The Role of Climate Variability in the Spread of Malaria in Bangladeshi Highlands

Background Malaria is a major public health problem in Bangladesh, frequently occurring as epidemics since the 1990s. Many factors affect increases in malaria cases, including changes in land use, drug resistance, malaria control programs, socioeconomic issues, and climatic factors. No study has examined the relationship between malaria epidemics and climatic factors in Bangladesh. Here, we investigate the relationship between climatic parameters [rainfall, temperature, humidity, sea surface temperature (SST), El Niño-Southern Oscillation (ENSO), the normalized difference vegetation index (NDVI)], and malaria cases over the last 20 years in the malaria endemic district of Chittagong Hill Tracts (CHT). Methods and Principal Findings Monthly malaria case data from January 1989 to December 2008, monthly rainfall, temperature, humidity sea surface temperature in the Bay of Bengal and ENSO index at the Niño Region 3 (NIÑO3) were used. A generalized linear negative binomial regression model was developed using the number of monthly malaria cases and each of the climatic parameters. After adjusting for potential mutual confounding between climatic factors there was no evidence for any association between the number of malaria cases and temperature, rainfall and humidity. Only a low NDVI was associated with an increase in the number of malaria cases. There was no evidence of an association between malaria cases and SST in the Bay of Bengal and NIÑO3. Conclusion and Significance It seems counterintuitive that a low NDVI, an indicator of low vegetation greenness, is associated with increases in malaria cases, since the primary vectors in Bangladesh, such as An. dirus, are associated with forests. This relationship can be explained by the drying up of rivers and streams creating suitable breeding sites for the vector fauna. Bangladesh has very high vector species diversity and vectors suited to these habitats may be responsible for the observed results.

[1]  R. C. Thomson.  Studies on the Behaviour of Anopheles minimus. Part I. The Selection of the Breeding Place and the Influence of Light and Shade. , 1940 .

[2]  R. Rosenberg,et al.  Forest malaria in Bangladesh. I. Parasitology. , 1982, The American journal of tropical medicine and hygiene.

[3]  R. Rosenberg.  Forest malaria in Bangladesh. III. Breeding habits of anopheles dirus. , 1982, The American journal of tropical medicine and hygiene.

[4]  R. Simon,et al.  Flexible regression models with cubic splines. , 1989, Statistics in medicine.

[5]  M. Loevinsohn,et al.  Climatic warming and increased malaria incidence in Rwanda , 1994, The Lancet.

[6]  Thomas M. Smith,et al.  Improved Global Sea Surface Temperature Analyses Using Optimum Interpolation , 1994 .

[7]  J Rotmans,et al.  Potential impact of global climate change on malaria risk. , 1995, Environmental health perspectives.

[8]  M. Bouma,et al.  The EI Niño Southern Oscillation and the historic malaria epidemics on the Indian subcontinent and Sri Lanka: an early warning system for future epidemics? , 1996, Tropical medicine & international health : TM & IH.

[9]  R. Gupta.  Correlation of rainfall with upsurge of malaria in Rajasthan. , 1996, The Journal of the Association of Physicians of India.

[10]  J. Jones,et al.  Climate change and human health. , 1997, South African medical journal = Suid-Afrikaanse tydskrif vir geneeskunde.

[11]  F. L. Almeida,et al.  Monitoring the abundance of Aedes (Ochlerotatus) albifasciatus (Macquart 1838) (Diptera: Culicidae) to the south of Mar Chiquita Lake, central Argentina, with the aid of remote sensing. , 1997, Annals of tropical medicine and parasitology.

[12]  B. Goswami,et al.  A dipole mode in the tropical Indian Ocean , 1999, Nature.

[13]  K. Lindblade,et al.  Highland malaria in Uganda: prospective analysis of an epidemic associated with El Niño. , 1999, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[14]  A. Talisuna,et al.  Rainfall pattern, El Niño and malaria in Uganda. , 1999, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[15]  Malaria, 1982-1997. , 1999, Releve epidemiologique hebdomadaire.

[16]  Joel Schwartz,et al.  Transitional Regression Models, with Application to Environmental Time Series , 2000 .

[17]  Steven W Lindsay,et al.  Effect of 1997–98 EI Niño on highland malaria in Tanzania , 2000, The Lancet.

[18]  J. Patz,et al.  Effects of environmental change on emerging parasitic diseases. , 2000, International journal for parasitology.

[19]  Mutsuo Kobayashi,et al.  Analysis of malaria endemic areas on the Indochina Peninsula using remote sensing. , 2002, Japanese journal of infectious diseases.

[20]  V. Sharma,et al.  Patterns of rainfall and malaria in Madhya Pradesh, central India , 2002, Annals of tropical medicine and parasitology.

[21]  Thomas M. Smith,et al.  An Improved In Situ and Satellite SST Analysis for Climate , 2002 .

[22]  Shilu Tong,et al.  Climatic variables and transmission of malaria: a 12-year data analysis in Shuchen County, China. , 2003, Public health reports.

[23]  C. Wongsrichanalai,et al.  Drug-resistant malaria in Bangladesh: an in vitro assessment. , 2003, The American journal of tropical medicine and hygiene.

[24]  R. Sutherst,et al.  Global Change and Human Vulnerability to Vector-Borne Diseases , 2004, Clinical Microbiology Reviews.

[25]  A. Githeko,et al.  Association between climate variability and malaria epidemics in the East African highlands. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[26]  S. Hay,et al.  Climate variability and malaria epidemics in the highlands of East Africa. , 2005, Trends in parasitology.

[27]  M. Thomson,et al.  Use of rainfall and sea surface temperature monitoring for malaria early warning in Botswana. , 2005, The American journal of tropical medicine and hygiene.

[28]  S. Tong,et al.  El Nino-Southern Oscillation and vector-borne diseases in Anhui, China. , 2005, Vector borne and zoonotic diseases.

[29]  Weltgesundheitsorganisation.  World malaria report , 2005 .

[30]  L. Barat.  Four malaria success stories: how malaria burden was successfully reduced in Brazil, Eritrea, India, and Vietnam. , 2006, The American journal of tropical medicine and hygiene.

[31]  L. F. Chaves,et al.  Malaria resurgence in the East African highlands: temperature trends revisited. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[32]  V. Wiwanitkit.  Correlation between rainfall and the prevalence of malaria in Thailand. , 2006, The Journal of infection.

[33]  R. Dhiman,et al.  Climate change and malaria in India , 2006 .

[34]  A. Wickremasinghe,et al.  Anopheline breeding in river bed pools below major dams in Sri Lanka. , 2006, Acta tropica.

[35]  F. Kogan,et al.  SHORT REPORT: ANALYSIS OF MALARIA CASES IN BANGLADESH WITH REMOTE SENSING DATA , 2006 .

[36]  Pierre Defourny,et al.  The Anopheles dirus complex: spatial distribution and environmental drivers , 2007, Malaria Journal.

[37]  Andrew P. Morse,et al.  Malaria early warnings based on seasonal climate forecasts from multi-model ensembles , 2006, Nature.

[38]  J. Matsumoto,et al.  Teleconnections between the sea surface temperature in the Bay of Bengal and monsoon rainfall in Bangladesh , 2006 .

[39]  T. Abeku,et al.  Response to Malaria Epidemics in Africa , 2007, Emerging infectious diseases.

[40]  V. Louis,et al.  Effect of meteorological factors on clinical malaria risk among children: an assessment using village-based meteorological stations and community-based parasitological survey , 2007, BMC public health.

[41]  M. Tibayrenc.  Encyclopedia of infectious diseases : modern methodologies , 2007 .

[42]  P. Vounatsou,et al.  Temporal correlation between malaria and rainfall in Sri Lanka , 2008, Malaria Journal.

[43]  A. Barnston,et al.  The role of ENSO in understanding changes in Colombia's annual malaria burden by region, 1960–2006 , 2009, Malaria Journal.

[44]  M. Thomson,et al.  Effectiveness of malaria control during changing climate conditions in Eritrea, 1998–2003 , 2008, Tropical medicine & international health : TM & IH.

[45]  S. Liang,et al.  One-year delayed effect of fog on malaria transmission: a time-series analysis in the rain forest area of Mengla County, south-west China , 2008, Malaria Journal.

[46]  C. Dye,et al.  World Malaria Report, 2008. , 2008 .

[47]  J. Gaudart,et al.  Modelling malaria incidence with environmental dependency in a locality of Sudanese savannah area, Mali , 2009, Malaria Journal.

[48]  M. Molyneux,et al.  Effect of Transmission Setting and Mixed Species Infections on Clinical Measures of Malaria in Malawi , 2008, PloS one.

[49]  R. Haque,et al.  Prevalence of anopheline species and their Plasmodium infection status in epidemic-prone border areas of Bangladesh , 2010, Malaria Journal.

[50]  Masahiro Hashizume,et al.  The Indian Ocean Dipole and malaria risk in the highlands of western Kenya , 2009, Proceedings of the National Academy of Sciences.

[51]  J. Pilz,et al.  Bayesian modelling of the effect of climate on malaria in Burundi , 2010, Malaria Journal.

[52]  U. Haque,et al.  Malaria Prevalence in Endemic Districts of Bangladesh , 2009, PloS one.

[53]  U. Haque,et al.  Knowledge on the transmission, prevention and treatment of malaria among two endemic populations of Bangladesh and their health-seeking behaviour , 2009, Malaria Journal.