1887

Abstract

Cholera is a severe diarrhoeal disease that spreads rapidly and affects millions of people each year, resulting in tens of thousands of deaths. The disease is caused by O1 and is characterized by watery diarrhoea that can be lethal if not properly treated. Cholera had not been reported in South America from the late 1800s until 1991, when it was introduced in Peru, wreaking havoc in one of the biggest epidemics reported to date. Within a year, the disease had spread to most of the Latin American region, resulting in millions of cases and thousands of deaths in all affected countries. Despite its aggressive entry, cholera virtually disappeared from the continent after 1999. The progression of the entire epidemic was well documented, making it an ideal model to understand cholera dynamics. In this review, we highlight how the synergy of socioeconomic, political and ecological factors led to the emergence, rapid spread and eventual disappearance of cholera in Latin America. We discuss how measures implemented during the cholera epidemic drastically changed its course and continental dynamics. Finally, we synthesize our findings and highlight potential lessons that can be learned for efficient and standardized cholera management programmes during future outbreaks in non-endemic areas.

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2021-01-08
2024-03-29
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References

  1. Ali M, Nelson AR, Lopez AL, Sack DA. Updated global burden of cholera in endemic countries. PLoS Negl Trop Dis 2015; 9:e0003832 [View Article]
    [Google Scholar]
  2. Clemens JD, Nair GB, Ahmed T, Qadri F, Holmgren J. Cholera. Lancet 2017; 390:1539–1549 [View Article]
    [Google Scholar]
  3. Harris JB, LaRocque RC, Qadri F, Ryan ET, Calderwood SB. Cholera. Lancet 2012; 379:2466–2476 [View Article]
    [Google Scholar]
  4. Islam MT, Alam M, Boucher Y. Emergence, ecology and dispersal of the pandemic generating Vibrio cholerae lineage. Int Microbiol 2017; 20:106–115
    [Google Scholar]
  5. Mutreja A, Kim DW, Thomson NR, Connor TR, Lee JH et al. Evidence for several waves of global transmission in the seventh cholera pandemic. Nature 2011; 477:462–465 [View Article]
    [Google Scholar]
  6. Domman D, Quilici M-L, Dorman MJ, Njamkepo E, Mutreja A et al. Integrated view of Vibrio cholerae in the Americas. Science 2017; 358:789–793 [View Article]
    [Google Scholar]
  7. Weill F-X, Domman D, Njamkepo E, Tarr C, Rauzier J, Fawal N, Keddy KH et al. Genomic history of the seventh pandemic of cholera in Africa. Science 2017; 358:785–789 [View Article]
    [Google Scholar]
  8. Lantagne D, Balakrish Nair G, Lanata CF, Cravioto A. The cholera outbreak in Haiti: where and how did it begin?. Wildlife and Emerging Zoonotic Diseases: The Biology, Circumstances and Consequences of Cross-Species Transmission Springer: Curr Top Microbiol Immunol; 2013 pp 145–164
    [Google Scholar]
  9. Qadri F, Islam T, Clemens JD. Cholera in Yemen — an old foe rearing its ugly head. N Engl J Med 2017; 377:2005–2007 [View Article]
    [Google Scholar]
  10. Almagro-Moreno S, Boyd EF. Sialic acid catabolism confers a competitive advantage to pathogenic Vibrio cholerae in the mouse intestine. Infect Immun 2009; 77:3807–3816 [View Article]
    [Google Scholar]
  11. Karaolis DK, Johnson JA, Bailey CC, Boedeker EC, Kaper JB et al. A Vibrio cholerae pathogenicity island associated with epidemic and pandemic strains. Proc Natl Acad Sci U S A 1998; 95:3134–3139 [View Article]
    [Google Scholar]
  12. Shapiro BJ, Levade I, Kovacikova G, Taylor RK, Almagro-Moreno S. Origins of pandemic Vibrio cholerae from environmental gene pools. Nat Microbiol 2017; 2:16240 [View Article]
    [Google Scholar]
  13. Waldor MK, Mekalanos JJ. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 1996; 272:1910–1914 [View Article]
    [Google Scholar]
  14. Dafae F, Bopp C, Kargbo D, Stroika S, Kamara A et al. Cholera epidemic associated with consumption of unsafe drinking water and street-vended water-Eastern Freetown, Sierra Leone, 2012. Am J Trop Med Hyg 2014; 90:518–523
    [Google Scholar]
  15. Lessler J, Moore S, Shannon K, Zelaya C, Azman AS. Epidemic risk from cholera introductions into Mexico. PLoS Curr 2014; 6: [View Article]
    [Google Scholar]
  16. Makoni M. Inside Zimbabwe’s efforts to tame cholera. Lancet 2018; 392:e8 [View Article]
    [Google Scholar]
  17. Ohene-Adjei K, Kenu E, Bandoh DA, Addo PNO, Noora CL et al. Epidemiological link of a major cholera outbreak in greater Accra region of Ghana, 2014. BMC Public Health 2017; 17:1–10 [View Article]
    [Google Scholar]
  18. Ujjiga TTA, Wamala JF, Mogga JJH, Othwonh TO, Mutonga D et al. Risk factors for sustained cholera transmission, Juba County, South Sudan, 2014. Emerg Infect Dis 2015; 21:1849–1852 [View Article]
    [Google Scholar]
  19. Galdós-Tangüis H. El cólera en El mundo. La epidemia de cólera de 1991 en El Perú (Cholera in the world. The Peruvian cholera epidemic from 1991). Gaceta Sanitaria 1994; 8:139–145
    [Google Scholar]
  20. Cerda R, Lee PT, Rodrigo Cerda PTL. Modern cholera in the Americas: an opportunistic societal infection. Am J Public Health 2013; 103:1934–1937 [View Article]
    [Google Scholar]
  21. Tauxe R, Mintz ED, Quick RE. Epidemic cholera in the new world: translating field epidemiology into new prevention strategies. Emerg Infect Dis 1995; 1:141–146 [View Article]
    [Google Scholar]
  22. Tauxe RV, Blake PA. Epidemic cholera in Latin America. JAMA 1992; 267:1388–1390 [View Article]
    [Google Scholar]
  23. Harvez CB, Ávila VS. La epidemia del colera en America Latina: reemergencia Y morbimortalidad (the cholera epidemic in Latin America: reemergence, morbidity, and mortality). Rev Panam Salud Publica 2013; 33:40–46
    [Google Scholar]
  24. Smirnova A, Sterrett N, Mujica OJ, Munayco C, Suárez L et al. Spatial dynamics and the basic reproduction number of the 1991–1997 cholera epidemic in Peru. PLoS Negl Trop Dis 2020; 14:e0008045 [View Article]
    [Google Scholar]
  25. Almagro-Moreno S, Taylor RK. Cholera: environmental reservoirs and impact on disease transmission. Microbiol Spect 2013; 1:149–165
    [Google Scholar]
  26. Colwell RR, Kaper J, Joseph SW. Vibrio cholerae, Vibrio parahaemolyticus, and other vibrios: occurrence and distribution in Chesapeake Bay. Science 1977; 198:394–396 [View Article]
    [Google Scholar]
  27. Islam MS, Hasan MK, Miah MA, Qadri F, Yunus M et al. Isolation of Vibrio cholerae 0139 Bengal from water in Bangladesh. Lancet 1993; 342:430 [View Article]
    [Google Scholar]
  28. Davies BW, Bogard RW, Young TS, Mekalanos JJ. Coordinated regulation of accessory genetic elements produces cyclic Di-Nucleotides for V. cholerae Virulence. Cell 2012; 149:358–370 [View Article]
    [Google Scholar]
  29. Dziejman M, Balon E, Boyd D, Fraser CM, Heidelberg JF et al. Comparative genomic analysis of Vibrio cholerae: genes that correlate with cholera endemic and pandemic disease. Proc Natl Acad Sci U S A 2002; 99:1556–1561 [View Article]
    [Google Scholar]
  30. Almagro-Moreno S, Pruss K, Taylor RK. Intestinal colonization dynamics of Vibrio cholerae . PLoS Pathog 2015; 11:e1004787 [View Article]
    [Google Scholar]
  31. Conner JG, Teschler JK, Jones CJ, Yildiz FH. Staying alive: Vibrio cholerae’s cycle of environmental survival, transmission, and dissemination. Microbiol Spect 2016; 4:VMBF-0015-2015 [View Article]
    [Google Scholar]
  32. Lutz C, Erken M, Noorian P, Sun S, McDougald D. Environmental reservoirs and mechanisms of persistence of Vibrio cholerae . Front Microbiol 2013; 4:375 [View Article]
    [Google Scholar]
  33. Yildiz FH, Schoolnik GK. Vibrio cholerae O1 El Tor: identification of a gene cluster required for the rugose colony type, exopolysaccharide production, chlorine resistance, and biofilm formation. Proc Natl Acad Sci U S A 1999; 96:4028–4033 [View Article]
    [Google Scholar]
  34. Silva AJ, Benitez JA. Vibrio cholerae biofilms and cholera pathogenesis. PLoS Negl Trop Dis 2016; 10:e0004330 [View Article]
    [Google Scholar]
  35. Taylor RK, Miller VL, Furlong DB, Mekalanos JJ. Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proc Natl Acad Sci U S A 1987; 84:2833–2837 [View Article]
    [Google Scholar]
  36. Finkelstein RA, LoSpalluto JJ. Pathogenesis of experimental cholera. Preparation and isolation of choleragen and choleragenoid. J Exp Med 1969; 130:185–202
    [Google Scholar]
  37. Rivera-Chávez F, Mekalanos JJ. Cholera toxin promotes pathogen acquisition of host-derived nutrients. Nature 2019; 572:244–248 [View Article]
    [Google Scholar]
  38. Sánchez J, Holmgren J. Virulence factors, pathogenesis and vaccine protection in cholera and ETEC diarrhea. Curr Opin Immunol 2005; 17:388–398 [View Article]
    [Google Scholar]
  39. Begue RE, Castellares G, Hayashi KE, Ruiz R, Meza R et al. Diarrheal disease in Peru after the introduction of cholera. Am J Trop Med Hyg 1994; 51:585–589 [View Article][PubMed]
    [Google Scholar]
  40. Cama RI, Parashar UD, Taylor DN, Hickey T, Figueroa D et al. Enteropathogens and other factors associated with severe disease in children with acute watery diarrhea in Lima, Peru. J Infect Dis 1999; 179:1139–1144 [View Article]
    [Google Scholar]
  41. Kaper JB, Morris JG, Levine MM. Cholera. Clin Microbiol Rev 1995; 8:48–86 [View Article]
    [Google Scholar]
  42. Sack DA, Sack RB, Nair GB, Siddique AK. Cholera. Lancet 2004; 363:223–233 [View Article]
    [Google Scholar]
  43. Hahn S, Kim Y, Garner P. Cochrane Infectious Diseases Group Reduced osmolarity oral rehydration solution for treating dehydration caused by acute diarrhoea in children. Cochrane Database Syst Rev 2002; 84:775 [View Article]
    [Google Scholar]
  44. Tauxe RV, Daniels NA, Gunnlaugsson G, Wells JG, Mintz ED et al. First do no harm: making oral rehydration solution safer in a cholera epidemic. Am J Trop Med Hyg 1999; 60:1051–1055
    [Google Scholar]
  45. Lindenbaum J, Greenough WB, Islam MR. Antibiotic therapy of cholera. Bull World Health Organ 1967a; 36:871–883
    [Google Scholar]
  46. Lindenbaum J, Greenough WB, Islam MR. Antibiotic therapy of cholera in children. Bull World Health Organ 1967b; 37:529–538
    [Google Scholar]
  47. Nelson EJ, Nelson DS, Salam MA, Sack DA. Antibiotics for both moderate and severe cholera. N Engl J Med 2011; 364:5–7 [View Article]
    [Google Scholar]
  48. Ryan ET, Calderwood SB. Cholera vaccines. Clin Infect Dis 2000; 31:561–565 [View Article]
    [Google Scholar]
  49. Wong KK, Burdette E, Mahon BE, Mintz ED, Ryan ET et al. Recommendations of the advisory committee on immunization practices for use of cholera vaccine. Morb Mortal Wkly Rep 2017; 66:482–485 [View Article]
    [Google Scholar]
  50. Gotuzzo E, Cieza J, Estremadoyro L, Seas C. Cholera. lessons from the epidemic in Peru. Infect Dis Clin North Am 1994; 8:183–205
    [Google Scholar]
  51. Guthmann JP. Epidemic cholera in Latin America: spread and routes of transmission. J Trop Med Hyg 1995; 98:419–427
    [Google Scholar]
  52. Ramírez IJ, Grady SC, Glantz MH, Ramírez IJ, Grady SC. Reexamining El Niño and cholera in Peru: a climate Affairs approach. Wea Climate Soc 2013; 5:148–161 [View Article]
    [Google Scholar]
  53. Seas C, Miranda J, Gil AI, Leon-Barua R, Patz J et al. New insights on the emergence of cholera in Latin America during 1991: the Peruvian experience. Am J Trop Med Hyg 2000; 62:513–517 [View Article][PubMed]
    [Google Scholar]
  54. Bravo Cruz N, Guillén A. Historical report: first isolation of Vibrio cholerae serogroup O1 biovar El Tor serovar Inaba during the cholerae epidemic in Peru – 1991. Rev Peru Med Exp Salud Publica 2011; 28:136–139
    [Google Scholar]
  55. Izurieta R, Malavade SS, Narvaez A, Mitra A, Ochoa T et al. Cholera in Ecuador: current relevance of past lessons learnt. J Glob Infect Dis 2011; 3:189 [View Article]
    [Google Scholar]
  56. Azarian T, Ali A, Johnson JA, Jubair M, Cella E et al. Non-toxigenic environmental Vibrio cholerae O1 strain from Haiti provides evidence of pre-pandemic cholera in Hispaniola. Sci Rep 2016; 6:e00157 [View Article]
    [Google Scholar]
  57. Wachsmuth IK, Evins GM, Fields PI, Olsvik O, Popovic T et al. The molecular epidemiology of cholera in Latin America. J Infect Dis 1993; 167:621–626 [View Article]
    [Google Scholar]
  58. Evins GM, Cameron DN, Wells JG, Greene KD, Popovic T et al. The emerging diversity of the electrophoretic types of Vibrio cholerae in the Western hemisphere. J Infect Dis 1995; 172:173–179 [View Article]
    [Google Scholar]
  59. Popovic T, Bopp C, Olsvik O, Wachsmuth K. Epidemiologic application of a standardized ribotype scheme for Vibrio cholerae O1. J Clin Microbiol 1993; 31:2474–2482 [View Article]
    [Google Scholar]
  60. Morris K. Illness from Hurricane Mitch starts to rise. Lancet 1998; 352:1766 [View Article]
    [Google Scholar]
  61. Ries AA, Vugia DJ, Beingolea L, Palacios AM, Vasquez E et al. Cholera in Piura, Peru: a modern urban epidemic. J Infect Dis 1992; 166:1429–1433 [View Article]
    [Google Scholar]
  62. Morris JG, Sztein MB, Rice EW, Nataro JP, Losonsky GA et al. Vibrio cholerae 01 can assume a chlorine-resistant rugose survival form that is virulent for humans. J Infect Dis 1996; 174:1364–1368 [View Article]
    [Google Scholar]
  63. Rice E, Johnson C, Clark R, Fox K, Reasoner D et al. Chlorine and survival of "rugose" Vibrio cholerae . The Lancet 1992; 340:740 [View Article]
    [Google Scholar]
  64. Tickner J, Gouveia-Vigeant T. The 1991 cholera epidemic in Peru: not a case of precaution gone awry. Risk Analysis 2005; 25:495–502 [View Article]
    [Google Scholar]
  65. Ibarra JO, Alvarado DE. Antimicrobial resistance of clinical and environmental strains of Vibrio cholerae isolated in Lima-Peru during epidemics of 1991 and 1998. Braz J Infect Dis 2007; 11:100–105 [View Article]
    [Google Scholar]
  66. Ali A, Rashid MH, Karaolis DKR. High-Frequency Rugose Exopolysaccharide Production by Vibrio cholerae . Appl Environ Microbiol 2002; 68:5773–5778 [View Article]
    [Google Scholar]
  67. Nusrin S, Gil AI, Bhuiyan NA, Safa A, Asakura M et al. Peruvian Vibrio cholerae O1 El Tor strains possess a distinct region in the Vibrio seventh pandemic island-II that differentiates them from the prototype seventh pandemic El Tor strains. J Med Microbiol 2009; 58:342–354 [View Article]
    [Google Scholar]
  68. Levine MM, Nalin DR, Craig JP, Hoover D, Bergquist EJ et al. Immunity of cholera in man: relative role of antibacterial versus antitoxic immunity. Trans R Soc Trop Med Hyg 1979; 73:3–9 [View Article]
    [Google Scholar]
  69. Levine MM, Black RE, Clements ML, Nalin DR, Cisneros L. Volunteer studies in development of vaccines against cholera and enterotoxigenic Escherichia coli: a review. Acute Enteric Infections in Children New Prospects for Treatment and Prevention Elsevier/North: Holland Biomedical Press; 1981b pp 443–459
    [Google Scholar]
  70. Barua D, Paguio AS. ABO blood groups and cholera. Ann Hum Biol 1977; 4:489–492 [View Article]
    [Google Scholar]
  71. Harris JB, Khan AI, LaRocque RC, Dorer DJ, Chowdhury F et al. Blood group, immunity, and risk of infection with Vibrio cholerae in an area of endemicity. Infect Immun 2005; 73:7422–7427 [View Article]
    [Google Scholar]
  72. Maguiña Vargas C, Seas Ramos C, Galán Rodas E, Santana Canchanya JJ. Historia del cólera en El Perú en 1991 (history of cholera in Peru). Acta Médica Peruana 2010; 27:212–217
    [Google Scholar]
  73. Franco AA, Fix AD, Prada A, Paredes E, Palomino JC et al. Cholera in Lima, Peru, correlates with prior isolation of Vibrio cholerae from the environment. Am J Epidemiol 1997; 146:1067–1075 [View Article]
    [Google Scholar]
  74. Jayakumar J, Balasubramanian D, Reddi G, Almagro‐Moreno S. Synergistic role of abiotic factors driving viable but non‐culturable Vibrio cholerae . Environ Microbiol Rep 2020; 12:454–465 [View Article]
    [Google Scholar]
  75. Gil AI, Louis VR, Rivera ING, Lipp E, Huq A et al. Occurrence and distribution of Vibrio cholerae in the coastal environment of Peru. Environ Microbiol 2004; 6:699–706 [View Article]
    [Google Scholar]
  76. Jutla AS, Akanda AS, Griffiths JK, Colwell R, Islam S. Warming oceans, phytoplankton, and river discharge: implications for cholera outbreaks. Am J Trop Med Hyg 2011; 85:303–308 [View Article]
    [Google Scholar]
  77. Shultz JM, Russell J, Espinel Z. Epidemiology of tropical cyclones: the dynamics of disaster, disease, and development. Epidemiol Rev 2005; 27:21–35 [View Article]
    [Google Scholar]
  78. Akanda AS, Jutla AS, Colwell RR. Global diarrhoea action plan needs integrated climate-based surveillance. Lancet Glob Health 2014; 2:e69–e70 [View Article]
    [Google Scholar]
  79. Lobitz B, Beck L, Huq A, Wood B, Fuchs G 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; 97:1438–1443 [View Article]
    [Google Scholar]
  80. Pascual M, Rodó X, Ellner SP, Colwell R, Bouma MJ. Cholera dynamics and El Nino-Southern oscillation. Science 2000; 289:1766–1769 [View Article]
    [Google Scholar]
  81. Rodó X, Pascual M, Fuchs G, Faruque ASG. ENSO and cholera: a nonstationary link related to climate change?. Proc Natl Acad Sci U S A 2002; 99:12901–12906 [View Article]
    [Google Scholar]
  82. Colwell RR. Global climate and infectious disease: the cholera paradigm. Science 1996; 274:2025–2031 [View Article]
    [Google Scholar]
  83. Huq A, Hasan N, Akanda A, Whitcombe E, Colwell R et al. Environmental factors influencing epidemic cholera. Am J Trop Med Hyg 2013; 89:597–607
    [Google Scholar]
  84. Gavilán RG, Martinez-Urtaza J. Environmental drivers of emergence and spreading of Vibrio epidemics in South America. Rev Peru Med Exp Salud Publica 2011; 28:109––115
    [Google Scholar]
  85. Colwell RR. Viable but nonculturable bacteria: a survival strategy. J Infect Chemother 2000; 6:121–125 [View Article]
    [Google Scholar]
  86. Anderson RM, May RM. Directly transmitted infections diseases: control by vaccination. Science 1982; 215:1053–1060 [View Article]
    [Google Scholar]
  87. Meszaros VA, Miller-Dickson MD, Baffour-Awuah F, Almagro-Moreno S, Ogbunugafor CB. Direct transmission via households informs models of disease and intervention dynamics in cholera. PLoS One 2020; 15:e0229837 [View Article]
    [Google Scholar]
  88. Quick RE, Gerber ML, Palacios AM, Beingolea L, Vargas R et al. Using a knowledge, attitudes and practices survey to supplement findings of an outbreak investigation: cholera prevention measures during the 1991 epidemic in Peru. Int J Epidemiol 1996; 25:872–878 [View Article]
    [Google Scholar]
  89. Petrera M. The economic impact of the cholera epidemic, Peru, 1991. Epidemiol Bull 1992; 13:9–11
    [Google Scholar]
  90. Salazar-Lindo E, Alegre M, Rodriguez M, Carrion P, Razzeto N. The Peruvian cholera epidemic and the role of chlorination in its control and prevention. ircwash.org 1993; 2:401–413
    [Google Scholar]
  91. Swerdlow DL et al. Waterborne transmission of epidemic cholera in Trujillo, Peru: lessons for a continent at risk. Lancet 1992; 340:28–32 [View Article]
    [Google Scholar]
  92. Anderson C Cholera epidemic traced to risk miscalculation. Nature 1991; 354:255 [View Article]
    [Google Scholar]
  93. Rabbani GH, Greenough WB. Food as a vehicle of transmission of cholera. J Diarrhoeal Dis Res 1999; 17:1–9
    [Google Scholar]
  94. Mujica O, Seminario L, Taxe R, Beingolea L, Palacios A et al. Investigación epidemiológica del Cólera en El Perú: Lecciones para un continente en riesgo. Revista Medica Herediana 1991; 2:309
    [Google Scholar]
  95. Levine MM, Black RE, Clements ML, Cisneros L, Nalin DR et al. Duration of infection-derived immunity to cholera. J Infect Dis 1981a; 143:818–820 [View Article]
    [Google Scholar]
  96. Ryan ET, Calderwood SB, Qadri F. Live attenuated oral cholera vaccines. Expert Rev Vaccines 2006; 5:483–494 [View Article]
    [Google Scholar]
  97. King AA, Ionides EL, Pascual M, Bouma MJ. Inapparent infections and cholera dynamics. Nature 2008; 454:877–880 [View Article]
    [Google Scholar]
  98. Qadri F, Wierzba TF, Ali M, Chowdhury F, Khan AI et al. Efficacy of a single-dose, inactivated oral cholera vaccine in Bangladesh. N Engl J Med 2016; 374:1723–1732 [View Article]
    [Google Scholar]
  99. Qadri F, Azad AK, Flora MS, Khan AI, Islam MT et al. Emergency deployment of oral cholera vaccine for the Rohingya in Bangladesh. Lancet 2018; 391:1877–1879 [View Article]
    [Google Scholar]
  100. Ahmed MU, Baquilod M, Deola C, Tu ND, Anh DD et al. Cholera prevention and control in Asian countries. BMC Proc 2018; 12:e0003832 [View Article]
    [Google Scholar]
  101. D’Mello-Guyett L, Gallandat K, Van den Bergh R, Taylor D, Bulit G et al. Prevention and control of cholera with household and community water, sanitation and hygiene (wash) interventions: a scoping review of current international guidelines. PLoS One 2020; 15:e0226549 [View Article]
    [Google Scholar]
  102. Raila EM, Anderson DO. Healthcare waste management during disasters and its effects on climate change: lessons from 2010 earthquake and cholera tragedies in Haiti. Waste Manag Res 2017; 35:236–245 [View Article]
    [Google Scholar]
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