Cholera is an acute diarrheal disease caused by the bacterium Vibrio cholerae (V. cholerae). Cholera incidence has been greatly reduced due to improved environmental conditions and the implementation of intervention measures [1, 2]. However, it remains a global threat to public health and has emerged in some areas [2]. It is estimated that cholera cases range from 1.3 million to 4.0 million each year worldwide, resulting in 21,000 to 143,000 deaths [3]. Evidence suggests that climate change and variability play an important role in the emerging and reemerging of cholera [2, 4, 5]. Specifically, factors including rainfall patterns, sea surface temperature, and El Niño Southern Oscillation (EÑSO) are linked to the occurrence of cholera [4-7]. Seasonality patterns also indicate an association between cholera occurrence and climatic factors [8, 9]. The outbreaks of cholera are more frequently observed in warmer seasons while vary in different latitudes [9], suggesting the need to further investigate the effect of climate on cholera transmission [5].

Cholera lends itself to analyses of the role of climate in infectious disease, coupled to population dynamics of pathogenic microorganisms, for several reasons. First, the disease has a historical context linking it to specific seasons and biogeographical zones. In addition, the population dynamics of V. cholerae in the environment are strongly controlled by environmental factors, such as water temperature, salinity, and the presence of copepods, which are, in turn, controlled by larger-scale climate variability [5].

It is projected that surface temperature will rise in the 21^st century under all assessed emission scenarios [10]. For example, temperature may increase by 1.4 −3.1°C by the end of the century under medium emission scenarios. It is likely that heatwaves will become more frequent and extreme precipitation will become more intense. Evidence shows that extreme weather events and climatic variations have a profound influence on human health and infectious disease transmission [11, 12]. Heatwaves are expected to lead to an increase in cholera outbreaks because V. cholerae population may increase as temperature rises [13, 14]. Studies in the Baltic Sea area, the Chesapeake Bay, and the coast of Bangladesh also demonstrated that climate factors, such as temperature and rainfall have driven the prevalence of V. cholerae both geographically and temporally [6, 13-15]. The connection between temperature and cholera risk is expected because the increase of the abundance of V. cholerae has been linked to increased water temperature in several coastal areas [15-17]. A positive association between temperature and cholera risk has also been observed [18]. Therefore, future climate change will likely increase the risk of cholera outbreaks [2].

The increase in the number of cholera cases was also observed with high and low rainfall in Bangladesh [19]. Several studies identified a positive association between temperature and cholera incidence [8, 20]. It was reported that the increase in minimum temperature by 1°C was associated with 6% increase in cholera incidence in Matlab, Bangladesh [8]. It was also observed that cholera outbreaks had a significant association with the annual bimodal cycle of sea surface temperature [20].

El Niño-Southern Oscillation (ENSO), Indian Ocean Dipole (IOD) and Cholera Dynamics in Bangladesh

It has been reported that the El Niño-Southern Oscillation (ENSO) plays a role in the interannual variation of endemic cholera in Bangladesh [4, 21, 22]. Sea surface temperature (SST) and sea surface height (SSH) in the Bay of Bengal have been proposed to influence the incidence of cholera in Dhaka [4, 23]. The strong correlation between SST in the Bay of Bengal and outbreaks of cholera may occur because the warm waters along the coast, coupled with phytoplankton blooms driven by warm ocean temperatures, are favorable for V. cholerae multiplication [5, 20].

EÑSO has showed a positive effect on cholera incidence with a 2-month lag in the fall period in Bangladesh [7, 22] while the effect may change at different time periods [22]. Analysis of a monthly 18-year cholera time series from Bangladesh shows that the temporal variability of cholera exhibits an interannual component at the dominant frequency of El Niño-Southern Oscillation (ENSO). Results from nonlinear time series analysis support a role for both ENSO and previous disease levels in the dynamics of cholera. Cholera patterns are linked to the previously described changes in the atmospheric circulation of south Asia and, consistent with these changes, to regional temperature anomalies [7].

The Indian Ocean Dipole (IOD) is another climate mode that arises from ocean-atmosphere interactions that cause interannual climate variability in the tropical Indian Ocean [24-26].

A positive IOD indicates SST anomalies, with warmer than normal SSTs over the western basin and cooler than usual SSTs in the eastern basin near Sumatra. Conversely, a negative IOD indicates warmer than normal SSTs over the eastern basin and cooler than usual SSTs in the western tropical Indian Ocean. Although the extent to which the IOD is independent of ENSO has been debated [27], there is growing evidence that this air-sea interaction is specific to the Indian Ocean [26, 28, 29].

The IOD has been reported to affect regional ocean climate [26]. IOD events strongly influence sea level variations in the Bay of Bengal and sea level anomalies in the northern Bay may influence flooding and outbreaks of cholera in Bangladesh [30]. The IOD also plays an important role as a modulator of the Indian monsoon rainfall [26, 31, 32]. Rainfall and associated river levels have also been reported to influence cholera patterns in Bangladesh and a short-term temporal association between IOD and cholera incidence in Bangladesh has been reported [19, 33].

References

1. Ali M, Lopez AL, You YA, Kim YE, Sah B, Maskery B, et al. The global burden of cholera. Bull World Health Organ. 2012;90(3):209-18a. doi: 10.2471/blt.11.093427.
2. Wu J, Yunus M, Ali M, Escamilla V, Emch M. Influences of heatwave, rainfall, and tree cover on cholera in Bangladesh. Environ Int. 2018;120:304-11. doi: 10.1016/j.envint.2018.08.012.
3. Ali M, Nelson AR, Lopez AL, Sack DA. Updated global burden of cholera in endemic countries. PLoS Negl Trop Dis. 2015;9(6):e0003832. doi: 10.1371/journal.pntd.0003832.
4. Colwell RR. Global climate and infectious disease: the cholera paradigm. Science. 1996;274(5295):2025-31. doi: 10.1126/science.274.5295.2025.
5. Lipp EK, Huq A, Colwell RR. Effects of global climate on infectious disease: the cholera model. Clin Microbiol Rev. 2002;15(4):757-70. doi: 10.1128/cmr.15.4.757-770.2002.
6. Constantin de Magny G, Colwell RR. Cholera and climate: a demonstrated relationship. Trans Am Clin Climatol Assoc. 2009;120:119-28. doi,
7. Pascual M, Rodó X, Ellner SP, Colwell R, Bouma MJ. Cholera dynamics and El Niño-Southern Oscillation. Science. 2000;289(5485):1766-9. doi: 10.1126/science.289.5485.1766.
8. Ali M, Kim DR, Yunus M, Emch M. Time series analysis of cholera in Matlab, Bangladesh, during 1988-2001. J Health Popul Nutr. 2013;31(1):11-9. doi: 10.3329/jhpn.v31i1.14744.
9. Emch M, Feldacker C, Islam MS, Ali M. Seasonality of cholera from 1974 to 2005: a review of global patterns. Int J Health Geogr. 2008;7:31. doi: 10.1186/1476-072x-7-31.
10. Field CB, Barros VR. Climate change 2014–Impacts, adaptation and vulnerability: Regional aspects: Cambridge University Press; 2014.
11. Patz JA, Campbell-Lendrum D, Holloway T, Foley JA. Impact of regional climate change on human health. Nature. 2005;438(7066):310-7. doi: 10.1038/nature04188.
12. Wu X, Lu Y, Zhou S, Chen L, Xu B. Impact of climate change on human infectious diseases: Empirical evidence and human adaptation. Environ Int. 2016;86:14-23. doi: 10.1016/j.envint.2015.09.007.
13. Baker-Austin C, Trinanes JA, Taylor NG, Hartnell R, Siitonen A, Martinez-Urtaza J. Emerging Vibrio risk at high latitudes in response to ocean warming. Nature Climate Change. 2013;3(1):73-7. doi,
14. Levy S. Warming trend: how climate shapes Vibrio ecology. Environ Health Perspect. 2015;123(4):A82-9. doi: 10.1289/ehp.123-A82.
15. Huq A, Sack RB, Nizam A, Longini IM, Nair GB, Ali A, et al. Critical factors influencing the occurrence of Vibrio cholerae in the environment of Bangladesh. Appl Environ Microbiol. 2005;71(8):4645-54. doi: 10.1128/aem.71.8.4645-4654.2005.
16. Heidelberg JF, Heidelberg KB, Colwell RR. Seasonality of Chesapeake Bay bacterioplankton species. Appl Environ Microbiol. 2002;68(11):5488-97. doi: 10.1128/aem.68.11.5488-5497.2002.
17. Louis VR, Russek-Cohen E, Choopun N, Rivera IN, Gangle B, Jiang SC, et al. Predictability of Vibrio cholerae in Chesapeake Bay. Appl Environ Microbiol. 2003;69(5):2773-85. doi: 10.1128/aem.69.5.2773-2785.2003.
18. Reyburn R, Kim DR, Emch M, Khatib A, von Seidlein L, Ali M. Climate variability and the outbreaks of cholera in Zanzibar, East Africa: a time series analysis. Am J Trop Med Hyg. 2011;84(6):862-9. doi: 10.4269/ajtmh.2011.10-0277.
19. Hashizume M, Armstrong B, Hajat S, Wagatsuma Y, Faruque AS, Hayashi T, et al. The effect of rainfall on the incidence of cholera in Bangladesh. Epidemiology. 2008;19(1):103-10. doi: 10.1097/EDE.0b013e31815c09ea.
20. Lobitz B, Beck L, Huq A, Wood B, Fuchs G, Faruque AS, et al. Climate and infectious disease: use of remote sensing for detection of Vibrio cholerae by indirect measurement. Proc Natl Acad Sci U S A. 2000;97(4):1438-43. doi: 10.1073/pnas.97.4.1438.
21. Bouma MJ, Pascual M. Seasonal and interannual cycles of endemic cholera in Bengal 1891–1940 in relation to climate and geography. The ecology and etiology of newly emerging marine diseases: Springer; 2001. p. 147-56.
22. Rodo X, Pascual M, Fuchs G, Faruque AS. ENSO and cholera: a nonstationary link related to climate change? Proc Natl Acad Sci U S A. 2002;99(20):12901-6. doi: 10.1073/pnas.182203999.
23. Constantin de Magny G, Murtugudde R, Sapiano MR, Nizam A, Brown CW, Busalacchi AJ, et al. Environmental signatures associated with cholera epidemics. Proc Natl Acad Sci U S A. 2008;105(46):17676-81. doi: 10.1073/pnas.0809654105.
24. Saji NH, Goswami BN, Vinayachandran PN, Yamagata T. A dipole mode in the tropical Indian Ocean. Nature. 1999;401(6751):360-3. doi: 10.1038/43854.
25. Webster PJ, Moore AM, Loschnigg JP, Leben RR. Coupled ocean-atmosphere dynamics in the Indian Ocean during 1997-98. Nature. 1999;401(6751):356-60. doi: 10.1038/43848.
26. Hashizume M, Chaves LF, Faruque ASG, Yunus M, Streatfield K, Moji K. A differential effect of Indian ocean dipole and El Niño on cholera dynamics in Bangladesh. PloS one. 2013;8(3):e60001-e. doi: 10.1371/journal.pone.0060001.
27. Jensen TG. Introduction: special issue on Indian Ocean climate. Journal of Climate. 2007;20(13):2869-71. doi,
28. Fischer AS, Terray P, Guilyardi E, Gualdi S, Delecluse P. Two independent triggers for the Indian Ocean dipole/zonal mode in a coupled GCM. Journal of climate. 2005;18(17):3428-49. doi,
29. Hong CC, Lu MM, Kanamitsu M. Temporal and spatial characteristics of positive and negative Indian Ocean dipole with and without ENSO. Journal of Geophysical Research: Atmospheres. 2008;113(D8). doi,
30. Han W, Webster PJ. Forcing mechanisms of sea level interannual variability in the Bay of Bengal. Journal of Physical Oceanography. 2002;32(1):216-39. doi,
31. Ajayamohan R, Rao SA. Indian Ocean dipole modulates the number of extreme rainfall events over India in a warming environment. Journal of the Meteorological Society of Japan Ser II. 2008;86(1):245-52. doi,
32. Ashok K, Guan Z, Yamagata T. Impact of the Indian Ocean dipole on the relationship between the Indian monsoon rainfall and ENSO. Geophysical research letters. 2001;28(23):4499-502. doi,
33. Akanda AS, Jutla AS, Islam S. Dual peak cholera transmission in Bengal Delta: a hydroclimatological explanation. Geophysical Research Letters. 2009;36(19). doi,