Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Primer
  • Published:

Vibrio spp. infections

An Author Correction to this article was published on 19 February 2021

Abstract

Vibrio is a genus of ubiquitous bacteria found in a wide variety of aquatic and marine habitats; of the >100 described Vibrio spp., ~12 cause infections in humans. Vibrio cholerae can cause cholera, a severe diarrhoeal disease that can be quickly fatal if untreated and is typically transmitted via contaminated water and person-to-person contact. Non-cholera Vibrio spp. (for example, Vibrio parahaemolyticus, Vibrio alginolyticus and Vibrio vulnificus) cause vibriosis — infections normally acquired through exposure to sea water or through consumption of raw or undercooked contaminated seafood. Non-cholera bacteria can lead to several clinical manifestations, most commonly mild, self-limiting gastroenteritis, with the exception of V. vulnificus, an opportunistic pathogen with a high mortality that causes wound infections that can rapidly lead to septicaemia. Treatment for Vibrio spp. infection largely depends on the causative pathogen: for example, rehydration therapy for V. cholerae infection and debridement of infected tissues for V. vulnificus-associated wound infections, with antibiotic therapy for severe cholera and systemic infections. Although cholera is preventable and effective oral cholera vaccines are available, outbreaks can be triggered by natural or man-made events that contaminate drinking water or compromise access to safe water and sanitation. The incidence of vibriosis is rising, perhaps owing in part to the spread of Vibrio spp. favoured by climate change and rising sea water temperature.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: A unifying theme of Vibrio spp.
Fig. 2: Vibrio cholerae and Vibrio parahaemolyticus pandemic spread.
Fig. 3: Foodborne infections reported in the United States.
Fig. 4: Pathogenesis of cholera in humans.
Fig. 5: Vibrio vulnificus wound infection.
Fig. 6: Effect of climate change on Vibrio spp. infections.

Similar content being viewed by others

References

  1. Baker-Austin, C., Trinanes, J., Gonzalez-Escalona, N. & Martinez-Urtaza, J. Non-Cholera vibrios: the microbial barometer of climate change. Trends Microbiol. 25, 76–84 (2017).

    CAS  PubMed  Google Scholar 

  2. Oliver, J. D. Wound infections caused by Vibrio vulnificus and other marine bacteria. Epidemiol. Infect. 133, 383–391 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Shah Faruque, M. & Epidemiology, G. B. N. in The Biology of Vibrios (Thompson, F. L. et al.) 394 (ASM Press, 2006).

  4. Altekruse, S. F. et al. Vibrio gastroenteritis in the US Gulf of Mexico region: the role of raw oysters. Epidemiol. Infect. 124, 489–495 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Howard-Jones, N. Robert Koch and the cholera vibrio: a centenary. Br. Med. J. Clin. Res. Ed 288, 379–381 (1984).

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Vezzulli, L., Colwell, R. R. & Pruzzo, C. Ocean warming and spread of pathogenic vibrios in the aquatic environment. Microb. Ecol. 65, 817–825 (2013).

    PubMed  Google Scholar 

  7. Newton, A., Kendall, M., Vugia, D. J., Henao, O. L. & Mahon, B. E. Increasing rates of vibriosis in the United States, 1996-2010: Review of surveillance data from 2 systems. Clin. Infect. Dis. 54, 391–395 (2012). This paper provides an epidemiological overview outlining the increasing risks associated with Vibrio spp. in the United States.

    Google Scholar 

  8. Scallan, E. et al. Foodborne illness acquired in the United States — Major pathogens. Emerg. Infect. Dis. 17, 7–15 (2011).

    PubMed  PubMed Central  Google Scholar 

  9. Iwamoto, M., Ayers, T., Mahon, B. E. & Swerdlow, D. L. Epidemiology of seafood-associated infections in the United States. Clin. Microbiol. Rev. 23, 399–411 (2010).

    PubMed  PubMed Central  Google Scholar 

  10. World Health Organization. Weekly epidemiological record. Weekly epidemiological record 21, 421–428 (2016).

    Google Scholar 

  11. Zuckerman, J. N., Rombo, L. & Fisch, A. The true burden and risk of cholera: implications for prevention and control. Lancet Infect. Dis. 7, 521–530 (2017).

    Google Scholar 

  12. World Health Organization. Cholera. WHO http://www.who.int/mediacentre/factsheets/fs107/en/ (2017).

  13. Ali, M. et al. Le fardeau mondial du choléra. Bull. World Health Organ. 90, 209–218 (2012).

    PubMed  PubMed Central  Google Scholar 

  14. Sack, D. A., Sack, R. B., Nair, G. B. & Siddique, A. K. Cholera. Lancet (Lond., Engl.) 363, 223–233 (2004).

    CAS  Google Scholar 

  15. Pollitzer, R., Swaroop, S., Burrows, W. & WHO. Cholera / R. Pollitzer; with a chapter on world incidence, written in collaboration with S. Swaroop, and a chapter on problems in immunology and an annex, written in collaboration with W. Burrows. (WHO, 1959).

  16. Barua, D. in Cholera 1–5 (eds Barua, D. & Greenough, W. B. 3rd) 1–36 (Plenum Medical Book, 1992).

  17. Poirier, M. J., Izurieta, R., Malavade, S. S. & McDonald, M. D. Re-emergence of Cholera in the Americas: risks, susceptibility, and ecology. J. Glob. Infect. Dis. 4, 162–171 (2012).

    PubMed  PubMed Central  Google Scholar 

  18. Orata, F. D., Keim, P. S. & Boucher, Y. The 2010 Cholera outbreak in Haiti: how science solved a controversy. PLOS Pathog. 10, e1003967 (2014).

    PubMed  PubMed Central  Google Scholar 

  19. Weill, F.-X. et al. Genomic history of the seventh pandemic of cholera in Africa. Science 358, 785–789 (2017).

    CAS  PubMed  Google Scholar 

  20. Domman, D. et al. Integrated view of Vibrio cholerae in the Americas. Science 358, 789–793 (2017).

    CAS  PubMed  Google Scholar 

  21. Colwell, R. R. Global climate and infectious disease: the cholera paradigm. Science 274, 2025–2031 (1996). This article provides a comprehensive overview on the effect of climate on cholera epidemics.

    CAS  PubMed  Google Scholar 

  22. 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).

    PubMed  PubMed Central  Google Scholar 

  23. 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).

    PubMed  Google Scholar 

  24. Lobitz, B. et al. Climate and infectious disease: use of remote sensing for detection of Vibrio cholerae by indirect measurement. Proc. Natl Acad. Sci. USA 97, 1438–1443 (2000).

    CAS  PubMed  Google Scholar 

  25. Pascual, M., Rodo, X., Ellner, S. P., Colwell, R. & Bouma, M. J. Cholera dynamics and El Nino-Southern Oscillation. Science 289, 1766–1769 (2000).

    CAS  PubMed  Google Scholar 

  26. Huq, A. et al. Critical factors influencing the occurrence of Vibrio cholerae in the environment of Bangladesh. Appl. Environ. Microbiol. 71, 4645–4654 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Huq, A. et al. Environmental factors influencing epidemic Cholera. Am. J. Trop. Med. Hyg. 89, 597–607 (2013).

    PubMed  PubMed Central  Google Scholar 

  28. Worden, A. Z. et al. Trophic regulation of Vibrio cholerae in coastal marine waters. Environ. Microbiol. 8, 21–29 (2006).

    CAS  PubMed  Google Scholar 

  29. Hashizume, M. et al. The effect of rainfall on the incidence of cholera in Bangladesh. Epidemiology 19, 103–110 (2008).

    PubMed  Google Scholar 

  30. Koelle, K. The impact of climate on the disease dynamics of cholera. Clin. Microbiol. Infect. 15, 29–31 (2009).

    PubMed  Google Scholar 

  31. Ramamurthy, T. & Sharma, N. C. Cholera outbreaks in India. Curr. Top. Microbiol. Immunol. 379, 49–85 (2014).

    PubMed  Google Scholar 

  32. Ries, A. A. et al. Cholera in Piura, Peru: a modern urban epidemic. J. Infect. Dis. 166, 1429–1433 (1992).

    CAS  PubMed  Google Scholar 

  33. Goh, K. T., Teo, S. H., Lam, S. & Ling, M. K. Person-to-person transmission of cholera in a psychiatric hospital. J. Infect. 20, 193–200 (2017).

    Google Scholar 

  34. Sugimoto, J. D. et al. Household transmission of Vibrio cholerae in Bangladesh. PLoS Negl. Trop. Dis. 8, e3314 (2014).

    PubMed  PubMed Central  Google Scholar 

  35. Rabbani, G. H. & Greenough, W. B. 3rd. Food as a vehicle of transmission of cholera. J. Diarrhoeal Dis. Res. 17, 1–9 (1999).

    CAS  PubMed  Google Scholar 

  36. Alam, M. et al. Seasonal cholera caused by Vibrio cholerae serogroups O1 and O139 in the coastal aquatic environment of Bangladesh. Appl. Environ. Microbiol. 72, 4096–4104 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. 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 diarrhea in Bangladesh. J. Clin. Microbiol. 40, 3296–3299 (2002).

    PubMed  PubMed Central  Google Scholar 

  38. Reina, J. The 8th cholera pandemic: Vibrio cholerae serogroup 0139 (Bengala strain). Enferm. Infecc. Microbiol. Clin. 13, 246–251 (1995).

    CAS  PubMed  Google Scholar 

  39. Chowdhury, F. et al. Vibrio cholerae serogroup O139: isolation from Cholera patients and asymptomatic household family members in Bangladesh between 2013 and 2014. PLoS Negl. Trop. Dis. 9, e0004183 (2015).

    PubMed  PubMed Central  Google Scholar 

  40. Deshayes, S. et al. Non-O1, non-O139 Vibrio cholerae bacteraemia: case report and literature review. Springerplus 4, 1–9 (2015).

    Google Scholar 

  41. Baker-Austin, C. et al. Heat wave-associated vibriosis, Sweden and Finland, 2014. Emerg. Infect. Dis. 22 (2016).

  42. Baker-Austin, C., Stockley, L., Rangdale, R. & Martinez-Urtaza, J. Environmental occurrence and clinical impact of Vibrio vulnificus and Vibrio parahaemolyticus: A European perspective. Environ. Microbiol. Rep. 2, 7–18 (2010).

    PubMed  Google Scholar 

  43. Barker, W. H. J. in International Symposium on Vibrio parahaemolyticus (eds Fujino, T., Sakaguchi, G., Sakazaki, R. & Takeda, Y.) 47–52 (Saikon Publishing Co., Ltd., 1974).

  44. Dadisman, T. A. J., Nelson, R., Molenda, J. R. & Garber, H. J. Vibrio parahaemolyticus gastroenteritis in Maryland. I. Clinical and epidemiologic aspects. Am. J. Epidemiol. 96, 414–426 (1972).

    PubMed  Google Scholar 

  45. Fishbein, M., Wentz, B. & Landry, W. L. in International Symposium on Vibrio parahaemolyticus (eds Fujino, T., Sakaguchi, G., Sakazaki, R. & Takeda, Y.) 53–58 (Saikon Publishing Co., Ltd., 1974).

  46. Joseph, S. W., Colwell, R. R. & Kaper, J. B. Vibrio parahaemolyticus and related halophilic Vibrios. Crit. Rev. Microbiol. 10, 77–124 (1982).

    CAS  PubMed  Google Scholar 

  47. Nair, G. B. et al. Global dissemination of Vibrio parahaemolyticus serotype O3:K6 and its serovariants. Clin. Microbiol. Rev. 20, 39–48 (2007). This paper presents a succinct and historical overview of the pandemic spread of V. parahaemolyticus.

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Okuda, J. et al. Emergence of a unique O3:K6 clone of Vibrio parahaemolyticus in Calcutta, India, and isolation of strains from the same clonal group from Southeast Asian travelers arriving in Japan. J. Clin. Microbiol. 35, 3150–3155 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Martinez-Urtaza, J., Bowers, J. C., Trinanes, J. & DePaola, A. Climate anomalies and the increasing risk of Vibrio parahaemolyticus and Vibrio vulnificus illnesses. Food Res. Int. 43, 1780–1790 (2010).

    Google Scholar 

  50. Li, Y. et al. Vibrio parahaemolyticus, Southern Coastal region of China 2007–2012. Emerg. Infect. Dis. 20, 2012–2015 (2014).

    Google Scholar 

  51. Martinez-Urtaza, J. et al. Spread of Pacific Northwest Vibrio parahaemolyticus strain. N. Engl. J. Med. 369, 1573–1574 (2013). This study is the first to show the pandemic spread of ST36 clonal type V. parahaemolyticus.

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Martinez-Urtaza, J. et al. Epidemiological investigation of a foodborne outbreak in Spain associated with U. S. West Coast genotypes of Vibrio parahaemolyticus. SpringerPlus 5, 87 (2016).

    PubMed  PubMed Central  Google Scholar 

  53. Wagley, S. et al. Galleria mellonella as an infection model to investigate virulence of Vibrio parahaemolyticus. Virulence 9, 197–207 (2017).

    PubMed  PubMed Central  Google Scholar 

  54. Food and Agriculture Organization of the United Nations. Risk Assessment of Vibrio parahaemolyticus in Seafood. FAO (2011).

  55. Jones, M. K. & Oliver, J. D. Vibrio vulnificus: Disease and pathogenesis. Infect. Immun. 77, 1723–1733 (2009). This article presents one of the most cited reviews on the virulence of V. vulnificus.

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Centers for Disease Control. Vibrio vulnificus infections associated with raw oyster consumption. Morb. Mortal. Wkly. Rep. 42, 405–407 (1993).

    Google Scholar 

  57. Scaglione, S. et al. The epidemiology of cirrhosis in the United States: a population-based study. J. Clin. Gastroenterol. 49, 690–696 (2015).

    PubMed  Google Scholar 

  58. Rippey, S. R. Infectious diseases associated with molluscan shellfish consumption. Clin. Microbiol. Rev. 7, 419–425 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Fouz, B., Roig, F. J. & Amaro, C. Phenotypic and genotypic characterization of a new fish-virulent Vibrio vulnificus serovar that lacks potential to infect humans. Microbiology 153, 1926–1934 (2007).

    CAS  PubMed  Google Scholar 

  60. Bisharat, N. et al. Clinical, epidemiological, and microbiological features of Vibrio vulnificus biogroup 3 causing outbreaks of wound infection and bacteraemia in Israel. Israel Vibrio Study Group. Lancet 354, 1421–1424 (1999). This paper provides the first description of V. vulnificus biotype 3.

    CAS  PubMed  Google Scholar 

  61. Hori, M. et al. A case of Vibrio vulnificus infection complicated with fulminant purpura: gene and biotype analysis of the pathogen. JMM Case Reports 4, e005096 (2017).

    PubMed  PubMed Central  Google Scholar 

  62. Baker-Austin, C. et al. Emerging Vibrio risk at high latitudes in response to ocean warming. Nat. Clim. Chang. 3, 73–77 (2012). This article presents the first study to show the spread of pathogenic Vibrio spp. into temperate regions and the role of climate on mediating risk.

    Google Scholar 

  63. Zhao, H. et al. Correlations between clinical features and mortality in patients with Vibrio vulnificus infection. PLoS One 10, e0136019 (2015).

    PubMed  PubMed Central  Google Scholar 

  64. Chuang, Y. C., Yuan, C. Y., Liu, C. Y., Lan, C. K. & Huang, A. H. Vibrio vulnificus infection in Taiwan: report of 28 cases and review of clinical manifestations and treatment. Clin. Infect. Dis. 15, 271–276 (1992).

    CAS  PubMed  Google Scholar 

  65. Raszl, S. M., Froelich, B. A., Vieira, C. R. W., Blackwood, A. D. & Noble, R. T. Vibrio parahaemolyticus and Vibrio vulnificus in South America: water, seafood and human infections. J. Appl. Microbiol. 121, 1201–1222 (2016).

    CAS  PubMed  Google Scholar 

  66. Osaka, K., Komatsuzaki, M., Takahashi, H., Sakano, S. & Okabe, N. Vibrio vulnificus septicaemia in Japan: an estimated number of infections and physicians’ knowledge of the syndrome. Epidemiol. Infect. 132, 993–996 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Park, S. D., Shon, H. S. & Joh, N. J. Vibrio vulnificus septicemia in Korea: clinical and epidemiologic findings in seventy patients. J. Am. Acad. Dermatol. 24, 397–403 (1991).

    CAS  PubMed  Google Scholar 

  68. Weis, K. E., Hammond, R. M., Hutchinson, R. & Blackmore, C. G. M. Vibrio illness in Florida, 1998–2007. Epidemiol. Infect. 139, 591–598 (2011).

    CAS  PubMed  Google Scholar 

  69. World Health Organization & Food and Agriculture Organization of the United Nations. Microbiological Risk Assessment Series (WHO & FAO, 2004).

  70. Gangarosa, E. F., Beisel, W. R., Benyajati, C., Sprinz, H. & Piyaratn, P. The nature of the gastrointestinal lesion in asiatic cholera and its relation to pathogenesis: a biopsy study. Am. J. Trop. Med. Hyg. 9, 125–135 (1960).

    CAS  PubMed  Google Scholar 

  71. D. E., S. N. Enterotoxicity of bacteria-free culture-filtrate of Vibrio cholerae. Nature 183, 1533–1534 (1959).

    CAS  Google Scholar 

  72. Levine, M. M., Kaper, J. B., Black, R. E. & Clements, M. L. New knowledge on pathogenesis of bacterial enteric infections as applied to vaccine development. Microbiol. Rev. 47, 510–550 (1983).

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Ritchie, J. M. & Waldor, M. K. Vibrio cholerae interactions with the gastrointestinal tract: lessons from animal studies. Curr. Top. Microbiol. Immunol. 337, 37–59 (2009).

    CAS  PubMed  Google Scholar 

  74. Nelson, J., Eric & Harris, Jason & Glenn Morris, J. & Calderwood, B. Stephen & Camilli, A. Cholera transmission: The host, pathogen and bacteriophage dynamic. Nat. Rev. Microbiol. 7, 693–702 (2009).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  76. 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).

    CAS  PubMed  Google Scholar 

  77. Bartlett, T. M. et al. A periplasmic polymer curves Vibrio cholerae and promotes pathogenesis. Cell 168, 172–185.e15 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Chao, M. C., Abel, S., Davis, B. M. & Waldor, M. K. The design and analysis of transposon insertion sequencing experiments. Nat. Rev. Microbiol. 14, 119–128 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Weber, G. G. & Klose, K. E., K. The complexity of ToxT-dependent transcription in Vibrio cholerae. Indian J. Med. Res. 133, 201–206 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Rutherford, S. T. & Bassler, B. L. Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb. Perspect. Med. 2, 1–25 (2012).

    Google Scholar 

  81. Chao, M. C. et al. A cytosine methyltransferase modulates the cell envelope stress response in the Cholera pathogen. PLoS Genet. 11, e1005666 (2015).

    PubMed  PubMed Central  Google Scholar 

  82. Millet, Y. A. et al. Insights into Vibrio cholerae intestinal colonization from monitoring fluorescently labeled bacteria. PLoS Pathog. 10, e1004405 (2014).

    PubMed  PubMed Central  Google Scholar 

  83. Davis, B. M., Moyer, K. E., Boyd, E. F. & Waldor, M. K. CTX prophages in classical biotype Vibrio cholerae: functional phage genes but dysfunctional phage genomes. J. Bacteriol. 182, 6992–6998 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Faruque, S. M. et al. Emergence and evolution of Vibrio cholerae O139. Proc. Natl Acad. Sci. USA 100, 1304–1309 (2003).

    CAS  PubMed  Google Scholar 

  85. Nishibuchi, M. & Kaper, J. B. Thermostable direct hemolysin gene of Vibrio parahaemolyticus: a virulence gene acquired by a marine bacterium. Infect. Immun. 63, 2093–2099 (1995). This study analyses tdh , which is used as a genetic marker for virulence in the diagnosis of pathogenic V. parahaemolyticus.

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Letchumanan, V., Chan, K. G. & Lee, L. H. Vibrio parahaemolyticus: A review on the pathogenesis, prevalence, and advance molecular identification techniques. Front. Microbiol. 5, 1–13 (2014).

    Google Scholar 

  87. Honda, T., Ni, Y. & Miwatani, T. Purification and characterization of a hemolysin produced by a clinical isolate of kanagawa phenomenon-negative Vibrio parahaemolyticus and related to the thermostable direct hemolysin. 56, 961–965 (1988).

  88. Ottaviani, D. et al. Nontoxigenic Vibrio parahaemolyticus strains causing acute gastroenteritis. J. Clin. Microbiol. 50, 4141–4143 (2012).

    PubMed  PubMed Central  Google Scholar 

  89. Park, K.-S. et al. Functional characterization of two type III secretion systems of Vibrio parahaemolyticus. Infect. Immun. 72, 6659–6665 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  90. Makino, K. et al. Genome sequence of Vibrio parahaemolyticus: a pathogenic mechanism distinct from that of V. cholerae. Lancet 361, 743–749 (2003). This first report of the whole genome of V. parahaemolyticus has been used as a reference in any further studies with the identification of the major pathogenic islands associated with virulence.

    CAS  PubMed  Google Scholar 

  91. Ritchie, J. M. et al. Inflammation and disintegration of intestinal villi in an experimental model for Vibrio parahaemolyticus-induced diarrhea. PLoS Pathog. 8, e1002593 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Portaliou, A. G., Tsolis, K. C., Loos, M. S., Zorzini, V. & Economou, A. Type III Secretion: Building and Operating a Remarkable Nanomachine. Trends Biochem. Sci. 41, 175–189 (2016).

    CAS  PubMed  Google Scholar 

  93. Hubbard, T. P. et al. Genetic analysis of Vibrio parahaemolyticus intestinal colonization. Proc. Natl Acad. Sci. USA 113, 6283–6288 (2016).

    CAS  PubMed  Google Scholar 

  94. Wang, R. et al. The pathogenesis, detection, and prevention of Vibrio parahaemolyticus. Front. Microbiol. 6, 144 (2015).

    PubMed  PubMed Central  Google Scholar 

  95. US Food and Drug Administration. Quantitative Risk Assessment on the Public Health Impact of Pathogenic Vibrio parahaemolyticus in Raw Oysters. FDA (2005).

  96. Simpson, L. M. & Oliver, J. D. Ability of Vibrio vulnificus to obtain iron from transferrin and other iron-binding proteins. Curr. Microbiol. 15, 155–157 (1987).

    CAS  Google Scholar 

  97. Arezes, J. et al. Hepcidin-induced hypoferremia is a critical host defense mechanism against the siderophilic bacterium Vibrio vulnificus. Cell Host Microbe 17, 47–57 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  98. Payne, S. M., Mey, A. R. & Wyckoff, E. E. Vibrio iron transport: evolutionary adaptation to life in multiple environments. Microbiol. Mol. Biol. Rev. 80, 69–90 (2016).

    CAS  PubMed  Google Scholar 

  99. Pajuelo, D. et al. Iron and Fur in the life cycle of the zoonotic pathogen Vibrio vulnificus. Environ. Microbiol. 18, 4005–4022 (2016).

    CAS  PubMed  Google Scholar 

  100. Bahrani, K. J. D. O. Studies on the lipopolysaccharide of a virulent and an avirulent strain of Vibrio vulnificus. Biochem. Cell Biol. 68, 547–551 (1990).

    CAS  PubMed  Google Scholar 

  101. Merkel, S. M., Alexander, S., Zufall, E., Oliver, J. D. & Huet-Hudson, Y. M. Essential role for estrogen in protection against Vibrio vulnificus-induced endotoxic shock. Infect. Immun. 69, 6119–6122 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  102. Roig, F. J., González-Candelas, F. & Amaro, C. Domain organization and evolution of multifunctional autoprocessing repeats-in-toxin (MARTX) toxin in vibrio vulnificus. Appl. Environ. Microbiol. 77, 657–668 (2011).

    CAS  PubMed  Google Scholar 

  103. Gavin, H. E., Beubier, N. T. & Satchell, K. J. F. The effector domain region of the Vibrio vulnificus MARTX toxin confers biphasic epithelial barrier disruption and is essential for systemic spread from the intestine. PLoS Pathog. 13, e1006119 (2017).

    PubMed  PubMed Central  Google Scholar 

  104. Jang, K. K. et al. Identification and characterization of Vibrio vulnificus plpA encoding a phospholipase A2 essential for pathogenesis. J. Biol. Chem. 292, 17129–17143 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  105. Duong-Nu, T.-M. et al. All three TonB systems are required for Vibrio vulnificus CMCP6 tissue invasiveness by controlling flagellum expression. Infect. Immun. 84, 254–265 (2015).

    PubMed  PubMed Central  Google Scholar 

  106. Lee, S.-J. et al. VvpE mediates the intestinal colonization of Vibrio vulnificus by the disruption of tight junctions. Int. J. Med. Microbiol. 306, 10–19 (2016).

    CAS  PubMed  Google Scholar 

  107. Jang, K. K., Gil, S. Y., Lim, J. G. & Choi, S. H. Regulatory characteristics of Vibrio vulnificus gbpA gene encoding a mucin-binding protein essential for pathogenesis. J. Biol. Chem. 291, 5774–5787 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  108. Gauthier, J. D. et al. Role of GacA in virulence of Vibrio vulnificus. Microbiology 156, 3722–3733 (2010).

    CAS  PubMed  Google Scholar 

  109. Rosche, T. M., Yano, Y. & Oliver, J. D. A rapid and simple PCR analysis indicates there are two subgroups of Vibrio vulnificus which correlate with clinical or environmental isolation. Microbiol. Immunol. 49, 381–389 (2005). This article describes a PCR method to rapidly differentiate the two genotypes of V. vulnificus and their correlation to isolation source.

    CAS  PubMed  Google Scholar 

  110. Morrison, S. S. et al. Pyrosequencing-based comparative genome analysis of Vibrio vulnificus environmental isolates. PLoS One 7, e37553 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  111. Gulig, P. A. et al. SOLiD sequencing of four Vibrio vulnificus genomes enables comparative genomic analysis and identification of candidate clade-specific virulence genes. BMC Genomics 11, 512 (2010).

    PubMed  PubMed Central  Google Scholar 

  112. Waldor, M. K. & Mekalanos, J. J. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272, 1910–1914 (1996). This paper presents the first description of the structural genes for CT encoded by a filamentous bacteriophage.

    CAS  PubMed  Google Scholar 

  113. Faruque, S. M. & Mekalanos, J. J. Pathogenicity islands and phages in Vibrio cholerae evolution. Trends Microbiol. 11, 505–510 (2003).

    CAS  PubMed  Google Scholar 

  114. Meibom, K. L., Blokesch, M., Dolganov, N. A., Wu, C.-Y. & Schoolnik, G. K. Chitin induces natural competence in Vibrio cholerae. Science 310, 1824–1827 (2005). This study shows the crucial role of chitin in the acquisition of new genetic material via natural transformation; the role of chitin is crucial to understand the role of zooplankton in the evolution and life cycle of Vibrio spp.

    CAS  PubMed  Google Scholar 

  115. Neiman, J., Guo, Y. & Rowe-Magnus, D. A. Chitin-induced carbotype conversion in Vibrio vulnificus. Infect. Immun. 79, 3195–3203 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  116. Boyd, E. F. et al. Molecular analysis of the emergence of pandemic Vibrio parahaemolyticus. BMC Microbiol. 8, 110 (2008).

    PubMed  PubMed Central  Google Scholar 

  117. Liu, M. & Chen, S. A novel adhesive factor contributing to the virulence of Vibrio parahaemolyticus. Sci. Rep. 5, 14449 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  118. World Health Organization. 10 facts on cholera. World Health Organization http://www.who.int/features/factfiles/cholera/en/ (2016).

  119. 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).

    PubMed  PubMed Central  Google Scholar 

  120. Qadri, F., Svennerholm, A.-M., Faruque, A. S. G. & Sack, R. B. Enterotoxigenic Escherichia coli in Developing Countries: Epidemiology, Microbiology, Clinical Features, Treatment, and Prevention. Clin. Microbiol. Rev. 18, 465–483 (2005).

    PubMed  PubMed Central  Google Scholar 

  121. Andrew Azman, S., Kara Rudolph, E. & Derek Cummings, A. T. J. L. The incubation period of cholera: A systematic review. J. Infect. 66, 432–438 (2013).

    PubMed  Google Scholar 

  122. World Health Organization. Prevention and control of cholera outbreaks: WHO policy and recommendations. WHO http://www.who.int/cholera/prevention_control/recommendations/en/index5.html (2017).

  123. World Health Organization. The Use of Cholera Rapid Diagnostic Tests — Interim Report. WHO (2016).

  124. Mukherjee, P. et al. Evaluation of a rapid immunochromatographic dipstick kit for diagnosis of cholera emphasizes its outbreak utility. Jpn J. Infect. Dis. 63, 234–238 (2010).

    PubMed  Google Scholar 

  125. Wang, X.-Y. et al. Field evaluation of a rapid immunochromatographic dipstick test for the diagnosis of cholera in a high-risk population. BMC Infect. Dis. 6, 17 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  126. Dick, M. H., Guillerm, M., Moussy, F. & Chaignat, C. L. Review of two decades of Cholera diagnostics — how far have we really come? PLoS Negl. Trop. Dis. 6, e1845 (2012).

    PubMed  PubMed Central  Google Scholar 

  127. Centers for Disease Control. Vibrio species causing Vibriosis CDC (2017).

  128. Høi, L., Dalsgaard, I. & Dalsgaard, A. Improved isolation of Vibrio vulnificus from seawater and sediment with cellobiose-colistin agar. 64, 1721–1724 (1998).

  129. Hill, W. E. et al. Polymerase chain reaction identification of Vibrio vulnificus in artificially contaminated oysters. Appl. Environ. Microbiol. 57, 707–711 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  130. Bej, A. K. et al. Detection of total and hemolysin producing Vibrio parahaemolyticus in shellfish using multiplex PCR amplification of tl, tdh, and trh. J. Microbiol. Methods 36, 215–225 (1999).

    CAS  PubMed  Google Scholar 

  131. Chun, J., Huq, A. & Colwell, R. R. Analysis of 16S-23S rRNA intergenic spacer regions of Vibrio cholerae and Vibrio mimicus. Appl. Environ. Microbiol. 65, 2202–2208 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  132. Nordstrom, J. L., Vickery, M. C. L., Blackstone, G. M., Murray, S. L. & DePaola, A. Development of a multiplex real-time PCR assay with an internal amplification control for the detection of total and pathogenic Vibrio parahaemolyticus bacteria in oysters. Appl. Environ. Microbiol. 73, 5840–5847 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  133. Taiwo, M. et al. Comparison of toxR and tlh based PCR assays for Vibrio parahaemolyticus. Food Control 77, 116–120 (2017).

    CAS  Google Scholar 

  134. Campbell, M. S. & Wright, A. C. Real-time PCR analysis of Vibrio vulnificus from oysters. Appl. Environ. Microbiol. 69, 7137–7144 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  135. Lyon, W. J. TaqMan, P. C. R. for detection of Vibrio cholerae O1, O139, non-O1, and non-O139 in pure cultures, raw oysters, and synthetic seawater. Appl. Environ. Microbiol. 67, 4685–4693 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  136. Shirail, H. et al. Polymerase chain reaction for detection of the Cholera enterotoxin operon of Vibrio cholerae. J. Clin. Microbiol. 29, 2517–2521 (1991).

    Google Scholar 

  137. Roig, F. J., Sanjuan, E., Llorens, A. & Amaro, C. pilF Polymorphism-based PCR to distinguish Vibrio vulnificus strains potentially dangerous to public health. Appl. Environ. Microbiol. 76, 1328–1333 (2010).

    CAS  PubMed  Google Scholar 

  138. Han, F. & Ge, B. Multiplex PCR assays for simultaneous detection and characterization of Vibrio vulnificus strains. Lett. Appl. Microbiol. 51, 234–240 (2010).

    CAS  PubMed  Google Scholar 

  139. Myers, M. L., Panicker, G. & Bej, A. K. PCR detection of a newly emerged pandemic Vibrio parahaemolyticus O3: K6 pathogen in pure cultures and seeded waters from the Gulf of Mexico. Appl. Environ. Microbiol. 69, 2194–2200 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  140. Whistler, C. A. et al. Use of whole-genome phylogeny and comparisons for development of a multiplex PCR assay to identify sequence type 36 Vibrio parahaemolyticus. J. Clin. Microbiol. 53, 1864–1872 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  141. Martinez-Urtaza, J., Lozano-Leon, A., Viña-Feas, A., de Novoa, J. & Garcia-Martin, O. Differences in the API 20E biochemical patterns of clinical and environmental Vibrio parahaemolyticus isolates. FEMS Microbiol. Lett. 255, 75–81 (2006).

    CAS  PubMed  Google Scholar 

  142. Croci, L. et al. Comparison of different biochemical and molecular methods for the identification of Vibrio parahaemolyticus. J. Appl. Microbiol. 102, 229–237 (2007).

    CAS  PubMed  Google Scholar 

  143. George, C. M. et al. Randomized controlled trial of hospital-based hygiene and water treatment intervention (CHoBI7) to reduce Cholera. Emerg. Infect. Dis. 22, 233–241 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  144. Sinclair, D., Abba, K., Zaman, K., Qadri, F. & Graves, P. M. Oral vaccines for preventing cholera. Cochrane Database Syst. Rev. 3, CD008603 (2011).

    Google Scholar 

  145. US Food and Drug Administration. VAXCHORA. FDA https://www.fda.gov/BiologicsBloodVaccines/Vaccines/ApprovedProducts/ucm505866.htm (2018).

  146. Hsiao, A., Desai, S. N., Mogasale, V., Excler, J.-L. & Digilio, L. Lessons learnt from 12 oral cholera vaccine campaigns in resource-poor settings. Bull. World Health Organ. 95, 303–312 (2017).

    PubMed  PubMed Central  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  148. Anh, D. et al. Safety and immunogenicity of a reformulated Vietnamese bivalent killed, whole-cell, oral cholera vaccine in adults. Vaccines 25, 1149–1155 (2007).

    CAS  Google Scholar 

  149. Frew, S. E., Liu, V. Y. & Singer, P. A. A business plan to help the ‘global South’ in its fight against neglected diseases. Health Aff. (Millwood). 28, 1760–1773 (2009).

    PubMed  Google Scholar 

  150. Levine, M. M. et al. PaxVax CVD 103-HgR single-dose live oral cholera vaccine. Expert Rev. Vaccines 16, 197–213 (2017).

    CAS  PubMed  Google Scholar 

  151. Karlsson, S. L. et al. Development of stable Vibrio cholerae O1 Hikojima type vaccine strains co–expressing the Inaba and Ogawa lipopolysaccharide antigens. PLoS One 9, e108521 (2014).

    PubMed  PubMed Central  Google Scholar 

  152. World Health Organization. Immunisation standards: inactivated oral single dose vial. WHO http://www.who.int/immunization_standards/vaccine_quality/pq_298_euvichol_1dose_eubiologics/en/ (2017).

  153. World Health Organization. Weekly epidemiological record. Weekly epidemiological record 92, 437–452 (2017).

  154. World Health Organization. Weekly epidemiological record. Weekly epidemiological record 92, 301–320 (2017).

    Google Scholar 

  155. Khan, A. I. et al. Safety of the oral cholera vaccine in pregnancy: Retrospective findings from a subgroup following mass vaccination campaign in Dhaka. Bangladesh. Vaccine 35, 1538–1543 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  156. Bhattacharya, S. K. et al. 5 year efficacy of a bivalent killed whole-cell oral cholera vaccine in Kolkata, India: a cluster-randomised, double-blind, placebo-controlled trial. Lancet Infect. Dis. 13, 1050–1056 (2013).

    CAS  PubMed  Google Scholar 

  157. Qadri, F. et al. Efficacy of a single-dose, inactivated oral Cholera vaccine in Bangladesh. N. Engl. J. Med. 374, 1723–1732 (2016).

    CAS  PubMed  Google Scholar 

  158. Vugia, D. J., Tabnak, F., Newton, A. E., Hernandez, M. & Griffin, P. M. Impact of 2003 State Regulation on Raw Oyster – associated Vibrio vulnificus Illnesses and Deaths, California, USA. Emerg. Infect. Dis. 19, 1276–1280 (2013).

    PubMed  PubMed Central  Google Scholar 

  159. Potasman, I., Paz, A. & Odeh, M. Infectious outbreaks associated with bivalve shellfish consumption: a worldwide perspective. Clin. Infect. Dis. 35, 921–928 (2002).

    PubMed  Google Scholar 

  160. European Centre for Disease Prevention and Control. Vibrio Risk Portal. E3 Geoportal https://e3geoportal.ecdc.europa.eu/SitePages/Vibrio%20Map%20Viewer.aspx (2018).

  161. Lee, T. H., Cha, S. S., Lee, C. S., Rhee, J. H. & Chung, K. M. Monoclonal antibodies against Vibrio vulnificus RtxA1 elicit protective immunity through distinct mechanisms. Infect. Immun. 82, 4813–4823 (2014).

    PubMed  PubMed Central  Google Scholar 

  162. Harris, J. B., LaRocque, R. C., Qadri, F., Ryan, E. T. & Calderwood, S. B. Cholera. Lancet 379, 2466–2476 (2012).

    PubMed  PubMed Central  Google Scholar 

  163. World Health Organization. Treatment Diarrhoea: Manual — A manual for Physicians Other Senior Health Workers. WHO (1990).

  164. Alam, N. H. & Ashraf, H. Treatment of infectious diarrhea in children. Paediatr. Drugs 5, 151–165 (2003).

    PubMed  Google Scholar 

  165. Ahmed, T. et al. Mortality in severely malnourished children with diarrhoea and use of a standardised management protocol. Lancet 353, 1919–1922 (1999).

    CAS  PubMed  Google Scholar 

  166. Lindenbaum, J., Greenough, W. B. & Islam, M. R. Antibiotic therapy of Cholera in children. Bull. World Health Organ. 37, 529–538 (1967).

    CAS  PubMed  PubMed Central  Google Scholar 

  167. Bardhan, P. K. in Conn’s current therapy (eds Rakel, R. E. & Bope, E. T.) 18–24 (Saunders, 2005).

  168. Munita, J. M. & Arias, C. A. Mechanisms of Antibiotic Resistance. Microbiol. Spectr. 4 (2016).

  169. Kaushik, J. S., Gupta, P., Faridi, M. M. & Das, S. Single dose azithromycin versus ciprofloxacin for cholera in children: a randomized controlled trial. Indian Pediatr. 47, 309–315 (2010).

    PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  171. World Health Organization WHO/Unicef joint statement: Clin. Management Acute Diarrhoea. WHO (2004).

  172. Larson, C. P., Roy, S. K., Khan, A. I., Rahman, A. S. & Qadri, F. Zinc treatment to under-five children: applications to improve child survival and reduce burden of disease. J. Health. Popul. Nutr. 26, 356–365 (2008).

    PubMed  PubMed Central  Google Scholar 

  173. World Health Organization. Pocket book of hospital care for children. WHO (2013).

  174. Ivers, L. C. Eliminating Cholera transmission in Haiti. N. Engl. J. Med. 376, 101–103 (2017).

    PubMed  Google Scholar 

  175. World Health Organization. Situation Report — Cholera, Yemen. WHO (2017).

  176. Yen, M., Cairns, L. S. & Camilli, A. A cocktail of three virulent bacteriophages prevents Vibrio cholerae infection in animal models. Nat. Commun. 8, 1–7 (2017).

    Google Scholar 

  177. Reilly, G. D. D., Reilly, C. A. A., Smith, E. G. G. & Baker-Austin, C. Vibrio alginolyticus-associated wound infection acquired in British waters, Guernsey, July 2011. Eurosurveillance 16, 3 (2011).

    Google Scholar 

  178. Klontz, K. C. et al. Syndromes of Vibrio vulnificus infections. Clinical and epidemiologic features in Florida cases, 1981–1987. Ann. Intern. Med. 109, 318–323 (1988).

    CAS  PubMed  Google Scholar 

  179. Shaw, K. S. et al. Antimicrobial susceptibility of Vibrio vulnificus and Vibrio parahaemolyticus recovered from recreational and commercial areas of Chesapeake Bay and Maryland coastal bays. PLoS One 9, e89616 (2014).

    PubMed  PubMed Central  Google Scholar 

  180. Daniels, N. A. et al. Vibrio parahaemolyticus infections in the United States, 1973–1998. J. Infect. Dis. 181, 1661–1666 (2000).

    CAS  PubMed  Google Scholar 

  181. Wong, K. C., Brown, A. M., Luscombe, G. M., Wong, S. J. & Mendis, K. Antibiotic use for Vibrio infections: important insights from surveillance data. BMC Infect. Dis. 15, 226 (2015).

    PubMed  PubMed Central  Google Scholar 

  182. Baker-Austin, C. et al. Antibiotic resistance in the shellfish pathogen Vibrio parahaemolyticus isolated from the coastal water and sediment of Georgia and SC. USA. J. Food Prot. 71, 2552–2558 (2008).

    CAS  PubMed  Google Scholar 

  183. Baker-Austin, C. et al. Multi-site analysis reveals widespread antibiotic resistance in the marine pathogen Vibrio vulnificus. Microb. Ecol. 57, 151–159 (2009).

    CAS  PubMed  Google Scholar 

  184. Monira, S. et al. Metagenomic profile of gut microbiota in children during cholera and recovery. Gut Pathog. 5, 1 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  185. Monira, S. et al. Multi-drug resistant pathogenic bacteria in the gut of young children in Bangladesh. Gut Pathog. 9, 19 (2017).

    PubMed  PubMed Central  Google Scholar 

  186. Subramanian, S. et al. HHS Publ. Access. 510, 417–421 (2014).

    CAS  Google Scholar 

  187. Schaetti, C. et al. Costs of illness due to Cholera, costs of immunization and cost-effectiveness of an oral Cholera mass vaccination campaign in Zanzibar. PLoS Negl. Trop. Dis. 6, e1844 (2012).

    PubMed  PubMed Central  Google Scholar 

  188. Ralston, E. P., Kite-Powell, H. & Beet, A. An estimate of the cost of acute health effects from food- and water-borne marine pathogens and toxins in the USA. J. Water Health 9, 680–694 (2011).

    PubMed  PubMed Central  Google Scholar 

  189. Hendren, N., Sukumar, S. & Glazer, C. S. Vibrio vulnificus septic shock due to a contaminated tattoo. BMJ Case Rep. https://doi.org/10.1136/bcr-2017-220199 (2017).

  190. Fraser, C. M. et al. DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406, 477–483 (2000). This article presents the first report of the genome sequence of the two chromosomes of V. cholerae, providing key insights to understand the evolution and virulence of this pathogen.

    PubMed  Google Scholar 

  191. Mutreja, A. et al. Evidence for several waves of global transmission in the seventh cholera pandemic. Nature 477, 462–465 (2011). This study is the first to use whole-genome sequencing to elucidate the epidemiology and global dispersal of the seventh pandemic of V. cholerae.

    CAS  PubMed  PubMed Central  Google Scholar 

  192. Schaetti, C. et al. Comparing sociocultural features of cholera in three endemic African settings. BMC Med. 11, 206 (2013).

    PubMed  PubMed Central  Google Scholar 

  193. Sundaram, N. et al. Sociocultural determinants of anticipated oral cholera vaccine acceptance in three African settings: a meta-analytic approach. BMC Publ. Health 16, 1–11 (2016).

    Google Scholar 

  194. Jensen, Ma, 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).

    CAS  PubMed  Google Scholar 

  195. Lima, F. P. & Wethey, D. S. Three decades of high-resolution coastal sea surface temperatures reveal more than warming. Nat. Commun. 3, 704 (2012).

    PubMed  Google Scholar 

  196. Vezzulli, L. et al. Long-term effects of ocean warming on the prokaryotic community: evidence from the vibrios. ISME J. 6, 21–30 (2012). This study shows the role of rapid climate warming on changing the abundance of Vibrio spp. in the marine environment using novel retrospective molecular methods.

    PubMed  Google Scholar 

  197. Vezzulli, L. et al. Climate influence on Vibrio and associated human diseases during the past half-century in the coastal North Atlantic. Proc. Natl Acad. Sci. USA 113, E5062–E5071 (2016).

    CAS  PubMed  Google Scholar 

  198. McLaughlin, J. B. et al. Outbreak of Vibrio parahaemolyticus gastroenteritis associated with Alaskan oysters. N. Engl. J. Med. 353, 1463–1470 (2005).

    CAS  PubMed  Google Scholar 

  199. González-Escalona, N. et al. Vibrio parahaemolyticus Diarrhea, Chile, 1998 and 2004. Emerg. Infect. Dis. 11, 129–131 (2005).

    PubMed  PubMed Central  Google Scholar 

  200. Tatem, A. J., Rogers, D. J. & Hay, S. I. Global Transport Networks and Infectious Disease Spread. Adv. Parasitol. 52, 293–343 (2006).

    Google Scholar 

  201. Martinez-Urtaza, J. M. et al. Genomic variation and evolution of Vibrio parahaemolyticus ST36 over the course of a transcontinental epidemic expansion. mBio 8, e01425–17 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  202. Rivera, I. N. G., Souza, K. M. C., Souza, C. P. & Lopes, R. M. Free-living and plankton-associated vibrios: assessment in ballast water, harbor areas, and coastal ecosystems in Brazil. Front. Microbiol. 3, 1–8 (2012).

    Google Scholar 

  203. McCarthy, S. A. & Khambaty, F. M. International dissemination of epidemic Vibrio cholerae by cargo ship ballast and other nonpotable waters. Appl. Environ. Microbiol. 60, 2597–2601 (1994). This study is the first to describe the role of cargo ships in the dispersal of pathogenic Vibrio spp. via discharges of ballast water.

    CAS  PubMed  PubMed Central  Google Scholar 

  204. Ruiz, G. M. et al. Global spread of microorganisms by ships. Nature 408, 49–50 (2000).

    CAS  PubMed  Google Scholar 

  205. Jacobs, J., Moore, S. K., Kunkel, K. E. & Sun, L. A framework for examining climate-driven changes to the seasonality and geographical range of coastal pathogens and harmful algae. Clim. Risk Manag. 8, 16–27 (2015).

    Google Scholar 

  206. Schets, F. M., van den Berg, H. H. J. L., Marchese, A., Garbom, S. & de Roda Husman, A. M. Potentially human pathogenic vibrios in marine and fresh bathing waters related to environmental conditions and disease outcome. Int. J. Hyg. Environ. Health 214, 399–406 (2011).

    CAS  PubMed  Google Scholar 

  207. Schets, F. M. et al. Vibrio alginolyticus infections in the Netherlands after swimming in the North Sea. Eurosurveillance 11, E061109.3 (2006).

    CAS  PubMed  Google Scholar 

  208. Ramamurthy, T., Chowdhury, G., Pazhani, G. P. & Shinoda, S. Vibrio fluvialis: an emerging human pathogen. Front. Microbiol. 5, 91 (2014).

    PubMed  PubMed Central  Google Scholar 

  209. Igbinosa, E. O. & Okoh, A. I. Vibrio fluvialis: An unusual enteric pathogen of increasing public health concern. Int. J. Environ. Res. Publ. Health 7, 3628–3643 (2010).

    Google Scholar 

  210. Centers for Disease Control Cholera in Haiti. CDC https://www.cdc.gov/cholera/haiti/index.html#one (2017).

  211. Chin, C.-S. et al. The Origin of the Haitian Cholera Outbreak Strain. N. Engl. J. Med. 364, 33–42 (2011).

    CAS  PubMed  Google Scholar 

  212. Frerichs, R. R., Keim, P. S., Barrais, R. & Piarroux, R. Nepalese origin of cholera epidemic in Haiti. Clin. Microbiol. Infect. 18, E158–E163 (2012).

    CAS  PubMed  Google Scholar 

  213. Alam, M. T. et al. Monitoring water sources for environmental reservoirs of toxigenic Vibrio cholerae O1. Haiti. Emerg. Infect. Dis. 20, 356–363 (2014).

    PubMed  PubMed Central  Google Scholar 

  214. Alam, M. T. et al. Increased isolation frequency of toxigenic Vibrio cholerae O1 from environmental monitoring sites in Haiti. PLoS One 10, e0124098 (2015).

    PubMed  PubMed Central  Google Scholar 

  215. Reen, F. J., Almagro-Moreno, S., Ussery, D. & Boyd, E. F. The genomic code: inferring Vibrionaceae niche specialization. Nat. Rev. Microbiol. 4, 697–704 (2006).

    CAS  PubMed  Google Scholar 

  216. 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).

    CAS  PubMed  Google Scholar 

  217. Sultana, M. et al. Biofilms Comprise a Component of the Annual Cycle of Vibrio cholerae in the Bay of Bengal Estuary. mBio 9, 1–13 (2018).

    Google Scholar 

  218. Gonzalez-Escalona, N. et al. Determination of molecular phylogenetics of Vibrio parahaemolyticus strains by multilocus sequence typing. J. Bacteriol. 190, 2831–2840 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  219. Quilici, M.-L., Robert-Pillot, A., Picart, J. & Fournier, J.-M. Pandemic Vibrio parahaemolyticus O3:K6 spread, France. Emerg. Infect. Dis. 11, 1148–1149 (2005).

    PubMed  PubMed Central  Google Scholar 

  220. Martinez-Urtaza, J. et al. Characterization of pathogenic Vibrio parahaemolyticus isolates from clinical sources in Spain and comparison with Asian and North American pandemic isolates. J. Clin. Microbiol. 42, 4672–4678 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  221. Ansaruzzaman, M. et al. Pandemic serovars (O3:K6 and O4:K68) of Vibrio parahaemolyticus associated with diarrhea in Mozambique: spread of the pandemic into the African continent. J. Clin. Microbiol. 43, 2559–2562 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  222. Ottaviani, D. et al. First clinical report of pandemic Vibrio parahaemolyticus O3:K6 infection in Italy. J. Clin. Microbiol. 46, 2144–2145 (2008).

    PubMed  PubMed Central  Google Scholar 

  223. Centers for Disease Control and Prevention Preliminary Incidence and Trends of Infections with Pathogens Transmitted Commonly Through Food — Foodborne Diseases Active Surveillance Network, 10 U.S. Sites, 2006–2014. Morbidity and Mortality Weekly Report 64, 495–499 (2015).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Contributions

Introduction (C.B.-A.); Epidemiology (A.A., M.A. and J.M.-U.); Mechanisms/pathophysiology (J.D.O. and M.K.W.); Diagnosis, screening and prevention (J.D.O. and F.Q.); Management (J.D.O. and F.Q.); Quality of life (M.A. and C.B.-A.); Outlook (A.A., C.B.-A. and J.M.-U.); Overview of Primer (C.B.-A.).

Corresponding author

Correspondence to Craig Baker-Austin.

Ethics declarations

Competing interests

All authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Related link

WHO Global Health Observatory Map Gallery: http://gamapserver.who.int/mapLibrary/Files/Maps/Global_Cholera(WER)_2016.png

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Baker-Austin, C., Oliver, J.D., Alam, M. et al. Vibrio spp. infections. Nat Rev Dis Primers 4, 1–19 (2018). https://doi.org/10.1038/s41572-018-0005-8

Download citation

  • Published:

  • Issue date:

  • DOI: https://doi.org/10.1038/s41572-018-0005-8

This article is cited by

Search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Microbiology