The influence of climatic conditions on the transmission dynamics of the 2009 A/H1N1 influenza pandemic in Chile

BMC Infectious Diseases

Andrea Olea²  Jose E Villarroel²  Monica Chiu²  Claudia Villarroel⁶  Mauricio Lima³  Mark A Miller⁵  Lone Simonsen¹  Viviana Sotomayor²  Rodrigo Fuentes²  Cécile Viboud⁵  Sherry Towers⁴  Gerardo Chowell⁵ 

[1] Department of Global Health, School of Public Health and Health Services, George Washington University, Washington DC, USA;Department of Epidemiology, Ministerio de Salud, Santiago, Chile;Center for Advanced Studies in Ecology and Biodiversity, Pontificia Universidad Católica de Chile, Santiago, Chile;Department of Mathematics, Purdue University, West Lafayette, IN, USA;Division of Epidemiology and Population Studies, Fogarty International Center, National Institutes of Health, Bethesda, MD, USA;Applied Meteorology, Dirección Meteorológica de Chile, Santiago, Chile

关键词: Chile;    Temperature;    Climatological variables, Specific humidity;    School cycles;    Spatial heterogeneity;    Reproduction number;    Influenza-like-illness;    Acute respiratory infection;    A/H1N1 influenza pandemic;   

Others  :  1159592
DOI  :  10.1186/1471-2334-12-298

 received in 2012-04-17, accepted in 2012-11-05,  发布年份 2012

【 摘 要 】

Background

The role of demographic factors, climatic conditions, school cycles, and connectivity patterns in shaping the spatio-temporal dynamics of pandemic influenza is not clearly understood. Here we analyzed the spatial, age and temporal evolution of the 2009 A/H1N1 influenza pandemic in Chile, a southern hemisphere country covering a long and narrow strip comprising latitudes 17°S to 56°S.

Methods

We analyzed the dissemination patterns of the 2009 A/H1N1 pandemic across 15 regions of Chile based on daily hospitalizations for severe acute respiratory disease and laboratory confirmed A/H1N1 influenza infection from 01-May to 31-December, 2009. We explored the association between timing of pandemic onset and peak pandemic activity and several geographical and demographic indicators, school vacations, climatic factors, and international passengers. We also estimated the reproduction number (R) based on the growth rate of the exponential pandemic phase by date of symptoms onset, estimated using maximum likelihood methods.

Results

While earlier pandemic onset was associated with larger population size, there was no association with connectivity, demographic, school or climatic factors. In contrast, there was a latitudinal gradient in peak pandemic timing, representing a 16-39-day lag in disease activity from the southern regions relative to the northernmost region (P < 0.001). Geographical differences in latitude of Chilean regions, maximum temperature and specific humidity explained 68.5% of the variability in peak timing (P = 0.01). In addition, there was a decreasing gradient in reproduction number from south to north Chile (P < 0.0001). The regional mean R estimates were 1.6-2.0, 1.3-1.5, and 1.2-1.3 for southern, central and northern regions, respectively, which were not affected by the winter vacation period.

Conclusions

There was a lag in the period of most intense 2009 pandemic influenza activity following a South to North traveling pattern across regions of Chile, significantly associated with geographical differences in minimum temperature and specific humidity. The latitudinal gradient in timing of pandemic activity was accompanied by a gradient in reproduction number (P < 0.0001). Intensified surveillance strategies in colder and drier southern regions could lead to earlier detection of pandemic influenza viruses and improved control outcomes.

【 授权许可】

   
2012 Chowell et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】

• [1]Chowell G, Echevarría-Zuno S, Viboud C, Simonsen L, Tamerius J, Miller MA, Borja-Aburto VH: Characterizing the Epidemiology of the 2009 Influenza A/H1N1 Pandemic in Mexico. PloS Medicine 2011, 8(5):e1000436.
• [2]Chowell G, Viboud C, Munayco CV, Gomez J, Simonsen L, Miller MA, Tamerius J, Fiestas V, Halsey ES, Laguna-Torres VA: Spatial and temporal characteristics of the 2009 A/H1N1 influenza pandemic in Peru. PLoS One 2011, 6(6):e21287.
• [3]Chao DL, Elizabeth Halloran M, Longini IM Jr: School Opening Dates Predict Pandemic Influenza A(H1N1) Outbreaks in the United States. J Infect Dis 2010, 202(6):877-880.
• [4]Wu JT, Cowling BJ, Lau EH, Ip DK, Ho LM, Tsang T, Chuang SK, Leung PY, Lo SV, Liu SH, et al.: School closure and mitigation of pandemic (H1N1) 2009, Hong Kong. Emerg Infect Dis 2010, 16(3):538-541.
• [5]Opatowski L, Fraser C, Griffin J, de Silva E, Van Kerkhove MD, Lyons EJ, Cauchemez S, Ferguson NM: Transmission characteristics of the 2009 H1N1 influenza pandemic: comparison of 8 Southern hemisphere countries. PLoS Pathog 2011, 7(9):e1002225.
• [6]Tamerius J, Nelson MI, Zhou SZ, Viboud C, Miller MA, Alonso WJ: Global influenza seasonality: reconciling patterns across temperate and tropical regions. Environ Health Perspect 2011, 119(4):439-445.
• [7]Tang JW: The effect of environmental parameters on the survival of airborne infectious agents. J R Soc Interface 2009, 6(Suppl 6):S737-S746.
• [8]Steel J, Staeheli P, Mubareka S, Garcia-Sastre A, Palese P, Lowen AC: Transmission of pandemic H1N1 influenza virus and impact of prior exposure to seasonal strains or interferon treatment. J Virol 2011, 84(1):21-26.
• [9]H1N1 Flu. Centers for Disease Control and Prevention. Available from: http://www.cdc.gov/h1n1flu/qa.htm webcite
• [10]Ghani AC, Baguelin M, Griffin J, Flasche S, Pebody R, van Hoek AJ, Cauchemez S, Hall IM, Donnelly C, Robertson C, et al.: The Early Transmission Dynamics of H1N1pdm Influenza in the United Kingdom. PLoS Curr Influenza 2010. RRN1130
• [11]Ministerio de Salud de Argentina. Situacion de Influenza A(H1N1) - Parte 87. Available from. http://municipios.msal.gov.ar/h1n1/parte_influenza/parte_87_28-01-2010.pdf webcite (accessed on 02/17/2010)
• [12]Investigators AI, Webb S, Pettilä V, Seppelt I, Bellomo R, Bailey M, Cooper D, Cretikos M, Davies A, Finfer S, et al.: Critical Care Services and 2009 H1N1 Influenza in Australia and New Zealand. N Engl J Med 2009, 361(20):1925-1934.
• [13]Bishop JF, Murnane MP, Owen R: Australia's winter with the 2009 pandemic influenza A (H1N1) virus. N Engl J Med 2009, 361(27):2591-2594.
• [14]Gog JR, Ballesteros S, Viboud C, Simonsen L, Edelman L, Grenfell BT: Spatio-temporal patterns of the 2009 pandemic influenza in the US. In The Third International Conference on Infectious Disease Dynamics. Boston, MA, USA; 2011.
• [15]Shaman J, Goldstein E, Lipsitch M: Absolute humidity and pandemic versus epidemic influenza. Am J Epidemiol 2011, 173(2):127-135.
• [16]Swine influenza A (H1N1) infection in two children--Southern California, March-April 2009 MMWR Morb Mortal Wkly Rep 2009, 58(15):400-402.
• [17]Outbreak of swine-origin influenza A (H1N1) virus infection - Mexico, March-April 2009 MMWR Morb Mortal Wkly Rep 2009, 58(17):467-470.
• [18]Van Kerkhove MD, Mounts AW, Mall S, Vandemaele KA, Chamberland M, dos Santos T, Fitzner J, Widdowson MA, Michalove J, Bresee J, et al.: Epidemiologic and virologic assessment of the 2009 influenza A (H1N1) pandemic on selected temperate countries in the Southern Hemisphere: Argentina, Australia, Chile, New Zealand and South Africa. Influenza Other Respi Viruses 2011, 5(6):e487-e498.
• [19]Ugarte S, Arancibia F, Soto R: Influenza A pandemics: clinical and organizational aspects: the experience in Chile. Crit Care Med 2010, 38(4):133-137.
• [20]Lessler J, dos Santos T, Aguilera X, Brookmeyer R, Cummings DA: H1N1pdm in the Americas. Epidemics 2010, 2(3):132-138.
• [21]Ministerio de Salud, Chile. Influenza Pandemica (H1N1) 2009. Circular de vigilancia epidemiológica de influenza. Available from: http://epi.minsal.cl/epi/html/normas/circul/CircularInfluenzaESTACIONALyPANDEMICA.pdf webcite
• [22]Fang LQ, Wang LP, de Vlas SJ, Liang S, Tong SL, Li YL, Li YP, Qian Q, Yang H, Zhou MG, et al.: Distribution and risk factors of 2009 pandemic influenza A (H1N1) in mainland China. Am J Epidemiol 2012, 175(9):890-897.
• [23]Instituto Nacional de Estadísticas (INE). Estadísticas Demográficas y Vitales, 2009. Available from: http://www.ine.cl/canales/chile_estadistico/demografia_y_vitales/demo_y_vita.php webcite
• [24]Lowen AC, Mubareka S, Steel J, Palese P: Influenza virus transmission is dependent on relative humidity and temperature. PLoS Pathog 2007, 3(10):1470-1476.
• [25]Steel J, Palese P, Lowen AC: Transmission of a 2009 pandemic influenza virus shows a sensitivity to temperature and humidity similar to that of an H3N2 seasonal strain. J Virol 2011, 85(3):1400-1402.
• [26]Lowen AC, Steel J, Mubareka S, Palese P: High temperature (30 degrees C) blocks aerosol but not contact transmission of influenza virus. J Virol 2008, 82(11):5650-5652.
• [27]Mubareka S, Lowen AC, Steel J, Coates AL, Garcia-Sastre A, Palese P: Transmission of influenza virus via aerosols and fomites in the guinea pig model. J Infect Dis 2009, 199(6):858-865.
• [28]Shaman J, Kohn M: Absolute humidity modulates influenza survival, transmission, and seasonality. Proc Natl Acad Sci U S A 2009, 106(9):3243-3248.
• [29]Shaman J, Pitzer VE, Viboud C, Grenfell BT, Lipsitch M: Absolute humidity and the seasonal onset of influenza in the continental United States. PLoS Biol 2010, 8(2):e1000316.
• [30]Dirección Meteorológica de Chile. Accessed: 01/2012. Website: http://www.meteochile.cl/ webcite
• [31]Junta de Aeronáutica Civil (JAC). Air traffic statistics for 2009. Available from: http://www.jac-chile.cl/estadisticas/15-informes-estadisticos-mensuales-del-trafico-aereo/17-estadisticas-ano-2009.html webcite
• [32]Armada de Chile. General Directorate of Maritime Territory and Merchant Marine (DIRECTEMAR). Maritime Statistical Bulletin 2010. Available from: http://web.directemar.cl/estadisticas/maritimo/h_default.htm webcite
• [33]Cliff AD, Ord JK: Spatial processes: models and applications. Pion Limited, London; 1981.
• [34]Edgington ES, Onghena P: Randomization tests. Chapman & Hall/CRC, Boca Raton, Florida; 2007.
• [35]Monto AS, Koopman JS, Longini IM Jr: Tecumseh study of illness. XIII. Influenza infection and disease, 1976–1981. Am J Epidemiol 1985, 121(6):811-822.
• [36]Cauchemez S, Ferguson NM, Wachtel C, Tegnell A, Saour G, Duncan B, Nicoll A: Closure of schools during an influenza pandemic. Lancet Infect Dis 2009, 9(8):473-481.
• [37]Cauchemez S, Valleron AJ, Boelle PY, Flahault A, Ferguson NM: Estimating the impact of school closure on influenza transmission from Sentinel data. Nature 2008, 452(7188):750-754.
• [38]Chowell G, Viboud C, Simonsen L, Miller MA: Measuring the benefits of school closure interventions to mitigate influenza. Expert Rev Respir Med 2011, 5(5):597-599.
• [39]Anderson RM, May RM: Infectious diseases of humans. Oxford University Press, Oxford; 1991.
• [40]Chowell G, Ammon CE, Hengartner NW, Hyman JM: Estimation of the reproductive number of the Spanish flu epidemic in Geneva, Switzerland. Vaccine 2006, 24(44–46):6747-6750.
• [41]Wallinga J, Lipsitch M: How generation intervals shape the relationship between growth rates and reproductive numbers. Proc Biol Sci 2007, 274(1609):599-604.
• [42]Lipsitch M, Cohen T, Cooper B, Robins JM, Ma S, James L, Gopalakrishna G, Chew SK, Tan CC, Samore MH, et al.: Transmission dynamics and control of severe acute respiratory syndrome. Science 2003, 300(5627):1966-1970.
• [43]Fraser C, Donnelly CA, Cauchemez S, Hanage WP, Van Kerkhove MD, Hollingsworth TD, Griffin J, Baggaley RF, Jenkins HE, Lyons EJ, et al.: Pandemic potential of a strain of influenza A (H1N1): early findings. Science 2009, 324(5934):1557-1561.
• [44]Yang Y, Sugimoto JD, Halloran ME, Basta NE, Chao DL, Matrajt L, Potter G, Kenah E, Longini IM Jr: The transmissibility and control of pandemic influenza A (H1N1) virus. Science 2009, 326(5953):729-733.
• [45]Cauchemez S, Donnelly CA, Reed C, Ghani AC, Fraser C, Kent CK, Finelli L, Ferguson NM: Household transmission of 2009 pandemic influenza A (H1N1) virus in the United States. N Engl J Med 2009, 361(27):2619-2627.
• [46]Cowling BJ, Chan KH, Fang VJ, Lau LL, So HC, Fung RO, Ma ES, Kwong AS, Chan CW, Tsui WW, et al.: Comparative epidemiology of pandemic and seasonal influenza A in households. N Engl J Med 2010, 362(23):2175-2184.
• [47]Torres JP, O'Ryan M, Herve B, Espinoza R, Acuna G, Manalich J, Chomali M: Impact of the novel influenza A (H1N1) during the 2009 autumn-winter season in a large hospital setting in Santiago, Chile. Clin Infect Dis 2010, 50(6):860-868.
• [48]Pedroni E, Garcia M, Espinola V, Guerrero A, Gonzalez C, Olea A, Calvo M, Martorell B, Winkler M, Carrasco M, et al.: Outbreak of 2009 pandemic influenza A(H1N1), Los Lagos, Chile, April-June 2009. Euro Surveill 2010, 15(1):pii: 19456.
• [49]Schuck-Paim C, Viboud C, Simonsen L, Miller MA, Moura FE, Fernandes RM, Carvalho ML, Alonso WJ: Were equatorial regions less affected by the 2009 influenza pandemic? The brazilian experience. PLoS One 2012, 7(8):e41918.
• [50]Alonso WJ, Viboud C, Simonsen L, Hirano EW, Daufenbach LZ, Miller MA: Seasonality of influenza in Brazil: a traveling wave from the Amazon to the subtropics. Am J Epidemiol 2007, 165(12):1434-1442.
• [51]Chowell G, Viboud C, Simonsen L, Miller M, Alonso WJ: The reproduction number of seasonal influenza epidemics in Brazil, 1996–2006. Proc Biol Sci 2010, 277(1689):1857-1866.
• [52]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):447-451.
• [53]Chowell G, Bettencourt LM, Johnson N, Alonso WJ, Viboud C: The 1918–1919 influenza pandemic in England and Wales: spatial patterns in transmissibility and mortality impact. Proc Biol Sci 2008, 275(1634):501-509.
• [54]Eggo RM, Cauchemez S, Ferguson NM: Spatial dynamics of the 1918 influenza pandemic in England, Wales and the United States. J R Soc Interface 2011, 8(55):233-243.
• [55]Hsieh YH: Pandemic influenza A (H1N1) during winter influenza season in the southern hemisphere. Influenza Other Respi Viruses 2010, 4(4):187-197.
• [56]Nishiura H, Chowell G, Safan M, Castillo-Chavez C: Pros and cons of estimating the reproduction number from early epidemic growth rate of influenza A (H1N1) 2009. Theor Biol Med Model 2010, 7:1. BioMed Central Full Text
• [57]Paine S, Mercer GN, Kelly PM, Bandaranayake D, Baker MG, Huang QS, Mackereth G, Bissielo A, Glass K, Hope V: Transmissibility of 2009 pandemic influenza A(H1N1) in New Zealand: effective reproduction number and influence of age, ethnicity and importations. Euro Surveill 2010, 15(24):pii: 19591.
• [58]McBryde E, Bergeri I, van Gemert C, Rotty J, Headley E, Simpson K, Lester R, Hellard M, Fielding J: Early transmission characteristics of influenza A(H1N1)v in Australia: Victorian state, 16 May - 3 June 2009. Euro Surveill 2009, 14(42):pii: 19363.
• [59]Tuite AR, Greer AL, Whelan M, Winter AL, Lee B, Yan P, Wu J, Moghadas S, Buckeridge D, Pourbohloul B, et al.: Estimated epidemiologic parameters and morbidity associated with pandemic H1N1 influenza. CMAJ 2010, 182(2):131-136.
• [60]White LF, Wallinga J, Finelli L, Reed C, Riley S, Lipsitch M, Pagano M: Estimation of the reproductive number and the serial interval in early phase of the 2009 influenza A/H1N1 pandemic in the USA. Influenza Other Respi Viruses 2009, 3(6):267-276.
• [61]Dorigatti I, Cauchemez S, Pugliese A, Ferguson NM: A new approach to characterising infectious disease transmission dynamics from sentinel surveillance: Application to the Italian 2009–2010 A/H1N1 influenza pandemic. Epidemics 2011, 4(1):9-21.
• [62]Nishiura H, Wilson N, Baker MG: Estimating the reproduction number of the novel influenza A virus (H1N1) in a Southern Hemisphere setting: preliminary estimate in New Zealand. N Z Med J 2009, 122(1299):73-77.
• [63]Balcan D, Hu H, Goncalves B, Bajardi P, Poletto C, Ramasco JJ, Paolotti D, Perra N, Tizzoni M, Van den Broeck W, et al.: Seasonal transmission potential and activity peaks of the new influenza A(H1N1): a Monte Carlo likelihood analysis based on human mobility. BMC Med 2009, 7:45. BioMed Central Full Text
• [64]Nishiura H, Castillo-Chavez C, Safan M, Chowell G: Transmission potential of the new influenza A(H1N1) virus and its age-specificity in Japan. Euro Surveill 2009, 14(22):pii: 19227.
• [65]Lessler J, Reich NG, Cummings DA, Nair HP, Jordan HT, Thompson N: Outbreak of 2009 pandemic influenza A (H1N1) at a New York City school. N Engl J Med 2009, 361(27):2628-2636.
• [66]Secretaria de Salud. Current situation of the 2009 H1N1pdm influenza pandemic in Mexico [In Spanish]. Available from: http://portal.salud.gob.mx/sites/salud/descargas/pdf/influenza/situacion_actual_epidemia_091209.pdf webcite (accessed on 12/15/2009)
• [67]Chowell G, Nishiura H, Bettencourt LM: Comparative estimation of the reproduction number for pandemic influenza from daily case notification data. J R Soc Interface 2007, 4(12):155-166.
• [68]Katriel G, Yaari R, Huppert A, Roll U, Stone L: Modelling the initial phase of an epidemic using incidence and infection network data: 2009 H1N1 pandemic in Israel as a case study. J R Soc Interface 2011, 8(59):856-867.
• [69]Nishiura H, Roberts MG: Estimation of the reproduction number for 2009 pandemic influenza A(H1N1) in the presence of imported cases. Euro Surveill 2011, 15(29):pii: 19622.