Cholera Outbreaks in Africa

  • Martin A. MengelEmail author
  • Isabelle Delrieu
  • Leonard Heyerdahl
  • Bradford D. Gessner
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 379)


During the current seventh cholera pandemic, Africa bore the major brunt of global disease burden. More than 40 years after its resurgence in Africa in 1970, cholera remains a grave public health problem, characterized by large disease burden, frequent outbreaks, persistent endemicity, and high CFRs, particularly in the region of the central African Great Lakes which might act as reservoirs for cholera. There, cases occur year round with a rise in incidence during the rainy season. Elsewhere in sub-Saharan Africa, cholera occurs mostly in outbreaks of varying size with a constant threat of widespread epidemics. Between 1970 and 2011, African countries reported 3,221,050 suspected cholera cases to the World Health Organization, representing 46 % of all cases reported globally. Excluding the Haitian epidemic, sub-Saharan Africa accounted for 86 % of reported cases and 99 % of deaths worldwide in 2011. The number of cholera cases is possibly much higher than what is reported to the WHO due to the variation in modalities, completeness, and case definition of national cholera data. One source on country specific incidence rates for Africa, adjusting for underreporting, estimates 1,341,080 cases and 160,930 deaths (52.6 % of 2,548,227 estimated cases and 79.6 % of 209,216 estimated deaths worldwide). Another estimates 1,411,453 cases and 53,632 deaths per year, respectively (50 % of 2,836,669 estimated cases and 58.6 % of 91,490 estimated deaths worldwide). Within Africa, half of all cases between 1970 and 2011 were notified from only seven countries: Angola, Democratic Republic of the Congo, Mozambique, Nigeria, Somalia, Tanzania, and South Africa. In contrast to a global trend of decreasing case fatality ratios (CFRs), CFRs have remained stable in Africa at approximately 2 %. Early propagation of cholera outbreaks depends largely on the extent of individual bacterial shedding, host and organism characteristics, the likelihood of people coming into contact with an infectious dose of Vibrio cholerae and on the virulence of the implicated strain. Cholera transmission can then be amplified by several factors including contamination of human water- or food sources; climate and extreme weather events; political and economic crises; high population density combined with poor quality informal housing and poor hygiene practices; spread beyond a local community through human travel and animals, e.g., water birds. At an individual level, cholera risk may increase with decreasing immunity and hypochlorhydria, such as that induced by Helicobacter pylori infection, which is endemic in much of Africa, and may increase individual susceptibility and cholera incidence. Since contaminated water is the main vehicle for the spread of cholera, the obvious long-term solution to eradicate the disease is the provision of safe water to all African populations. This requires considerable human and financial resources and time. In the short and medium term, vaccination may help to prevent and control the spread of cholera outbreaks. Regardless of the intervention, further understanding of cholera biology and epidemiology is essential to identify populations and areas at increased risk and thus ensure the most efficient use of scarce resources for the prevention and control of cholera.


Refugee Camp Cholera Outbreak Case Fatality Ratio National Surveillance System Cholera Case 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The authors would like to thank Lan Ngo and Sabrina Gaber for their enormous help in completing this chapter. Lan Ngo for the many hours of ceaseless search of cholera literature and news and Sabrina Gaber for her valuable work editing the text.


  1. Acosta CJ, Galindo CM, Kimario J, Senkoro K, Urassa H, Casals C, Corachán M, Eseko N, Tanner M, Mshinda H, Lwilla F, Vila J, Alonso PL (2001) Cholera outbreak in southern Tanzania: risk factors and patterns of transmission. Emerg Infect Dis 7(3):583–587PubMedCentralPubMedGoogle Scholar
  2. Adagbada AO, Adesida SA, Nwaokorie FO, Niemogha MT, Coker AO (2012) Cholera epidemiology in Nigeria: an overview. Pan Afr Med J 12:59PubMedCentralPubMedGoogle Scholar
  3. Ahmed S, Bardhan PK, Iqbal A, Mazumder RN, Khan AI, Islam MS, Siddique AK, Cravioto A (2011) The 2008 cholera epidemic in Zimbabwe: experience of the icddr, b team in the field. J Health Popul Nutr 29(5):541–546PubMedCentralPubMedGoogle Scholar
  4. Ako AA, Nkeng GE, Takem GE (2009) Water quality and occurrence of water-borne diseases in the Douala 4th District, Cameroon Water SciT echnol 59(12):2321–2329Google Scholar
  5. Alajo SO, Nakavuma J, Erume J (2006) Cholera in endemic districts in Uganda during El Niño rains: 2002–2003. Afr Health Sci 6(2):93–97PubMedCentralPubMedGoogle Scholar
  6. Albert MJ, Neira M, Motarjemi Y (1997) The role of food in the epidemiology of cholera. World Health Stat Q 50(1–2):111–118PubMedGoogle Scholar
  7. Ali M, Emch M, Park JK, Yunus M, Clemens J (2011) Natural cholera infection-derived immunity in an endemic setting. J Infect Dis 204:912–918PubMedCentralPubMedGoogle Scholar
  8. Ali M, Lopez AL, You YA, Kim YE, Sah B, Maskery B, Clemens J (2012) The global burden of cholera. Bull WHO 90:209–218APubMedCentralPubMedGoogle Scholar
  9. Anand JK (1995) Cholera treatment in Goma. Lancet 345(8964):1568PubMedGoogle Scholar
  10. Assako RJ, Abomo DM, Tchuikoua LB (2004) Etude géographique de l’épidémie de choléra à Douala ou la qualité de vie à l’épreuve des pratiques urbainesGoogle Scholar
  11. Bart KJ, Huq Z, Moslemuddin K, Mosley WH (1970) Seroepidemiologic studies during a simultaneous epidemic of infection with El Tor Ogawa and Classical Inaba Vibrio cholerae. J Infect Dis 121:17–24PubMedGoogle Scholar
  12. Barua D (1972) The global epidemiology of cholera in recent years. Proc R Soc Med 65(5):423–428PubMedCentralPubMedGoogle Scholar
  13. Bateman C (2009a) Cholera—getting the basics right. S Afr Med J 99(3):138–140PubMedGoogle Scholar
  14. Bateman C (2009b) SA medical schools to rescue Zimbabwe’s aspirant doctors. S Afr Med J 99(4):214, 216, 218Google Scholar
  15. Bhattacharya S, Black R, Bourgeois L, Clemens J, Cravioto A, Deen JL, Dougan G, Glass R, Grais RF, Greco M, Gust I, Holmgren J, Kariuki S, Lambert PH, Liu MA, Longini I, Nair GB, Norrby R, Nossal GJ, Ogra P, Sansonetti P, von Seidlein L, Songane F, Svennerholm AM, Steele D, Walker R (2009) Public health. The cholera crisis in Africa. Science 324(5929):885PubMedGoogle Scholar
  16. Birmingham ME, Lee LA, Ndayimirije N, Nkurikiye S, Hersh BS, Wells JG, Deming MS (1997) Epidemic cholera in Burundi: patterns of transmission in the great rift valley lake region. Lancet 349(9057):981–985PubMedGoogle Scholar
  17. Boelaert M, Suetens C, van Soest M, Henkens M, Rigal J, de Graaf P (1995) Cholera treatment in Goma. Lancet 345(8964):1567PubMedGoogle Scholar
  18. Bompangue D, Giraudoux P, Handschumacher P, Piarroux M, Sudre B, Ekwanzala M, Kebela I, Piarroux R (2008) Lakes as source of cholera outbreaks, Democratic Republic of Congo. Emerg Infect Dis 14(5):798–800PubMedCentralPubMedGoogle Scholar
  19. Bompangue D, Giraudoux P, Piarroux M, Mutombo G, Shamavu R, Sudre B, Mutombo A, Mondonge V, Piarroux R (2009) Cholera epidemics, war and disasters around Goma and Lake Kivu: an eight-year survey. PLoS Negl Trop Dis 3(5):436Google Scholar
  20. 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(11):2026–2034PubMedGoogle Scholar
  21. Bopp CA, Ries AA, Wells JG (1999) Laboratory methods for the diagnosis of epidemic dysentery and cholera. Centers for Disease Control and PreventionGoogle Scholar
  22. Bouju J, Bocoum H, Ouattara F, Touré L (2009) Les incivilités de la société civile Espace public urbain, société civile et gouvernance communale à Bobo-Dioulasso et Bamako (Communes 1 et 2)Google Scholar
  23. Breslauer DN, Maamari RN, Switz NA et al (2009) Mobile phone based clinical microscopy for global health applications. PLoS One 4:6320Google Scholar
  24. Broza M, Gancz H, Halpern M, Kashi Y (2005) Adult non-biting midges: possible windborne carriers of Vibrio cholerae non-O1 non-O139. Environ Microbiol 7(4):576–585PubMedGoogle Scholar
  25. Bhattacharya S, Sur D, Ali M, Kanungo S, Ae You Y, Manna B, Sah B, Niyogi SK, Park JK, Sarkar B, Puri MK, Kim DR, Deen JL, Holmgren J, Carbis R, Singh Dhingra M, Donner A, Nair GB, Lopez AL, Wierzba TF, Clemens JD (2013) 5 year efficacy of a bivalent killed whole-cell oral cholera vaccine in Kolkata, India: a cluster-randomized. double-blind, placebo-controlled trial. Lancet Infect Dis. 2013 Dec 13(12):1050–1056Google Scholar
  26. Bwire G, Malimbo M, Makumbi I, Kagirita A, Wamala JF, Kalyebi P, Bingi A, Gitta S, Mukanga D, Dahlke M (2013) Cholera surveillance—Uganda, 2007–2011. J Infect Dis. 208(1):S78–S85Google Scholar
  27. Cash RA, Music SI, Libonati JP, Craig JP, Pierce NF, Hornick RB (1974) Response of man to infection with Vibrio cholerae. II. Protection from illness afforded by previous disease and vaccine. J Infect Dis 130:325–333PubMedGoogle Scholar
  28. CEPED (2009) Estimated urbanization levels in West African Societies between 1950 and 2020. July 2009—Issue 57—GBGoogle Scholar
  29. Clemens JD, van Loon F, Sack DA, Rao MR, Ahmed F, ChakrabortY J, Kay BA, Khan MR, Yunus MD, Harris JR et al (1991) Biotype as determinant of natural immunizing effect of cholera. Lancet 337:883–884PubMedGoogle Scholar
  30. Codeço, Cláudia T (2001) Endemic and Epidemic Dynamics of Cholera: the Role of the Aquatic Reservoir. BMC Infect Dis 1(1) doi:  10.1186/1471-2334-1-1. Accessed 2 Feb 2001
  31. Colombo MM, Francisco M, Ferreira BD, Rubino S, Cappuccinelli P (1993) The early stage of the recurrent cholera epidemic in Luanda. Angola Eur J Epidemiol 9(5):563–565Google Scholar
  32. Colwell RR (1996) Global climate and infectious disease: the cholera paradigm. Science 274:2025–2031PubMedGoogle Scholar
  33. Colwell RR, Huq A, Islam MS, Aziz KM, Yunus M, Khan NH, Mahmud A, Sack RB, Nair GB, Chakraborty J, Sack DA, Russek-Cohen E (2003) Reduction of cholera in Bangladeshi villages by simple filtration. Proc Natl Acad Sci USA 100:1051–1055PubMedCentralPubMedGoogle Scholar
  34. Daniels NA, Simons SL, Rodrigues A, Gunnlaugsson G, Forster TS, Wells JG, Hutwagner L, Tauxe RV, Mintz ED (1999) First do no harm: making oral rehydration solution safer in a cholera epidemic. Am J Trop Med Hyg 60(6):1051–1055PubMedGoogle Scholar
  35. deMagny GC, Guégan JF, Petit M, Cazelles B (2007) Regional-scale climate-variability synchrony of cholera epidemics in West Africa. BMC Infect Dis 19(7):20Google Scholar
  36. deMagny GC, Thiaw W, Kumar V, Manga NM, Diop BM, Gueye L, Kamara M, Roche B, Murtugudde R, Colwell RR (2012) Cholera outbreak in senegal in 2005: was climate a factor? PLoS One 7(8):e44577Google Scholar
  37. Deen JL, Von Seidlein L, Clemens JD (2011) Multidisciplinary studies of disease burden in the Diseases of the Most Impoverished Program. J Health Popul Nutr 22:232–239Google Scholar
  38. Djomassi LD, Gessner BD, Andze GO, Mballa GA (2013) Cholera epidemiology in Cameroon based on national surveillance data. J Infect Dis 208(1):S92–S97Google Scholar
  39. Dubois AE, Sinkala M, Kalluri P, Makasa-Chikoya M, Quick RE (2006) Epidemic cholera in urban Zambia: hand soap and dried fish as protective factors. Epidemiol Infect 134(6):1226–1230PubMedCentralPubMedGoogle Scholar
  40. Duval P, Champetier de Ribes G, Ranjalahy J, Quilici ML, Fournier JM (1999) Cholera in Madagascar. Lancet 353(9169):2068PubMedGoogle Scholar
  41. Eichenberg M (2011) Africa in the time of cholera: a history of pandemics from 1817 to the present. Cambridge University Press, CambridgeGoogle Scholar
  42. Einarsdóttir J, Passa A, Gunnlaugsson G (2001) Health education and cholera in rural Guinea-Bissau. Int J Infect Dis 5(3):133–138PubMedGoogle Scholar
  43. Emch M, Feldacker C, Islam MS, Ali M (2008) Seasonality of cholera from 1974 to 2005: a review of global patterns. Int J Health Geogr 20(7):31Google Scholar
  44. Essuman KM (1992) Fermented fish in Africa: a study on processing marketing and consumptionGoogle Scholar
  45. Estrada-García T, Mintz ED (1996) Cholera: foodborne transmission and its prevention. Eur J Epidemiol 12(5):461–469PubMedGoogle Scholar
  46. Feikin DR, Tabu CW, Gichuki J (2010) Does water hyacinth on East African lakes promote cholera outbreaks? Am J Trop Med Hyg 83(2):370–373PubMedCentralPubMedGoogle Scholar
  47. Felsenfeld O (1965) Notes on food, beverages, and fomites contaminated with Vibrio cholerae. Bull WHO 33:725–734PubMedCentralPubMedGoogle Scholar
  48. Gangarosa EJ (1971) The epidemiology of cholera: past and present. Bull N Y Acad Med 47:1140PubMedCentralPubMedGoogle Scholar
  49. Gayer M, Legros D, Formenty P, Connolly MA (2007) Conflict and emerging infectious diseases. Emerg Infect Dis 13(11):1625–1631PubMedCentralPubMedGoogle Scholar
  50. Germani Y, Quilici ML, Glaziou P, Mattera D, Morvan J, Fournier JM (1998) Emergence of cholera in the Central African Republic. Eur J Clin Microbiol Infect Dis 17(12):888–890PubMedGoogle Scholar
  51. Glass RI, Becker S, Huq MI, Stoll BJ, Khan MU, Merson MH, Lee JV, Black RE (1982) Endemic cholera in rural Bangladesh, 1966–1980. Am J Epidmiol 116:959–970Google Scholar
  52. Goodgame RW, Greenough WB (1975) Cholera in Africa: a message for the West. Ann Intern Med 82:101–106 Google Scholar
  53. Goma Epidemiology Group (1995) Public health impact of Rwandan refugee crisis: what happened in Goma, Zaire, in July, 1994? Lancet 345:339–344Google Scholar
  54. Griffith DC, Kelly-Hope LA, Miller MA (2006) Review of reported cholera outbreaks worldwide, 1995–2005. Am J Trop Med Hyg 75(5):973–977PubMedGoogle Scholar
  55. Guévart E, Noeske J, Solle J, Essomba JM, Edjenguele M, Bita A, Mouangue A, Manga B (2006) Factors contributing to endemic cholera in Douala, Cameroon. Med Trop 66(3):283–291. French: Déterminants du choléra à douala. Med Trop 66:283–291Google Scholar
  56. Gujral L, Sema C, Rebaudet S, Taibo CLA, Manjate AA, Piarroux R, Gessner BD (2013) Jani IV cholera epidemiology in Mozambique using national surveillance data. J Infect Dis 208(1):107–114Google Scholar
  57. Guillermet E, Colombini A, Gessner BD and Breugelmans G (2012) Literature review of anthropological studies on diarrhea in the DRC, in anticipation of a potential rotavirus vaccine introductionGoogle Scholar
  58. Gunnlaugsson G, Angulo FJ, Einarsdóttir J, Passa A, Tauxe RV (2000) Epidemic cholera in Guinea-Bissau: the challenge of preventing deaths in rural West Africa. Int J Infect Dis 4(1):8–13PubMedGoogle Scholar
  59. Gunnlaugsson G, Einarsdóttir J, Angulo FJ, Mentambanar SA, Passa A, Tauxe RV (1998) Funerals during the 1994 cholera epidemic in Guinea-Bissau, West Africa: the need for disinfection of bodies of persons dying of cholera. Epidemiol Infect 120(1):7–15PubMedCentralPubMedGoogle Scholar
  60. Halpern M, Senderovich Y, Izhaki I (2008) Waterfowl: the missing link in epidemic and pandemic cholera dissemination? PLoS Pathog 4(10):e1000173PubMedCentralPubMedGoogle Scholar
  61. Harris JB, LaRocque RC, Qadri F, Ryan ET, Calderwood SB (2012) Seminar Cholera. Lancet 379:2466–2476PubMedCentralPubMedGoogle Scholar
  62. Harris JB, LaRocque RC, Chowdhury F, Khan AI, Logvinenko T, Faruque AS, Ryan ET, Qadri F, Calderwood SB (2008) Susceptibility to Vibrio cholerae infection in a cohort of household contacts of patients with cholera in Bangladesh. PLoS Negl Trop Dis 2(4):e221PubMedCentralPubMedGoogle Scholar
  63. Hutin Y, Luby S, Paquet C (2003) A large cholera outbreak in Kano City, Nigeria: the importance of hand washing with soap and the danger of street-vended water. J Water Health 1:45–52PubMedGoogle Scholar
  64. International Organization for Migration (IOM) (2010) Eye on migration news bulletin, (3)Google Scholar
  65. IRIN AFRIQUE DE L’OUEST: Choléra, quelles sont les solutions ? 2012Google Scholar
  66. IVI international vaccine institute: program activities and progress (2013) Accessed 19 Mar 2013
  67. Kalipeni E, Oppong J (1998) The refugee crisis in Africa and implications for health and disease: a political ecology approach. Soc Sci Med 46(12):1637–1653PubMedGoogle Scholar
  68. Kaper JB, Morris JG Jr, Levine MM (1995) Cholera. Clin Microbiol Rev 8(1):48–86PubMedCentralPubMedGoogle Scholar
  69. Keddy KH, Nadan S, Govind C, Sturm AW (2007) Group for enteric, respiratory and meningeal disease surveillance in South Africa. Evidence for a clonally different origin of the two cholera epidemics of 2001–2002 and 1980–1987 in South Africa. J Med Microbiol 56(12):1644–1650Google Scholar
  70. Kelly-Hope LA (2008) Conflict and emerging infectious diseases. Emerg Infect Dis 14(6):1004–1005PubMedCentralPubMedGoogle Scholar
  71. King AA, Ionides EL, Pascual M, Bouma MJ (2008) Inapparent infections and cholera dynamics. Nature 2008(454):877–880Google Scholar
  72. Koelle K, Rodo X, Pascual M, Yunus M, Mostafa G (2005) Refractory periods and climate forcing in cholera dynamics. Nature 436:696–700PubMedGoogle Scholar
  73. Kolle W, Wassermann A, Kossel H, Neisser A (1903) Handbook of pathogenic microorganisms. Am J Med Sci 125:706Google Scholar
  74. Kotloff K, Nataro J, Blackwelder W, Nasrin D, Farag H, Panchalingam S, Wu Y, Sow S, Sur D, Breiman R, Faruque A, Zaidi A, Saha D, Alonso P, Tamboura B, Sanogo D, Onwuchekwa U, Manna B, Ramamurthy T, Kanungo S, Ochieng J, Omore R, Oundo J, Hossain A, Das S, Ahmed S, Qureshi S, Quadri F, Adegbola R, Antonio M, Hossain J, Akinsola A, Mandomando I, Nhampossa T, Acácio S, Biswas K, O’Reilly C, Mintz E, Berkeley L, Muhsen K, Sommerfelt H, Robins-Browne R, Levine M (2013) Burden and etiology of diarrheal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet 382(9888):209–222. doi:  10.1016/S0140-6736(13)60844-2)
  75. Küstner HG, Gibson IH, Carmichael TR, Van Zyl L, Chouler CA, Hyde JP, du Plessis JN (1981) The spread of cholera in South Africa. S Afr Med J 60(3):87–90PubMedGoogle Scholar
  76. Kyelem CG, Bougouma A, Thiombiano RS, Salou-Kagoné IA, Sangaré L, Ouédraogo R. (2011) Cholera epidemic in Burkina Faso in 2005: epidemiologic and diagnostic aspects. Pan Afr Med J 8:1Google Scholar
  77. Lanata CF, Mendoza W, Black RE (2002) Improving diarrhea estimates. World Health Organization, GenevaGoogle Scholar
  78. Lawoyin TO, Ogunbodede NA, Olumide EA, Onadeko MO (1999) Outbreak of cholera in Ibadan, Nigeria. Eur J Epidemiol 15(4):365–370Google Scholar
  79. Legros D, McCormick M, Mugero C, Skinnider M, Bek’Obita DD, Okware SI (2000) Epidemiology of cholera outbreak in Kampala, Uganda. East Afr Med J 77(7):347–349PubMedGoogle Scholar
  80. Lipp EK, Huq A, Colwell RR (2002) Effects of global climate on infectious disease: the cholera model. Clin Microbiol Rev 15(4):757–770PubMedCentralPubMedGoogle Scholar
  81. Lobitz B, Beck L, Huq A, Wood B, Fuchs G, Faruque AS, Colwell R (2000) Climate and infectious disease: use of remote sensing for detection of Vibrio cholerae by indirect measurement. Proc Natl Acad Sci USA 97:1438–1443PubMedCentralPubMedGoogle Scholar
  82. Lucas ME, Deen JL, von Seidlein L, Wang XY, Ampuero J, Puri M, Ali M, Ansaruzzaman M, Amos J, Macuamule A, Cavailler P, Guerin PJ, Mahoudeau C, Kahozi-Sangwa P, Chaignat CL, Barreto A, Songane FF, Clemens JD (2005) Effectiveness of mass oral cholera vaccination in Beira, Mozambique. N Engl J Med 352:757–767PubMedGoogle Scholar
  83. Luque Fernández MA, Bauernfeind A, Jiménez JD, Gil CL, El Omeiri N, Guibert DH (2009) Influence of temperature and rainfall on the evolution of cholera epidemics in Lusaka, Zambia, 2003–2006: analysis of a time series. Trans R Soc Trop Med Hyg 103(2):137–143PubMedGoogle Scholar
  84. Luque Fernandez MA, Schomaker M, Mason PR, Fesselet JF, Baudot Y, Boulle A, Maes P (2012) Elevation and cholera: an epidemiological spatial analysis of the cholera epidemic in Harare, Zimbabwe, 2008–2009. BMC Public Health 12(1):442PubMedCentralPubMedGoogle Scholar
  85. Luquero FJ, Banga CN, Remartínez D, Palma PP, Baron E, Grais RF (2011) Cholera epidemic in Guinea-Bissau (2008): the importance of “place”. PLoS One 6(5):e19005PubMedCentralPubMedGoogle Scholar
  86. Macnamara NC (1876) A history of Asiatic cholera. MacMillan, LondonGoogle Scholar
  87. Mahamud AS, Ahmed JA, Nyoka R, Auko E, Kahi V, Ndirangu J, Nguhi M, Burton JW, Muhindo BZ, Breiman RF, Eidex RB (2012) Epidemic cholera in Kakuma refugee camp, Kenya, 2009: the importance of sanitation and soap. J Infect Dev Ctries 6(3):234–241PubMedGoogle Scholar
  88. Manga NM, Ndour CT, Diop SA, Dia NM, Ka-Sall R, Diop BM, Sow AI, Sow PS (2008) Cholera in Senegal from 2004 to 2006: lessons learned from successive outbreaks. Med Trop 68(6):589–592Google Scholar
  89. Mari L, Bertuzzo E, Righetto L, Casagrandi R, Gatto M, Rodriguez-Iturbe I, Rinaldo A. (2012) Modelling cholera epidemics: the role of waterways, human mobility and sanitation. J R Soc Interface 9(67):376–388PubMedCentralPubMedGoogle Scholar
  90. Mason PR (2009) Zimbabwe experiences the worst epidemic of cholera in Africa. J Infect 3(2):148–151Google Scholar
  91. Matzger H, BMGF, Why Fishermen & Data are Key for Combating Cholera . 2012Google Scholar
  92. McCormack WM, Islam MS, Fahimuddin M, Mosley WH (1969) A community study of inapparent cholera infections. Am J Epidemiol 89:658–664PubMedGoogle Scholar
  93. Mendelsohn J, Dawson T (2008) Climate and cholera in KwaZulu-Natal, South Africa: the role of environmental factors and implications for epidemic preparedness. Int J Hyg Environ Health 211(1–2):156–162PubMedGoogle Scholar
  94. Merrell DS, Butler SM, Qadri F, Dolganov NA, Alam A, Cohen MB, Calderwood SB, Schoolnik GK, Camilli A (2002) Host-induced epidemic spread of the cholera bacterium. Nature 417(6889):642–645PubMedCentralPubMedGoogle Scholar
  95. Ministry of Health DRC (2012) Situation épidémiologique du choléra en République Démocratique du Congo en 2011. Cholera Division of the Ministry of Health, Democratic Republic of the Congo (DRC)Google Scholar
  96. MMWR (Morbidity and Mortality Weekly Report) September 3, 2004 Centers for disease control and prevention (CDC). Cholera epidemic associated with raw vegetables—Lusaka, Zambia, 2003–2004. 53(34):783–786Google Scholar
  97. Morris JG Jr (2011) Cholera—modern pandemic disease of ancient lineage. Emerg Infect Dis 17(11):2099–2104PubMedCentralPubMedGoogle Scholar
  98. Mugoya I, Kariuki S, Algal T, Njuguna C, Omolon J, Jorge J, Kalan R, Niota C, Teethe C, Bedno S, Breiman RF (2005) Feikin DR (2008) Rapid spread of Vibrio cholerae O1 throughout Kenya. Am J Trop Med Hyg 78(3):527–533Google Scholar
  99. Mukandavire Z, Liao S, Wang J, Gaff H, Smith DL (2011) Morris JG Jr (2011) Estimating the reproductive numbers for the 2008–2009 cholera outbreaks in Zimbabwe. Proc Natl Acad Sci USA 108(21):8767–8772PubMedCentralPubMedGoogle Scholar
  100. Mulholland K (1985) Cholera in Sudan: An account of an epidemic in a refugee camp in eastern Sudan, May–June 1985. Disasters 9(4):247–258Google Scholar
  101. Mutonga D, Langat D, Mwangi D, Tonui J, Njeru M, Abade A et al (2013) Cholera epidemiology in Kenya based on national surveillance data from 1997–2010. J Infect Dis 208(1):S55–S61PubMedGoogle Scholar
  102. Muula AS (2009) My Africa. Poverty, health, disease, and medical journalism. Croat Med J 50(6):598–599PubMedCentralPubMedGoogle Scholar
  103. Nelson EJ, Harris JB, Morris JG Jr, Calderwood SB, Camilli A (2009) Cholera transmission: the host, pathogen and bacteriophage dynamic. Nat Rev Microbiol 7(10):693–702PubMedGoogle Scholar
  104. Nguyen VD, Sreenivasan N, Lam E, Ayers T, Kargbo D, Dafae F, Jambai A, Alemu W, Kamara A, Islam MS, Stroika S, Bopp C, Quick R, Mintz ED, Brunkard JM (2014) Cholera epidemic associated with consumption of unsafe drinking water and street-vended water–eastern freetown, Sierra Leone, 2012. Am J Trop Med Hyg 90(3):518–523. doi:  10.4269/ajtmh.13-0567. Epub 2014 Jan 27
  105. Nzirorera S (2008) Prevention and hygiene-awareness efforts aim to stave off cholera in Guinea-BissauGoogle Scholar
  106. O’Donoghue R (2005) Rhodes university, South Africa. cholera in KwaZulu-Natal: probing institutional governmentality and indigenous hand-washing practicesGoogle Scholar
  107. Olago D, Marshall M, Wandiga SO, Opondo M, Yanda PZ, Kanalawe R, Githeko AK, Downs T, Opere A, Kavumvuli R, Kirumira E, Ogallo L, Mugambi P, Apindi E, Githui F, Kathuri J, Olaka L, Sigalla R, Nanyunja R, Baguma T, Achola P (2007) Climatic, socio-economic, and health factors affecting human vulnerability to cholera in the Lake Victoria basin, East Africa. Ambio 36(4):350–358PubMedGoogle Scholar
  108. Orfeuil JP (2002) La mobilité dans le mondeGoogle Scholar
  109. Osei FB, Duker AA (2008) Spatial and demographic patterns of cholera in Ashanti region - Ghana. Int J Health Geogr 7:44PubMedCentralPubMedGoogle Scholar
  110. Ouedraogo RT, Njanpop-Lafourcade B-M, Jaillard P et al (2009) Mobile laboratory to improve response to meningitis epidemics, Burkina Faso epidemic season 2004. Field actions science reports. J Field Actions 1Google Scholar
  111. Pascual M, Rodó X, Ellner SP, Colwell R, Bouma MJ (2000) Cholera dynamics and El Niño-Southern Oscillation. Science 289:1766–1769PubMedGoogle Scholar
  112. Pasetti MF, Levine MM (2012) Insights from natural infection-derived immunity to cholera instruct vaccine efforts. Clin Vaccine Immunol 19:1707–1711PubMedCentralPubMedGoogle Scholar
  113. Paz S (2009) Impact of temperature variability on cholera incidence in Southeastern Africa, 1971–2006. Ecohealth 6(3):340–345PubMedGoogle Scholar
  114. Paz S, Broza M (2007) Wind direction and its linkage with Vibrio cholerae dissemination. Environ Health Perspect 115(2):195–200PubMedCentralPubMedGoogle Scholar
  115. Penrose K, de Castro MC, Werema J, Ryan ET (2010) Informal urban settlements and cholera risk in Dar-as-Salaam, Tanzania. PLoS Negl Trop Dis 4(3):e631PubMedCentralPubMedGoogle Scholar
  116. Perry Phil MSJ, Donini-Lenhoff F (2010) Stigmatization complicates infectious disease managementGoogle Scholar
  117. Piarroux R, Bompangue D, Oger PY, Haaser F, Boinet A, Vandevelde T (2009) From research to field action: example of the fight against cholera in the democratic Republic of Congo. Field Actions Sci Rep 2:69–77Google Scholar
  118. Piarroux R, Faucher B (2012) Cholera epidemics in 2010: respective roles of environment, strain changes, and human-driven dissemination. Clin Microbiol Infect 18(3):231–238PubMedGoogle Scholar
  119. Poda JN, Gagliardi R, Kam FO, Niameogo AT (2003) La perception des populations des maladies diarrhéiques au Burkina Faso: une piste pour l’éducation aux problèmes de santé,VertigO–la revue électronique en sciences de l’environnementGoogle Scholar
  120. Qadri F, Hasan JA, Hossain J et al (1995) Evaluation of the monoclonal antibody-based kit Bengal SMART for rapid detection of Vibrio cholerae O139 synonym Bengal in stool samples. J Clin Microbiol 33:732–734PubMedCentralPubMedGoogle Scholar
  121. Quilici ML, Massenet D, Gake B, Bwalki B, Olson DM (2010) Vibrio cholerae O1 variant with reduced susceptibility to ciprofloxacin, Western Africa. Emerg Infect Dis 16(11):1804–1805PubMedCentralPubMedGoogle Scholar
  122. Qureshi K, Mølbak K, Sandström A, Kofoed PE, Rodrigues A, Dias F, Aaby P, Svennerholm AM (2006) Breast milk reduces the risk of illness in children of mothers with cholera: observations from an epidemic of cholera in Guinea-Bissau. Pediatr Infect Dis J 25(12):1163–1166PubMedGoogle Scholar
  123. Rabbani GH, Greenough WB (1999) Food as a vehicle of transmission of cholera. J Diarrheal Dis Res 17(1):1–9Google Scholar
  124. Rebaudet S, Sudre B, Piarroux R (2013) A review of cholera in coastal Africa. J Infect Dis 208(1):S98–S106Google Scholar
  125. Retzky A (2012) Professor Virginia cornish working to engineer yeast to detect cholera. In: Columbia University. Accessed 19 Mar 2013
  126. 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(6):862–869. (Erratum in: Am J Trop Med Hyg 2011 Jul;85(1):191)Google Scholar
  127. Rodrigues A, Brun H, Sandstrom A (1997) Risk factors for cholera infection in the initial phase of an epidemic in Guinea-Bissau: protection by lime juice. Am J Trop Med Hyg 57(5):601–604PubMedGoogle Scholar
  128. Rodrigues A, Sandström A, Cá T, Steinsland H, Jensen H, Aaby P (2000) Protection from cholera by adding lime juice to food - results from community and laboratory studies in Guinea-Bissau, West Africa. Trop Med Int Health 5(6):418–422PubMedGoogle Scholar
  129. Sabinot C (2009) Dynamique des savoirs et des Savoir-faire dans un contexte pluriculturel, étude comparative des activités littorales au GabonGoogle Scholar
  130. Sack DA (2013) Global cholera burden estimates. In: Johns hopkins bloomberg school of public health. Accessed 15 Nov 2013
  131. Sasaki S, Suzuki H, Fujino Y, Kimura Y, Cheelo M (2009) Impact of drainage networks on cholera outbreaks in Lusaka, Zambia. Am J Public Health 99(11):1982–1987PubMedCentralPubMedGoogle Scholar
  132. Sasaki S, Suzuki H, Igarashi K, Tambatamba B, Mulenga P (2008) Spatial analysis of risk factor of cholera outbreak for 2003-2004 in a peri-urban area of Lusaka, Zambia. Am J Trop Med Hyg 79(3):414–421PubMedGoogle Scholar
  133. Schaetti C, Hutubessy R, Ali SM, Pach A, Weiss MG, Chaignat CL, Khatib AM (2009) Oral cholera vaccine use in Zanzibar: socioeconomic and behavioral features affecting demand and acceptance. BMC Public Health 9:99PubMedCentralPubMedGoogle Scholar
  134. Schaetti C, Khatib IS, Hutubessy R, Chaignat CL, Weiss M-G (2010) Social and cultural features of cholera and shigellosis in peri-urban and rural communities of ZanzibarGoogle Scholar
  135. Scheelbeek P, Treglown S, Reid T, Maes P (2009) Household fish preparation hygiene and cholera transmission in Monrovia, Liberia. J Infect Dev Ctries 3(9):727–731PubMedGoogle Scholar
  136. Schubert J, Diwete J (2008) Étude qualitative sur la prise en charge de la diarrhée et l’introduction du zinc en RDC (Katanga, Kasaï oriental, Kinshasa)Google Scholar
  137. Schürmann D, Ebert N, Kampf D, Baumann B, Frei U, Suttorp N (2002) Domestic cholera in Germany associated with fresh fish imported from Nigeria. Eur J Clin Microbiol Infect Dis 21(11):827–828PubMedGoogle Scholar
  138. Shapiro RL, Otieno MR, Adcock PM, Phillips-Howard PA, Hawley WA, Kumar L, Waiyaki P, Nahlen BL, Slutsker L (1999) Transmission of epidemic Vibrio cholerae O1 in rural western Kenya associated with drinking water from Lake Victoria: an environmental reservoir for cholera? Am J Trop Med Hyg 60(2):271–276PubMedGoogle Scholar
  139. Shikanga OT, Mutonga D, Abade M, Amwayi S, Ope M, Limo H, Mintz ED, Quick RE, Breiman RF, Feikin DR (2009) High mortality in a cholera outbreak in western Kenya after post-election violence in 2008. Am J Trop Med Hyg 81(6):1085–1090PubMedGoogle Scholar
  140. Shultz A, Omolon JO, Burke H, Qassim M, Ochieng JB, Weinberg M, Feikin DR, Breiman RF (2009) Cholera outbreak in Kenyan refugee camp: risk factors for illness and importance of sanitation. Am J Trop Med Hyg 80(4):640–645PubMedGoogle Scholar
  141. Soura B, Baya B, Rossier C (2008) Institut Superieur des Sciences de la Population Université de Ouagadougou. Utilisation des médicaments de la rue à Ouagadougou effet de niveau de vie ou effet de niveau d’éducation ?Google Scholar
  142. St Louis ME, Porter JD, Helal A, Drame K, Hargrett-Bean N, Wells JG, Tauxe RV (1990) Epidemic cholera in West Africa: The role of food handling and high-risk foods. Am J Epidemiol 131:719–728PubMedGoogle Scholar
  143. Staro F (2011) Entre savoirs experts et mauvais sort Pratiques d’utilisation de l’eau et perception de l’épidémie duGoogle Scholar
  144. Swerdlow DL, Malanga G, Begokyan G et al (1991) Epidemic of antimicrobial resistant Vibrio cholera O1 infections in a refugee camp, Malawi. In: Program and abstracts of the 31st interscience conference on antimicrobial agents and chemotheraphy, vol. 529. p 187Google Scholar
  145. Swerdlow DL, Malenga G, Begkoyian G, Nyangulu D, Toole M, Waldman RJ, Puhr DN, Tauxe RV (1997) Epidemic cholera among refugees in Malawi, Africa: treatment and transmission. Epidemiol Infect 118(3):207–214PubMedCentralPubMedGoogle Scholar
  146. Tauxe RV, Holmberg SD, Dodin A, Wells JV, Blake PA (1988) Epidemic cholera in Mali: high mortality and multiple routes of transmission in a famine area. Epidemiol Infect 100:279–289PubMedCentralPubMedGoogle Scholar
  147. Trærup SL, Ortiz RA, Markandya A (2011) The costs of climate change: a study of cholera in Tanzania. Int J Environ Res Public Health 8(12):4386–4405PubMedCentralPubMedGoogle Scholar
  148. Truscott R (2008) Zimbabwe faces a “major health disaster”, as hospitals close. BMJ 337:a2710PubMedGoogle Scholar
  149. Umoh JU, Adesiyun AA, Adekeye JO, Nadarajah M (1983) Epidemiological features of an outbreak of gastroenteritis/cholera in Katsina, Northern Nigeria. J Hyg (Lond) 91(1):101–111Google Scholar
  150. UNICEF (2013) Accessed 25 May 2013
  151. Utsalo SJ, Eko FO, Umoh F, Asindi AA (1999) Faecal excretion of Vibrio cholerae during convalescence of cholera patients in Calabar, Nigeria. Eur J Epidemiol 15(4):379–381PubMedGoogle Scholar
  152. Van Loon FP, Clemens JD, Shahrier M, Sack DA, Stephensen CB, Khan MR, Rabbani GH, Rao MR, Banik AK (1990) Low gastric acid as a risk factor for cholera transmission: application of a new non-invasive gastric acid field test. J Clin Epidemiol 43:1361–1367PubMedGoogle Scholar
  153. Von Seidlein L (2013) J Infect Dis 208(1):S8-S14Google Scholar
  154. Weil AG, Ragheb J, Niazi TN, Bhatia S (2012) Am J Trop Med Hyg 87(5):921–6. doi:  10.4269/ajtmh.2012.12-0323. Epub 2012 Sep 10
  155. Wendo C (2003) Cholera spreads in Liberia. Lancet 362(9388):966PubMedGoogle Scholar
  156. WHO (2005) International health regulations, 2nd edn. World Health Organization, GenevaGoogle Scholar
  157. WHO (2009) Global task force on cholera control. Cholera country profile: Sierra Leone. Accessed 7 Sept 2009
  158. WHO (2010) Global health observatory, MDG-7 Environment sustainability, population using improved sanitation. Accessed 21 Dec 2012
  159. WHO Global Health Observatory (GHO) (2012) . Accessed 15 Jan 2013
  160. WHO (2013) Global health observatory. Accessed 15 Jan 2013
  161. WHO (2013) Integrated disease surveillance. In: World Health Organization. Accessed 18 Mar 2013
  162. Zuckerman JN, Rombo L, Fisch A (2007) The true burden and risk of cholera: implications for prevention and control. Lancet Infect Dis 7(8):521–530PubMedGoogle Scholar
  163. Zurovac D, Talisuna AO, Snow RW (2012) Mobile phone text messaging: tool for malaria control in Africa. PLoS Medicine 9:e1001176PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Martin A. Mengel
    • 1
    Email author
  • Isabelle Delrieu
    • 1
  • Leonard Heyerdahl
    • 1
  • Bradford D. Gessner
    • 1
  1. 1.Agence de Médecine PréventiveParisFrance

Personalised recommendations