Refractory periods and climate forcing in cholera dynamics

Abstract

Outbreaks of many infectious diseases, including cholera, malaria and dengue, vary over characteristic periods longer than 1 year1,2. Evidence that climate variability drives these interannual cycles has been highly controversial, chiefly because it is difficult to isolate the contribution of environmental forcing while taking into account nonlinear epidemiological dynamics generated by mechanisms such as host immunity2,3,4. Here we show that a critical interplay of environmental forcing, specifically climate variability, and temporary immunity explains the interannual disease cycles present in a four-decade cholera time series from Matlab, Bangladesh. We reconstruct the transmission rate, the key epidemiological parameter affected by extrinsic forcing, over time for the predominant strain (El Tor) with a nonlinear population model that permits a contributing effect of intrinsic immunity. Transmission shows clear interannual variability with a strong correspondence to climate patterns at long periods (over 7 years, for monsoon rains and Brahmaputra river discharge) and at shorter periods (under 7 years, for flood extent in Bangladesh, sea surface temperatures in the Bay of Bengal and the El Niño–Southern Oscillation). The importance of the interplay between extrinsic and intrinsic factors in determining disease dynamics is illustrated during refractory periods, when population susceptibility levels are low as the result of immunity and the size of cholera outbreaks only weakly reflects climate forcing.

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Figure 1: Time series of cholera cases from 1966 to 2002, aggregated monthly.
Figure 2: Results of the nonlinear disease model.
Figure 3: Cholera refractory periods.
Figure 4: Environmental drivers and transmission.

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Acknowledgements

We thank B. Sack for discussions on cholera immunity, K. Streatfield for support with the cholera data, A. Dobson for comments on the manuscript, P. Webster and the Climate Forecast Applications Project at Georgia Tech for the river discharge data, and the Bangladesh Water Development Board, Dhaka, Bangladesh, for flood area data. M.P. acknowledges the joint support of the NSF-NIH (Ecology of Infectious Diseases) and NOAA (Oceans and Health), as well as funding from NOAA's Joint Program on Climate Variability and Human Health, with EPRI–NSF–NASA, under which the work was initiated. Further support was provided by the James S. McDonnell Foundation Centennial fellowship to M.P. and by ICREA and an AGAUR-DURSI grant to X.R.

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Correspondence to Mercedes Pascual.

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Supplementary Notes

This contains text on the statistical procedure for fitting the extended nonlinear disease model. It also contains three Supplementary Figures. Supplementary Figure S1 presents the results of the Scale-Dependent Correlation (SDC) analysis, revealing that only one particular biotype at a time is responsible for the response of cases to climate for a given El Niño event. Supplementary Figure S2 shows that the 1982-83 ENSO years exhibited intense drought conditions with a comparison between rainfall deviations for the 1982/1983 El Niño event and deviations for the other El Niño events over the time period 1976-2003. Supplementary Figure S3 provides evidence for the uniqueness of this drought's spatial extent. (PDF 587 kb)

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Koelle, K., Rodó, X., Pascual, M. et al. Refractory periods and climate forcing in cholera dynamics. Nature 436, 696–700 (2005). https://doi.org/10.1038/nature03820

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