Characterization of Regional Influenza Seasonality Patterns in China and Implications for Vaccination Strategies: Spatio-Temporal Modeling of Surveillance Data

PLoS Medicine

Volumn 10, Issue 11, 2013, Pages

  Yu, Hongjie ^a   Alonso, Wladimir J ^b   Feng, Luzhao ^a   Tan, Yi ^b   Shu, Yuelong ^c   Yang, Weizhong ^a   Viboud, Cécile ^b  

^a CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c China CDC   (China)

Author keywords

[No Author keywords available]

Indexed keywords

RAIN;

ARTICLE; CHINA; CLIMATE; DISEASE SURVEILLANCE; HUMAN; INFLUENZA A; INFLUENZA B; INFLUENZA VACCINATION; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEASONAL INFLUENZA; SEASONAL VARIATION; SENSITIVITY ANALYSIS; TEMPERATURE;

BAYES THEOREM; CHINA; CLIMATE; EPIDEMICS; GEOGRAPHIC MAPPING; HOSPITALS; HUMANS; INCIDENCE; INFLUENZA A VIRUS; INFLUENZA B VIRUS; INFLUENZA, HUMAN; LINEAR MODELS; MODELS, BIOLOGICAL; POPULATION SURVEILLANCE; SEASONS; SOCIOECONOMIC FACTORS; TEMPERATURE; VACCINATION;

EID: 84888999503     PISSN: 15491277     EISSN: 15491676     Source Type: Journal    
DOI: 10.1371/journal.pmed.1001552     Document Type: Article

References (56)

1. Viboud C, Alonso WJ, Simonsen L, (2006) Influenza in tropical regions. PLoS Med 3: e89 doi:10.1371/journal.pmed.0030089.
2. Azziz Baumgartner E, Dao CN, Nasreen S, Bhuiyan MU, Mah EMS, et al. (2012) Seasonality, timing, and climate drivers of influenza activity worldwide. J Infect Dis 206: 838-846.
3. Bloom-Feshbach K, Alonso WJ, Charu V, Tamerius J, Simonsen L, et al. (2012) Latitudinal variations in seasonal activity of influenza and respiratory syncytial virus (RSV): a global comparative review. PLoS One 8: e54445 doi:10.1371/journal.pone.0054445.
4. Zou J, Yang H, Cui H, Shu Y, Xu P, et al. (2013) Geographic divisions and modeling of virological data on seasonal influenza in the Chinese mainland during the 2006-2009 monitoring years. PLoS One 8: e58434 doi:10.1371/journal.pone.0058434.
5. Shaman J, Goldstein E, Lipsitch M, (2011) Absolute humidity and pandemic versus epidemic influenza. Am J Epidemiol 173: 127-135.
6. Shaman J, Kohn M, (2009) Absolute humidity modulates influenza survival, transmission, and seasonality. Proc Natl Acad Sci U S A 106: 3243-3248.
7. Shaman J, Pitzer VE, Viboud C, Grenfell BT, Lipsitch M, (2010) Absolute humidity and the seasonal onset of influenza in the continental United States. PLoS Biol 8: e1000316 doi:10.1371/journal.pbio.1000316.
8. Tamerius J, Shaman J, Alonso WJ, Bloom-Feshbach K, Uejio CK, et al. (2012) Environmental predictors of seasonal influenza epidemics across temperate and tropical climates. PLoS Pathog 9: e1003194 doi:10.1371/journal.ppat.1003194.
9. de Mello WA, de Paiva TM, Ishida MA, Benega MA, Dos Santos MC, et al. (2009) The dilemma of influenza vaccine recommendations when applied to the tropics: the Brazilian case examined under alternative scenarios. PLoS One 4: e5095 doi:10.1371/journal.pone.0005095.
10. Gupta V, Dawood FS, Muangchana C, Lan PT, Xeuatvongsa A, et al. (2012) Influenza vaccination guidelines and vaccine sales in southeast Asia: 2008-2011. PLoS One 7: e52842 doi:10.1371/journal.pone.0052842.
11. Feng L, Shay DK, Jiang Y, Zhou H, Chen X, et al. (2012) Influenza-associated mortality in temperate and subtropical Chinese cities, 2003-2008. Bull World Health Organ 90: 279-288B.
12. Cohen C, Simonsen L, Kang JW, Miller M, McAnerney J, et al. (2010) Elevated influenza-related excess mortality in South African elderly individuals, 1998-2005. Clin Infect Dis 51: 1362-1369.
13. Cohen C, Simonsen L, Sample J, Kang JW, Miller M, et al. (2012) Influenza-related mortality among adults age 25-54 years with AIDS in South Africa and the United States of America. Clin Infect Dis 55: 996-1003.
14. Homaira N, Luby SP, Alamgir AS, Islam K, Paul R, et al. (2012) Influenza-associated mortality in 2009 in four sentinel sites in Bangladesh. Bull World Health Organ 90: 272-278.
15. Yu H, Feng L, Viboud CG, Shay DK, Jiang Y, et al. (2013) Regional variation in mortality impact of the 2009 A(H1N1) influenza pandemic in China. Influenza Other Respi Viruses In press.
16. Feng L, Mounts AW, Feng Y, Luo Y, Yang P, et al. (2010) Seasonal influenza vaccine supply and target vaccinated population in China, 2004-2009. Vaccine 28: 6778-6782.
17. Shu YL, Fang LQ, de Vlas SJ, Gao Y, Richardus JH, et al. (2010) Dual seasonal patterns for influenza, China. Emerg Infect Dis 16: 725-726.
18. Du X, Dong L, Lan Y, Peng Y, Wu A, et al. (2012) Mapping of H3N2 influenza antigenic evolution in China reveals a strategy for vaccine strain recommendation. Nat Commun 3: 709.
19. Chinese Center for Disease Control and Prevention (2010) Influenza sentinel surveillance protocol (2005-2010). Available: http://www.chinacdc.cn/jkzt/crb/lxxgm/jc/200509/t20050908_24127.htm.
20. National Bureau of Statistics of China (2011) China Statistical Yearbook. Beijing: China Statistics Press.
21. Garske T, Yu H, Peng Z, Ye M, Zhou H, et al. (2011) Travel patterns in China. PLoS One 6: e16364 doi:10.1371/journal.pone.0016364.
22. National Meteorological Information Center CMACMDSSS (2012) Available: http://cdc.cma.gov.cn/.
23. Zheng J, Yin Y, Li B, (2010) A new scheme for climate regionalization in China. Acta Geographica Sinica 65: 3-13.
24. Broutin H, Viboud C, Grenfell BT, Miller MA, Rohani P, (2010) Impact of vaccination and birth rate on the epidemiology of pertussis: a comparative study in 64 countries. Proc Biol Sci 277: 3239-3245.
25. Zhou H, Thompson W, Viboud C, Ringholz C, Cheng P-Y, et al. (2012) Hospitalizations associated with influenza and respiratory syncytial virus in the United States, 1993--2008. Clin Infect Dis 54: 1427-1436.
26. Alonso WJ, Viboud C, Simonsen L, Hirano EW, Daufenbach LZ, et al. (2007) Seasonality of influenza in Brazil: a traveling wave from the Amazon to the subtropics. Am J Epidemiol 165: 1434-1442.
27. Viboud C, Bjornstad ON, Smith DL, Simonsen L, Miller MA, et al. (2006) Synchrony, waves, and spatial hierarchies in the spread of influenza. Science 312: 447-451.
28. Naumova EN, Jagai JS, Matyas B, DeMaria A Jr, MacNeill IB, et al. (2007) Seasonality in six enterically transmitted diseases and ambient temperature. Epidemiol Infect 135: 281-292.
29. Rogers DJ, Hay SI, Packer MJ, (1996) Predicting the distribution of tsetse flies in West Africa using temporal Fourier processed meteorological satellite data. Ann Trop Med Parasitol 90: 225-241.
30. Thompson WW, Shay DK, Weintraub E, Brammer L, Cox N, et al. (2003) Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA 289: 179-186.
31. Ward JH, (1963) Hierarchical grouping to optimize an objective function. J Am Stat Assoc 58: 236-244.
32. Székely GJ, Rizzo ML, (2005) Hierarchical clustering via joint between-within distances: extending ward's minimum variance method. J Classif 22: 151-183.
33. (2012) Cluster package in R. Available: http://cran.r-project.org/web/packages/cluster/cluster.pdf.
34. Finkelman BS, Viboud C, Koelle K, Ferrari MJ, Bharti N, et al. (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 doi:10.1371/journal.pone.0001296.
35. Western Pacific Region Global Influenza Surveillance and Response System (2012) Epidemiological and virological characteristics of influenza in the Western Pacific Region of the World Health Organization, 2006-2010. PLoS One 7: e37568 doi:10.1371/journal.pone.0037568.
36. Yang L, Wong CM, Lau EH, Chan KP, Ou CQ, et al. (2008) Synchrony of clinical and laboratory surveillance for influenza in Hong Kong. PLoS One 3: e1399 doi:10.1371/journal.pone.0001399.
37. Cheng X, Tan Y, He M, Lam TT, Lu X, et al. (2012) Epidemiological dynamics and phylogeography of influenza in southern China. J Infect Dis.
38. Weinberger DM, Grove Krause TG, Molbak K, Cliff AD, Briem H, et al. (2012) Influenza epidemics in Iceland over nine decades: Changes in timing and synchrony with the United States and Europe. Am J Epidemiol 207: 106-114.
39. Dosseh A, Ndiaye K, Spiegel A, Sagna M, Mathiot C, (2000) Epidemiological and virological influenza survey in Dakar, Senegal: 1996-1998. Am J Trop Med Hyg 62: 639-643.
40. Lowen AC, Mubareka S, Steel J, Palese P, (2007) Influenza virus transmission is dependent on relative humidity and temperature. PLoS Pathog 3: 1470-1476 doi:10.1371/journal.ppat.0030151.
41. Pica N, Chou YY, Bouvier NM, Palese P, (2012) Transmission of influenza B viruses in the guinea pig. J Virol 86: 4279-4287.
42. Chen R, Holmes EC, (2008) The evolutionary dynamics of human influenza B virus. J Mol Evol 66: 655-663.
43. Kelly HA, Grant KA, Williams S, Fielding J, Smith D, (2009) Epidemiological characteristics of pandemic influenza H1N1 2009 and seasonal influenza infection. Med J Aust 191: 146-149.
44. Olson DR, Heffernan RT, Paladini M, Konty K, Weiss D, et al. (2007) Monitoring the impact of influenza by age: emergency department fever and respiratory complaint surveillance in New York City. PLoS Med 4: e247 doi:10.1371/journal.pmed.0040247.
45. Yu H, Huang J, Huai Y, Guan X, Klen J, et al. (2013) The substantial hospitalization burden of influenza in central China: surveillance for severe, acute respiratory infection and influenza viruses, 2010-2012. Influenza Other Respi Viruses In press.
46. Wright PF, Sannella E, Shi JR, Zhu Y, Ikizler MR, et al. (2008) Antibody responses after inactivated influenza vaccine in young children. Pediatr Infect Dis J 27: 1004-1008.
47. Ochiai H, Shibata M, Kamimura K, Niwayama S, (1986) Evaluation of the efficacy of split-product trivalent A(H1N1), A(H3N2), and B influenza vaccines: reactogenicity, immunogenicity and persistence of antibodies following two doses of vaccines. Microbiol Immunol 30: 1141-1149.
48. Smith DJ, Lapedes AS, de Jong JC, Bestebroer TM, Rimmelzwaan GF, et al. (2004) Mapping the antigenic and genetic evolution of influenza virus. Science 305: 371-376.
49. Tamerius J, Nelson MI, Zhou SZ, Viboud C, Miller MA, et al. (2011) Global influenza seasonality: reconciling patterns across temperate and tropical regions. Environ Health Perspect 119: 439-445.
50. Patel MM, Pitzer V, Alonso WJ, Vera D, Lopman BA, et al. (2012) Global seasonality of Rotavirus disease. Pediatr Infect Dis J 32: e134-147.
51. Alonso WJ, McCormick BJ, (2012) EPIPOI: a user-friendly analytical tool for the extraction and visualization of temporal parameters from epidemiological time series. BMC Public Health 12: 982.
52. Chowell G, Viboud C, Simonsen L, Miller M, Alonso WJ, (2010) The reproduction number of seasonal influenza epidemics in Brazil, 1996-2006. Proc Biol Sci 277: 1857-1866.
53. Chowell G, Miller MA, Viboud C, (2008) Seasonal influenza in the United States, France, and Australia: transmission and prospects for control. Epidemiol Infect 136: 852-864.
54. Opatowski L, Fraser C, Griffin J, de Silva E, Van Kerkhove MD, et al. (2011) Transmission characteristics of the 2009 H1N1 influenza pandemic: comparison of 8 southern hemisphere countries. Plos Pathogens 7: e1002225 doi:10.1371/journal.ppat.1002225.
55. 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 doi:10.1371/journal.ppat.1000918.
56. Russell CA, Jones TC, Barr IG, Cox NJ, Garten RJ, et al. (2008) The global circulation of seasonal influenza A (H3N2) viruses. Science 320: 340-346.