Primer | Published:

Vibrio spp. infections

Nature Reviews Disease Primersvolume 4, Article number: 8 (2018) | Download Citation


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.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from $8.99

All prices are NET prices.

Additional information

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

WHO Global Health Observatory Map Gallery:


  1. 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).

  2. 2.

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

  3. 3.

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

  4. 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).

  5. 5.

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

  6. 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).

  7. 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.

  8. 8.

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

  9. 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).

  10. 10.

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

  11. 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).

  12. 12.

    World Health Organization. Cholera. WHO (2017).

  13. 13.

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

  14. 14.

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

  15. 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. 16.

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

  17. 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).

  18. 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).

  19. 19.

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

  20. 20.

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

  21. 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.

  22. 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).

  23. 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).

  24. 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).

  25. 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).

  26. 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).

  27. 27.

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

  28. 28.

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

  29. 29.

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

  30. 30.

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

  31. 31.

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

  32. 32.

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

  33. 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).

  34. 34.

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

  35. 35.

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

  36. 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).

  37. 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).

  38. 38.

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

  39. 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).

  40. 40.

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

  41. 41.

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

  42. 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).

  43. 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. 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).

  45. 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. 46.

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

  47. 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.

  48. 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).

  49. 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).

  50. 50.

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

  51. 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.

  52. 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).

  53. 53.

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

  54. 54.

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

  55. 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.

  56. 56.

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

  57. 57.

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

  58. 58.

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

  59. 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).

  60. 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.

  61. 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).

  62. 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.

  63. 63.

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

  64. 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).

  65. 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).

  66. 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).

  67. 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).

  68. 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).

  69. 69.

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

  70. 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).

  71. 71.

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

  72. 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).

  73. 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).

  74. 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).

  75. 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).

  76. 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).

  77. 77.

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

  78. 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).

  79. 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).

  80. 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).

  81. 81.

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

  82. 82.

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

  83. 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).

  84. 84.

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

  85. 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.

  86. 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).

  87. 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. 88.

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

  89. 89.

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

  90. 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.

  91. 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).

  92. 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).

  93. 93.

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

  94. 94.

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

  95. 95.

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

  96. 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).

  97. 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).

  98. 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).

  99. 99.

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

  100. 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).

  101. 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).

  102. 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).

  103. 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).

  104. 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).

  105. 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).

  106. 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).

  107. 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).

  108. 108.

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

  109. 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.

  110. 110.

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

  111. 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).

  112. 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.

  113. 113.

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

  114. 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.

  115. 115.

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

  116. 116.

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

  117. 117.

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

  118. 118.

    World Health Organization. 10 facts on cholera. World Health Organization (2016).

  119. 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).

  120. 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).

  121. 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).

  122. 122.

    World Health Organization. Prevention and control of cholera outbreaks: WHO policy and recommendations. WHO (2017).

  123. 123.

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

  124. 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).

  125. 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).

  126. 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).

  127. 127.

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

  128. 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. 129.

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

  130. 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).

  131. 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).

  132. 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).

  133. 133.

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

  134. 134.

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

  135. 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).

  136. 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).

  137. 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).

  138. 138.

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

  139. 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).

  140. 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).

  141. 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).

  142. 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).

  143. 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).

  144. 144.

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

  145. 145.

    US Food and Drug Administration. VAXCHORA. FDA (2018).

  146. 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).

  147. 147.

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

  148. 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).

  149. 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).

  150. 150.

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

  151. 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).

  152. 152.

    World Health Organization. Immunisation standards: inactivated oral single dose vial. WHO (2017).

  153. 153.

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

  154. 154.

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

  155. 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).

  156. 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).

  157. 157.

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

  158. 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).

  159. 159.

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

  160. 160.

    European Centre for Disease Prevention and Control. Vibrio Risk Portal. E3 Geoportal (2018).

  161. 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).

  162. 162.

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

  163. 163.

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

  164. 164.

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

  165. 165.

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

  166. 166.

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

  167. 167.

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

  168. 168.

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

  169. 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).

  170. 170.

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

  171. 171.

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

  172. 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).

  173. 173.

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

  174. 174.

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

  175. 175.

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

  176. 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).

  177. 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).

  178. 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).

  179. 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).

  180. 180.

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

  181. 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).

  182. 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).

  183. 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).

  184. 184.

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

  185. 185.

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

  186. 186.

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

  187. 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).

  188. 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).

  189. 189.

    Hendren, N., Sukumar, S. & Glazer, C. S. Vibrio vulnificus septic shock due to a contaminated tattoo. BMJ Case Rep. (2017).

  190. 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.

  191. 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.

  192. 192.

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

  193. 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).

  194. 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).

  195. 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).

  196. 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.

  197. 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).

  198. 198.

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

  199. 199.

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

  200. 200.

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

  201. 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).

  202. 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).

  203. 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.

  204. 204.

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

  205. 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).

  206. 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).

  207. 207.

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

  208. 208.

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

  209. 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).

  210. 210.

    Centers for Disease Control Cholera in Haiti. CDC (2017).

  211. 211.

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

  212. 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).

  213. 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).

  214. 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).

  215. 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).

  216. 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).

  217. 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).

  218. 218.

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

  219. 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).

  220. 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).

  221. 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).

  222. 222.

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

  223. 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).

Download references

Author information


  1. Centre for Environment, Fisheries and Aquaculture Science (CEFAS), Weymouth, UK

    • Craig Baker-Austin
    •  & Jaime Martinez-Urtaza
  2. Department of Biological Sciences, University of North Carolina, Charlotte, NC, USA

    • James D. Oliver
  3. Duke University Marine Laboratory, Beaufort, NC, USA

    • James D. Oliver
  4. icddr,b, formerly known as the International Centre for Diarrhoeal Disease Research, Dhaka, Bangladesh

    • Munirul Alam
    •  & Firdausi Qadri
  5. Department of Environmental and Global Health, College of Public Health & Health Professions and Emerging Pathogens Institute (EPI), University of Florida, Gainesville, FL, USA

    • Afsar Ali
  6. Department of Microbiology, Harvard Medical School, Boston, MA, USA

    • Matthew K. Waldor


  1. Search for Craig Baker-Austin in:

  2. Search for James D. Oliver in:

  3. Search for Munirul Alam in:

  4. Search for Afsar Ali in:

  5. Search for Matthew K. Waldor in:

  6. Search for Firdausi Qadri in:

  7. Search for Jaime Martinez-Urtaza in:


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.).

Competing interests

All authors declare no competing interests.

Corresponding author

Correspondence to Craig Baker-Austin.

About this article

Publication history