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


Background:
The complexity of influenza seasonal patterns in the inter-tropical zone impedes the establishment of effective routine immunization programs. China is a climatologically and economically diverse country, which has yet to establish a national influenza vaccination program. Here we characterize the diversity of influenza seasonality in China and make recommendations to guide future vaccination programs.

Methods and Findings:
We compiled weekly reports of laboratory-confirmed influenza A and B infections from sentinel hospitals in cities representing 30 Chinese provinces, 2005–2011, and data on population demographics, mobility patterns, socio-economic, and climate factors. We applied linear regression models with harmonic terms to estimate influenza seasonal characteristics, including the amplitude of annual and semi-annual periodicities, their ratio, and peak timing. Hierarchical Bayesian modeling and hierarchical clustering were used to identify predictors of influenza seasonal characteristics and define epidemiologically-relevant regions. The annual periodicity of influenza A epidemics increased with latitude (mean amplitude of annual cycle standardized by mean incidence, 140% [95% CI 128%–151%] in the north versus 37% [95% CI 27%–47%] in the south, p<0.0001). Epidemics peaked in January–February in Northern China (latitude ≥33°N) and April–June in southernmost regions (latitude <27°N). Provinces at intermediate latitudes experienced dominant semi-annual influenza A periodicity with peaks in January–February and June–August (periodicity ratio >0.6 in provinces located within 27.4°N–31.3°N, slope of latitudinal gradient with latitude −0.016 [95% CI −0.025 to −0.008], p<0.001). In contrast, influenza B activity predominated in colder months throughout most of China. Climate factors were the strongest predictors of influenza seasonality, including minimum temperature, hours of sunshine, and maximum rainfall. Our main study limitations include a short surveillance period and sparse influenza sampling in some of the southern provinces.

Conclusions:
Regional-specific influenza vaccination strategies would be optimal in China; in particular, annual campaigns should be initiated 4–6 months apart in Northern and Southern China. Influenza surveillance should be strengthened in mid-latitude provinces, given the complexity of seasonal patterns in this region. More broadly, our findings are consistent with the role of climatic factors on influenza transmission dynamics.

Please see later in the article for the Editors' Summary


Vyšlo v časopise: Characterization of Regional Influenza Seasonality Patterns in China and Implications for Vaccination Strategies: Spatio-Temporal Modeling of Surveillance Data. PLoS Med 10(11): e32767. doi:10.1371/journal.pmed.1001552
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pmed.1001552

Souhrn

Background:
The complexity of influenza seasonal patterns in the inter-tropical zone impedes the establishment of effective routine immunization programs. China is a climatologically and economically diverse country, which has yet to establish a national influenza vaccination program. Here we characterize the diversity of influenza seasonality in China and make recommendations to guide future vaccination programs.

Methods and Findings:
We compiled weekly reports of laboratory-confirmed influenza A and B infections from sentinel hospitals in cities representing 30 Chinese provinces, 2005–2011, and data on population demographics, mobility patterns, socio-economic, and climate factors. We applied linear regression models with harmonic terms to estimate influenza seasonal characteristics, including the amplitude of annual and semi-annual periodicities, their ratio, and peak timing. Hierarchical Bayesian modeling and hierarchical clustering were used to identify predictors of influenza seasonal characteristics and define epidemiologically-relevant regions. The annual periodicity of influenza A epidemics increased with latitude (mean amplitude of annual cycle standardized by mean incidence, 140% [95% CI 128%–151%] in the north versus 37% [95% CI 27%–47%] in the south, p<0.0001). Epidemics peaked in January–February in Northern China (latitude ≥33°N) and April–June in southernmost regions (latitude <27°N). Provinces at intermediate latitudes experienced dominant semi-annual influenza A periodicity with peaks in January–February and June–August (periodicity ratio >0.6 in provinces located within 27.4°N–31.3°N, slope of latitudinal gradient with latitude −0.016 [95% CI −0.025 to −0.008], p<0.001). In contrast, influenza B activity predominated in colder months throughout most of China. Climate factors were the strongest predictors of influenza seasonality, including minimum temperature, hours of sunshine, and maximum rainfall. Our main study limitations include a short surveillance period and sparse influenza sampling in some of the southern provinces.

Conclusions:
Regional-specific influenza vaccination strategies would be optimal in China; in particular, annual campaigns should be initiated 4–6 months apart in Northern and Southern China. Influenza surveillance should be strengthened in mid-latitude provinces, given the complexity of seasonal patterns in this region. More broadly, our findings are consistent with the role of climatic factors on influenza transmission dynamics.

Please see later in the article for the Editors' Summary


Zdroje

1. ViboudC, AlonsoWJ, SimonsenL (2006) Influenza in tropical regions. PLoS Med 3: e89 doi:10.1371/journal.pmed.0030089

2. Azziz BaumgartnerE, DaoCN, NasreenS, BhuiyanMU, MahEMS, et al. (2012) Seasonality, timing, and climate drivers of influenza activity worldwide. J Infect Dis 206: 838–846.

3. Bloom-FeshbachK, AlonsoWJ, CharuV, TameriusJ, SimonsenL, 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. ZouJ, YangH, CuiH, ShuY, XuP, 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. ShamanJ, GoldsteinE, LipsitchM (2011) Absolute humidity and pandemic versus epidemic influenza. Am J Epidemiol 173: 127–135.

6. ShamanJ, KohnM (2009) Absolute humidity modulates influenza survival, transmission, and seasonality. Proc Natl Acad Sci U S A 106: 3243–3248.

7. ShamanJ, PitzerVE, ViboudC, GrenfellBT, LipsitchM (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. TameriusJ, ShamanJ, AlonsoWJ, Bloom-FeshbachK, UejioCK, 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 MelloWA, de PaivaTM, IshidaMA, BenegaMA, Dos SantosMC, 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. GuptaV, DawoodFS, MuangchanaC, LanPT, XeuatvongsaA, 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. FengL, ShayDK, JiangY, ZhouH, ChenX, et al. (2012) Influenza-associated mortality in temperate and subtropical Chinese cities, 2003–2008. Bull World Health Organ 90: 279–288B.

12. CohenC, SimonsenL, KangJW, MillerM, McAnerneyJ, et al. (2010) Elevated influenza-related excess mortality in South African elderly individuals, 1998–2005. Clin Infect Dis 51: 1362–1369.

13. CohenC, SimonsenL, SampleJ, KangJW, MillerM, 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. HomairaN, LubySP, AlamgirAS, IslamK, PaulR, et al. (2012) Influenza-associated mortality in 2009 in four sentinel sites in Bangladesh. Bull World Health Organ 90: 272–278.

15. YuH, FengL, ViboudCG, ShayDK, JiangY, et al. (2013) Regional variation in mortality impact of the 2009 A(H1N1) influenza pandemic in China. Influenza Other Respi Viruses In press.

16. FengL, MountsAW, FengY, LuoY, YangP, et al. (2010) Seasonal influenza vaccine supply and target vaccinated population in China, 2004–2009. Vaccine 28: 6778–6782.

17. ShuYL, FangLQ, de VlasSJ, GaoY, RichardusJH, et al. (2010) Dual seasonal patterns for influenza, China. Emerg Infect Dis 16: 725–726.

18. DuX, DongL, LanY, PengY, WuA, 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. GarskeT, YuH, PengZ, YeM, ZhouH, 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. ZhengJ, YinY, LiB (2010) A new scheme for climate regionalization in China. Acta Geographica Sinica 65: 3–13.

24. BroutinH, ViboudC, GrenfellBT, MillerMA, RohaniP (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. ZhouH, ThompsonW, ViboudC, RingholzC, ChengP-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. AlonsoWJ, ViboudC, SimonsenL, HiranoEW, DaufenbachLZ, et al. (2007) Seasonality of influenza in Brazil: a traveling wave from the Amazon to the subtropics. Am J Epidemiol 165: 1434–1442.

27. ViboudC, BjornstadON, SmithDL, SimonsenL, MillerMA, et al. (2006) Synchrony, waves, and spatial hierarchies in the spread of influenza. Science 312: 447–451.

28. NaumovaEN, JagaiJS, MatyasB, DeMariaAJr, MacNeillIB, et al. (2007) Seasonality in six enterically transmitted diseases and ambient temperature. Epidemiol Infect 135: 281–292.

29. RogersDJ, HaySI, PackerMJ (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. ThompsonWW, ShayDK, WeintraubE, BrammerL, CoxN, et al. (2003) Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA 289: 179–186.

31. WardJH (1963) Hierarchical grouping to optimize an objective function. J Am Stat Assoc 58: 236–244.

32. SzékelyGJ, RizzoML (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. FinkelmanBS, ViboudC, KoelleK, FerrariMJ, BhartiN, 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. YangL, WongCM, LauEH, ChanKP, OuCQ, 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. ChengX, TanY, HeM, LamTT, LuX, et al. (2012) Epidemiological dynamics and phylogeography of influenza in southern China. J Infect Dis

38. WeinbergerDM, Grove KrauseTG, MolbakK, CliffAD, BriemH, 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. DossehA, NdiayeK, SpiegelA, SagnaM, MathiotC (2000) Epidemiological and virological influenza survey in Dakar, Senegal: 1996–1998. Am J Trop Med Hyg 62: 639–643.

40. LowenAC, MubarekaS, SteelJ, PaleseP (2007) Influenza virus transmission is dependent on relative humidity and temperature. PLoS Pathog 3: 1470–1476 doi:10.1371/journal.ppat.0030151

41. PicaN, ChouYY, BouvierNM, PaleseP (2012) Transmission of influenza B viruses in the guinea pig. J Virol 86: 4279–4287.

42. ChenR, HolmesEC (2008) The evolutionary dynamics of human influenza B virus. J Mol Evol 66: 655–663.

43. KellyHA, GrantKA, WilliamsS, FieldingJ, SmithD (2009) Epidemiological characteristics of pandemic influenza H1N1 2009 and seasonal influenza infection. Med J Aust 191: 146–149.

44. OlsonDR, HeffernanRT, PaladiniM, KontyK, WeissD, 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. YuH, HuangJ, HuaiY, GuanX, KlenJ, 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. WrightPF, SannellaE, ShiJR, ZhuY, IkizlerMR, et al. (2008) Antibody responses after inactivated influenza vaccine in young children. Pediatr Infect Dis J 27: 1004–1008.

47. OchiaiH, ShibataM, KamimuraK, NiwayamaS (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. SmithDJ, LapedesAS, de JongJC, BestebroerTM, RimmelzwaanGF, et al. (2004) Mapping the antigenic and genetic evolution of influenza virus. Science 305: 371–376.

49. TameriusJ, NelsonMI, ZhouSZ, ViboudC, MillerMA, et al. (2011) Global influenza seasonality: reconciling patterns across temperate and tropical regions. Environ Health Perspect 119: 439–445.

50. PatelMM, PitzerV, AlonsoWJ, VeraD, LopmanBA, et al. (2012) Global seasonality of Rotavirus disease. Pediatr Infect Dis J 32: e134–147.

51. AlonsoWJ, McCormickBJ (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. ChowellG, ViboudC, SimonsenL, MillerM, AlonsoWJ (2010) The reproduction number of seasonal influenza epidemics in Brazil, 1996–2006. Proc Biol Sci 277: 1857–1866.

53. ChowellG, MillerMA, ViboudC (2008) Seasonal influenza in the United States, France, and Australia: transmission and prospects for control. Epidemiol Infect 136: 852–864.

54. OpatowskiL, FraserC, GriffinJ, de SilvaE, Van KerkhoveMD, 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. BedfordT, CobeyS, BeerliP, PascualM (2010) Global migration dynamics underlie evolution and persistence of human influenza A (H3N2). PLoS Pathog 6: e1000918 doi:10.1371/journal.ppat.1000918

56. RussellCA, JonesTC, BarrIG, CoxNJ, GartenRJ, et al. (2008) The global circulation of seasonal influenza A (H3N2) viruses. Science 320: 340–346.

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