• 1.

    Zuckerman JN, Rombo L, Fisch A, 2007. The true burden and risk of cholera: implications for prevention and control. Lancet Infect Dis 7: 521530.

    • Search Google Scholar
    • Export Citation
  • 2.

    Levine MM, Black RE, Clements ML, Cisneros L, Nalin DR, Young CR, 1981. Duration of infection-derived immunity to cholera. J Infect Dis 143: 818820.

  • 3.

    Woodward WE, 1971. Cholera reinfection in man. J Infect Dis 123: 6166.

  • 4.

    Glass RI, Becker S, Huq MI, Stoll BJ, Khan MU, Merson MH, Lee JV, Black RE, 1982. Endemic cholera in rural Bangladesh, 1966–1980. Am J Epidemiol 116: 959970.

    • Search Google Scholar
    • Export Citation
  • 5.

    Ali M, Emch M, Park JK, Yunus M, Clemens J, 2011. Natural cholera infection-derived immunity in an endemic setting. J Infect Dis 204: 912918.

  • 6.

    Holmgren J, Svennerholm AM, 1977. Mechanisms of disease and immunity in cholera: a review. J Infect Dis 136 (Suppl): S105S112.

  • 7.

    Harris JB, Larocque RC, Chowdhury F, Khan AI, Logvinenko T, Faruque AS, Ryan ET, Qadri F, Calderwood SB, 2008. Susceptibility to Vibrio cholerae infection in a cohort of household contacts of patients with cholera in Bangladesh. PLoS Negl Trop Dis 2: e221.

    • Search Google Scholar
    • Export Citation
  • 8.

    Tacket CO, Cohen MB, Wasserman SS, Losonsky G, Livio S, Kotloff K, Edelman R, Kaper JB, Cryz SJ, Giannella RA, Schiff G, Levine MM, 1999. Randomized, double-blind, placebo-controlled, multicentered trial of the efficacy of a single dose of live oral cholera vaccine CVD 103-HgR in preventing cholera following challenge with Vibrio cholerae O1 El tor inaba three months after vaccination. Infect Immun 67: 63416345.

    • Search Google Scholar
    • Export Citation
  • 9.

    Saha D, LaRocque RC, Khan AI, Harris JB, Begum YA, Akramuzzaman SM, Faruque AS, Ryan ET, Qadri F, Calderwood SB, 2004. Incomplete correlation of serum vibriocidal antibody titer with protection from Vibrio cholerae infection in urban Bangladesh. J Infect Dis 189: 23182322.

    • Search Google Scholar
    • Export Citation
  • 10.

    Glass RI, Svennerholm AM, Khan MR, Huda S, Huq MI, Holmgren J, 1985. Seroepidemiological studies of El Tor cholera in Bangladesh: association of serum antibody levels with protection. J Infect Dis 151: 236242.

    • Search Google Scholar
    • Export Citation
  • 11.

    Mosley WH, Ahmad S, Benenson AS, Ahmed A, 1968. The relationship of vibriocidal antibody titre to susceptibility to cholera in family contacts of cholera patients. Bull World Health Organ 38: 777785.

    • Search Google Scholar
    • Export Citation
  • 12.

    Clements ML, Levine MM, Young CR, Black RE, Lim YL, Robins-Browne RM, Craig JP, 1982. Magnitude, kinetics, and duration of vibriocidal antibody responses in North Americans after ingestion of Vibrio cholerae. J Infect Dis 145: 465473.

    • Search Google Scholar
    • Export Citation
  • 13.

    Qadri F, Azim T, Chowdhury A, Hossain J, Sack RB, Albert MJ, 1994. Production, characterization, and application of monoclonal antibodies to Vibrio cholerae O139 synonym Bengal. Clin Diagn Lab Immunol 1: 5154.

    • Search Google Scholar
    • Export Citation
  • 14.

    World Health Organization, 2005. The Treatment of Diarrhea: A Manual for Physicians and Other Senior Health Workers, 4th Ed. Geneva, Switzerland: World Health Organization.

    • Search Google Scholar
    • Export Citation
  • 15.

    Qadri F, Wenneras C, Albert MJ, Hossain J, Mannoor K, Begum YA, Mohi G, Salam MA, Sack RB, Svennerholm AM, 1997. Comparison of immune responses in patients infected with Vibrio cholerae O139 and O1. Infect Immun 65: 35713576.

    • Search Google Scholar
    • Export Citation
  • 16.

    Kendall EA, Tarique AA, Hossain A, Alam MM, Arifuzzaman M, Akhtar N, Chowdhury F, Khan AI, Larocque RC, Harris JB, Ryan ET, Qadri F, Calderwood SB, 2010. Development of immunoglobulin M memory to both a T-cell-independent and a T-cell-dependent antigen following infection with Vibrio cholerae O1 in Bangladesh. Infect Immun 78: 253259.

    • Search Google Scholar
    • Export Citation
  • 17.

    Mosley WH, Benenson AS, Barui R, 1968. A serological survey for cholera antibodies in rural east Pakistan. 1. The distribution of antibody in the control population of a cholera-vaccine field-trial area and the relation of antibody titre to the pattern of endemic cholera. Bull World Health Organ 38: 327334.

    • Search Google Scholar
    • Export Citation
  • 18.

    Mosley WH, McCormack WM, Ahmed A, Chowdhury AK, Barui RK, 1969. Report of the 1966–67 cholera vaccine field trial in rural East Pakistan. 2. Results of the serological surveys in the study population—the relationship of case rate to antibody titre and an estimate of the inapparent infection rate with Vibrio cholerae. Bull World Health Organ 40: 187197.

    • Search Google Scholar
    • Export Citation
  • 19.

    Gangarosa EJ, DeWitt WE, Feeley JC, Adams MR, 1970. Significance of vibriocidal antibodies with regard to immunity to cholera. J Infect Dis 121 (Suppl 121): 36.

    • Search Google Scholar
    • Export Citation
  • 20.

    Morris JG Jr, Takeda T, Tall BD, Losonsky GA, Bhattacharya SK, Forrest BD, Kay BA, Nishibuchi M, 1990. Experimental non-O group 1 Vibrio cholerae gastroenteritis in humans. J Clin Invest 85: 697705.

    • Search Google Scholar
    • Export Citation
  • 21.

    Lefkowitz A, Fout GS, Losonsky G, Wasserman SS, Israel E, Morris JG Jr, 1992. A serosurvey of pathogens associated with shellfish: prevalence of antibodies to Vibrio species and Norwalk virus in the Chesapeake Bay region. Am J Epidemiol 135: 369380.

    • Search Google Scholar
    • Export Citation
  • 22.

    Chowdhury F, Begum YA, Alam MM, Khan AI, Ahmed T, Bhuiyan MS, Harris JB, LaRocque RC, Faruque AS, Endtz H, Ryan ET, Cravioto A, Svennerholm AM, Calderwood SB, Qadri F, 2008. Concomitant enterotoxigenic Escherichia coli infection induces increased immune responses to Vibrio cholerae O1 antigens in patients with cholera in Bangladesh. Infect Immun 78: 21172124.

    • Search Google Scholar
    • Export Citation
  • 23.

    Qadri F, Mohi G, Hossain J, Azim T, Khan AM, Salam MA, Sack RB, Albert MJ, Svennerholm AM, 1995. Comparison of the vibriocidal antibody response in cholera due to Vibrio cholerae O139 Bengal with the response in cholera due to Vibrio cholerae O1. Clin Diagn Lab Immunol 2: 685688.

    • Search Google Scholar
    • Export Citation
  • 24.

    Weil AA, Khan AI, Chowdhury F, Larocque RC, Faruque AS, Ryan ET, Calderwood SB, Qadri F, Harris JB, 2009. Clinical outcomes in household contacts of patients with cholera in Bangladesh. Clin Infect Dis 49: 14731479.

    • Search Google Scholar
    • Export Citation
  • 25.

    Dalsgaard A, Skov MN, Serichantalergs O, Echeverria P, Meza R, Taylor DN, 1997. Molecular evolution of Vibrio cholerae O1 strains isolated in Lima, Peru, from 1991 to 1995. J Clin Microbiol 35: 11511156.

    • Search Google Scholar
    • Export Citation
  • 26.

    Longini IM Jr, Yunus M, Zaman K, Siddique AK, Sack RB, Nizam A, 2002. Epidemic and endemic cholera trends over a 33-year period in Bangladesh. J Infect Dis 186: 246251.

    • Search Google Scholar
    • Export Citation
  • 27.

    Harris AM, Chowdhury F, Begum YA, Khan AI, Faruque AS, Svennerholm AM, Harris JB, Ryan ET, Cravioto A, Calderwood SB, Qadri F, 2008. Shifting prevalence of major diarrheal pathogens in patients seeking hospital care during floods in 1998, 2004, and 2007 in Dhaka, Bangladesh. Am J Trop Med Hyg 79: 708714.

    • Search Google Scholar
    • Export Citation
  • 28.

    Khan AI, Chowdhury F, Harris JB, Larocque RC, Faruque AS, Ryan ET, Calderwood SB, Qadri F, 2010. Comparison of clinical features and immunological parameters of patients with dehydrating diarrhoea infected with Inaba or Ogawa serotypes of Vibrio cholerae O1. Scand J Infect Dis 42: 4856.

    • Search Google Scholar
    • Export Citation
  • 29.

    Leung DT, Rahman MA, Mohasin M, Riyadh MA, Patel SM, Alam MM, Chowdhury F, Khan AI, Kalivoda EJ, Aktar A, Bhuiyan MS, LaRocque RC, Harris JB, Calderwood SB, Qadri F, Ryan ET, 2011. Comparison of memory B cell, antibody-secreting cell, and plasma antibody responses in young children, older children, and adults with infection caused by Vibrio cholerae O1 El Tor Ogawa in Bangladesh. Clin Vaccine Immunol 18: 13171325.

    • Search Google Scholar
    • Export Citation
  • 30.

    Stroeher UH, Karageorgos LE, Morona R, Manning PA, 1992. Serotype conversion in Vibrio cholerae O1. Proc Natl Acad Sci USA 89: 25662570.

 
 
 

 

 
 
 

 

 

 

 

 

 

Frequency of Reexposure to Vibrio cholerae O1 Evaluated by Subsequent Vibriocidal Titer Rise after an Episode of Severe Cholera in a Highly Endemic Area in Bangladesh

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  • Department of Medicine, Harvard Medical School, Boston, Massachusetts; Centre for Vaccine Sciences, International Centre for Diarrhoeal Disease Research, Bangladesh Dhaka, Bangladesh; Division of Infectious Diseases, Massachusetts General Hospital, Boston, Massachusetts; Department of Pediatrics, Harvard Medical School, Boston, Massachusetts; Department of Immunology and Infectious Diseases, Harvard School of Public Health, Boston, Massachusetts; Department of Microbiology and Immunobiology, Harvard Medical School, Boston, Massachusetts

Vibriocidal antibody is a marker of recent exposure to Vibrio cholerae O1 infection. We examined vibriocidal titers for 1 year after an episode of severe cholera in patients in Dhaka, Bangladesh; 16 of 53 (30%) patients had a fourfold or greater increase in vibriocidal titer between 6 and 12 months after an episode of severe cholera, suggesting reexposure to the organism. Among patients with rises in titers during follow-up, the patients initially infected with serotype Ogawa had earlier rises in titer than the patients initially infected with serotype Inaba. These data and others suggest that an episode of severe cholera protects against symptomatic disease for several years, but reexposure to the organism occurs frequently in an endemic area, with immunological boosts beginning as early as 6 months after severe disease. Repeated exposures to V. cholerae in endemic areas may be a necessary component for long-lasting protection against severe disease.

Author Notes

* Address correspondence to Stephen B. Calderwood, Division of Infectious Diseases, Massachusetts General Hospital, 55 Fruit Street, Boston, MA 02481. E-mail: scalderwood@partners.org† These authors are co-first authors.‡ These authors are co-senior authors.

Financial support: This work was supported by a Partners Healthcare Center of Expertise in Global and Humanitarian Health Travel Grant (to A.A.W.); Fogarty International Clinical Research Scholars Award R24 TW007988 (to F.C. and A.I.K.) from the Fogarty International Center; American Recovery and Reinvestment Act (ARRA) Post-Doctoral Fellowship in Global Infectious Diseases TW05572 (to D.T.L.); a Postdoctoral Fellowship in Tropical Infectious Diseases from the American Society for Tropical Medicine and Hygiene—Burroughs Wellcome Fund (to D.T.L.); the Harvard Initiative for Global Health Post-Doctoral Fellowship in Global Infectious Diseases (to D.T.L); a Training Grant in Vaccine Development and Public Health TW005572 (to T.U., E.T.R., and F.Q.); Career Development Awards K08 AI089721 (to R.C.C.), K01 TW07144 (to R.C.L.), and K01 TW07409 (to J.B.H.); a Physician Scientist Early Career Award from the Howard Hughes Medical Institute (to R.C.L.); National Institutes of Health Grants U01 AI077883 (to E.T.R.), AI058935 (to E.T.R. and S.B.C.), and R03 AI063079 (to F.Q.); and the Swedish Agency for International Development and Cooperation (F.Q.).

Authors' addresses: Ana A. Weil, Department of Medicine, Massachusetts General Hospital, Boston, MA, E-mail: aweil@partners.org. Fahima Chowdhury, Ashraful I. Khan, Daniel T. Leung, Taher Uddin, Yasmin Ara Begum, Nirod Chandra Saha, and Firdausi Qadri, Centre for Vaccine Sciences, International Centre for Diarrhoeal Disease Research, Bangladesh, Dhaka, Bangladesh, E-mails: fchowdhury@icddrb.org, ashrafk@icddrb.org, dleung@partners.org, taher_imm@icddrb.org, yasmin@icddrb.org, nirod@icddrb.org, and fqadri@icddrb.org. Richelle C. Charles, Regina C. LaRocque, Jason B. Harris, Edward T. Ryan, and Stephen B. Calderwood, Division of Infectious Diseases, Massachusetts General Hospital, Boston, MA, E-mails: rccharles@partners.org, rclarocque@partners.org, jbharris@partners.org, etryan@partners.org, and scalderwood@partners.org.

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