Skip to main content
PMC home page
Infection and Immunity logoLink to Infection and Immunity
. 1997 Sep;65(9):3571–3576. doi: 10.1128/iai.65.9.3571-3576.1997

Comparison of immune responses in patients infected with Vibrio cholerae O139 and O1.

F Qadri 1, C Wennerås 1, M J Albert 1, J Hossain 1, K Mannoor 1, Y A Begum 1, G Mohi 1, M A Salam 1, R B Sack 1, A M Svennerholm 1
PMCID: PMC175508  PMID: 9284121

Abstract

Vibrio cholerae O139 has recently emerged as the second etiologic agent of cholera in Asia. A study was carried out to evaluate the induction of specific immune responses to the organism in V. cholerae O139-infected patients. The immune responses to V. cholerae O139 Bengal were studied in patients by measuring antibody-secreting cells (ASC), as well as vibriocidal and antitoxic antibodies in the circulation. These responses were compared with those in patients with V. cholerae O1 disease. Strong immunoglobulin A (IgA) and IgM ASC responses were seen against the homologous lipopolysaccharide or serogroup of V. cholerae. The magnitude and isotype of the responses were similar in O139- and O1-infected patients. Vibriocidal antibody responses were seen against bacteria of the homologous but not heterologous serogroup, and these responses reflect the lack of cross-protection between the infections caused by the two serogroups. The two groups of patients showed comparable cholera toxin-specific ASC responses, with the IgG isotype dominating over the IgA isotype, as well as comparable antitoxic immune responses in plasma. These results suggest that despite having a polysaccharide capsule, V. cholerae O139 induces systemic and intestine-derived ASC responses in peripheral blood comparable to those seen in patients with V. cholerae O1 disease.

Full Text

The Full Text of this article is available as a PDF (143.5 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Albert M. J., Alam K., Ansaruzzaman M., Qadri F., Sack R. B. Lack of cross-protection against diarrhea due to Vibrio cholerae O139 (Bengal strain) after oral immunization of rabbits with V. cholerae O1 vaccine strain CVD103-HgR. J Infect Dis. 1994 Jan;169(1):230–231. doi: 10.1093/infdis/169.1.230. [DOI] [PubMed] [Google Scholar]
  2. Albert M. J. Epidemiology & molecular biology of Vibrio cholerae O139 Bengal. Indian J Med Res. 1996 Jul;104:14–27. [PubMed] [Google Scholar]
  3. Albert M. J., Siddique A. K., Islam M. S., Faruque A. S., Ansaruzzaman M., Faruque S. M., Sack R. B. Large outbreak of clinical cholera due to Vibrio cholerae non-O1 in Bangladesh. Lancet. 1993 Mar 13;341(8846):704–704. doi: 10.1016/0140-6736(93)90481-u. [DOI] [PubMed] [Google Scholar]
  4. BENENSON A. S., ISLAM M. R., GREENOUGH W. B., 3rd RAPID IDENTIFICATION OF VIBRIO CHOLERAE BY DARKFIELD MICROSCOPY. Bull World Health Organ. 1964;30:827–831. [PMC free article] [PubMed] [Google Scholar]
  5. Coster T. S., Killeen K. P., Waldor M. K., Beattie D. T., Spriggs D. R., Kenner J. R., Trofa A., Sadoff J. C., Mekalanos J. J., Taylor D. N. Safety, immunogenicity, and efficacy of live attenuated Vibrio cholerae O139 vaccine prototype. Lancet. 1995 Apr 15;345(8955):949–952. doi: 10.1016/s0140-6736(95)90698-3. [DOI] [PubMed] [Google Scholar]
  6. Cox A. D., Perry M. B. Structural analysis of the O-antigen-core region of the lipopolysaccharide from Vibrio cholerae O139. Carbohydr Res. 1996 Aug 26;290(1):59–65. doi: 10.1016/0008-6215(96)00131-0. [DOI] [PubMed] [Google Scholar]
  7. Czerkinsky C., Moldoveanu Z., Mestecky J., Nilsson L. A., Ouchterlony O. A novel two colour ELISPOT assay. I. Simultaneous detection of distinct types of antibody-secreting cells. J Immunol Methods. 1988 Nov 25;115(1):31–37. doi: 10.1016/0022-1759(88)90306-7. [DOI] [PubMed] [Google Scholar]
  8. Czerkinsky C., Prince S. J., Michalek S. M., Jackson S., Russell M. W., Moldoveanu Z., McGhee J. R., Mestecky J. IgA antibody-producing cells in peripheral blood after antigen ingestion: evidence for a common mucosal immune system in humans. Proc Natl Acad Sci U S A. 1987 Apr;84(8):2449–2453. doi: 10.1073/pnas.84.8.2449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Czerkinsky C., Svennerholm A. M., Holmgren J. Induction and assessment of immunity at enteromucosal surfaces in humans: implications for vaccine development. Clin Infect Dis. 1993 Mar;16 (Suppl 2):S106–S116. doi: 10.1093/clinids/16.supplement_2.s106. [DOI] [PubMed] [Google Scholar]
  10. Favre D., Cryz S. J., Jr, Viret J. F. Construction and characterization of a potential live oral carrier-based vaccine against Vibrio cholerae O139. Infect Immun. 1996 Sep;64(9):3565–3570. doi: 10.1128/iai.64.9.3565-3570.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Glass R. I., Svennerholm A. M., Khan M. R., Huda S., Huq M. I., Holmgren J. Seroepidemiological studies of El Tor cholera in Bangladesh: association of serum antibody levels with protection. J Infect Dis. 1985 Feb;151(2):236–242. doi: 10.1093/infdis/151.2.236. [DOI] [PubMed] [Google Scholar]
  12. Hisatsune K., Kondo S., Isshiki Y., Iguchi T., Kawamata Y., Shimada T. O-antigenic lipopolysaccharide of Vibrio cholerae O139 Bengal, a new epidemic strain for recent cholera in the Indian subcontinent. Biochem Biophys Res Commun. 1993 Nov 15;196(3):1309–1315. doi: 10.1006/bbrc.1993.2395. [DOI] [PubMed] [Google Scholar]
  13. Jertborn M., Svennerholm A. M., Holmgren J. Intestinal and systemic immune responses in humans after oral immunization with a bivalent B subunit-O1/O139 whole cell cholera vaccine. Vaccine. 1996 Oct;14(15):1459–1465. doi: 10.1016/s0264-410x(96)00071-0. [DOI] [PubMed] [Google Scholar]
  14. Jertborn M., Svennerholm A. M., Holmgren J. Saliva, breast milk, and serum antibody responses as indirect measures of intestinal immunity after oral cholera vaccination or natural disease. J Clin Microbiol. 1986 Aug;24(2):203–209. doi: 10.1128/jcm.24.2.203-209.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Johnson J. A., Salles C. A., Panigrahi P., Albert M. J., Wright A. C., Johnson R. J., Morris J. G., Jr Vibrio cholerae O139 synonym bengal is closely related to Vibrio cholerae El Tor but has important differences. Infect Immun. 1994 May;62(5):2108–2110. doi: 10.1128/iai.62.5.2108-2110.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jonson G., Osek J., Svennerholm A. M., Holmgren J. Immune mechanisms and protective antigens of Vibrio cholerae serogroup O139 as a basis for vaccine development. Infect Immun. 1996 Sep;64(9):3778–3785. doi: 10.1128/iai.64.9.3778-3785.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kantele A. M., Takanen R., Arvilommi H. Immune response to acute diarrhea seen as circulating antibody-secreting cells. J Infect Dis. 1988 Nov;158(5):1011–1016. doi: 10.1093/infdis/158.5.1011. [DOI] [PubMed] [Google Scholar]
  18. Kantele A., Arvilommi H., Jokinen I. Specific immunoglobulin-secreting human blood cells after peroral vaccination against Salmonella typhi. J Infect Dis. 1986 Jun;153(6):1126–1131. doi: 10.1093/infdis/153.6.1126. [DOI] [PubMed] [Google Scholar]
  19. Li A., Kärnell A., Huan P. T., Cam P. D., Minh N. B., Trâm L. N., Quy N. P., Trach D. D., Karlsson K., Lindberg G. Safety and immunogenicity of the live oral auxotrophic Shigella flexneri SFL124 in adult Vietnamese volunteers. Vaccine. 1993;11(2):180–189. doi: 10.1016/0264-410x(93)90015-p. [DOI] [PubMed] [Google Scholar]
  20. Losonsky G. A., Tacket C. O., Wasserman S. S., Kaper J. B., Levine M. M. Secondary Vibrio cholerae-specific cellular antibody responses following wild-type homologous challenge in people vaccinated with CVD 103-HgR live oral cholera vaccine: changes with time and lack of correlation with protection. Infect Immun. 1993 Feb;61(2):729–733. doi: 10.1128/iai.61.2.729-733.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. MONSUR K. A. A highly selective gelatin-taurocholate-tellurite medium for the isolation of Vibrio cholerae. Trans R Soc Trop Med Hyg. 1961 Sep;55:440–442. doi: 10.1016/0035-9203(61)90090-6. [DOI] [PubMed] [Google Scholar]
  22. McDermott M. R., Bienenstock J. Evidence for a common mucosal immunologic system. I. Migration of B immunoblasts into intestinal, respiratory, and genital tissues. J Immunol. 1979 May;122(5):1892–1898. [PubMed] [Google Scholar]
  23. Morris J. G., Jr, Losonsky G. E., Johnson J. A., Tacket C. O., Nataro J. P., Panigrahi P., Levin M. M. Clinical and immunologic characteristics of Vibrio cholerae O139 Bengal infection in North American volunteers. J Infect Dis. 1995 Apr;171(4):903–908. doi: 10.1093/infdis/171.4.903. [DOI] [PubMed] [Google Scholar]
  24. Orr N., Robin G., Lowell G., Cohen D. Presence of specific immunoglobulin A-secreting cells in peripheral blood after natural infection with Shigella sonnei. J Clin Microbiol. 1992 Aug;30(8):2165–2168. doi: 10.1128/jcm.30.8.2165-2168.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Qadri F., Azim T., Chowdhury A., Hossain J., Sack R. B., Albert M. J. Production, characterization, and application of monoclonal antibodies to Vibrio cholerae O139 synonym Bengal. Clin Diagn Lab Immunol. 1994 Jan;1(1):51–54. doi: 10.1128/cdli.1.1.51-54.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Qadri F., Haq S., Hossain S. A., Ciznar I., Tzipori S. The association of haemagglutination and adhesion with lipopolysaccharide of Shigella dysenteriae serotype 1. J Med Microbiol. 1991 May;34(5):259–264. doi: 10.1099/00222615-34-5-259. [DOI] [PubMed] [Google Scholar]
  27. Qadri F., Jonson G., Begum Y. A., Wennerås C., Albert M. J., Salam M. A., Svennerholm A. M. Immune response to the mannose-sensitive hemagglutinin in patients with cholera due to Vibrio cholerae O1 and O0139. Clin Diagn Lab Immunol. 1997 Jul;4(4):429–434. doi: 10.1128/cdli.4.4.429-434.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Qadri F., Mohi G., Hossain J., Azim T., Khan A. M., Salam M. A., Sack R. B., Albert M. J., Svennerholm A. M. 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. 1995 Nov;2(6):685–688. doi: 10.1128/cdli.2.6.685-688.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Quiding M., Nordström I., Kilander A., Andersson G., Hanson L. A., Holmgren J., Czerkinsky C. Intestinal immune responses in humans. Oral cholera vaccination induces strong intestinal antibody responses and interferon-gamma production and evokes local immunological memory. J Clin Invest. 1991 Jul;88(1):143–148. doi: 10.1172/JCI115270. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Rahman M., Sack D. A., Mahmood S., Hossain A. Rapid diagnosis of cholera by coagglutination test using 4-h fecal enrichment cultures. J Clin Microbiol. 1987 Nov;25(11):2204–2206. doi: 10.1128/jcm.25.11.2204-2206.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sanchez J., Holmgren J. Recombinant system for overexpression of cholera toxin B subunit in Vibrio cholerae as a basis for vaccine development. Proc Natl Acad Sci U S A. 1989 Jan;86(2):481–485. doi: 10.1073/pnas.86.2.481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Svennerholm A. M., Holmgren J., Black R., Levine M., Merson M. Serologic differentiation between antitoxin responses to infection with Vibrio cholerae and enterotoxin-producing Escherichia coli. J Infect Dis. 1983 Mar;147(3):514–522. doi: 10.1093/infdis/147.3.514. [DOI] [PubMed] [Google Scholar]
  33. Svennerholm A. M., Wikström M., Lindblad M., Holmgren J. Monoclonal antibodies against Escherichia coli heat-stable toxin (STa) and their use in a diagnostic ST ganglioside GM1-enzyme-linked immunosorbent assay. J Clin Microbiol. 1986 Oct;24(4):585–590. doi: 10.1128/jcm.24.4.585-590.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Waldor M. K., Colwell R., Mekalanos J. J. The Vibrio cholerae O139 serogroup antigen includes an O-antigen capsule and lipopolysaccharide virulence determinants. Proc Natl Acad Sci U S A. 1994 Nov 22;91(24):11388–11392. doi: 10.1073/pnas.91.24.11388. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Weintraub A., Widmalm G., Jansson P. E., Jansson M., Hultenby K., Albert M. J. Vibrio cholerae O139 Bengal possesses a capsular polysaccharide which may confer increased virulence. Microb Pathog. 1994 Mar;16(3):235–241. doi: 10.1006/mpat.1994.1024. [DOI] [PubMed] [Google Scholar]
  36. Wennerås C., Svennerholm A. M., Ahrén C., Czerkinsky C. Antibody-secreting cells in human peripheral blood after oral immunization with an inactivated enterotoxigenic Escherichia coli vaccine. Infect Immun. 1992 Jul;60(7):2605–2611. doi: 10.1128/iai.60.7.2605-2611.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES