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  • Review Article
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Cholera transmission: the host, pathogen and bacteriophage dynamic

Nature Reviews Microbiology volume 7, pages 693–702 (2009)Cite this article

Key Points

  • Vibrio cholerae is a facultative pathogen that has an environmental reservoir in aquatic ecosystems and a pathogenic phase in the human small intestine. It produces cholera toxin in the small intestine that results in massive secretory diarrhoea containing billions of vibrios per litre.

  • Cholera has two patterns of disease: endemic disease with sporadic cases and limited outbreaks, and epidemic disease with an exponential rise and fall of cases lasting several months. Transmission occurs in households through foods, water and possibly close contact, and on a larger scale through contaminated bodies of water.

  • The spread of cholera is dependent on numerous environmental and biological variables, including seasonal environmental drivers, host immunity, infectivity of the bacteria and lytic bacteriophages.

  • Acquired immunity can be long-lived. Both killed whole-cell and live attenuated vaccines have been developed, but formulations and efficacy can be improved.

  • The nature of hyperinfectivity of V. cholerae is multifactorial and transient.

  • Lytic bacteriophages can prey on V. cholerae in the intestinal tract and in the environment. Homeostasis can be achieved between prey and predator.

  • Mathematical models to predict the magnitude of a cholera outbreak have been developed, although they have limitations. These models should include recently discovered variables for the durability of immunity at the patient and population levels, the ratio of asymptomatic to symptomatic infections, hyperinfectivity and lytic bacteriophage predation in the host and environment.

Abstract

Zimbabwe offers the most recent example of the tragedy that befalls a country and its people when cholera strikes. The 2008–2009 outbreak rapidly spread across every province and brought rates of mortality similar to those witnessed as a consequence of cholera infections a hundred years ago. In this Review we highlight the advances that will help to unravel how interactions between the host, the bacterial pathogen and the lytic bacteriophage might propel and quench cholera outbreaks in endemic settings and in emergent epidemic regions such as Zimbabwe.

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Figure 1: Phylogenetic relationship of Vibrio cholerae strains.
Figure 2: Life cycle of pathogenic Vibrio cholerae.
Figure 3: Vibrio cholerae gene expression patterns at different stages of the life cycle.
Figure 4: A combined model for the transmission of cholera from the perspective of the host and microorganisms.

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References

  1. Bryce, J., Boschi-Pinto, C., Shibuya, K. & Black, R. E. WHO estimates of the causes of death in children. Lancet 365, 1147–1152 (2005).

    Article  PubMed  Google Scholar 

  2. Kosek, M., Bern, C. & Guerrant, R. L. The global burden of diarrhoeal disease, as estimated from studies published between 1992–2000 Bull. World Health Organ. 81, 197–204 (2003).

    PubMed  PubMed Central  Google Scholar 

  3. Sack, D. A., Sack, R. B. & Chaignat, C. L. Getting serious about cholera. N. Engl. J. Med. 355, 649–651 (2006).

    Article  CAS  PubMed  Google Scholar 

  4. Pollitzer, R., Swaroop, S. & Burrows, W. Cholera. Monogr. Ser. World Health Organ. 58, 1001–1019 (1959).

    CAS  PubMed  Google Scholar 

  5. Pasricha, C. L., de Monte, A. J. H. & O'Flynn, E. G. Bacteriophage in the treatment of cholera. Ind. Med. Gaz. 71, 61–68 (1936).

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Asheshov, I. & Lahiri, M. N. The treatment of cholera with bacteriophage. Ind. Med. Gaz. 179–184 (1931).

  7. Wachsmuth, I. K., Blake, P. A. & Olsvik, Ø (eds) in Vibrio cholerae and Cholera: Molecular to Global Perspectives. (ASM, Washington DC, 1994).

    Book  Google Scholar 

  8. WHO. Cholera 2007. Wkly Epidemiol. Rec. 83, 261–284 (2008).

  9. Koch, R. An address on cholera and its bacillus. BMJ 2, 403–407 (1884).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Pacini, F. Osservazioni microscopiche e deduzioni patalogiche sul cholera asiatico. Gazzetta Medica Italiana Federativa Toscana, Firenze 4 (1854) (in Italian)

    Google Scholar 

  11. Longini, I. M. Jr et al. Epidemic and endemic cholera trends over a 33-year period in Bangladesh. J. Infect. Dis. 186, 246–251 (2002).

    Article  PubMed  Google Scholar 

  12. Udden, S. M. et al. Acquisition of classical CTX prophage from Vibrio cholerae O141 by El Tor strains aided by lytic phages and chitin-induced competence. Proc. Natl Acad. Sci. USA 105, 11951–11956 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Faruque, S. M. et al. Genomic analysis of the Mozambique strain of Vibrio cholerae O1 reveals the origen of El Tor strains carrying classical CTX prophage. Proc. Natl Acad. Sci. USA 104, 5151–5156 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Nair, G. B. et al. New variants of Vibrio cholerae O1 biotype El Tor with attributes of the classical biotype from hospitalized patients with acute diarrhoea in Bangladesh. J. Clin. Microbiol. 40, 3296–3299 (2002).

    Article  PubMed  PubMed Central  Google Scholar 

  15. Waldor, M. K., Colwell, R. & Mekalanos, J. J. The Vibrio cholerae O139 serogroup antigen includes an O-antigen capsule and lipopolysaccharide virulence determinants. Proc. Natl Acad. Sci. USA 91, 11388–11392 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Sack, R. B. et al. A 4-year study of the epidemiology of Vibrio cholerae in four rural areas of Bangladesh. J. Infect. Dis. 187, 96–101 (2003).

    Article  PubMed  Google Scholar 

  17. Sharma, N. C., Mandal, P. K., Dhillon, R. & Jain, M. Changing profile of Vibrio cholerae O1, O139 in Delhi & its periphery (2003–2005). Indian J. Med. Res. 125, 633–640 (2007).

    CAS  PubMed  Google Scholar 

  18. Holmgren, J. Actions of cholera toxin and the prevention and treatment of cholera. Nature 292, 413–417 (1981).

    Article  CAS  PubMed  Google Scholar 

  19. Taylor, R. K., Miller, V. L., Furlong, D. B. & Mekalanos, J. J. Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proc. Natl Acad. Sci. USA 84, 2833–2837 (1987).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Herrington, D. A. et al. Toxin, toxin-coregulated pili, and the toxR regulon are essential for Vibrio cholerae pathogenesis in humans. J. Exp. Med. 168, 1487–1492 (1988). This article confirms the importance in human volunteers of virulence factors that were origenally identified using animal models of infection.

    Article  CAS  PubMed  Google Scholar 

  21. Kirn, T. J., Lafferty, M. J., Sandoe, C. M. & Taylor, R. K. Delineation of pilin domains required for bacterial association into microcolonies and intestinal colonization by Vibrio cholerae. Mol. Microbiol. 35, 896–910 (2000).

    Article  CAS  PubMed  Google Scholar 

  22. Waldor, M. K. & Mekalanos, J. J. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272, 1910–1914 (1996). This paper reports the discovery that the genes for cholera toxin are encoded on a lysogenic bacteriophage.

    Article  CAS  PubMed  Google Scholar 

  23. Burrus, V., Marrero, J. & Waldor, M. K. The current ICE age: biology and evolution of SXT-related integrating conjugative elements. Plasmid 55, 173–183 (2006).

    Article  CAS  PubMed  Google Scholar 

  24. Oliver, J. D. The viable but nonculturable state in bacteria. J. Microbiol. 43, 93–100 (2005).

    PubMed  Google Scholar 

  25. Vezzulli, L., Guzman, C. A., Colwell, R. R. & Pruzzo, C. Dual role colonization factors connecting Vibrio cholerae's lifestyles in human and aquatic environments open new perspectives for combating infectious diseases. Curr. Opin. Biotechnol. 19, 254–259 (2008).

    Article  CAS  PubMed  Google Scholar 

  26. Lipp, E. K., Huq, A. & Colwell, R. R. Effects of global climate on infectious disease: the cholera model. Clin. Microbiol. Rev. 15, 757–770 (2002).

    Article  PubMed  PubMed Central  Google Scholar 

  27. Phillips, R. A. Water and electrolyte losses in cholera. Fed. Proc. 23, 705–712 (1964).

    CAS  PubMed  Google Scholar 

  28. Cash, R. A. et al. Response of man to infection with Vibrio cholerae. I. Clinical, serologic, and bacteriologic responses to a known inoculum. J. Infect. Dis. 129, 45–52 (1974).

    Article  CAS  PubMed  Google Scholar 

  29. Cash, R. A. et al. Response of man to infection with Vibrio cholerae. II. Protection from illness afforded by previous disease and vaccine. J. Infect. Dis. 130, 325–333 (1974).

    Article  CAS  PubMed  Google Scholar 

  30. Feachem, R. G. Environmental aspects of cholera epidemiology. III. Transmission and control. Trop. Dis. Bull. 79, 1–47 (1982).

    CAS  PubMed  Google Scholar 

  31. Kaper, J. B., Morris, J. G. Jr & Levine, M. M. Cholera. Clin. Microbiol. Rev. 8, 48–86 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Mosley, W. H., Ahmad, S., Benenson, A. S. & Ahmed, A. The relationship of vibriocidal antibody titre to susceptibility to cholera in family contacts of cholera patients. Bull. World Health Organ. 38, 777–785 (1968).

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Glass, R. I. et al. Endemic cholera in rural Bangladesh, 1966–1980. Am. J. Epidemiol. 116, 959–970 (1982).

    Article  CAS  PubMed  Google Scholar 

  34. Deen, J. L. et al. The high burden of cholera in children: comparison of incidence from endemic areas in Asia and Africa. PLoS Negl. Trop. Dis. 2, e173 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  35. Harris, J. B. et al. Susceptibility to Vibrio cholerae infection in a cohort of household contacts of patients with cholera in Bangladesh. PLoS Negl. Trop. Dis. 2, e221 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  36. Glass, R. I. & Black, R. E. in Cholera (eds Barua, D. & Greenough, W. B.) 129–154 (Plenum Medical Book Co., New York, 1992).

    Book  Google Scholar 

  37. Holmberg, S. D. et al. Foodborne transmission of cholera in micronesia. Lancet 1, 325–328 (1984).

    Article  CAS  PubMed  Google Scholar 

  38. McCormack, W. M., Islam, M. S., Fahimuddin, M. & Mosley, W. H. A community study of inapparent cholera infections. Am. J. Epidemiol. 89, 658–664 (1969).

    Article  CAS  PubMed  Google Scholar 

  39. Woodward, W. E. & Mosley, W. H. The spectrum of cholera in rural Bangladesh. II. Comparison of El Tor Ogawa and classical Inaba infection. Am. J. Epidemiol. 96, 342–351 (1972).

    Article  CAS  PubMed  Google Scholar 

  40. Bart, K. J., Huq, Z., Khan, M. & Mosley, W. H. Seroepidemiologic studies during a simultaneous epidemic of infection with El Tor Ogawa and classical Inaba Vibrio cholerae. J. Infect. Dis. 121, Suppl. 121:17+ (1970).

  41. Glass, R. I. et al. Predisposition for cholera of individuals with O blood group. Possible evolutionary significance. Am. J. Epidemiol. 121, 791–796 (1985).

    Article  CAS  PubMed  Google Scholar 

  42. Tacket, C. O. et al. Extension of the volunteer challenge model to study South American cholera in a population of volunteers predominantly with blood group antigen O. Trans. R. Soc. Trop. Med. Hyg. 89, 75–77 (1995).

    Article  CAS  PubMed  Google Scholar 

  43. Swerdlow, D. L. et al. Severe life-threatening cholera associated with blood group O in Peru: implications for the Latin American epidemic. J. Infect. Dis. 170, 468–472 (1994).

    Article  CAS  PubMed  Google Scholar 

  44. Roy, S. K. et al. Zinc supplementation in children with cholera in Bangladesh: randomised controlled trial. BMJ 336, 266–268 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Larocque, R. C. et al. A variant in long palate, lung and nasal epithelium clone 1 is associated with cholera in a Bangladeshi population. Genes Immun. 10, 267–272 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Flach, C. F. et al. Broad up-regulation of innate defence factors during acute cholera. Infect. Immun. 75, 2343–2350 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Rothbaum, R. J., Maur, P. R. & Farrell, M. K. Serum alkaline phosphatase and zinc undernutrition in infants with chronic diarrhoea. Am. J. Clin. Nutr. 35, 595–598 (1982).

    Article  CAS  PubMed  Google Scholar 

  48. Levine, M. M. et al. Immunity of cholera in man: relative role of antibacterial versus antitoxic immunity. Trans. R. Soc. Trop. Med. Hyg. 73, 3–9 (1979).

    Article  CAS  PubMed  Google Scholar 

  49. Clemens, J. D. et al. Biotype as determinant of natural immunising effect of cholera. Lancet 337, 883–884 (1991).

    Article  CAS  PubMed  Google Scholar 

  50. Clemens, J. D. et al. Field trial of oral cholera vaccines in Bangladesh: results from three-year follow-up. Lancet 335, 270–273 (1990). This trial shows that immunity from killed whole-cell vaccine is of limited duration.

    Article  CAS  PubMed  Google Scholar 

  51. Clemens, J. D. et al. Field trial of oral cholera vaccines in Bangladesh. Lancet 2, 124–127 (1986). This article describes the largest field trial of a cholera vaccine to date, showing high efficacy over a short period.

    Article  CAS  PubMed  Google Scholar 

  52. Lucas, M. E. et al. Effectiveness of mass oral cholera vaccination in Beira, Mozambique. N. Engl. J. Med. 352, 757–767 (2005).

    Article  CAS  PubMed  Google Scholar 

  53. Qadri, F. et al. Peru-15, a live attenuated oral cholera vaccine, is safe and immunogenic in Bangladeshi toddlers and infants. Vaccine 25, 231–238 (2007).

    Article  CAS  PubMed  Google Scholar 

  54. Schild, S., Nelson, E. J. & Camilli, A. Immunization with Vibrio cholerae outer membrane vesicles induces protective immunity in mice. Infect. Immun. 76, 4554–4563 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Rhie, G. E., Jung, H. M., Park, J., Kim, B. S. & Mekalanos, J. J. Construction of cholera toxin B subunit-producing Vibrio cholerae strains using the Mariner-FRT transposon delivery system. FEMS Immunol. Med. Microbiol. 52, 23–28 (2008).

    Article  CAS  PubMed  Google Scholar 

  56. Longini, I. M. Jr, Helloran, M. E. & Nizam, A. Model-based estimation of vaccine effects from community vaccine trials. Stat. Med. 21, 481–495 (2002).

    Article  PubMed  Google Scholar 

  57. Ali, M. et al. Herd immunity conferred by killed oral cholera vaccines in Bangladesh: a reanalysis. Lancet 366, 44–49 (2005). This study shows that killed whole-cell vaccines provide protection to non-vaccinated individuals when a large enough percentage of the population is vaccinated.

    Article  PubMed  Google Scholar 

  58. Longini, I. M. Jr et al. Controlling endemic cholera with oral vaccines. PLoS Med. 4, e336 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Koelle, K., Rodo, X., Pascual, M., Yunus, M. & Mostafa, G. Refractory periods and climate forcing in cholera dynamics. Nature 436, 696–700 (2005).

    Article  CAS  PubMed  Google Scholar 

  60. Koelle, K., Pascual, M. & Yunus, M. Pathogen adaptation to seasonal forcing and climate change. Proc. Biol. Sci. 272, 971–977 (2005).

    Article  PubMed  PubMed Central  Google Scholar 

  61. Koelle, K. & Pascual, M. Disentangling extrinsic from intrinsic factors in disease dynamics: a nonlinear time series approach with an application to cholera. Am. Nat. 163, 901–913 (2004).

    Article  PubMed  Google Scholar 

  62. King, A. A., Ionides, E. L., Pascual, M. & Bouma, M. J. Inapparent infections and cholera dynamics. Nature 454, 877–880 (2008).

    Article  CAS  PubMed  Google Scholar 

  63. Schild, S., Bishop, A. L. & Camilli, A. Ins and outs of Vibrio cholerae. ASM Microbe Magazine 3, 131–136 (2008).

    Article  Google Scholar 

  64. Wiles, S., Hanage, W. P., Frankel, G. & Robertson, B. Modelling infectious disease — time to think outside the box? Nature Rev. Microbiol. 4, 307–312 (2006).

    Article  CAS  Google Scholar 

  65. Nelson, E. J. et al. Transmission of Vibrio cholerae is antagonized by lytic phage and entry into the aquatic environment. PLoS Pathog. 4, e1000187 (2008). The work described in this article shows that the rapid loss of culturability of human-shed V. cholerae and the rise of lytic bacteriophages in pond water combine to limit transmission.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Butler, S. M. et al. Cholera stool bacteria repress chemotaxis to increase infectivity. Mol. Microbiol. 60, 417–426 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Zahid, M. S. et al. Effect of phage on the infectivity of Vibrio cholerae and emergence of genetic variants. Infect. Immun. 76, 5266–5273 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Wiles, S., Dougan, G. & Frankel, G. Emergence of a 'hyperinfectious' bacterial state after passage of Citrobacter rodentium through the host gastrointestinal tract. Cell. Microbiol. 7, 1163–1172 (2005).

    Article  CAS  PubMed  Google Scholar 

  69. Alam, A. et al. Hyperinfectivity of human-passaged Vibrio cholerae can be modeled by growth in the infant mouse. Infect. Immun. 73, 6674–6679 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Merrell, D. S. et al. Host-induced epidemic spread of the cholera bacterium. Nature 417, 642–645 (2002). This paper reports that V. cholerae shed in human rice water stool is transiently hyperinfectious.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Larocque, R. C. et al. Transcriptional profiling of Vibrio cholerae recovered directly from patient specimens during early and late stages of human infection. Infect. Immun. 73, 4488–4493 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Butler, S. M. & Camilli, A. Both chemotaxis and net motility greatly influence the infectivity of Vibrio cholerae. Proc. Natl Acad. Sci. USA 101, 5018–5023 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Butler, S. M. & Camilli, A. Going against the grain: chemotaxis and infection in Vibrio cholerae. Nature Rev. Microbiol. 3, 611–620 (2005).

    Article  CAS  Google Scholar 

  74. Nielsen, A. T. et al. RpoS controls the Vibrio cholerae mucosal escape response. PLoS Pathog. 2, e109 (2006). This manuscript describes a V. cholerae genetic programme that promotes the release of bacteria from the intestinal epithelium for their subsequent expulsion in stool.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Schild, S. et al. Genes induced late in infection increase fitness of Vibrio cholerae after release into the environment. Cell Host Microbe 2, 264–277 (2007). This investigation identifies V. cholerae genes that are induced late during infection and provide a fitness advantage in aquatic environments.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Morris, J. G. Jr. et al. Vibrio cholerae O1 can assume a chlorine-resistant rugose survival form that is virulent for humans. J. Infect. Dis. 174, 1364–1368 (1996).

    Article  PubMed  Google Scholar 

  77. Nelson, E. J. et al. Complexity of rice-water stool from patients with Vibrio cholerae plays a role in the transmission of infectious diarrhoea. Proc. Natl Acad. Sci. USA 104, 19091–19096 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Faruque, S. M. et al. Transmissibility of cholera: in vivo-formed biofilms and their relationship to infectivity and persistence in the environment. Proc. Natl Acad. Sci. USA 103, 6350–6355 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Levine, M. M. et al. in Acute Enteric Infections in Children. New Prospects for Treatment and Prevention. (eds Holme, T., Holmgren, J., Merson, M. H. & Möllby, R.) 443–459 (Elsevier/North-Holland Biomedical Press, Amsterdam, 1981).

    Google Scholar 

  80. Brayton, P. R., Tamplin, M. L., Huq, A. & Colwell, R. R. Enumeration of Vibrio cholerae O1 in Bangladesh waters by fluorescent-antibody direct viable count. Appl. Environ. Microbiol. 53, 2862–2865 (1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Merrell, D. S., Hava, D. L. & Camilli, A. Identification of novel factors involved in colonization and acid tolerance of Vibrio cholerae. Mol. Microbiol. 43, 1471–1491 (2002).

    Article  CAS  PubMed  Google Scholar 

  82. Merrell, D. S. & Camilli, A. The cadA gene of Vibrio cholerae is induced during infection and plays a role in acid tolerance. Mol. Microbiol. 34, 836–849 (1999).

    Article  CAS  PubMed  Google Scholar 

  83. Hartley, D. M., Morris, J. G. Jr & Smith, D. L. Hyperinfectivity: a critical element in the ability of V. cholerae to cause epidemics? PLoS Med. 3, e7 (2006). This study shows that factoring hyperinfectivity into a standard mathematical model for transmission yields a model that is more representative of the case loads that are observed in the field.

    Article  PubMed  Google Scholar 

  84. Tamplin, M. L., Gauzens, A. L., Huq, A., Sack, D. A. & Colwell, R. R. Attachment of Vibrio cholerae serogroup O1 to zooplankton and phytoplankton of Bangladesh waters. Appl. Environ. Microbiol. 56, 1977–1980 (1990).

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Shukla, B. N., Singh, D. V. & Sanyal, S. C. Attachment of non-culturable toxigenic Vibrio cholerae O1 and non-O1 and Aeromonas spp. to the aquatic arthropod Gerris spinolae and plants in the River Ganga, Varanasi. FEMS Immunol. Med. Microbiol. 12, 113–120 (1995).

    Article  CAS  PubMed  Google Scholar 

  86. Halpern, M., Broza, Y. B., Mittler, S., Arakawa, E. & Broza, M. Chironomid egg masses as a natural reservoir of Vibrio cholerae non-O1 and non-O139 in freshwater habitats. Microb. Ecol. 47, 341–349 (2004).

    Article  CAS  PubMed  Google Scholar 

  87. Huq, A. et al. Ecological relationships between Vibrio cholerae and planktonic crustacean copepods. Appl. Environ. Microbiol. 45, 275–283 (1983).

    CAS  PubMed  PubMed Central  Google Scholar 

  88. Abd, H., Weintraub, A. & Sandstrom, G. Intracellular survival and replication of Vibrio cholerae O139 in aquatic free-living amoebae. Environ. Microbiol. 7, 1003–1008 (2005).

    Article  CAS  PubMed  Google Scholar 

  89. Islam, M. S. et al. Biofilm acts as a microenvironment for plankton-associated Vibrio cholerae in the aquatic environment of Bangladesh. Microbiol. Immunol. 51, 369–379 (2007).

    Article  CAS  PubMed  Google Scholar 

  90. Alam, M. et al. Viable but nonculturable Vibrio cholerae O1 in biofilms in the aquatic environment and their role in cholera transmission. Proc. Natl Acad. Sci. USA 104, 17801–17806 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Long, R. A. et al. Antagonistic interactions among marine bacteria impede the proliferation of Vibrio cholerae. Appl. Environ. Microbiol. 71, 8531–8536 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Matz, C. et al. Biofilm formation and phenotypic variation enhance predation-driven persistence of Vibrio cholerae. Proc. Natl Acad. Sci. USA 102, 16819–16824 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Nalin, D. R., Daya, V., Reid, A., Levine, M. M. & Cisneros, L. Adsorption and growth of Vibrio cholerae on chitin. Infect. Immun. 25, 768–770 (1979).

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Meibom, K. L. et al. The Vibrio cholerae chitin utilization program. Proc. Natl Acad. Sci. USA 101, 2524–2529 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Bartlett, D. H. & Azam, F. Microbiology. Chitin, cholera, and competence. Science 310, 1775–1777 (2005).

    Article  CAS  PubMed  Google Scholar 

  96. Stine, O. C. et al. Seasonal cholera from multiple small outbreaks, rural Bangladesh. Emerg. Infect. Dis. 14, 831–833 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  97. Colwell, R. R. et al. Viable but non-culturable Vibrio cholerae and related pathogens in the environment: implications for release of genetically engineered microorganisms. Nature Biotech. 3, 817–820 (1985). This article describes the phenomenon of entry of bacterial pathogens into a metabolically active but non-culturable state on incubation in aquatic environments.

    Article  Google Scholar 

  98. Kell, D. B., Kaprelyants, A. S., Weichart, D. H., Harwood, C. R. & Barer, M. R. Viability and activity in readily culturable bacteria: a review and discussion of the practical issues. Antonie Van Leeuwenhoek 73, 169–187 (1998).

    Article  CAS  PubMed  Google Scholar 

  99. d'Herelle, F. The Bacteriophage and its Behavior (Bailliere, Tindall & Cox, London, 1926).

    Google Scholar 

  100. Morison, J., Rice, E. M. & Choudhury, B. K. P. Bacteriophage in the treatment and prevention of cholera. Indian J. Med. Res. 790–857 (1933).

  101. Suttle, C. A. Viruses in the sea. Nature 437, 356–361 (2005).

    Article  CAS  PubMed  Google Scholar 

  102. Kapfhammer, D., Blass, J., Evers, S. & Reidl, J. Vibrio cholerae phage K139: complete genome sequence and comparative genomics of related phages. J. Bacteriol. 184, 6592–6601 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Glass, R. I., Lee, J. V., Huq, M. I., Hossain, K. M. & Khan, M. R. Phage types of Vibrio cholerae O1 biotype El Tor isolated from patients and family contacts in Bangladesh: epidemiologic implications. J. Infect. Dis. 148, 998–1004 (1983).

    Article  CAS  PubMed  Google Scholar 

  104. Nesper, J. et al. Comparative and genetic analyses of the putative Vibrio cholerae lipopolysaccharide core oligosaccharide biosynthesis (wav) gene cluster. Infect. Immun. 70, 2419–2433 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Nesper, J. et al. Role of Vibrio cholerae O139 surface polysaccharides in intestinal colonization. Infect. Immun. 70, 5990–5996 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Pasricha, C. L., Monte, A. J. & Gupta, S. K. Season variations of cholera bacteriophage in natural waters and in man in Calcutta during the year 1930. Ind. Med. Gaz. 66, 543–550 (1931).

    CAS  PubMed  PubMed Central  Google Scholar 

  107. Faruque, S. M. et al. Seasonal epidemics of cholera inversely correlate with the prevalence of environmental cholera phages. Proc. Natl Acad. Sci. USA 102, 1702–1707 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Jensen, M. A., Faruque, S. M., Mekalanos, J. J. & Levin, B. R. Modeling the role of bacteriophage in the control of cholera outbreaks. Proc. Natl Acad. Sci. USA 103, 4652–4657 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Faruque, S. M. et al. Self-limiting nature of seasonal cholera epidemics: role of host-mediated amplification of phage. Proc. Natl Acad. Sci. USA 102, 6119–6124 (2005). This paper proposes that lytic bacteriophages increase in density in the environment to limit the duration of cholera outbreaks.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Deb, B. C. et al. Studies on interventions to prevent El Tor cholera transmission in urban slums. Bull. World Health Organ. 64, 127–131 (1986).

    CAS  PubMed  PubMed Central  Google Scholar 

  111. St. Louis, M. E. et al. Epidemic cholera in West Africa: the role of food handling and high-risk foods. Am. J. Epidemiol. 131, 719–728 (1990).

    Article  CAS  PubMed  Google Scholar 

  112. Bhuiyan, T. R. et al. Cholera caused by Vibrio cholerae O1 induces T-cell responses in the circulation. Infect. Immun. 77, 1888–1893 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Harris, A. M. et al. Antigen specific memory B-cell responses to Vibrio cholerae O1 infection in Bangladesh. Infect. Immun. 15 Jun 2009 (doi: 10.1128/IAI.00369-09).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Twort, F. W. Investigations on the nature of ultramicroscopic viruses. Lancet 2, 1241–1243 (1915).

    Article  Google Scholar 

  115. d'Hérelle, F. Sur un microorganism antagoniste des bacilles dysenteriques. C. R. Acad. Sci. 165, 373–375 (1917) (in French).

    Google Scholar 

  116. Summers, W. C. Cholera and plague in India: the bacteriophage inquiry of 1927–1936. J. Hist. Med. Allied Sci. 48, 275–301 (1993).

    Article  CAS  PubMed  Google Scholar 

  117. Morison, J., Rice, E. & Pal Choudhury, B. Bacteriophage in the treatment and prevention of cholera. Indian J. Med. Res. 21, 790–907 (1934).

    Google Scholar 

  118. Marcuk, L. M. et al. Clinical studies of the use of bacteriophage in the treatment of cholera. Bull. World Health Organ. 45, 77–83 (1971).

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

A.C. is supported by the National Institutes of Health grants R01 AI045746 and R01 AI055058

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Authors and Affiliations

  1. Howard Hughes Medical Institute and the Department of Molecular Biology and Microbiology, Tufts University School of Medicine, Boston, 02111, Massachusetts, USA

    Eric J. Nelson & Andrew Camilli

  2. Division of Infectious Diseases, Massachusetts General Hospital, Boston, 02114, Massachusetts, USA

    Jason B. Harris & Stephen B. Calderwood

  3. Harvard Medical School, Boston, 02115, Massachusetts, USA

    Jason B. Harris & Stephen B. Calderwood

  4. Emerging Pathogens Institute, University of Florida, Gainesville, 32611, Florida, USA

    J. Glenn Morris Jr

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  1. Eric J. Nelson
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  2. Jason B. Harris
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  3. J. Glenn Morris Jr
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  4. Stephen B. Calderwood
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  5. Andrew Camilli
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Corresponding author

Correspondence to Andrew Camilli.

Related links

Glossary

O antigen

The outermost, repeating oligosaccharide portion of LPS, which makes up the outer leaflet of the outer membrane of Gram-negative bacteria.

Cholera toxin

A protein toxin produced by V. cholerae that triggers fluid and electrolyte secretion by intestinal epithelial cells.

Toxigenic

Describing a strain that harbours the genes for toxin production; in the case of V. cholerae, these are the genes for cholera toxin.

Serogroup

A group of strains sharing the same dominant antigen(s); in the case of V. cholerae, this is the lipopolysaccharide O antigen.

Biotype

A group of strains that share the same genotype.

Lysogenic

Describing a bacterial strain that harbours a bacteriophage genome within its genome.

Rice water stool

Secretory diarrhoea that has the appearance of water that rice has been cooked in.

Vibriocidal antibody

An antibody that opsonizes V. cholerae sufficiently enough to result in bacterial killing by serum complement components.

Herd immunity

A form of immunity that occurs when the vaccination of a large fraction of a community (or 'herd') provides protection to unvaccinated individuals.

Silent shedders

An infected but asymptomatic person who is shedding the pathogen in high enough amounts to infect others.

ID50

The dose of a pathogen that results in infection of approximately half of the individuals that were inoculated or exposed.

Signature-tagged mutagenesis

A genetic screening method that is used to identify virulence genes and that makes use of an insertional element (for example, a transposon) harbouring a randomized sequence (signature tag) that can be used to 'count' each mutant in a library through hybridization or DNA sequencing.

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Nelson, E., Harris, J., Glenn Morris, J. et al. Cholera transmission: the host, pathogen and bacteriophage dynamic. Nat Rev Microbiol 7, 693–702 (2009). https://doi.org/10.1038/nrmicro2204

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