Cholera: an overview with reference to the Yemen epidemic

Abstract

Cholera is a secretory diarrhoeal disease caused by infection with Vibrio cholerae, primarily the V. cholerae O1 El Tor biotype. There are approximately 2.9 million cases in 69 endemic countries annually, resulting in 95 000 deaths. Cholera is associated with poor infrastructure and lack of access to sanitation and clean drinking water. The current cholera epidemic in Yemen, linked to spread of V. cholerae O1 (Ogawa serotype), is associated with the ongoing war. This has devastated infrastructure and health services. The World Health Organization had estimated that 172 286 suspected cases arose between 27th April and 19th June 2017, including 1170 deaths. While there are three oral cholera vaccines prequalified by the World Health Organization, there are issues surrounding vaccination campaigns in conflict situations, exacerbated by external factors such as a global vaccine shortage. Major movements of people complicates surveillance and administration of double doses of vaccines. Cholera therapy mainly depends on rehydration, with use of antibiotics in more severe infections. Concerns have arisen about the rise of antibiotic resistance in cholera, due to mobile genetic elements. In this review, we give an overview of cholera epidemiology, virulence, antibiotic resistance, therapy and vaccines, in the light of the ongoing epidemic in Yemen.

Keywords

cholera / epidemic / multi-drug resistant / catechin / luteolin / ToxT / CTXФ

References

[1] Ali M, Nelson AR, Lopez AL, Sack DA. Updated global burden of cholera in endemic countries. PLoS Negl Trop Dis 2015; 9(6): e0003832

[2] WHO. Cholera 2015. Weekly Epidemiological Report 2016; 91: 433–440

[3] WHO. 2016. Cholera Fact sheet.http://www.who.int/mediacentre/factsheets/fs107/en/ (Accessed June 14 2017)

[4] Luquero FJ, Rondy M, Boncy J, Munger A, Mekaoui H, Rymshaw E, Page AL, Toure B, Degail MA, Nicolas S, Grandesso F, Ginsbourger M, Polonsky J, Alberti KP, Terzian M, Olson D, Porten K, Ciglenecki I. Mortality rates during cholera epidemic, Haiti, 2010–2011. Emerg Infect Dis 2016; 22(3): 410–416

[5] Ohene S, Klenyuie W, Sarpeh M. Assessment of the response to cholera outbreaks in two districts in Ghana. Infect Dis Poverty 2016; 5(1): 99

[6] Steinberg EB, Greene KD, Bopp CA, Cameron DN, Wells JG, Mintz ED. Cholera in the United States, 1995–2000: trends at the end of the twentieth century. J Infect Dis 2001; 184(6): 799–802

[7] Loharikar A, Newton AE, Stroika S, Freeman M, Greene KD, Parsons MB, Bopp C, Talkington D, Mintz ED, Mahon BE. Cholera in the United States, 2001–2011: a reflection of patterns of global epidemiology and travel. Epidemiol Infect 2015; 143(4): 695–703

[8] Li XQ, Wang M, Deng ZA, Shen JC, Zhang XQ, Liu YF, Cai YS, Wu XW, Di B. Survivability and molecular variation in Vibrio cholerae from epidemic sites in China. Epidemiol Infect 2015; 143(2): 288–297

[9] WHO. 2017. Yemen: cholera outbreak. Daily Epidemiology Update. June 20 2017

[10] BBC World News. 2017. Yemen crisis: Who is fighting whom? http://www.bbc.com/news/world-middle-east-29319423 (accessed June 14 2017)

[11] WHO. 2016. Survey reveals extent of damage to Yemen’s health system. http://www.who.int/hac/crises/yem/releases/en/ (Accessed June 14 2017)

[12] Sakazaki R, Shimada T. Serovars of Vibrio cholerae identified during 1970–1975. Jpn J Med Sci Biol 1977; 30(5): 279–282

[13] Sakazaki R, Shimada T. Additional serovars and inter-O antigenic relationships of Vibrio cholerae. Jpn J Med Sci Biol 1977; 30(5): 275–277

[14] Shimada T, Arakawa E, Itoh K, Okitsu T, Matsushima A, Asai Y, Yamai S, Nakazato T, Nair GB, Albert MJ, Takeda Y. Extended serotyping scheme for Vibrio cholerae. Curr Microbiol 1994; 28(3): 175–178

[15] Banerjee R, Das B, Balakrish Nair G, Basak S. Dynamics in genome evolution of Vibrio cholerae. Infect Genet Evol 2014; 23: 32–41

[16] Kaper JB, Morris JG, Levine MM. Cholera. Clin Microbiol Rev 1995; 8(1): 48–86

[17] Wong KK, Burdette E, Mahon BE, Mintz ED, Ryan ET, Reingold AL. Recommendations of the Advisory Committee on Immunization Practices for Use of Cholera Vaccine. Atlanta: U.S. Center for Disease Control, 2017

[18] Kuna A, Gajewski M. Cholera — the new strike of an old foe. Int Marit Health 2017; 68(3): 163–167

[19] Nishiura H, Tsuzuki S, Yuan B, Yamaguchi T, Asai Y. Transmission dynamics of cholera in Yemen, 2017: a real time forecasting. Theor Biol Med Model 2017; 14(1): 14

[20] Naseer M, Jamali T. Epidemiology, determinants and dynamics of cholera in Pakistan: gaps and prospects for future research. J Coll Physicians Surg Pak 2014 11; 24(11): 855–860

[21] Siriphap A, Leekitcharoenphon P, Kaas RS, Theethakaew C, Aarestrup FM, Sutheinkul O, Hendriksen RS. Characterization and genetic variation of Vibrio cholerae isolated from clinical and environmental sources in Thailand. PLoS One 2017; 12(1): e0169324

[22] Chowdhury F, Mather AE, Begum YA, Asaduzzaman M, Baby N, Sharmin S, Biswas R, Uddin MI, LaRocque RC, Harris JB, Calderwood SB. Vibrio cholerae serogroup O139: isolation from cholera patients and asymptomatic household family members in Bangladesh between 2013 and 2014. PLoS Negl Trop Dis 2015; 9(11): e0004183

[23] Li BS, Xiao Y, Wang DC, Tan HL, Ke BX, He DM, Ke CW, Zhang YH. Genetic relatedness of selected clinical Vibrio cholerae O139 isolates from the southern coastal area of China over a 20-year period. Epidemiol Infect 2016; 144(12): 2679–2687

[24] Aldová E, Lázničková K, Štěpánková E, Lietava J. Isolation of nonagglutinable vibrios from an enteritis outbreak in Czechoslovakia. J Infect Dis 1968; 118(1): 25–31

[25] Kamal AM. Outbreak of gastro-enteritis by non-agglutinable (NAG) vibrios in the republic of the Sudan. J Egypt Public Health Assoc 1971; 46: 125–159

[26] Rahaman MH, Islam T, Colwell RR, Alam M. Molecular tools in understanding the evolution of Vibrio cholerae. Front Microbiol 2015; 6: 1040

[27] Blake PA. Vibrio cholerae and Cholera: Molecular to Global Perspectives. In: Wachsmuth IK, Blake PA, Olsvik Ø, eds. Washington, DC: Am So. Microbiol, 1994: 293–295

[28] Dziejman M, Balon E, Boyd D, Fraser CM, Heidelberg JF, Mekalanos JJ. Comparative genomic analysis of Vibrio cholerae: genes that correlate with cholera endemic and pandemic disease. Proc Natl Acad Sci USA 2002; 99(3): 1556–1561

[29] Eppinger M, Pearson T, Koenig SS, Pearson O, Hicks N, Agrawal S, Sanjar F, Galens K, Daugherty S, Crabtree J, Hendriksen RS, Price LB, Upadhyay BP, Shakya G, Fraser CM, Ravel J, Keim PS. Genomic epidemiology of the Haitian cholera outbreak: a single introduction followed by rapid, extensive, and continued spread characterized the onset of the epidemic. MBio 2014; 5(6): e01721–e14

[30] Langa JP, Sema C, De Deus N, Colombo MM, Taviani E. Epidemic waves of cholera in the last two decades in Mozambique. J Infect Dev Ctries 2015; 9(6): 635–641

[31] Nsagha DS, Atashili J, Fon PN, Tanue EA, Ayima CW, Kibu OD. Assessing the risk factors of cholera epidemic in the Buea Health District of Cameroon. BMC Public Health 2015; 15(1): 1128

[32] Nair GB, Faruque SM, Bhuiyan NA, Kamruzzaman M, Siddique AK, Sack DA. 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 2002; 40(9): 3296–3299

[33] Das B, Halder K, Pal P, Bhadra RK. Small chromosomal integration site of classical CTX prophage in Mozambique Vibrio cholerae O1 biotype El Tor strain. Arch Microbiol 2007; 188(6): 677–683

[34] Faruque SM, Tam VC, Chowdhury N, Diraphat P, Dziejman M, Heidelberg JF, Clemens JD, Mekalanos JJ, Nair GB. Genomic analysis of the Mozambique strain of Vibrio cholerae O1 reveals the origin of El Tor strains carrying classical CTX prophage. Proc Natl Acad Sci USA 2007; 104(12): 5151–5156

[35] Barua D. History of cholera. In: Barua D, Greenough WB (eds). Cholera. New York: Springer US, 1992: 1–36

[36] Bwire G, Munier A, Ouedraogo I, Heyerdahl L, Komakech H, Kagirita A, Wood R, Mhlanga R, Njanpop-Lafourcade B, Malimbo M, Makumbi I, Wandawa J, Gessner BD, Orach CG, Mengel MA. Epidemiology of cholera outbreaks and socio-economic characteristics of the communities in the fishing villages of Uganda: 2011–2015. PLoS Negl Trop Dis 2017; 11(3): e0005407

[37] Kachwamba Y, Mohammed AA, Lukupulo H, Urio L, Majigo M, Mosha F, Matonya M, Kishimba R, Mghamba J, Lusekelo J, Nyanga S, Almeida M, Li S, Domman D, Massele SY, Stine OC. Genetic characterization of Vibrio cholerae O1 isolates from outbreaks between 2011 and 2015 in Tanzania. BMC Infect Dis 2017; 17(1): 157

[38] Dalusi L, Lyimo TJ, Lugomela C, Hosea KMM, Sjöling S. Toxigenic Vibrio cholerae identified in estuaries of Tanzania using PCR techniques. FEMS Microbiol Lett 2015; 362(5): fnv009

[39] Moore S, Miwanda B, Sadji AY, Thefenne H, Jeddi F, Rebaudet S, De Boeck H, Bidjada B, Depina JJ, Bompangue D, Abedi AA, Koivogui L, Keita S, Garnotel E, Plisnier PD, Ruimy R, Thomson N, Muyembe JJ, Piarroux R. Relationship between distinct African cholera epidemics revealed via MLVA haplotyping of 337 Vibrio cholerae isolates. PLoS Negl Trop Dis 2015; 9(6): e0003817

[40] Parker LA, Rumunu J, Jamet C, Kenyi Y, Lino RL, Wamala JF, Mpairwe AM, Ciglenecki I, Luquero FJ, Azman AS, Cabrol JC. Adapting to the global shortage of cholera vaccines: targeted single dose cholera vaccine in response to an outbreak in South Sudan. Lancet Infect Dis 2017; 17(4): e123–e127

[41] Bwire G, Mwesawina M, Baluku Y, Kanyanda SS, Orach CG. Cross-border cholera outbreaks in Sub-Saharan Africa, the mystery behind the silent illness: what needs to be done? PLoS One 2016; 11(6): e0156674

[42] Masoumi-Asl H, Gouya MM, Rahbar M, Sabourian R. The epidemiology and antimicrobial resistance of cholera cases in Iran during 2013. Iran J Microbiol 2016; 8(4): 232–237

[43] Ngwa MC, Liang S, Kracalik IT, Morris L, Blackburn JK, Mbam LM, Pouth SF, Teboh A, Yang Y, Arabi M, Sugimoto JD. Cholera in Cameroon, 2000–2012: spatial and temporal analysis at the operational (health district) and sub climate levels. PLoS Negl Trop Dis 2016; 10(11): e0005105

[44] Jutla A, Aldaach H, Billian H, Akanda A, Huq A, Colwell R. Satellite based assessment of hydroclimatic conditions related to cholera in Zimbabwe. PLoS One 2015; 10(9): e0137828

[45] Nelson CB, Mogasale V, Bari TI, Clemens JD. Considerations around the introduction of a cholera vaccine in Bangladesh. Vaccine 2014; 32(52): 7033–7036

[46] Righetto L, Zaman RU, Mahmud ZH, Bertuzzo E, Mari L, Casagrandi R, Gatto M, Islam S, Rinaldo A. Detection of Vibrio cholerae O1 and O139 in environmental waters of rural Bangladesh: a flow-cytometry-based field trial. Epidemiol Infect 2015; 143(11): 2330–2342

[47] Kumar P, Mishra DK, Deshmukh DG, Jain M, Zade AM, Ingole KV, Goel AK, Yadava PK. Vibrio cholerae O1 Ogawa El Tor strains with the ctxB7 allele driving cholera outbreaks in south-western India in 2012. Infect Genet Evol 2014; 25: 93–96

[48] Klinzing DC, Choi SY, Hasan NA, Matias RR, Tayag E, Geronimo J, Skowronski E, Rashed SM, Kawashima K, Rosenzweig CN, Gibbons HS. Molecular tools in understanding the evolution of Vibrio cholerae. Front Microbiol 2015; 6: 1040

[49] Das SK, Begum D, Ahmed S, Ferdous F, Farzana FD, Chisti MJ, Latham JR, Talukder KA, Rahman MM, Begum YA, Faruque ASG, Malek MA, Qadri F, Ahmed T, Alam N. Geographical diversity in seasonality of major diarrhoeal pathogens in Bangladesh observed between 2010 and 2012. Epidemiol Infect 2014; 142(12): 2530–2541

[50] Rashed SM, Hasan NA, Alam M, Sadique A, Sultana M, Hoq MM, Sack RB, Colwell RR, Huq A. Vibrio cholerae O1 with reduced susceptibility to ciprofloxacin and azithromycin isolated from a rural coastal area of Bangladesh. Front Microbiol 2017; 8: 252

[51] Kar SK, Pal BB, Khuntia HK, Achary KG, Khuntia CP. Emergence and spread of tetracycline resistant Vibrio cholerae O1 El Tor variant during 2010 cholera epidemic in the tribal areas of Odisha, India. Int J Infect Dis 2015; 33: 45–49

[52] Bhattacharya D, Dey S, Roy S, Parande MV, Telsang M, Seema MH, Parande AV, Mantur BG. Multidrug-resistant Vibrio cholerae O1 was responsible for a cholera outbreak in 2013 in Bagalkot, North Karnataka. Jpn J Infect Dis 2015; 68(4): 347–350

[53] Torane V, Kuyare S, Nataraj G, Mehta P, Dutta S, Sarkar B. Phenotypic and antibiogram pattern of V. cholerae isolates from a tertiary care hospital in Mumbai during 2004–2013: a retrospective cross-sectional study. BMJ Open 2016; 6(11): e012638

[54] Reimer AR, Van Domselaar G, Stroika S, Walker M, Kent H, Tarr C, Talkington D, Rowe L, Olsen-Rasmussen M, Frace M, Sammons S. Comparative genomics of Vibrio cholerae from Haiti, Asia, and Africa. Emerg Infect Dis 2011; 17(11): 2113

[55] Hendriksen RS, Price LB, Schupp JM, Gillece JD, Kaas RS, Engelthaler DM, Bortolaia V, Pearson T, Waters AE, Upadhyay BP, Shrestha SD. Population genetics of Vibrio cholerae from Nepal in 2010: evidence on the origin of the Haitian outbreak. MBio 2011; 2(4): e00157–e11

[56] Orata FD, Keim PS, Boucher Y. The 2010 cholera outbreak in Haiti: how science solved a controversy. PLoS Pathog 2014; 10(4): e1003967

[57] Piarroux R, Barrais R, Faucher B, Haus R, Piarroux M, Gaudart J, Magloire R, Raoult D. Understanding the cholera epidemic, Haiti. Emerg Infect Dis 2011; 17(7): 1161–1168

[58] Ivers LC, Walton DA. The “first” case of cholera in Haiti: lessons for global health. Am J Trop Med Hyg 2012; 86(1): 36–38

[59] Kahler AM, Haley BJ, Chen A, Mull BJ, Tarr CL, Turnsek M, Katz LS, Humphrys MS, Derado G, Freeman N, Boncy J, Colwell RR, Huq A, Hill VR. Environmental surveillance for toxigenic Vibrio cholerae in surface waters of Haiti. Am J Trop Med Hyg 2015; 92(1):118–125

[60] Alam MT, Weppelmann TA, Longini I, De Rochars VMB, Morris JG, Ali A. Increased isolation frequency of toxigenic Vibrio cholerae O1 from environmental monitoring sites in Haiti. PLoS One 2015; 10(4): e0124098

[61] Lantagne D, Nair GB, Lanata CF, Cravioto A. The cholera outbreak in Haiti: where and how did it begin? In: Nair GB, Takeda Y. Cholera Outbreaks. Berlin Heidelberg: Springer, 2013: 145–164

[62] Lewnard JA, Antillón M, Gonsalves G, Miller AM, Ko AI, Pitzer VE. Strategies to prevent cholera introduction during international personnel deployments: a computational modeling analysis based on the 2010 Haiti outbreak. PLoS Med 2016; 13(1): e1001947

[63] Satchell KJF, Jones CJ, Wong J, Queen J, Agarwal S, Yildiz FH. Phenotypic analysis reveals that the 2010 Haiti cholera epidemic is linked to a hypervirulent strain. Infect Immun 2016; 84(9): 2473–2481

[64] Grandesso F, Allan M, Jean-Simon PS, Boncy J, Blake A, Pierre R, Alberti KP, Munger A, Elder G, Olson D, Porten K, Luquero FJ. Risk factors for cholera transmission in Haiti during inter-peak periods: insights to improve current control strategies from two case-control studies. Epidemiol Infect 2014; 142(8): 1625–1635

[65] Page A, Ciglenecki I, Jasmin ER, Desvignes L, Grandesso F, Polonsky J, Nicholas S, Alberti KP, Porten K, Luquero FJ. Geographic distribution and mortality risk factors during the cholera outbreak in a rural region of Haiti, 2010–2011. PLoS Negl Trop Dis 2015; 9(3): e0003605

[66] Aureli M, Mauri L, Ciampa MG, Prinetti A, Toffano G, Secchieri C, Sonnino S. GM1 ganglioside: past studies and future potential. Mol Neurobiol 2016; 53(3): 1824–1842

[67] Broeck DV, Horvath C, De Wolf MJ. Vibrio cholerae: cholera toxin. Int J Biochem Cell Biol 2007; 39(10): 1771–1775

[68] Heggelund JE, Burschowsky D, Bjørnestad VA, Hodnik V, Anderluh G, Krengel U. High-resolution crystal structures elucidate the molecular basis of cholera blood group dependence. PLoS Pathog 2016; 12(4): e1005567

[69] Phongsisay V, Iizasa EI, Hara H, Yoshida H. Evidence for TLR4 and FcRg–CARD9 activation by cholera toxin B subunit and its direct bindings to TREM2 and LMIR5 receptors. Mol Immunol 2015; 66(2): 463–471

[70] Waldor MK, Mekalanos JJ. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 1996; 272(5270): 1910–1914

[71] Heilpern AJ, Waldor MK. CTXФ infection of Vibrio cholerae requires the tolQRA gene products. J Bacteriol 2000; 182(6): 1739–1747

[72] Moyer KE, Kimsey HH, Waldor MK. Evidence for a rolling-circle mechanism of phage DNA synthesis from both replicative and integrated forms of CTXФ. Mol Microbiol 2001; 41(2): 311–323

[73] Das B, Bischerour J, Val ME, Barre FX. Molecular keys of the tropism of integration of the cholera toxin phage. Proc Natl Acad Sci USA 2010; 107(9): 4377–4382

[74] Quinones M, Kimsey HH, Waldor MK. LexA cleavage is required for CTX prophage induction. Mol Cell 2005; 17(2): 291–300

[75] Waldor MK, Rubin EJ, Pearson GD, Kimsey H, Mekalanos JJ. Regulation, replication, and integration functions of the Vibrio cholerae CTXF are encoded by region RS2. Mol Microbiol 1997; 24(5): 917–926

[76] Martínez E, Paly E, Barre F. CTXФ replication depends on the histone-like HU protein and the UvrD helicase. PLoS Genet 2015; 11(5): e1005256

[77] DiRita VJ, Parsot C, Jander G, Mekalanos JJ. Regulatory cascade controls virulence in Vibrio cholerae. Proc Natl Acad Sci USA 1991; 88(12): 5403–5407

[78] Lowden MJ, Skorupski K, Pellegrini M, Chiorazzo MG, Taylor RK, Kull FJ. Structure of Vibrio cholerae ToxT reveals a mechanism for fatty acid regulation of virulence genes. Proc Natl Acad Sci USA 2010; 107(7): 2860–2865

[79] Matson JS, Withey JH, DiRita VJ. Regulatory networks controlling Vibrio cholerae virulence gene expression. Infect Immun 2007; 75(12): 5542–5549

[80] Global Task Force on Cholera Control (GTFCC). Cholera outbreak: assessing the outbreak response and improving preparedness. Geneva: World Health Organization, 2010. Available from: http://www.who.int/cholera/publications/OutbreakAssessment/en/ (Accessed June 27 2017)

[81] Leibovici-Weissman Y, Neuberger A, Bitterman R, Sinclair D, Salam MA, Paul M. Antimicrobial drugs for treating cholera. Cochrane Database Syst Rev 2014; (6): 1

[82] Baron S, Lesne J, Jouy E, Larvor E, Kempf I, Boncy J, Rebaudet S, Piarroux R. Antimicrobial susceptibility of autochthonous aquatic Vibrio cholerae in Haiti. Front Microbiol 2016; 7: 1671

[83] Carraro N, Rivard N, Ceccarelli D, Colwell RR, Burrus V. IncA/C conjugative plasmids mobilize a new family of multidrug resistance islands in clinical Vibrio cholerae Non-O1/Non-O139 isolates from Haiti. MBio 2016; 7(4): e00509–e00516

[84] Ceccarelli D, Alam M, Huq A, Colwell RR. Reduced susceptibility to extended-spectrum β-lactams in Vibrio cholerae isolated in Bangladesh. Front Public Health 2016; 4: 231

[85] Wang R, Li J, Kan B. Sequences of a co-existing SXT element, a chromosomal integron (CI) and an IncA/C plasmid and their roles in multidrug resistance in a Vibrio cholerae O1 El Tor strain. Int J Antimicrob Agents 2016; 48(3): 305–309

[86] Mehla K, Ramana J. DBDiaSNP: an open-source knowledgebase of genetic polymorphisms and resistance genes related to diarrheal pathogens. OMICS 2015; 19(6): 354–360

[87] Bhattacharya MK, Kanungo S, Ramamurthy T, Rajendran K, Sinha A, Bhattacharya A, Sarkar BS. Comparison between single dose azithromycin and six doses, 3 day norfloxacin for treatment of cholera in adult. Int J Biomed Sci 2014; 10(4): 248–251

[88] Daniels NA, Shafaie A. A review of pathogenic Vibrio infections for clinicians. Infect Med 2000; 17(10): 665–685

[89] Ghosh A, Ramamurthy T. Antimicrobials and cholera: are we stranded? Indian J Med Res 2011; 133(2): 225

[90] Pugliese N, Maimone F, Scrascia M, Materu SF, Pazzani C. SXT-related integrating conjugative element and IncC plasmids in Vibrio cholerae O1 strains in Eastern Africa. J Antimicrob Chemother 2009; 63(3): 438–442

[91] Spagnoletti M, Ceccarelli D, Rieux A, Fondi M, Taviani E, Fani R, Colombo MM, Colwell RR, Balloux F. Acquisition and evolution of SXT-R391 integrative conjugative elements in the seventh-pandemic Vibrio cholerae lineage. MBio 2014; 5(4): e01356–e14

[92] Wang R, Yu D, Zhu L, Li J, Yue J, Kan B. IncA/C plasmids harboured in serious multidrug-resistant Vibrio cholerae serogroup O139 strains in China. Int J Antimicrob Agents 2015; 45(3): 249–254

[93] Wang R, Yu D, Yue J, Kan B. Variations in SXT elements in epidemic Vibrio cholerae O1 El Tor strains in China. Sci Rep 2016; 6(1): 22733

[94] Goel AK, Jiang SC. Genetic determinants of virulence, antibiogram and altered biotype among the Vibrio cholerae O1 isolates from different cholera outbreaks in India. Infect Genet Evol 2010; 10(6): 814–818

[95] Mutreja A, Kim DW, Thomson NR, Connor TR, Lee JH, Kariuki S, Croucher NJ, Choi SY, Harris SR, Lebens M, Niyogi SK, Kim EJ, Ramamurthy T, Chun J, Wood JLN, Clemens JD, Czerkinsky C, Nair GB, Holmgren J, Parkhill J, Dougan G. Evidence for several waves of global transmission in the seventh cholera pandemic. Nature 2011; 477(7365): 462–465

[96] Wozniak RA, Fouts DE, Spagnoletti M, Colombo MM, Ceccarelli D, Garriss G, Déry C, Burrus V, Waldor MK. Comparative ICE genomics: insights into the evolution of the SXT/R391 family of ICEs. PLoS Genet 2009; 5(12): e1000786

[97] Waldor MK, Tschäpe HE, Mekalanos JJ. A new type of conjugative transposon encodes resistance to sulfamethoxazole, trimethoprim, and streptomycin in Vibrio cholerae O139. J Bacteriol 1996; 178(14): 4157–4165

[98] Ceccarelli D, Spagnoletti M, Bacciu D, Danin-Poleg Y, Mendiratta DK, Kashi Y, Cappuccinelli P, Burrus V, Colombo MM. ICEVchInd5 is prevalent in epidemic Vibrio cholerae O1 El Tor strains isolated in India. Int J Med Microbiol 2011; 301(4): 318–324

[99] Sá LL, Fonseca ÉL, Pellegrini M, Freitas F, Loureiro EC, Vicente AC. Occurrence and composition of class 1 and class 2 integrons in clinical and environmental O1 and non-O1/non-O139 Vibrio cholerae strains from the Brazilian Amazon. Mem Inst Oswaldo Cruz 2010; 105(2): 229–232

[100] Costa DS, Araújo TSL, Sousa NA, Souza LKM, Pacífico DM, Sousa FBM, Nicolau LAD, Chaves LS, Barros FCN, Freitas ALP, Medeiros JVR. Sulphated polysaccharide isolated from the seaweed Gracilaria caudata exerts an antidiarrhoeal effect in rodents. Basic Clin Pharmacol Toxicol 2016; 118(6): 440–448

[101] Zahid MS, Awasthi SP, Asakura M, Chatterjee S, Hinenoya A, Faruque SM, Yamasaki S. Suppression of virulence of toxigenic Vibrio cholerae by anethole through the cyclic AMP (cAMP)-cAMP receptor protein signaling system. PLoS One 2015; 10(9): e0137529

[102] Perveen S, Chaudhary HS. In silico screening of antibacterial compounds from herbal sources against Vibrio cholerae. Pharmacogn Mag 2015; 11(44): S550–S555

[103] Thompson JA, Oliveira RA, Xavier KB. Can chatter between microbes prevent cholera? Trends Microbiol 2014; 22(12): 660–662

[104] Cil O, Phuan P, Gillespie AM, Lee S, Tradtrantip L, Yin J, Tse M, Zachos NC, Lin R, Donowitz M, Verkman AS. Benzopyrimido-pyrrolo-oxazine-dione CFTR inhibitor (R)-BPO-27 for antisecretory therapy of diarrheas caused by bacterial enterotoxins. FASEB J 2017; 31(2): 751–760

[105] Sarker P, Banik A, Stromberg R, Gudmundsson GH, Raqib R, Agerberth B. Treatment with entinostat heals experimental cholera by affecting physical and chemical barrier functions of intestinal epithelia. Antimicrob Agents Chemother 2017;61(7): e02570-16

[106] Mandal RS, Ta A, Sinha R, Theeya N, Ghosh A, Tasneem M, Bhunia A, Koley H, Das S. Ribavirin suppresses bacterial virulence by targeting LysR-type transcriptional regulators. Sci Rep 2016; 6(1): 39454

[107] Yen M, Cairns LS, Camilli A. A cocktail of three virulent bacteriophages prevents Vibrio cholerae infection in animal models. Nat Commun 2017; 8: 14187

[108] Solís-Sánchez A, Hernández-Chiñas U, Navarro-Ocaña A, De LM, Xicohtencatl-Cortes J, Eslava-Campos C. Genetic characterization of ØVC8 lytic phage for Vibrio cholerae O1. Virol J 2016; 13(1): 47

[109] Al-Fendi A, Shueb RH, Foo PC, Ravichandran M, Yean CY. Complete genome sequence of lytic bacteriophage VPUSM 8 against O1 El Tor Inaba Vibrio cholerae. Genome Announc 2017; 5(21): e00073–e17

[110] Woodbrey AK, Onyango EO, Pellegrini M, Kovacikova G, Taylor RK, Gribble GW, Kull FJ. A new class of inhibitors of the AraC family virulence regulator Vibrio cholerae ToxT. Sci Rep 2017; 7: 45011

[111] Withey JH, Nag D, Plecha SC, Sinha R, Koley H. Conjugated linoleic acid reduces cholera toxin production in vitro and in vivo by inhibiting Vibrio cholerae ToxT Activity. Antimicrob Agents Chemother 2015; 59(12): 7471–7476

[112] Leonardi W, Zilbermintz L, Cheng LW, Zozaya J, Tran SH, Elliott JH, Polukhina K, Manasherob R, Li A, Chi X, Gharaibeh D, Kenny T, Zamani R, Soloveva V, Haddow AD, Nasar F, Bavari S, Bassik MC, Cohen SN, Levitin A, Martchenko M. Bithionol blocks pathogenicity of bacterial toxins, ricin, and Zika virus. Sci Rep 2016; 6(1): 34475

[113] Cushnie TPT, Cushnie B, Lamb AJ. Alkaloids: an overview of their antibacterial, antibiotic-enhancing and antivirulence activities. Int J Antimicrob Agents 2014; 44(5): 377–386

[114] Bhattaram V, Upadhyay A, Yin H, Mooyottu S, Venkitanarayanan K. Effect of dietary minerals on virulence attributes of Vibrio cholerae. Front Microbiol 2017; 8: 911

[115] Faruque SM, Naser IB, Islam MJ, Faruque AS, Ghosh AN, Nair GB, Sack DA, Mekalanos JJ. Seasonal epidemics of cholera inversely correlate with the prevalence of environmental cholera phages. Proc Natl Acad Sci USA 2005; 102(5): 1702–1707

[116] Bhowmick TS, Koley H, Das M, Saha DR, Sarkar BL. Pathogenic potential of vibriophages against an experimental infection with Vibrio cholerae O1 in the RITARD model. Int J Antimicrob Agents 2009; 33(6): 569–573

[117] Jaiswal A, Koley H, Ghosh A, Palit A, Sarkar B. Efficacy of cocktail phage therapy in treating Vibrio cholerae infection in rabbit model. Microbes Infect 2013; 15(2): 152–156

[118] Jaiswal A, Koley H, Mitra S, Saha DR, Sarkar B. Comparative analysis of different oral approaches to treat Vibrio cholerae infection in adult mice. Int J Med Microbiol 2014; 304(3–4): 422–430

[119] Chaignat CL. What about cholera vaccines? Expert Rev Vaccines 2008; 7(4): 403–405

[120] Saha A, Rosewell A, Hayen A, MacIntyre CR, Qadri F. Improving immunization approaches to cholera. Expert Rev Vaccines 2017; 16(3): 235–248

[121] Lucas ME, Deen JL, von Seidlein L, Wang XY, Ampuero J, Puri M, Ali M, Ansaruzzaman M, Amos J, Macuamule A, Cavailler P, Guerin PJ, Mahoudeau C, Kahozi-Sangwa P, Chaignat CL, Barreto A, Songane FF, Clemens JD. Effectiveness of mass oral cholera vaccination in Beira, Mozambique. N Engl J Med 2005; 352(8): 757–767

[122] Khatib AM, Ali M, von Seidlein L, Kim DR, Hashim R, Reyburn R, Ley B, Thriemer K, Enwere G, Hutubessy R, Aguado MT, Kieny MP, Lopez AL, Wierzba TF, Ali SM, Saleh AA, Mukhopadhyay AK, Clemens J, Jiddawi MS, Deen J. Effectiveness of an oral cholera vaccine in Zanzibar: findings from a mass vaccination campaign and observational cohort study. Lancet Infect Dis 2012; 12(11): 837–844

[123] Saha A, Chowdhury MI, Khanam F, Bhuiyan MS, Chowdhury F, Khan AI, Khan IA, Clemens J, Ali M, Cravioto A, Qadri F. Safety and immunogenicity study of a killed bivalent (O1 and O139) whole-cell oral cholera vaccine Shanchol, in Bangladeshi adults and children as young as 1 year of age. Vaccine 2011; 29(46): 8285–8292

[124] Ivers LC, Teng JE, Lascher J, Raymond M, Weigel J, Victor N, Jerome JG, Hilaire IJ, Almazor CP, Ternier R, Cadet J. Use of oral cholera vaccine in Haiti: a rural demonstration project. Am J Trop Med Hyg 2013; 89(4): 617–624

[125] Ivers LC, Hilaire IJ, Teng JE, Almazor CP, Jerome JG, Ternier R, Boncy J, Buteau J, Murray MB, Harris JB, Franke MF. Effectiveness of reactive oral cholera vaccination in rural Haiti: a case-control study and bias-indicator analysis. Lancet Glob Health 2015; 3(3): e162–e168

[126] Rouzier V, Severe K, Juste MA, Peck M, Perodin C, Severe P, Deschamps MM, Verdier RI, Prince S, Francois J, Cadet JR. Cholera vaccination in urban Haiti. Am J Trop Med Hyg 2013; 89(4): 671–681

[127] Sévère K, Rouzier V, Anglade SB, Bertil C, Joseph P, Deroncelay A, Mabou MM, Wright PF, Guillaume FD, Pape JW. Effectiveness of oral cholera vaccine in Haiti: 37-month follow-up. Am J Trop Med Hyg 2016; 94(5): 1136–1142

[128] Qadri F, Ali M, Chowdhury F, Khan AI, Saha A, Khan IA, Begum YA, Bhuiyan TR, Chowdhury MI, Uddin MJ, Khan JA, Chowdhury AI, Rahman A, Siddique SA, Asaduzzaman M, Akter A, Khan A, Ae You Y, Siddik AU, Saha NC, Kabir A, Riaz BK, Biswas SK, Begum F, Unicomb L, Luby SP, Cravioto A, Clemens JD. Feasibility and effectiveness of oral cholera vaccine in an urban endemic setting in Bangladesh: a cluster randomised open-label trial. Lancet 2015; 386(10001): 1362–1371

[129] Bhattacharya SK, Sur D, Ali M, Kanungo S, You YA, Manna B, Sah B, Niyogi SK, Park JK, Sarkar B, Puri MK, Kim DR, Deen JL, Holmgren J, Carbis R, Dhingra MS, Donner A, Nair GB, Lopez AL, Wierzba TF, Clemens JD. 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 2013; 13(12): 1050–1056

[130] Phares CR, Date K, Travers P, Déglise C, Wongjindanon N, Ortega L, Bhuket PR. Mass vaccination with a two-dose oral cholera vaccine in a long-standing refugee camp, Thailand. Vaccine 2016; 34(1): 128–133

[131] Baik YO, Choi SK, Kim JW, Yang JS, Kim IY, Kim CW, Hong JH. Safety and immunogenicity assessment of an oral cholera vaccine through phase I clinical trial in Korea. J Korean Med Sci 2014; 29(4): 494–501

[132] Baik YO, Choi SK, Olveda RM, Espos RA, Ligsay AD, Montellano MB, Yeam JS, Yang JS, Park JY, Kim DR, Desai SN, Singh AP, Kim IY, Kim CW, Park S. A randomized, non-inferiority trial comparing two bivalent killed, whole cell, oral cholera vaccines (Euvichol vs Shanchol) in the Philippines. Vaccine 2015; 33(46): 6360–6365

[133] Sarker AR, Islam Z, Khan IA, Saha A, Chowdhury F, Khan AI, Cravioto A, Clemens JD, Qadri F, Khan JA. Estimating the cost of cholera-vaccine delivery from the societal point of view: a case of introduction of cholera vaccine in Bangladesh. Vaccine 2015; 33(38): 4916–4921

[134] Qadri F, Wierzba TF, Ali M, Chowdhury F, Khan AI, Saha A, Khan IA, Asaduzzaman M, Akter A, Khan A, Begum YA, Bhuiyan TR, Khanam F, Chowdhury MI, Islam T, Chowdhury AI, Rahman A, Siddique SA, You YA, Kim DR, Siddik AU, Saha NC, Kabir A, Cravioto A, Desai SN, Singh AP, Clemens JD. Efficacy of a single-dose, inactivated oral cholera vaccine in Bangladesh. N Engl J Med 2016; 374(18): 1723–1732

[135] Kanungo S, Desai SN, Nandy RK, Bhattacharya MK, Kim DR, Sinha A, Mahapatra T, Yang JS, Lopez AL, Manna B, Bannerjee B, Ali M, Dhingra MS, Chandra AM, Clemens JD, Sur D, Wierzba TF. Flexibility of oral cholera vaccine dosing—a randomized controlled trial measuring immune responses following alternative vaccination schedules in a cholera hyper-endemic zone. PLoS Negl Trop Dis 2015; 9(3): e0003574

[136] Moore SM, Lessler J. Optimal allocation of the limited oral cholera vaccine supply between endemic and epidemic settings. J R Soc Interface 2015; 12(111): 20150703

[137] Mahalanabis D, Ramamurthy T, Nair GB, Ghosh A, Shaikh S, Sen B, Thungapathra M, Ghosh RK, Pazhani GP, Nandy RK, Jana S, Bhattacharya SK. Randomized placebo controlled human volunteer trial of a live oral cholera vaccine VA1. 3 for safety and immune response. Vaccine 2009; 27(35): 4850–4856

[138] Kanungo S, Sen B, Ramamurthy T, Sur D, Manna B, Pazhani GP, Chowdhury G, Jhunjhunwala P, Nandy RK, Koley H, Bhattacharya MK, Gupta S, Goel G, Dey B, M T, Nair GB, Ghosh A, Mahalanabis D. Safety and immunogenicity of a live oral recombinant cholera vaccine VA1. 4: a randomized, placebo controlled trial in healthy adults in a cholera endemic area in Kolkata, India. PLoS One 2014; 9(7): e99381

[139] García HM, Thompson R, Valera R, Fando R, Fumane J, Jani I, Mirabal M, Armesto MI, Songane M, Luis S, Nzualo AM. A single dose of live-attenuated 638 Vibrio cholerae oral vaccine is safe and immunogenic in adult volunteers in Mozambique. Vaccimonitor 2011; 20(3): 1–8

[140] Alam MM, Bufano MK, Xu P, Kalsy A, Yu Y, Freeman YW, Sultana T, Rashu MR, Desai I, Eckhoff G, Leung DT, Charles RC, LaRocque RC, Harris JB, Clements JD, Calderwood SB, Qadri F, Vann WF, Kováč P, Ryan ET. Evaluation in mice of a conjugate vaccine for cholera made from Vibrio cholerae O1 (Ogawa) O-specific polysaccharide. PLoS Negl Trop Dis 2014; 8(2): e2683

[141] Sayeed MA, Bufano MK, Xu P, Eckhoff G, Charles RC, Alam MM, Sultana T, Rashu MR, Berger A, Gonzalez-Escobedo G, Mandlik A, Bhuiyan TR, Leung DT, LaRocque RC, Harris JB, Calderwood SB, Qadri F, Vann WF, Kováč P, Ryan ET. A cholera conjugate vaccine containing O-specific polysaccharide (OSP) of V. cholerae O1 Inaba and recombinant fragment of tetanus toxin heavy chain (OSP:rTTHc) induces serum, memory and lamina proprial responses against OSP and is protective in mice. PLoS Negl Trop Dis 2015; 9(7): e0003881

Compliance with ethics guidelines

Ali A. Rabaan declares no conflicts of interest. This manuscript is a review article and does not involve a research protocol requiring approval by the relevant institutional review board or ethics committee.

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