Skip to main content
Top
Published in: BMC Public Health 1/2014

Open Access 01-12-2014 | Research article

Climatic-driven seasonality of emerging dengue fever in Hanoi, Vietnam

Authors: Thi Thanh Toan Do, Pim Martens, Ngoc Hoat Luu, Pamela Wright, Marc Choisy

Published in: BMC Public Health | Issue 1/2014

Login to get access

Abstract

Background

Dengue fever (DF) has been emerging in Hanoi over the last decade. Both DF epidemiology and climate in Hanoi are strongly seasonal. This study aims at characterizing the seasonality of DF in Hanoi and its links to climatic variables as DF incidence increases from year to year.

Methods

Clinical suspected cases of DF from the 14 central districts of Hanoi were obtained from the Ministry of Health over a 8-year period (2002–2009). Wavelet decompositions were used to characterize the main periodic cycles of DF and climatic variables as well as the mean phase angles of these cycles. Cross-wavelet spectra between DF and each climatic variables were also computed. DF reproductive ratio was calculated from Soper’s formula and smoothed to highlight both its long-term trend and seasonality.

Results

Temperature, rainfall, and vapor pressure show strong seasonality. DF and relative humidity show both strong seasonality and a sub-annual periodicity. DF reproductive ratio is increasing through time and displays two clear peaks per year, reflecting the sub-annual periodicity of DF incidence. Temperature, rainfall and vapor pressure lead DF incidence by a lag of 8–10 weeks, constant through time. Relative humidity leads DF by a constant lag of 18 weeks for the annual cycle and a lag decreasing from 14 to 5 weeks for the sub-annual cycle.

Conclusion

Results are interpreted in terms of mosquito population dynamics and immunological interactions between the different dengue serotypes in the human compartment. Given its important population size, its strong seasonality and its dengue emergence, Hanoi offers an ideal natural experiment to test hypotheses on dengue serotypes interactions, knowledge of prime importance for vaccine development.
Appendix
Available only for authorised users
Literature
1.
go back to reference Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, Drake JM, Brownstein JS, Hoen AG, Sankoh O, Myers MF, George DB, Jaenisch T, William Wint GR, Simmons CP, Scott TW, Farrar JJ, Hay SI: The global distribution and burden of dengue. Nature. 2013, 496: 504-507. 10.1038/nature12060.CrossRefPubMedPubMedCentral Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, Drake JM, Brownstein JS, Hoen AG, Sankoh O, Myers MF, George DB, Jaenisch T, William Wint GR, Simmons CP, Scott TW, Farrar JJ, Hay SI: The global distribution and burden of dengue. Nature. 2013, 496: 504-507. 10.1038/nature12060.CrossRefPubMedPubMedCentral
2.
go back to reference Tien TKN, Ha DQ, Hien TK, Quang LC: Predictive indicators for forecasting epidemic of dengue/dengue haemorrhagic fever through epidemiological, virological and entomological surveillance. Dengue Bull. 1999, 23: 34-39. Tien TKN, Ha DQ, Hien TK, Quang LC: Predictive indicators for forecasting epidemic of dengue/dengue haemorrhagic fever through epidemiological, virological and entomological surveillance. Dengue Bull. 1999, 23: 34-39.
3.
go back to reference NIHE: Final Report on evaluation of communicable diseases surveillance system in Vietnam 2008. 2009, Hanoi: National Institute of Hygiene and Epidemiology NIHE: Final Report on evaluation of communicable diseases surveillance system in Vietnam 2008. 2009, Hanoi: National Institute of Hygiene and Epidemiology
4.
go back to reference Ha DQ, Ninh TU: Virological surveillance of dengue haemorrhagic fever in Vietnam, 1987–1999. Dengue Bull. 2000, 24: 18-23. Ha DQ, Ninh TU: Virological surveillance of dengue haemorrhagic fever in Vietnam, 1987–1999. Dengue Bull. 2000, 24: 18-23.
5.
go back to reference Cuong HQ, Hien NT, Duong TN, Phong TV, Cam NN, Farrar J, Nam VS, Thai KTD, Horby P: Quantifying the emergence of dengue in Hanoi, Vietnam: 1998–2009. PLoS Negl Trop Dis. 2011, 5 (9): e1322-10.1371/journal.pntd.0001322.CrossRefPubMedPubMedCentral Cuong HQ, Hien NT, Duong TN, Phong TV, Cam NN, Farrar J, Nam VS, Thai KTD, Horby P: Quantifying the emergence of dengue in Hanoi, Vietnam: 1998–2009. PLoS Negl Trop Dis. 2011, 5 (9): e1322-10.1371/journal.pntd.0001322.CrossRefPubMedPubMedCentral
6.
go back to reference Thai KTD, Cazelles B, Nguyen NV, Vo LT, Boni MF, Farrar J, Simmons CP, Rogier van Doorn H, de Vries PJ: Dengue Dynamics in Binh Thuan Province, Southern Vietnam: Periodicity, Synchronicity and Climate Variability. PLoS Negl Trop Dis. 2010, 4 (7): e747-10.1371/journal.pntd.0000747.CrossRefPubMedPubMedCentral Thai KTD, Cazelles B, Nguyen NV, Vo LT, Boni MF, Farrar J, Simmons CP, Rogier van Doorn H, de Vries PJ: Dengue Dynamics in Binh Thuan Province, Southern Vietnam: Periodicity, Synchronicity and Climate Variability. PLoS Negl Trop Dis. 2010, 4 (7): e747-10.1371/journal.pntd.0000747.CrossRefPubMedPubMedCentral
8.
go back to reference Toan DTT, Hu W, Thai PQ, Hoat LN, Wright P, Martens P: Hot spot detection and spatio-temporal dispersion of dengue fever in Hanoi, Vietnam. Global Health Action. 2013, 6: 18632-CrossRef Toan DTT, Hu W, Thai PQ, Hoat LN, Wright P, Martens P: Hot spot detection and spatio-temporal dispersion of dengue fever in Hanoi, Vietnam. Global Health Action. 2013, 6: 18632-CrossRef
9.
go back to reference Schreiber KV: An investigation of relationships between climate and dengue using a water budgeting technique. Int J Biometeorol. 2001, 45: 81-89. 10.1007/s004840100090.CrossRefPubMed Schreiber KV: An investigation of relationships between climate and dengue using a water budgeting technique. Int J Biometeorol. 2001, 45: 81-89. 10.1007/s004840100090.CrossRefPubMed
10.
go back to reference Hales S, de Wet N, Maindonald J, Woodward A: Potential effect of population and climate changes on global distribution of dengue fever: an empirical model. Lancet. 2002, 360 (9336): 830-834. 10.1016/S0140-6736(02)09964-6.CrossRefPubMed Hales S, de Wet N, Maindonald J, Woodward A: Potential effect of population and climate changes on global distribution of dengue fever: an empirical model. Lancet. 2002, 360 (9336): 830-834. 10.1016/S0140-6736(02)09964-6.CrossRefPubMed
11.
go back to reference Nagao Y, Tharava U, Chinumsup P, Tawatsin A, Chansang C, Campbell-Lendrum D: Climatic and social risk factors for Aedes infestation in rural Thailand. Trop Med Int Health. 2003, 8 (7): 650-659. 10.1046/j.1365-3156.2003.01075.x.CrossRefPubMed Nagao Y, Tharava U, Chinumsup P, Tawatsin A, Chansang C, Campbell-Lendrum D: Climatic and social risk factors for Aedes infestation in rural Thailand. Trop Med Int Health. 2003, 8 (7): 650-659. 10.1046/j.1365-3156.2003.01075.x.CrossRefPubMed
12.
go back to reference Depradine C, Lovell E: Climatological variables and the incidence of Dengue fever in Barbados. Int J Environ Health Res. 2004, 14 (6): 429-441. 10.1080/09603120400012868.CrossRefPubMed Depradine C, Lovell E: Climatological variables and the incidence of Dengue fever in Barbados. Int J Environ Health Res. 2004, 14 (6): 429-441. 10.1080/09603120400012868.CrossRefPubMed
13.
go back to reference Promprou S, Jaroensutasinee M, Jaroensutasinee K: Climatic factors affecting dengue haemorrhagic fever incidence in Southern Thailand. Dengue Bulletin. 2005, 29: 41-48. Promprou S, Jaroensutasinee M, Jaroensutasinee K: Climatic factors affecting dengue haemorrhagic fever incidence in Southern Thailand. Dengue Bulletin. 2005, 29: 41-48.
14.
go back to reference Promprou S, Jaroensutasinee M, Jaroensutasinee K: Impact of Climatic Factors on Dengue Haemorrhagic Fever Incidence in Southern Thailand. Walailak J Sci & Tech. 2005, 2 (1): 59-70. Promprou S, Jaroensutasinee M, Jaroensutasinee K: Impact of Climatic Factors on Dengue Haemorrhagic Fever Incidence in Southern Thailand. Walailak J Sci & Tech. 2005, 2 (1): 59-70.
15.
go back to reference Chowell G, Torre CA, Munayco_Escate C, Suarez-Ognio L, Lopez-Cruz R, Hyman JM, Castillo-Chavez C: Spatial and temporal dynamics of dengue fever in Peru: 1994–2006. Epidemiol Infect. 2008, 136 (12): 1667-1677. 10.1017/S0950268808000290.CrossRefPubMedPubMedCentral Chowell G, Torre CA, Munayco_Escate C, Suarez-Ognio L, Lopez-Cruz R, Hyman JM, Castillo-Chavez C: Spatial and temporal dynamics of dengue fever in Peru: 1994–2006. Epidemiol Infect. 2008, 136 (12): 1667-1677. 10.1017/S0950268808000290.CrossRefPubMedPubMedCentral
16.
go back to reference Hsieh YH, Chen CWS: Turning points, reproduction number, and impact of climatological events for multi-wave dengue outbreaks. Trop Med Int Health. 2009, 16: 1-11. Hsieh YH, Chen CWS: Turning points, reproduction number, and impact of climatological events for multi-wave dengue outbreaks. Trop Med Int Health. 2009, 16: 1-11.
17.
go back to reference Johansson MA, Dominici F, Glass GE: Local and global effects of climate on dengue transmission in Puerto Rico. PLoS Negl Trop Dis. 2009, 3 (2): e382-10.1371/journal.pntd.0000382.CrossRefPubMedPubMedCentral Johansson MA, Dominici F, Glass GE: Local and global effects of climate on dengue transmission in Puerto Rico. PLoS Negl Trop Dis. 2009, 3 (2): e382-10.1371/journal.pntd.0000382.CrossRefPubMedPubMedCentral
18.
go back to reference Lu L, Lin H, Tian L, Yang W, Sun J, Liu Q: Time series analysis of dengue fever and weather in Guangzhou, China. BMC Public Health. 2009, 9: 395-10.1186/1471-2458-9-395.CrossRefPubMedPubMedCentral Lu L, Lin H, Tian L, Yang W, Sun J, Liu Q: Time series analysis of dengue fever and weather in Guangzhou, China. BMC Public Health. 2009, 9: 395-10.1186/1471-2458-9-395.CrossRefPubMedPubMedCentral
19.
go back to reference Hu W, Clements A, William G, Tong S: Dengue fever and El Nino/Southern Oscillation in Queensland, Australia: a time series predictive model. Occup Environ Med. 2010, 67 (5): 307-311. 10.1136/oem.2008.044966.CrossRefPubMed Hu W, Clements A, William G, Tong S: Dengue fever and El Nino/Southern Oscillation in Queensland, Australia: a time series predictive model. Occup Environ Med. 2010, 67 (5): 307-311. 10.1136/oem.2008.044966.CrossRefPubMed
20.
go back to reference Wu P-C, Guo H-R, Lung SC, Lin CY, HJa S: Weather as an effective predictor for occurrence of dengue fever in Taiwan. Acta Trop. 2007, 103: 50-57. 10.1016/j.actatropica.2007.05.014.CrossRefPubMed Wu P-C, Guo H-R, Lung SC, Lin CY, HJa S: Weather as an effective predictor for occurrence of dengue fever in Taiwan. Acta Trop. 2007, 103: 50-57. 10.1016/j.actatropica.2007.05.014.CrossRefPubMed
21.
go back to reference Gharbi M, Quenel P, Gustave J, Cassadou S, La Ruche G, Girdary L, Marrama L: Time series analysis of dengue incidence in Guadeloupe, French West Indies: forecasting models using climate variables as predictors. BMC Infect Dis. 2011, 9 (11): 166-CrossRef Gharbi M, Quenel P, Gustave J, Cassadou S, La Ruche G, Girdary L, Marrama L: Time series analysis of dengue incidence in Guadeloupe, French West Indies: forecasting models using climate variables as predictors. BMC Infect Dis. 2011, 9 (11): 166-CrossRef
22.
go back to reference Pham HV, Doan HT, Thao TTP, Minh NNT: Ecological factors associated with dengue fever in a Central Highlands province, Vietnam. BMC Infect Dis. 2011, 11: 172-10.1186/1471-2334-11-172.CrossRefPubMedPubMedCentral Pham HV, Doan HT, Thao TTP, Minh NNT: Ecological factors associated with dengue fever in a Central Highlands province, Vietnam. BMC Infect Dis. 2011, 11: 172-10.1186/1471-2334-11-172.CrossRefPubMedPubMedCentral
23.
go back to reference Pinto E, Coelho M, Oliver L, Massad E: The influence of climate variables on dengue in Singapore. Int J Environ Health Res. 2011, 21 (6): 415-426. 10.1080/09603123.2011.572279.CrossRefPubMed Pinto E, Coelho M, Oliver L, Massad E: The influence of climate variables on dengue in Singapore. Int J Environ Health Res. 2011, 21 (6): 415-426. 10.1080/09603123.2011.572279.CrossRefPubMed
24.
go back to reference Descloux E, Mangeas M, Menkes CE, Lengaigne M, Leroy A, Tehei T, Guillaumot L, Teurlai M, Gourinat AC, Benzler J, Pfannstiel A, Grangeon JP, Degallier N, Lamballerie X: Climate-based models for understanding and forecasting dengue epidemics. PLoS Negl Trop Dis. 2012, 6 (2): e1470-10.1371/journal.pntd.0001470.CrossRefPubMedPubMedCentral Descloux E, Mangeas M, Menkes CE, Lengaigne M, Leroy A, Tehei T, Guillaumot L, Teurlai M, Gourinat AC, Benzler J, Pfannstiel A, Grangeon JP, Degallier N, Lamballerie X: Climate-based models for understanding and forecasting dengue epidemics. PLoS Negl Trop Dis. 2012, 6 (2): e1470-10.1371/journal.pntd.0001470.CrossRefPubMedPubMedCentral
25.
go back to reference Hsieh YH, de Arazoza H, Lounes R: Temporal trends and regional variability of 2001–2002 multiwave DENV-3 epidemic in Havana City: did Hurricane Michelle contribute to its severity?. Trop Med Int Health. 2013, 18 (7): 830-838. 10.1111/tmi.12105.CrossRefPubMed Hsieh YH, de Arazoza H, Lounes R: Temporal trends and regional variability of 2001–2002 multiwave DENV-3 epidemic in Havana City: did Hurricane Michelle contribute to its severity?. Trop Med Int Health. 2013, 18 (7): 830-838. 10.1111/tmi.12105.CrossRefPubMed
26.
go back to reference Eastin MD, Delmelle E, Casas I, Wexler J, Self C: Intra- and inter-seasonal autoregressive prediction of dengue outbreaks using local weather and regional climate for a tropical environment in Colombia. Am J Trop Med Hyg. 2014, Available online at http://www.ajtmh.org/content/early/recent since 23 June 2014 Eastin MD, Delmelle E, Casas I, Wexler J, Self C: Intra- and inter-seasonal autoregressive prediction of dengue outbreaks using local weather and regional climate for a tropical environment in Colombia. Am J Trop Med Hyg. 2014, Available online at http://​www.​ajtmh.​org/​content/​early/​recent since 23 June 2014
27.
go back to reference Yi B, Zhang Z, Xu D, Xi Y, Fu J, Luo J, Yuan M, Liu S, Zuo Z: Relationship of dengue fever epidemic to Aedes density changed by climate factors in Guangdong Province. Wei Sheng Yan Jiu. 2003, 32 (2): 152-154.PubMed Yi B, Zhang Z, Xu D, Xi Y, Fu J, Luo J, Yuan M, Liu S, Zuo Z: Relationship of dengue fever epidemic to Aedes density changed by climate factors in Guangdong Province. Wei Sheng Yan Jiu. 2003, 32 (2): 152-154.PubMed
28.
go back to reference Shaman J, Kohn M: Absolute humidity modulates influenza survival, transmission, and seasonality. Proc Natl Acad Sci U S A. 2009, 106 (9): 3243-3248. 10.1073/pnas.0806852106.CrossRefPubMedPubMedCentral Shaman J, Kohn M: Absolute humidity modulates influenza survival, transmission, and seasonality. Proc Natl Acad Sci U S A. 2009, 106 (9): 3243-3248. 10.1073/pnas.0806852106.CrossRefPubMedPubMedCentral
30.
go back to reference Wallace JM, Hobbs PV: Atmospheric Science, An Introductory Survey. Academic New York. 2006, 2 Wallace JM, Hobbs PV: Atmospheric Science, An Introductory Survey. Academic New York. 2006, 2
31.
go back to reference Cazelles B, Chavez M, McMichael AJ, Hales S: Nonstationary influence of El Niño on the synchronous dengue epidemics in Thailand. PLoS Med. 2005, 2: 313-318. 10.1371/journal.pmed.0020313.CrossRef Cazelles B, Chavez M, McMichael AJ, Hales S: Nonstationary influence of El Niño on the synchronous dengue epidemics in Thailand. PLoS Med. 2005, 2: 313-318. 10.1371/journal.pmed.0020313.CrossRef
32.
go back to reference Cazelles B, Hales S: Infectious Diseases, Climate Influences, and Nonstationarity. PLoS Med. 2006, 3 (8): 328-10.1371/journal.pmed.0030328.CrossRef Cazelles B, Hales S: Infectious Diseases, Climate Influences, and Nonstationarity. PLoS Med. 2006, 3 (8): 328-10.1371/journal.pmed.0030328.CrossRef
33.
go back to reference Simões TC, Codeço CT, Nobre AA, Eiras AE: Modeling the Non-Stationary Climate Dependent Temporal Dynamics of Aedes aegypti. PLoS One. 2013, 8 (8): e64773-10.1371/journal.pone.0064773.CrossRefPubMedPubMedCentral Simões TC, Codeço CT, Nobre AA, Eiras AE: Modeling the Non-Stationary Climate Dependent Temporal Dynamics of Aedes aegypti. PLoS One. 2013, 8 (8): e64773-10.1371/journal.pone.0064773.CrossRefPubMedPubMedCentral
34.
go back to reference Cazelles B, Chavez M, Constantin de Magny G, Guegan JF, Hales S: Time-dependent spectral analysis of epidemiological time-series with wavelets. J R Soc Interface. 2007, 4 (15): 625-636. 10.1098/rsif.2007.0212.CrossRefPubMedPubMedCentral Cazelles B, Chavez M, Constantin de Magny G, Guegan JF, Hales S: Time-dependent spectral analysis of epidemiological time-series with wavelets. J R Soc Interface. 2007, 4 (15): 625-636. 10.1098/rsif.2007.0212.CrossRefPubMedPubMedCentral
35.
go back to reference Torrence C, Compo GP: A practical guide to wavelet analysis. Bull Am Meteorol Soc. 1998, 79: 61-78. 10.1175/1520-0477(1998)079<0061:APGTWA>2.0.CO;2.CrossRef Torrence C, Compo GP: A practical guide to wavelet analysis. Bull Am Meteorol Soc. 1998, 79: 61-78. 10.1175/1520-0477(1998)079<0061:APGTWA>2.0.CO;2.CrossRef
36.
go back to reference Soper HE: The Interpretation of Periodicity in Disease Prevalence. Roy Stat Soc A. 1929, 92: 34-61. 10.2307/2341437.CrossRef Soper HE: The Interpretation of Periodicity in Disease Prevalence. Roy Stat Soc A. 1929, 92: 34-61. 10.2307/2341437.CrossRef
37.
go back to reference Keeling MJ, Rohani P: Modeling Infectious Diseases in Humans and Animals. Princeton University Press. 2008, 5: 155-189. Keeling MJ, Rohani P: Modeling Infectious Diseases in Humans and Animals. Princeton University Press. 2008, 5: 155-189.
38.
go back to reference Andraud M, Hens N, Marais C, Beutels P: Dynamic epidemiological models for dengue transmission: a systematic review of structural approaches. PLoS One. 2012, 7 (11): e49085-10.1371/journal.pone.0049085.CrossRefPubMedPubMedCentral Andraud M, Hens N, Marais C, Beutels P: Dynamic epidemiological models for dengue transmission: a systematic review of structural approaches. PLoS One. 2012, 7 (11): e49085-10.1371/journal.pone.0049085.CrossRefPubMedPubMedCentral
39.
go back to reference RCoreTeam: R: A Language and Environment for Statistical Computing R. 2012, Vienna, Austria: Foundation for Statistical Computing RCoreTeam: R: A Language and Environment for Statistical Computing R. 2012, Vienna, Austria: Foundation for Statistical Computing
42.
go back to reference Thu HM, Aye KM, Thein S: The effect of temperature and humidity on dengue virus propagation in Aedes aegypti mosquitoes. Southeast Asian J Trop Med Public Health. 1998, 29: 280-284.PubMed Thu HM, Aye KM, Thein S: The effect of temperature and humidity on dengue virus propagation in Aedes aegypti mosquitoes. Southeast Asian J Trop Med Public Health. 1998, 29: 280-284.PubMed
43.
go back to reference Tipayamongkholgul M, Fang C-T, Klinchan S, Liu CM, King CC: Effects of the El Niño-Southern Oscillation on dengue epidemics in Thailand, 1996–2005. BMC Public Health. 2009, 9: 422-10.1186/1471-2458-9-422.CrossRefPubMedPubMedCentral Tipayamongkholgul M, Fang C-T, Klinchan S, Liu CM, King CC: Effects of the El Niño-Southern Oscillation on dengue epidemics in Thailand, 1996–2005. BMC Public Health. 2009, 9: 422-10.1186/1471-2458-9-422.CrossRefPubMedPubMedCentral
44.
go back to reference Wongkoon S, Jaroensutasinee M, Jaroensutasinee K: Climatic variability and dengue virus transmission in Chiang Rai, Thailand. Biomedica. 2011, 27 (19): 5-13. Wongkoon S, Jaroensutasinee M, Jaroensutasinee K: Climatic variability and dengue virus transmission in Chiang Rai, Thailand. Biomedica. 2011, 27 (19): 5-13.
45.
go back to reference Higa Y, Yen NT, Kawada H, Son TH, Hoa NT, Takagi M: Geographic Distribution of Aedes aegypti and Aedes albopicuts Collected from Used Tires in Vietnam. Am Mosq Control Assoc. 2010, 26 (1): 1-9. 10.2987/09-5945.1.CrossRef Higa Y, Yen NT, Kawada H, Son TH, Hoa NT, Takagi M: Geographic Distribution of Aedes aegypti and Aedes albopicuts Collected from Used Tires in Vietnam. Am Mosq Control Assoc. 2010, 26 (1): 1-9. 10.2987/09-5945.1.CrossRef
46.
go back to reference Recker M, Blyuss KB, Simmons CP, Hien TT, Wills B, Farrar J, Gupta S: Immunological serotype interactions and their effect on the epidemiological pattern of dengue. Proc R Soc B. 2009, 276 (1667): 2541-2548. 10.1098/rspb.2009.0331.CrossRefPubMedPubMedCentral Recker M, Blyuss KB, Simmons CP, Hien TT, Wills B, Farrar J, Gupta S: Immunological serotype interactions and their effect on the epidemiological pattern of dengue. Proc R Soc B. 2009, 276 (1667): 2541-2548. 10.1098/rspb.2009.0331.CrossRefPubMedPubMedCentral
Metadata
Title
Climatic-driven seasonality of emerging dengue fever in Hanoi, Vietnam
Authors
Thi Thanh Toan Do
Pim Martens
Ngoc Hoat Luu
Pamela Wright
Marc Choisy
Publication date
01-12-2014
Publisher
BioMed Central
Published in
BMC Public Health / Issue 1/2014
Electronic ISSN: 1471-2458
DOI
https://doi.org/10.1186/1471-2458-14-1078

Other articles of this Issue 1/2014

BMC Public Health 1/2014 Go to the issue