ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Colwell RR, 1996. Global climate and infectious disease: the cholera paradigm. Science 274: 2025–2031.
-
2.
Stine OC, Alam M, Tang L, Nair GB, Siddique AK, Faruque SM, Huq A, Colwell R, Sack RB, Morris JG Jr, 2008. Seasonal cholera from multiple small outbreaks in rural Bangladesh. Emerg Infect Dis 14: 831–833.
-
3.
Hasan NA, Choi S, Eppinger M, Clark PW, Chen A, Alam M, Haley BJ, Taviani E, Hine H, Su Q, Tallon LJ, Prosper JB, Furth K, Hoq MM, Li H, Fraser-Liggett C, Cravioto A, Huq A, Ravel J, Cebula T, Colwell RR, 2012. Genomic diversity of 2010 Haitian cholera outbreak strains. Proc Natl Acad Sci USA 109: E2010–E2017.
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Huq A, Colwell RR, 1996. Vibrios in the marine and estuarine environment: tracking Vibrio cholerae. Ecosyst Health 2: 198–214.
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5.
Lobitz BM, Beck LR, Huq A, Wood B, Fuchs G, Faruque ASG, Colwell RR, 2000. Climate and infectious disease: use of remote sensing for detection. Proc Natl Acad Sci USA 97: 1438–1443.
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Griffith DC, Kelly-Hope LA, Miller MA, 2006. Review of reported cholera outbreaks worldwide, 1995–2005. Am J Trop Med Hyg 75: 973–977.
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Akanda AS, Jutla AS, Islam S, 2009. Dual peak cholera transmission in Bengal Delta: a hydroclimatological explanation. Geophys Res Lett 36: L19401.
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Jutla AS, Akanda AS, Griffiths J, Islam S, Colwell RR, 2011. Warming oceans, phytoplankton, and river discharge: implications for cholera outbreaks. Am J Trop Med Hyg 85: 303–308.
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Enserink M, 2010. Infectious diseases: Haiti's outbreak is latest in cholera's new global assault. Science 330: 738–739.
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Centers for Disease Control, Lesson 1: Introduction to Epidemiology. Available at: http://www.cdc.gov/osels/scientific_edu/ss1978/lesson1/section11.htm. Accessed March 16, 2013.
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Akanda AS, Jutla AS, de Magny GC, Alam M, Siddique AK, Sack RB, Huq A, Colwell RR, Islam S, 2011a. Hydroclimatic influences on seasonal and spatial cholera transmission cycles: implications for public health intervention in the Bengal Delta. Water Resour Res 47: W00H07.
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12.
Rinaldo A, Bertuzzo E, Mari L, Righetto L, Blokesch M, Gatto M, Rodriguez-Iturbe I, 2012. Reassessment of the 2010–2011 Haiti cholera outbreak and rainfall-driven multiseason projections. Proc Natl Acad Sci USA 109: 6602–6607.
-
13.
Huq A, Sack RB, Nizam A, Longini IM, Nair GB, Ali A, Morris JG, Khan MNH, Siddique AK, Yunus M, Albert MJ, Sack DA, Colwell RR, 2005. Critical factors influencing the occurrence of Vibrio cholerae in the environment of Bangladesh. Appl Environ Microbiol 71: 4645–4654.
-
14.
Constantin de Magny G, Murtugudde R, Sapianob M, Nizam A, Brown C, Busalacchi A, Yunus M, Nair G, Gil A, Calkins J, Manna B, Rajendran K, Bhattacharya M, Huq A, Sack R, Colwell RR, 2008. Environmental signatures associated with cholera epidemics. Proc Natl Acad Sci USA 105: 17676–17681.
-
15.
Jutla AS, Akanda AS, Islam S, 2012. Satellite space-time variability of chlorophyll in Bay of Bengal: connections to cholera outbreaks. Remote Sens Environ 123: 196–206.
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16.
Bertuzzo E, Casagrandi R, Gatto M, Rodriguez-Iturbe I, Rinaldo A, 2009. On spatially explicit models of cholera epidemics. J R Soc. Interface 7: 321–333.
-
17.
Bertuzzo E, Azaele S, Maritan A, Gatto M, Rodriguez-Iturbe I, Rinaldo A, 2008. On the space-time evolution of a cholera epidemic. Water Resour Res 44: W01424.
-
18.
Das S, Gupta S, 2005. Diversity of Vibrio cholerae strains isolated in Delhi, India, during 1992–2000. J Health Popul Nutr 23: 44–51.
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19.
Bompangue Nkoko D, Giraudoux P, Plisnier PD, Tinda AM, Piarroux M, Sudre B, Horion S, Tamfum JJ, Ilunga BK, Piarroux R, 2011. Dynamics of cholera outbreaks in great lakes region of Africa, 1978–2008. Emerg Infect Dis 17: 2026–2034.
-
20.
Hashizume M, Armstrong B, Hajat S, Wagatsuma Y, Faruque AS, Hayashi T, Sack DA, 2008. The effect of rainfall on the incidence of cholera in Bangladesh. Epidemiology 19: 103–110.
-
21.
Hashizume M, Faruque AS, Terao T, Yunus M, Streatfield K, Yamamoto T, Moji K, 2011. The Indian Ocean dipole and cholera incidence in Bangladesh: a time-series analysis. Environ Health Perspect 119: 239–244.
-
22.
Cash BA, Rodó X, Kinter JL III, 2009. Links between tropical pacific SST and cholera incidence in Bangladesh: role of the western tropical and central extratropical pacific. J Clim 22: 1641–1660.
-
23.
Reyburn R, Kim DR, Emch M, Khatib A, Von Seidlein L, Ali M, 2011. Climate variability and the outbreaks of cholera in Zanzibar, east Africa: a time series analysis. Am J Trop Med Hyg 84: 862–869.
-
24.
Gurbanov S, Akhmadov R, Shamkhalova G, Akhmadova S, Haley BJ, Colwell RR, Huq A, 2012. Occurrence of Vibrio cholerae in municipal and natural waters and incidence of cholera in Azerbaijan. EcoHealth 8: 468–477.
-
25.
Mishra A, Taneja N, Sharma RK, Kumar R, Sharma NC, Sharma M, 2011. Amplified fragment length polymorphism of clinical and environmental Vibrio cholerae from a freshwater environment in a cholera-endemic area, India. BMC Infect Dis 11: 249.
-
26.
Taneja N, Biswal M, Tarai B, Sharma M, 2005. Emergence of Vibrio cholerae O1 biotype ElTor serotype Inaba in North India. Jpn J Infect Dis 58: 238–240.
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27.
Taneja N, Kaur J, Sharma K, Singh M, Kalra JK, Sharma NM, Sharma M, 2003. A recent outbreak of cholera due to Vibrio cholerae O1 Ogawa in and around Chandigarh, North India. Indian J Med Res 117: 243–246.
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28.
Taneja N, Mishra A, Sangar G, Singh G, Sharma M, 2009. Cholera outbreaks in north India due to new variants of Vibrio cholerae O1 El Tor. Emerg Infect Dis 15: 352.
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Taneja N, Samanta P, Mishra A, Sharma M, 2010. Emergence of tetracycline resistance in Vibrio cholerae O1 biotype El Tor serotype Ogawa from North India. Indian J Pathol Microbiol 53: 865–866.
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Akanda AS, Jutla AS, Gute DM, Evans T, Islam S, 2012. Reinforcing cholera intervention with prediction aided prevention. Bull World Health Organ 90: 243–244.
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Peterson D, Dettinger M, Cayan D, Dileo J, Isaacs C, Smith R, 1996. River salinity variations in response to discharge: Examples from Western United Stated during the early 1900s. Isaacs C, Tharp V, eds. Proceedings of the Twelfth Annual Pacific Workshop Interagency Ecological Program. Technical Report 46. California Department of Water Resources, 145–153.
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Tamplin ML, Gauzens AL, Huq A, Sack DA, Colwell RR, 1990. Attachment of Vibrio cholerae serogroup O1 to zooplankton and phytoplankton of Bangladesh waters. Appl Environ Microbiol 56: 1977–1980.
-
33.
Louis VR, Russek-Cohen E, Choopun N, Rivera IN, Gangle B, Jiang SC, Rubin A, Patz J, Huq A, Colwell RR, 2003. Predictability of Vibrio cholerae in Chesapeake Bay. Appl Environ Microbiol 69: 2773–2785.
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Environmental Factors Influencing Epidemic Cholera
Antarpreet Jutla
Antarpreet Jutla
Department of Civil and Environmental Engineering, West Virginia University, Morgantown, West Virginia; Maryland Pathogen Research Institute, University of Maryland, College Park, Maryland; Center for Bioinformatics and Computational Biology, University of Maryland, College Park, Maryland; Department of Civil and Environmental Engineering, University of Rhode Island, Kingston, Rhode Island; International Center for Diarrhoeal Disease Research, Dhaka, Bangladesh; Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland
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Elizabeth Whitcombe
Elizabeth Whitcombe
Department of Civil and Environmental Engineering, West Virginia University, Morgantown, West Virginia; Maryland Pathogen Research Institute, University of Maryland, College Park, Maryland; Center for Bioinformatics and Computational Biology, University of Maryland, College Park, Maryland; Department of Civil and Environmental Engineering, University of Rhode Island, Kingston, Rhode Island; International Center for Diarrhoeal Disease Research, Dhaka, Bangladesh; Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland
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Nur Hasan
Nur Hasan
Department of Civil and Environmental Engineering, West Virginia University, Morgantown, West Virginia; Maryland Pathogen Research Institute, University of Maryland, College Park, Maryland; Center for Bioinformatics and Computational Biology, University of Maryland, College Park, Maryland; Department of Civil and Environmental Engineering, University of Rhode Island, Kingston, Rhode Island; International Center for Diarrhoeal Disease Research, Dhaka, Bangladesh; Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland
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Bradd Haley
Bradd Haley
Department of Civil and Environmental Engineering, West Virginia University, Morgantown, West Virginia; Maryland Pathogen Research Institute, University of Maryland, College Park, Maryland; Center for Bioinformatics and Computational Biology, University of Maryland, College Park, Maryland; Department of Civil and Environmental Engineering, University of Rhode Island, Kingston, Rhode Island; International Center for Diarrhoeal Disease Research, Dhaka, Bangladesh; Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland
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Ali Akanda
Ali Akanda
Department of Civil and Environmental Engineering, West Virginia University, Morgantown, West Virginia; Maryland Pathogen Research Institute, University of Maryland, College Park, Maryland; Center for Bioinformatics and Computational Biology, University of Maryland, College Park, Maryland; Department of Civil and Environmental Engineering, University of Rhode Island, Kingston, Rhode Island; International Center for Diarrhoeal Disease Research, Dhaka, Bangladesh; Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland
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Anwar Huq
Anwar Huq
Department of Civil and Environmental Engineering, West Virginia University, Morgantown, West Virginia; Maryland Pathogen Research Institute, University of Maryland, College Park, Maryland; Center for Bioinformatics and Computational Biology, University of Maryland, College Park, Maryland; Department of Civil and Environmental Engineering, University of Rhode Island, Kingston, Rhode Island; International Center for Diarrhoeal Disease Research, Dhaka, Bangladesh; Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland
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Munir Alam
Munir Alam
Department of Civil and Environmental Engineering, West Virginia University, Morgantown, West Virginia; Maryland Pathogen Research Institute, University of Maryland, College Park, Maryland; Center for Bioinformatics and Computational Biology, University of Maryland, College Park, Maryland; Department of Civil and Environmental Engineering, University of Rhode Island, Kingston, Rhode Island; International Center for Diarrhoeal Disease Research, Dhaka, Bangladesh; Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland
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R. Bradley Sack
R. Bradley Sack
Department of Civil and Environmental Engineering, West Virginia University, Morgantown, West Virginia; Maryland Pathogen Research Institute, University of Maryland, College Park, Maryland; Center for Bioinformatics and Computational Biology, University of Maryland, College Park, Maryland; Department of Civil and Environmental Engineering, University of Rhode Island, Kingston, Rhode Island; International Center for Diarrhoeal Disease Research, Dhaka, Bangladesh; Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland
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Rita Colwell
Rita Colwell
Department of Civil and Environmental Engineering, West Virginia University, Morgantown, West Virginia; Maryland Pathogen Research Institute, University of Maryland, College Park, Maryland; Center for Bioinformatics and Computational Biology, University of Maryland, College Park, Maryland; Department of Civil and Environmental Engineering, University of Rhode Island, Kingston, Rhode Island; International Center for Diarrhoeal Disease Research, Dhaka, Bangladesh; Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland
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Cholera outbreak following the earthquake of 2010 in Haiti has reaffirmed that the disease is a major public health threat. Vibrio cholerae is autochthonous to aquatic environment, hence, it cannot be eradicated but hydroclimatology-based prediction and prevention is an achievable goal. Using data from the 1800s, we describe uniqueness in seasonality and mechanism of occurrence of cholera in the epidemic regions of Asia and Latin America. Epidemic regions are located near regional rivers and are characterized by sporadic outbreaks, which are likely to be initiated during episodes of prevailing warm air temperature with low river flows, creating favorable environmental conditions for growth of cholera bacteria. Heavy rainfall, through inundation or breakdown of sanitary infrastructure, accelerates interaction between contaminated water and human activities, resulting in an epidemic. This causal mechanism is markedly different from endemic cholera where tidal intrusion of seawater carrying bacteria from estuary to inland regions, results in outbreaks.
Author Notes
Authors' addresses: Antarpreet Jutla, Department of Civil and Environmental Engineering, West Virginia University, Morgantown, WV, E-mail: asjutla@mail.wvu.edu. Elizabeth Whitcombe, Nur Hasan, Bradd Haley, Anwar Huq, and Rita Colwell, University of Maryland, Maryland Pathogen Research Institute, College Park, MD, E-mails: ewhitcombe@xtra.co.nz, nur.hasan@cosmosid.net, bradd.haley@gmail.com, huqanwar@gmail.com, and rcolwell@umiacs.umd.edu. Ali Akanda, University of Rhode Island, Civil and Environmental Engineering, Kingston, RI, E-mail: akanda@egr.uri.edu. Munir Alam, International Centre for Diarrheal Disease Research, Bangladesh – Microbiology, Dhaka, Bangladesh, E-mail: munirul@icddrb.org. R. Bradley Sack, Johns Hopkins School of Public Health, Department of International Health, Baltimore, MD, E-mail: rsack@jhsph.edu.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Colwell RR, 1996. Global climate and infectious disease: the cholera paradigm. Science 274: 2025–2031.
-
2.
Stine OC, Alam M, Tang L, Nair GB, Siddique AK, Faruque SM, Huq A, Colwell R, Sack RB, Morris JG Jr, 2008. Seasonal cholera from multiple small outbreaks in rural Bangladesh. Emerg Infect Dis 14: 831–833.
-
3.
Hasan NA, Choi S, Eppinger M, Clark PW, Chen A, Alam M, Haley BJ, Taviani E, Hine H, Su Q, Tallon LJ, Prosper JB, Furth K, Hoq MM, Li H, Fraser-Liggett C, Cravioto A, Huq A, Ravel J, Cebula T, Colwell RR, 2012. Genomic diversity of 2010 Haitian cholera outbreak strains. Proc Natl Acad Sci USA 109: E2010–E2017.
-
4.
Huq A, Colwell RR, 1996. Vibrios in the marine and estuarine environment: tracking Vibrio cholerae. Ecosyst Health 2: 198–214.
-
5.
Lobitz BM, Beck LR, Huq A, Wood B, Fuchs G, Faruque ASG, Colwell RR, 2000. Climate and infectious disease: use of remote sensing for detection. Proc Natl Acad Sci USA 97: 1438–1443.
-
6.
Griffith DC, Kelly-Hope LA, Miller MA, 2006. Review of reported cholera outbreaks worldwide, 1995–2005. Am J Trop Med Hyg 75: 973–977.
-
7.
Akanda AS, Jutla AS, Islam S, 2009. Dual peak cholera transmission in Bengal Delta: a hydroclimatological explanation. Geophys Res Lett 36: L19401.
-
8.
Jutla AS, Akanda AS, Griffiths J, Islam S, Colwell RR, 2011. Warming oceans, phytoplankton, and river discharge: implications for cholera outbreaks. Am J Trop Med Hyg 85: 303–308.
-
9.
Enserink M, 2010. Infectious diseases: Haiti's outbreak is latest in cholera's new global assault. Science 330: 738–739.
-
10.
Centers for Disease Control, Lesson 1: Introduction to Epidemiology. Available at: http://www.cdc.gov/osels/scientific_edu/ss1978/lesson1/section11.htm. Accessed March 16, 2013.
-
11.
Akanda AS, Jutla AS, de Magny GC, Alam M, Siddique AK, Sack RB, Huq A, Colwell RR, Islam S, 2011a. Hydroclimatic influences on seasonal and spatial cholera transmission cycles: implications for public health intervention in the Bengal Delta. Water Resour Res 47: W00H07.
-
12.
Rinaldo A, Bertuzzo E, Mari L, Righetto L, Blokesch M, Gatto M, Rodriguez-Iturbe I, 2012. Reassessment of the 2010–2011 Haiti cholera outbreak and rainfall-driven multiseason projections. Proc Natl Acad Sci USA 109: 6602–6607.
-
13.
Huq A, Sack RB, Nizam A, Longini IM, Nair GB, Ali A, Morris JG, Khan MNH, Siddique AK, Yunus M, Albert MJ, Sack DA, Colwell RR, 2005. Critical factors influencing the occurrence of Vibrio cholerae in the environment of Bangladesh. Appl Environ Microbiol 71: 4645–4654.
-
14.
Constantin de Magny G, Murtugudde R, Sapianob M, Nizam A, Brown C, Busalacchi A, Yunus M, Nair G, Gil A, Calkins J, Manna B, Rajendran K, Bhattacharya M, Huq A, Sack R, Colwell RR, 2008. Environmental signatures associated with cholera epidemics. Proc Natl Acad Sci USA 105: 17676–17681.
-
15.
Jutla AS, Akanda AS, Islam S, 2012. Satellite space-time variability of chlorophyll in Bay of Bengal: connections to cholera outbreaks. Remote Sens Environ 123: 196–206.
-
16.
Bertuzzo E, Casagrandi R, Gatto M, Rodriguez-Iturbe I, Rinaldo A, 2009. On spatially explicit models of cholera epidemics. J R Soc. Interface 7: 321–333.
-
17.
Bertuzzo E, Azaele S, Maritan A, Gatto M, Rodriguez-Iturbe I, Rinaldo A, 2008. On the space-time evolution of a cholera epidemic. Water Resour Res 44: W01424.
-
18.
Das S, Gupta S, 2005. Diversity of Vibrio cholerae strains isolated in Delhi, India, during 1992–2000. J Health Popul Nutr 23: 44–51.
-
19.
Bompangue Nkoko D, Giraudoux P, Plisnier PD, Tinda AM, Piarroux M, Sudre B, Horion S, Tamfum JJ, Ilunga BK, Piarroux R, 2011. Dynamics of cholera outbreaks in great lakes region of Africa, 1978–2008. Emerg Infect Dis 17: 2026–2034.
-
20.
Hashizume M, Armstrong B, Hajat S, Wagatsuma Y, Faruque AS, Hayashi T, Sack DA, 2008. The effect of rainfall on the incidence of cholera in Bangladesh. Epidemiology 19: 103–110.
-
21.
Hashizume M, Faruque AS, Terao T, Yunus M, Streatfield K, Yamamoto T, Moji K, 2011. The Indian Ocean dipole and cholera incidence in Bangladesh: a time-series analysis. Environ Health Perspect 119: 239–244.
-
22.
Cash BA, Rodó X, Kinter JL III, 2009. Links between tropical pacific SST and cholera incidence in Bangladesh: role of the western tropical and central extratropical pacific. J Clim 22: 1641–1660.
-
23.
Reyburn R, Kim DR, Emch M, Khatib A, Von Seidlein L, Ali M, 2011. Climate variability and the outbreaks of cholera in Zanzibar, east Africa: a time series analysis. Am J Trop Med Hyg 84: 862–869.
-
24.
Gurbanov S, Akhmadov R, Shamkhalova G, Akhmadova S, Haley BJ, Colwell RR, Huq A, 2012. Occurrence of Vibrio cholerae in municipal and natural waters and incidence of cholera in Azerbaijan. EcoHealth 8: 468–477.
-
25.
Mishra A, Taneja N, Sharma RK, Kumar R, Sharma NC, Sharma M, 2011. Amplified fragment length polymorphism of clinical and environmental Vibrio cholerae from a freshwater environment in a cholera-endemic area, India. BMC Infect Dis 11: 249.
-
26.
Taneja N, Biswal M, Tarai B, Sharma M, 2005. Emergence of Vibrio cholerae O1 biotype ElTor serotype Inaba in North India. Jpn J Infect Dis 58: 238–240.
-
27.
Taneja N, Kaur J, Sharma K, Singh M, Kalra JK, Sharma NM, Sharma M, 2003. A recent outbreak of cholera due to Vibrio cholerae O1 Ogawa in and around Chandigarh, North India. Indian J Med Res 117: 243–246.
-
28.
Taneja N, Mishra A, Sangar G, Singh G, Sharma M, 2009. Cholera outbreaks in north India due to new variants of Vibrio cholerae O1 El Tor. Emerg Infect Dis 15: 352.
-
29.
Taneja N, Samanta P, Mishra A, Sharma M, 2010. Emergence of tetracycline resistance in Vibrio cholerae O1 biotype El Tor serotype Ogawa from North India. Indian J Pathol Microbiol 53: 865–866.
-
30.
Akanda AS, Jutla AS, Gute DM, Evans T, Islam S, 2012. Reinforcing cholera intervention with prediction aided prevention. Bull World Health Organ 90: 243–244.
-
31.
Peterson D, Dettinger M, Cayan D, Dileo J, Isaacs C, Smith R, 1996. River salinity variations in response to discharge: Examples from Western United Stated during the early 1900s. Isaacs C, Tharp V, eds. Proceedings of the Twelfth Annual Pacific Workshop Interagency Ecological Program. Technical Report 46. California Department of Water Resources, 145–153.
-
32.
Tamplin ML, Gauzens AL, Huq A, Sack DA, Colwell RR, 1990. Attachment of Vibrio cholerae serogroup O1 to zooplankton and phytoplankton of Bangladesh waters. Appl Environ Microbiol 56: 1977–1980.
-
33.
Louis VR, Russek-Cohen E, Choopun N, Rivera IN, Gangle B, Jiang SC, Rubin A, Patz J, Huq A, Colwell RR, 2003. Predictability of Vibrio cholerae in Chesapeake Bay. Appl Environ Microbiol 69: 2773–2785.
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