond AJ, Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. Bmc Evol Biol. 2007;7:214. 17996036
42. Shapiro B, Rambaut A, Drummond AJ. Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. Mol Biol Evol. 2006;23(1):7–9. 16177232
43. Nelson MI, Simonsen L, Viboud C, Miller MA, Taylor J, George KS, et al. Stochastic processes are key determinants of short-term evolution in influenza A virus. Plos Pathogens. 2006;2(12):1144–51.
44. Paradis E, Claude J, Strimmer K. APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics. 2004;20(2):289–90. 14734327
45. Bureau of Transportation Statistics. Air Carrier Statistics (Form 41 Traffic): T-100 Market (All Carriers). [Accessed 2013 June]; http://www.transtats.bts.gov/DL_SelectFields.asp?Table_ID=292.
46. Centers for Disease Control and Prevention. Seasonal Influenza Q&A. 2013 [Accessed 2014 May]; http://www.cdc.gov/flu/about/qa/disease.htm.
47. United States Census Bureau. 2000 County-to-County Worker Flow Files. 2000 [Accessed 2013 September]; http://www.census.gov/population/www/cen2000/commuting/index.html.
48. Reichardt J, Bornholdt S. Statistical mechanics of community detection. Physical review E, Statistical, nonlinear, and soft matter physics. 2006;74(1):016110. 16907154
49. Newman ME, Girvan M. Finding and evaluating community structure in networks. Physical review E, Statistical, nonlinear, and soft matter physics. 2004;69(2):026113. 14995526
50. Traag VA, Bruggeman J. Community detection in networks with positive and negative links. Physical review E, Statistical, nonlinear, and soft matter physics. 2009;80(3):036115. 19905188
51. Legendre P, Legendre L. Numerical Ecology. Amsterdam: Elsevier; 1998.
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
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