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Abstract

The drivers of influenza seasonality remain heavily debated, especially in tropical/subtropical regions where influenza activity can peak in winter, during the rainy season, or remain constant throughout the year. We compared the epidemiological and evolutionary patterns of seasonal influenza epidemics in Hong Kong and Shenzhen, two adjacent cities in subtropical southern China. This comparison represents a unique natural experiment, as connectivity between these two cities has increased over the past decade. We found that, whilst summer influenza epidemics in Shenzhen used to peak 1–3 months later than those in Hong Kong, the difference decreased after 2005 (<0.0001). Phylogenetic analysis revealed that influenza isolates from Shenzhen have become genetically closer to those circulating in Hong Kong over time ( = 0.045). Furthermore, although Shenzhen isolates used to be more distant from the global putative source of influenza viruses than isolates from Hong Kong (<0.001), this difference has narrowed ( = 0.02). Overall, our study reveals that influenza activities show remarkably distinct epidemiological and evolutionary patterns in adjacent subtropical cities and suggests that human mobility patterns can play a major role in influenza dynamics in the subtropics.

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2014-03-01
2024-03-28
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References

  1. Alonso W. J., Viboud C., Simonsen L., Hirano E. W., Daufenbach L. Z., Miller M. A. 2007; Seasonality of influenza in Brazil: a traveling wave from the Amazon to the subtropics. Am J Epidemiol 165:1434–1442 [View Article][PubMed]
    [Google Scholar]
  2. Azziz Baumgartner E., Dao C. N., Nasreen S., Bhuiyan M. U., Mah-E-Muneer S., Al Mamun A., Sharker M. A., Uz Zaman R., Cheng P. Y.other authors 2012; Seasonality, timing, and climate drivers of influenza activity worldwide. J Infect Dis 206:838–846 [View Article][PubMed]
    [Google Scholar]
  3. Bahl J., Nelson M. I., Chan K. H., Chen R., Vijaykrishna D., Halpin R. A., Stockwell T. B., Lin X., Wentworth D. E.other authors 2011; Temporally structured metapopulation dynamics and persistence of influenza A H3N2 virus in humans. Proc Natl Acad Sci U S A 108:19359–19364 [View Article][PubMed]
    [Google Scholar]
  4. Bedford T., Cobey S., Beerli P., Pascual M. 2010; Global migration dynamics underlie evolution and persistence of human influenza A (H3N2). PLoS Pathog 6:e1000918 [View Article][PubMed]
    [Google Scholar]
  5. Bloom-Feshbach K., Alonso W. J., Charu V., Tamerius J., Simonsen L., Miller M. A., Viboud C. 2013; Latitudinal variations in seasonal activity of influenza and respiratory syncytial virus (RSV): a global comparative review. PLoS ONE 8:e54445 [View Article][PubMed]
    [Google Scholar]
  6. Chan P. K., Mok H. Y., Lee T. C., Chu I. M., Lam W. Y., Sung J. J. 2009; Seasonal influenza activity in Hong Kong and its association with meteorological variations. J Med Virol 81:1797–1806 [View Article][PubMed]
    [Google Scholar]
  7. Cheng X., Tan Y., He M., Lam T. T., Lu X., Viboud C., He J., Zhang S., Lu J.other authors 2013; Epidemiological dynamics and phylogeography of influenza virus in southern China. J Infect Dis 207:106–114 [View Article][PubMed]
    [Google Scholar]
  8. Diebel J., Norda J. 2013a; Average weather for Chek Lap Kok, Hong Kong. [Accessed 31 October 2013] http://weatherspark.com/averages/33929/Chek-Lap-Kok-Kowloon-Hong-Kong
    [Google Scholar]
  9. Diebel J., Norda J. 2013b; Average weather for Shenzhen, China. [Accessed 31 October 2013] http://weatherspark.com/averages/34108/Shenzhen-Guangdong-China
    [Google Scholar]
  10. Finkelman B. S., Viboud C., Koelle K., Ferrari M. J., Bharti N., Grenfell B. T. 2007; Global patterns in seasonal activity of influenza A/H3N2, A/H1N1, and B from 1997 to 2005: viral coexistence and latitudinal gradients. PLoS ONE 2:e1296 [View Article][PubMed]
    [Google Scholar]
  11. Garske T., Yu H., Peng Z., Ye M., Zhou H., Cheng X., Wu J., Ferguson N. 2011; Travel patterns in China. PLoS ONE 6:e16364 [View Article][PubMed]
    [Google Scholar]
  12. Grenfell B. T., Bjørnstad O. N., Kappey J. 2001; Travelling waves and spatial hierarchies in measles epidemics. Nature 414:716–723 [View Article][PubMed]
    [Google Scholar]
  13. Hong Kong Tourism Board 2013; Visitor arrival statistics. January 2002–December 2012. [Accessed 22 April 2013] https://securepartnernet.hktb.com/en/my_partnernet/index.html?reqlogin=1&themeClassName=research_statistic
    [Google Scholar]
  14. Johansson M. A., Cummings D. A., Glass G. E. 2009; Multiyear climate variability and dengue–El Niño southern oscillation, weather, and dengue incidence in Puerto Rico, Mexico, and Thailand: a longitudinal data analysis. PLoS Med 6:e1000168 [View Article][PubMed]
    [Google Scholar]
  15. Lavenu A., Leruez-Ville M., Chaix M. L., Boelle P. Y., Rogez S., Freymuth F., Hay A., Rouzioux C., Carrat F. 2006; Detailed analysis of the genetic evolution of influenza virus during the course of an epidemic. Epidemiol Infect 134:514–520 [View Article][PubMed]
    [Google Scholar]
  16. Lee V. J., Yap J., Ong J. B., Chan K. P., Lin R. T., Chan S. P., Goh K. T., Leo Y. S., Chen M. I. 2009; Influenza excess mortality from 1950–2000 in tropical Singapore. PLoS ONE 4:e8096 [View Article][PubMed]
    [Google Scholar]
  17. Lipsitch M., Viboud C. 2009; Influenza seasonality: lifting the fog. Proc Natl Acad Sci U S A 106:3645–3646 [View Article][PubMed]
    [Google Scholar]
  18. Lowen A., Palese P. 2009; Transmission of influenza virus in temperate zones is predominantly by aerosol, in the tropics by contact: a hypothesis. PLoS Curr 1:RRN1002 [View Article][PubMed]
    [Google Scholar]
  19. R Development Core Team 2013; r: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing, 2010; [Accessed 30 April 2013] http://www.R-project.org/
    [Google Scholar]
  20. Rambaut A., Pybus O. G., Nelson M. I., Viboud C., Taubenberger J. K., Holmes E. C. 2008; The genomic and epidemiological dynamics of human influenza A virus. Nature 453:615–619 [View Article][PubMed]
    [Google Scholar]
  21. Roger B. 1997 Hong Kong: the Road to 1997 Cambridge: Cambridge University Press;
    [Google Scholar]
  22. Russell C. A., Jones T. C., Barr I. G., Cox N. J., Garten R. J., Gregory V., Gust I. D., Hampson A. W., Hay A. J.other authors 2008; The global circulation of seasonal influenza A (H3N2) viruses. Science 320:340–346 [View Article][PubMed]
    [Google Scholar]
  23. Shaman J., Pitzer V. E., Viboud C., Grenfell B. T., Lipsitch M. 2010; Absolute humidity and the seasonal onset of influenza in the continental United States. PLoS Biol 8:e1000316 [View Article][PubMed]
    [Google Scholar]
  24. Stamatakis A. 2006; RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690 [View Article][PubMed]
    [Google Scholar]
  25. Tamerius J., Nelson M. I., Zhou S. Z., Viboud C., Miller M. A., Alonso W. J. 2011; Global influenza seasonality: reconciling patterns across temperate and tropical regions. Environ Health Perspect 119:439–445 [View Article][PubMed]
    [Google Scholar]
  26. Tamerius J. D., Shaman J., Alonso W. J., Bloom-Feshbach K., Uejio C. K., Comrie A., Viboud C. 2013; Environmental predictors of seasonal influenza epidemics across temperate and tropical climates. PLoS Pathog 9:e1003194 [View Article][PubMed]
    [Google Scholar]
  27. The Government of the Hong Kong Special Administrative Region 2013; Individual visit scheme. [Accessed 22 April 2013] http://www.tourism.gov.hk/english/visitors/visitors_ind.html
    [Google Scholar]
  28. Turbelin C., Souty C., Pelat C., Hanslik T., Sarazin M., Blanchon T., Falchi A. 2013; Age distribution of influenza like illness cases during post-pandemic A(H3N2): comparison with the twelve previous seasons, in France. PLoS ONE 8:e65919 [View Article][PubMed]
    [Google Scholar]
  29. Viboud C., Boëlle P. Y., Pakdaman K., Carrat F., Valleron A. J., Flahault A. 2004; Influenza epidemics in the United States, France, and Australia, 1972–1997. Emerg Infect Dis 10:32–39 [View Article][PubMed]
    [Google Scholar]
  30. Viboud C., Alonso W. J., Simonsen L. 2006a; Influenza in tropical regions. PLoS Med 3:e89 [View Article][PubMed]
    [Google Scholar]
  31. Viboud C., Miller M. A., Grenfell B. T., Bjørnstad O. N., Simonsen L. 2006b; Air travel and the spread of influenza: important caveats. PLoS Med 3:e503 author reply e502. [Erratum PLoS Med 2007 4, e32.] [View Article][PubMed]
    [Google Scholar]
  32. Viboud C., Bjørnstad O. N., Smith D. L., Simonsen L., Miller M. A., Grenfell B. T. 2006c; Synchrony, waves, and spatial hierarchies in the spread of influenza. Science 312:447–451 [View Article][PubMed]
    [Google Scholar]
  33. Waicharoen S., Thawatsupha P., Chittaganpitch M., Maneewong P., Thanadachakul T., Sawanpanyalert P. 2008; Influenza viruses circulating in Thailand in 2004 and 2005. Jpn J Infect Dis 61:321–323[PubMed]
    [Google Scholar]
  34. Weinberger D. M., Krause T. G., Mølbak K., Cliff A., Briem H., Viboud C., Gottfredsson M. 2012; Influenza epidemics in Iceland over 9 decades: changes in timing and synchrony with the United States and Europe. Am J Epidemiol 176:649–655 [View Article][PubMed]
    [Google Scholar]
  35. Yang L., Wong C. M., Lau E. H., Chan K. P., Ou C. Q., Peiris J. S. 2008; Synchrony of clinical and laboratory surveillance for influenza in Hong Kong. PLoS ONE 3:e1399 [View Article][PubMed]
    [Google Scholar]
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