• 1.

    Faruque SM, Albert MJ, Mekalanos JJ, 1998. Epidemiology, genetics, and ecology of toxigenic Vibrio cholerae. Microbiol Mol Biol Rev 62: 1301.

  • 2.

    WHO/United Nations Children's Fund JMPfWSaS, 2013. Estimates on the Use of Water Sources and Sanitation Facilities. Available at: http://www.wssinfo.org/documents-links/documents/?tx_displaycontroller[type]=country_files. Accessed July 15, 2013.

    • Search Google Scholar
    • Export Citation
  • 3.

    Jenson D, Szabo V, Duke FH, 2011. Cholera in Haiti and other Caribbean regions, 19th Century. Emerg Infect Dis 17: 21302135.

  • 4.

    Barzilay EJ, Schaad N, Magloire R, Mung KS, Boncy J, Dahourou GA, Mintz ED, Steenland MW, Vertefeuille JF, Tappero JW, 2013. Cholera surveillance during the Haiti epidemic–the first 2 years. N Engl J Med 368: 599609.

    • Search Google Scholar
    • Export Citation
  • 5.

    Hill VR, Cohen N, Kahler AM, Jones JL, Bopp CA, Marano N, Tarr CL, Garrett NM, Boncy J, Henry A, Gomez GA, Wellman M, Curtis M, Freeman MM, Turnsek M, Benner RA, Dahourou G, Espey D, DePaola A, Tappero JW, Handzel T, Tauxe RV, 2011. Toxigenic Vibrio cholerae O1 in water and seafood, Haiti. Emerg Infect Dis 17: 21472150.

    • Search Google Scholar
    • Export Citation
  • 6.

    Alam MT, Weppelmann TA, Weber CD, Johnson JA, Rashid MH, Birch CS, Brumback BA, de Rochars V, Morris JG, Ali A, 2014. Monitoring water sources for environmental reservoirs of toxigenic Vibrio cholerae O1, Haiti. Emerg Infect Dis 20: 356363.

    • Search Google Scholar
    • Export Citation
  • 7.

    Huq A, Small EB, West PA, Huq MI, Rahman R, Colwell RR, 1983. Ecological relationships between Vibrio cholerae and planktonic crustacean copepods. Appl Environ Microbiol 45: 275283.

    • Search Google Scholar
    • Export Citation
  • 8.

    Tamplin ML, Gauzens AL, Huq A, Sack DA, Colwell RR, 1990. Attachment of Vibrio cholerae serogroup O1 to zooplankton and phytoplankton of Bangladesh waters. Appl Environ Microbiol 56: 19771980.

    • Search Google Scholar
    • Export Citation
  • 9.

    Colwell RR, Brayton PR, Grimes DJ, Roszak DB, Huq SA, Palmer LM, 1985. Viable but non-culturable Vibrio cholerae and related pathogens in the environment–implications for release of genetically engineered microorganisms. Biotechnology (N Y) 3: 817820.

    • Search Google Scholar
    • Export Citation
  • 10.

    Brayton PR, Tamplin ML, Huq A, Colwell RR, 1987. Enumeration of Vibrio cholerae O1 in Bangladesh waters by fluorescent antibody direct viable count. Appl Environ Microbiol 53: 28622865.

    • Search Google Scholar
    • Export Citation
  • 11.

    Chowdhury MA, Xu B, Montilla R, Hasan JA, Huq A, Colwell RR, 1995. A simplified immunofluorescence technique for detection of viable cells of Vibrio cholerae O1 and O139. J Microbiol Methods 24: 165170.

    • Search Google Scholar
    • Export Citation
  • 12.

    Blackstone GM, Nordstrom JL, Bowen MD, Meyer RF, Imbro P, DePaola A, 2007. Use of a real time PCR assay for detection of the ctxA gene of Vibrio cholerae in an environmental survey of Mobile Bay. J Microbiol Methods 68: 254259.

    • Search Google Scholar
    • Export Citation
  • 13.

    Smith CM, Hill VR, 2009. Dead-end hollow-fiber ultrafiltration for recovery of diverse microbes from water. Appl Environ Microbiol 75: 52845289.

    • Search Google Scholar
    • Export Citation
  • 14.

    Mull B, Hill VR, 2012. Recovery of diverse microbes in high turbidity surface water samples using dead-end ultrafiltration. J Microbiol Methods 91: 429433.

    • Search Google Scholar
    • Export Citation
  • 15.

    Alam M, Sadique A, Nur AH, Bhuiyan NA, Nair GB, Siddique AK, Sack DA, Ahsan S, Huq A, Sack RB, Colwell RR, 2006. Effect of transport at ambient temperature on detection and isolation of Vibrio cholerae from environmental samples. Appl Environ Microbiol 72: 21852190.

    • Search Google Scholar
    • Export Citation
  • 16.

    Huq A, Haley BJ, Taviani E, Chen A, Hasan NA, Colwell RR, 2012. Detection, isolation, and identification of Vibrio cholerae from the environment. Curr Prot Microbiol 26: 6A.5.16A.5.51.

    • Search Google Scholar
    • Export Citation
  • 17.

    Hill VR, Kahler AM, Jothikumar N, Johnson TB, Hahn D, Cromeans TL, 2007. Multistate evaluation of an ultrafiltration-based procedure for simultaneous recovery of enteric microbes in 100-liter tap water samples. Appl Environ Microbiol 73: 42184225.

    • Search Google Scholar
    • Export Citation
  • 18.

    Bauer A, Rorvik LM, 2007. A novel multiplex PCR for the identification of Vibrio parahaemolyticus, Vibrio cholerae and Vibrio vulnificus. Lett Appl Microbiol 45: 371375.

    • Search Google Scholar
    • Export Citation
  • 19.

    Hoshino K, Yamasaki S, Mukhopadhyay AK, Chakraborty S, Basu A, Bhattacharya SK, Nair GB, Shimada T, Takeda Y, 1998. Development and evaluation of a multiplex PCR assay for rapid detection of toxigenic Vibrio cholerae O1 and O139. FEMS Immunol Med Microbiol 20: 201207.

    • Search Google Scholar
    • Export Citation
  • 20.

    Talkington D, Bopp C, Tarr C, Parsons MB, Dahourou G, Freeman M, Joyce K, Turnsek M, Garrett N, Humphrys M, Gomez G, Stroika S, Boncy J, Ochieng B, Oundo J, Klena J, Smith A, Keddy K, Gerner-Smidt P, 2011. Characterization of toxigenic Vibrio cholerae from Haiti, 2010–2011. Emerg Infect Dis 17: 21222129.

    • Search Google Scholar
    • Export Citation
  • 21.

    Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S, 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 27312739.

    • Search Google Scholar
    • Export Citation
  • 22.

    Kislyuk AO, Katz LS, Agrawal S, Hagen MS, Conley AB, Jayaraman P, Nelakuditi V, Humphrey JC, Sammons SA, Govil D, Mair RD, Tatti KM, Tondella ML, Harcourt BH, Mayer LW, Jordan IK, 2010. A computational genomics pipeline for prokaryotic sequencing projects. Bioinformatics 26: 18191826.

    • Search Google Scholar
    • Export Citation
  • 23.

    Darling AC, Mau B, Blattner FR, Perna NT, 2004. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14: 13941403.

    • Search Google Scholar
    • Export Citation
  • 24.

    Edgar RC, 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 24602461.

  • 25.

    Edgar RC, 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 17921797.

  • 26.

    Stamatakis A, 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 26882690.

    • Search Google Scholar
    • Export Citation
  • 27.

    Liang KY, Zeger SL, 1986. Longitudinal data analysis using generalized linear models. Biometrika 73: 1322.

  • 28.

    Zeger SL, Liang KY, 1986. The analysis of discrete and continuous longitudinal data. Biometrics 42: 121130.

  • 29.

    WHO, 2011. Guidelines for Drinking-Water Quality. Geneva: World Health Organization Library Cataloguing-in-Publication Data.

  • 30.

    Katz LS, Petkau A, Beaulaurier J, Tyler S, Antonova ES, Turnsek MA, Guo Y, Wang S, Paxinos EE, Orata F, Gladney LM, Stroika S, Folster JP, Rowe L, Freeman MM, Knox N, Frace M, Boncy J, Graham M, Hammer BK, Boucher Y, Bashir A, Hanage WP, Van Domselaar G, Tarr CL, 2013. Evolutionary dynamics of Vibrio cholerae O1 following a single-source introduction to Haiti. MBio 4: e00398.

    • Search Google Scholar
    • Export Citation
  • 31.

    Reimer AR, Van Domselaar G, Stroika S, Walker M, Kent H, Tarr C, Talkington D, Rowe L, Olsen-Rasmussen M, Frace M, Sammons S, Dahourou GA, Boncy J, Smith AM, Mabon P, Petkau A, Graham M, Gilmour MW, Gerner-Smidt P, Task VC, 2011. Comparative genomics of Vibrio cholerae from Haiti, Asia, and Africa. Emerg Infect Dis 17: 21132121.

    • Search Google Scholar
    • Export Citation
  • 32.

    Huq A, Colwell RR, Rahman R, Ali A, Chowdhury MA, Parveen S, Sack DA, Russekcohen E, 1990. Detection of Vibrio cholerae O1 in the aquatic environment by fluorescent monoclonal antibody and culture methods. Appl Environ Microbiol 56: 23702373.

    • Search Google Scholar
    • Export Citation
  • 33.

    Gil AI, Louis VR, Rivera IN, Lipp E, Huq A, Lanata CF, Taylor DN, Russek-Cohen E, Choopun N, Sack RB, Colwell RR, 2004. Occurrence and distribution of Vibrio cholerae in the coastal environment of Peru. Environ Microbiol 6: 699706.

    • Search Google Scholar
    • Export Citation
  • 34.

    Colwell RR, Huq A, 1994. Environmental reservoir of Vibrio cholerae–the causative agent of cholera. Wilson ME, Levins R, Spielman A, eds. Disease in Evolution: Global Changes and Emergence of Infectious Diseases. New York: New York Academy Sciences, 4454.

    • Search Google Scholar
    • Export Citation
  • 35.

    Baron S, Lesne J, Moore S, Rossignol E, Rebaudet S, Gazin P, Barrais R, Magloire R, Boncy J, Piarroux R, 2013. No evidence of significant levels of toxigenic V. cholerae O1 in the Haitian aquatic environment during the 2012 rainy season. PLoS Curr 13: 5.

    • Search Google Scholar
    • Export Citation
  • 36.

    Waldor MK, Mekalanos JJ, 1996. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272: 19101914.

  • 37.

    Chakraborty S, Mukhopadhyay AK, Bhadra RK, Ghosh AN, Mitra R, Shimada T, Yamasaki S, Faruque SM, Takeda Y, Colwell RR, Nair GB, 2000. Virulence genes in environmental strains of Vibrio cholerae. Appl Environ Microbiol 66: 40224028.

    • Search Google Scholar
    • Export Citation
  • 38.

    Faruque SM, Chowdhury N, Kamruzzaman M, Dziejman M, Rahman MH, Sack DA, Nair GB, Mekalanos JJ, 2004. Genetic diversity and virulence potential of environmental Vibrio cholerae population in a cholera-endemic area. Proc Natl Acad Sci USA 101: 21232128.

    • Search Google Scholar
    • Export Citation
  • 39.

    Maiti D, Das B, Saha A, Nandy RK, Nair GB, Bhadra RK, 2006. Genetic organization of pre-CTX and CTX prophages in the genome of an environmental Vibrio cholerae non-O1, non-O139 strain. Microbiology-Sgm 152: 36333641.

    • Search Google Scholar
    • Export Citation
  • 40.

    Morris GK, Merson MH, Huq I, Kibrya AK, Black R, 1979. Comparison of four plating media for isolating Vibrio cholerae. J Clin Microbiol 9: 7983.

  • 41.

    Taylor JA, Barrow GI, 1981. A non-pathogenic vibrio for the routine quality control of TCBS cholera medium. J Clin Pathol 34: 208212.

 
 
 
 

 

 
 
 

 

 

 

 

 

 

Environmental Surveillance for Toxigenic Vibrio cholerae in Surface Waters of Haiti

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  • Centers for Disease Control and Prevention, Atlanta, Georgia; University of Maryland, College Park, Maryland; Haitian Ministry of Public Health and Population, National Public Health Laboratory, Port-au-Prince, Haiti

Epidemic cholera was reported in Haiti in 2010, with no information available on the occurrence or geographic distribution of toxigenic Vibrio cholerae in Haitian waters. In a series of field visits conducted in Haiti between 2011 and 2013, water and plankton samples were collected at 19 sites. Vibrio cholerae was detected using culture, polymerase chain reaction, and direct viable count methods (DFA-DVC). Cholera toxin genes were detected by polymerase chain reaction in broth enrichments of samples collected in all visits except March 2012. Toxigenic V. cholerae was isolated from river water in 2011 and 2013. Whole genome sequencing revealed that these isolates were a match to the outbreak strain. The DFA-DVC tests were positive for V. cholerae O1 in plankton samples collected from multiple sites. Results of this survey show that toxigenic V. cholerae could be recovered from surface waters in Haiti more than 2 years after the onset of the epidemic.

Author Notes

* Address correspondence to Vincent R. Hill, Centers for Disease Control and Prevention, 1600 Clifton Road, NE, Mailstop D-66, Atlanta, GA 30329. E-mail: vhill@cdc.gov

Financial support: Centers for Disease Control and Prevention, partial support at the University of Maryland came from NIH grant no. 2RO1A1039129-11A2 and NSF grant no. 0813066.

Authors' addresses: Amy M. Kahler, Bonnie J. Mull, Cheryl L. Tarr, Maryann Turnsek, Lee S. Katz, Michael S. Humphrys, Gordana Derado, and Vincent R. Hill, Division of Foodborne, Waterborne, and Environmental Diseases, Centers for Disease Control and Prevention, Atlanta, GA, E-mails: akahler@cdc.gov, bonniejmull@gmail.com, ctarr@cdc.gov, HUD4@cdc.gov, GZU2@cdc.gov, msh06f@gmail.com, uwx8@cdc.gov, and vhill@cdc.gov. Bradd J. Haley, Arlene Chen, Rita R. Colwell, and Anwar Huq, Maryland Pathogen Research Institute and Center for Bioinformatics and Computational Biology, University of Maryland, College Park, MD, E-mails: bradd.haley@gmail.com, achen87@umd.edu, rcolwell@umiacs.umd.edu, and huqanwar@gmail.com. Nicole Freeman and Jacques Boncy, National Public Health Laboratory, Haitian Ministry of Public Health and Population, Port-au-Prince, Haiti, E-mails: nicolemfreeman@gmail.com and jboncy2001@yahoo.fr.

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