Logo of jcmPermissionsJournals.ASM.orgJournalJCM ArticleJournal InfoAuthorsReviewers
J Clin Microbiol. 1995 Oct; 33(10): 2715–2722.
PMCID: PMC228562

Characterization of Vibrio cgolerae non-O1 serogroups obtained from an outbreak of diarrhea in Lima, Peru.


In February 1994, an outbreak of diarrhea caused by non-O1 Vibrio cholerae occurred among volunteers in a vaccine trial study area in Lima, Peru. Clinically, 95% of the patients presented with liquid diarrhea with either no or mild dehydration. Serogrouping of 58 isolates recovered from diarrheal patients affected in the outbreak revealed seven different serogroups, with serogroups O10 (21%) and O12 (65%) being predominant. Most of these isolates were susceptible to a variety of antimicrobial agents. None of the 58 isolates hybridized with a DNA probe previously used to detect the gene encoding the heat-stable enterotoxin NAG-ST or produced cholera toxin as assessed by GM1 ganglioside enzyme-linked immunosorbent assay. Ribotyping exhibited 10 different BglI ribotype patterns among the 58 V. cholera non-O1 strains studied. However, ribotyping showed that all isolates belonging to serogroup O12 exhibited identical ribotypes and that 83% of the serogroup O10 isolates belonged to another identical ribotype, thus showing excellent correlation between ribotypes and serogroups. Among a group of O10 and O12 isolates selected for virulence studies, none produced enterotoxin whereas the majority produced a cytotoxin, as assessed in Y1 and HeLa cells. These isolates were also negative for the gene encoding zonula occludens toxin (Zot) as assessed by a PCR assay. The isolates tested showed strong adherence and some degree of invasion in the HEp-2 cell assay, whereas none of the isolates was positive in the PCR assay for the gene encoding the toxin coregulated pilus subunit A antigen (tcpA).(ABSTRACT TRUNCATED AT 250 WORDS)

Full Text

The Full Text of this article is available as a PDF (961K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Albert MJ. Vibrio cholerae O139 Bengal. J Clin Microbiol. 1994 Oct;32(10):2345–2349. [PMC free article] [PubMed]
  • Albert MJ, Alam K, Ansaruzzaman M, Islam MM, Rahman AS, Haider K, Bhuiyan NA, Nahar S, Ryan N, Montanaro J, et al. Pathogenesis of Providencia alcalifaciens-induced diarrhea. Infect Immun. 1992 Dec;60(12):5017–5024. [PMC free article] [PubMed]
  • Arita M, Honda T, Miwatani T, Ohmori K, Takao T, Shimonishi Y. Purification and characterization of a new heat-stable enterotoxin produced by Vibrio cholerae non-O1 serogroup Hakata. Infect Immun. 1991 Jun;59(6):2186–2188. [PMC free article] [PubMed]
  • Arita M, Takeda T, Honda T, Miwatani T. Purification and characterization of Vibrio cholerae non-O1 heat-stable enterotoxin. Infect Immun. 1986 Apr;52(1):45–49. [PMC free article] [PubMed]
  • Bagchi K, Echeverria P, Arthur JD, Sethabutr O, Serichantalergs O, Hoge CW. Epidemic of diarrhea caused by Vibrio cholerae non-O1 that produced heat-stable toxin among Khmers in a camp in Thailand. J Clin Microbiol. 1993 May;31(5):1315–1317. [PMC free article] [PubMed]
  • Booth BA, Finkelstein RA. Presence of hemagglutinin/protease and other potential virulence factors in O1 and non-O1 Vibrio cholerae. J Infect Dis. 1986 Jul;154(1):183–186. [PubMed]
  • Craig JP, Yamamoto K, Takeda Y, Miwatani T. Production of cholera-like enterotoxin by a Vibrio cholerae non-O1 strain isolated from the environment. Infect Immun. 1981 Oct;34(1):90–97. [PMC free article] [PubMed]
  • Dakin WP, Howell DJ, Sutton RG, O'Keefe MF, Thomas P. Gastroenteritis due to non-agglutinable (non-cholera) vibrios. Med J Aust. 1974 Sep 28;2(13):487–490. [PubMed]
  • Dalsgaard A, Echeverria P, Larsen JL, Siebeling R, Serichantalergs O, Huss HH. Application of ribotyping for differentiating Vibrio cholerae non-O1 isolated from shrimp farms in Thailand. Appl Environ Microbiol. 1995 Jan;61(1):245–251. [PMC free article] [PubMed]
  • Dalsgaard A, Serichantalergs O, Pitarangsi C, Echeverria P. Molecular characterization and antibiotic susceptibility of Vibrio cholerae non-O1. Epidemiol Infect. 1995 Feb;114(1):51–63. [PMC free article] [PubMed]
  • Datta-Roy K, Banerjee K, De SP, Ghose AC. Comparative study of expression of hemagglutinins, hemolysins, and enterotoxins by clinical and environmental isolates of non-O1 Vibrio cholerae in relation to their enteropathogenicity. Appl Environ Microbiol. 1986 Oct;52(4):875–879. [PMC free article] [PubMed]
  • Faruque SM, Comstock L, Kaper JB, Albert MJ. Distribution of Zonula occludens toxin (zot) gene among clinical isolates of Vibrio cholerae O1 from Bangladesh and Africa. J Diarrhoeal Dis Res. 1994 Sep;12(3):222–224. [PubMed]
  • Gentry MK, Dalrymple JM. Quantitative microtiter cytotoxicity assay for Shigella toxin. J Clin Microbiol. 1980 Sep;12(3):361–366. [PMC free article] [PubMed]
  • Grimont F, Grimont PA. Ribosomal ribonucleic acid gene restriction patterns as potential taxonomic tools. Ann Inst Pasteur Microbiol. 1986 Sep-Oct;137B(2):165–175. [PubMed]
  • Hoge CW, Sethabutr O, Bodhidatta L, Echeverria P, Robertson DC, Morris JG., Jr Use of a synthetic oligonucleotide probe to detect strains of non-serovar O1 Vibrio cholerae carrying the gene for heat-stable enterotoxin (NAG-ST). J Clin Microbiol. 1990 Jun;28(6):1473–1476. [PMC free article] [PubMed]
  • Ichinose Y, Yamamoto K, Nakasone N, Tanabe MJ, Takeda T, Miwatani T, Iwanaga M. Enterotoxicity of El Tor-like hemolysin of non-O1 Vibrio cholerae. Infect Immun. 1987 May;55(5):1090–1093. [PMC free article] [PubMed]
  • Keasler SP, Hall RH. Detecting and biotyping Vibrio cholerae O1 with multiplex polymerase chain reaction. Lancet. 1993 Jun 26;341(8861):1661–1661. [PubMed]
  • Levine MM, Kaper JB, Herrington D, Losonsky G, Morris JG, Clements ML, Black RE, Tall B, Hall R. Volunteer studies of deletion mutants of Vibrio cholerae O1 prepared by recombinant techniques. Infect Immun. 1988 Jan;56(1):161–167. [PMC free article] [PubMed]
  • Maas R. An improved colony hybridization method with significantly increased sensitivity for detection of single genes. Plasmid. 1983 Nov;10(3):296–298. [PubMed]
  • McCardell BA, Madden JM, Shah DB. Isolation and characterization of a cytolysin produced by Vibrio cholerae serogroup non-O1. Can J Microbiol. 1985 Aug;31(8):711–720. [PubMed]
  • MONSUR KA. A highly selective gelatin-taurocholate-tellurite medium for the isolation of Vibrio cholerae. Trans R Soc Trop Med Hyg. 1961 Sep;55:440–442. [PubMed]
  • Moon HW, Whipp SC, Argenzio RA, Levine MM, Giannella RA. Attaching and effacing activities of rabbit and human enteropathogenic Escherichia coli in pig and rabbit intestines. Infect Immun. 1983 Sep;41(3):1340–1351. [PMC free article] [PubMed]
  • Morris JG, Jr, Takeda T, Tall BD, Losonsky GA, Bhattacharya SK, Forrest BD, Kay BA, Nishibuchi M. Experimental non-O group 1 Vibrio cholerae gastroenteritis in humans. J Clin Invest. 1990 Mar;85(3):697–705. [PMC free article] [PubMed]
  • Murray MG, Thompson WF. Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res. 1980 Oct 10;8(19):4321–4325. [PMC free article] [PubMed]
  • Näcescu N, Ciufecu C. Serotypes of Nag Vibrios isolated from clinical and environmental sources. Zentralbl Bakteriol Orig A. 1978 Apr;240(3):334–338. [PubMed]
  • Nakasone N, Iwanaga M. Pili of Vibrio cholerae non-O1. Infect Immun. 1990 Jun;58(6):1640–1646. [PMC free article] [PubMed]
  • O'Brien AD, Chen ME, Holmes RK, Kaper J, Levine MM. Environmental and human isolates of Vibrio cholerae and Vibrio parahaemolyticus produce a Shigella dysenteriae 1 (Shiga)-like cytotoxin. Lancet. 1984 Jan 14;1(8368):77–78. [PubMed]
  • Pal A, Ramamurthy T, Bhadra RK, Takeda T, Shimada T, Takeda Y, Nair GB, Pal SC, Chakrabarti S. Reassessment of the prevalence of heat-stable enterotoxin (NAG-ST) among environmental Vibrio cholerae non-O1 strains isolated from Calcutta, India, by using a NAG-ST DNA probe. Appl Environ Microbiol. 1992 Aug;58(8):2485–2489. [PMC free article] [PubMed]
  • Popovic T, Bopp C, Olsvik O, Wachsmuth K. Epidemiologic application of a standardized ribotype scheme for Vibrio cholerae O1. J Clin Microbiol. 1993 Sep;31(9):2474–2482. [PMC free article] [PubMed]
  • Ramamurthy T, Bag PK, Pal A, Bhattacharya SK, Bhattacharya MK, Shimada T, Takeda T, Karasawa T, Kurazono H, Takeda Y, et al. Virulence patterns of Vibrio cholerae non-O1 strains isolated from hospitalised patients with acute diarrhoea in Calcutta, India. J Med Microbiol. 1993 Oct;39(4):310–317. [PubMed]
  • Russell RG, Tall BD, Morris JG., Jr Non-O1 Vibrio cholerae intestinal pathology and invasion in the removable intestinal tie adult rabbit diarrhea model. Infect Immun. 1992 Feb;60(2):435–442. [PMC free article] [PubMed]
  • Sack DA, Sack RB. Test for enterotoxigenic Escherichia coli using Y-1 adrenal cells in miniculture. Infect Immun. 1975 Feb;11(2):334–336. [PMC free article] [PubMed]
  • Sack DA, Huda S, Neogi PK, Daniel RR, Spira WM. Microtiter ganglioside enzyme-linked immunosorbent assay for vibrio and Escherichia coli heat-labile enterotoxins and antitoxin. J Clin Microbiol. 1980 Jan;11(1):35–40. [PMC free article] [PubMed]
  • Sanchez JL, Vasquez B, Begue RE, Meza R, Castellares G, Cabezas C, Watts DM, Svennerholm AM, Sadoff JC, Taylor DN. Protective efficacy of oral whole-cell/recombinant-B-subunit cholera vaccine in Peruvian military recruits. Lancet. 1994 Nov 5;344(8932):1273–1276. [PubMed]
  • Sanyal SC, Singh SJ, Tiwari IC, Sen PC, Marwah SM, Hazarika UR, Singh H, Shimada T, Sakazaki R. Role of household animals in maintenance of cholera infection in a community. J Infect Dis. 1974 Dec;130(6):575–579. [PubMed]
  • Spira WM, Sack RB, Froehlich JL. Simple adult rabbit model for Vibrio cholerae and enterotoxigenic Escherichia coli diarrhea. Infect Immun. 1981 May;32(2):739–747. [PMC free article] [PubMed]
  • Waldor MK, Mekalanos JJ. ToxR regulates virulence gene expression in non-O1 strains of Vibrio cholerae that cause epidemic cholera. Infect Immun. 1994 Jan;62(1):72–78. [PMC free article] [PubMed]
  • Wright AC, Guo Y, Johnson JA, Nataro JP, Morris JG., Jr Development and testing of a nonradioactive DNA oligonucleotide probe that is specific for Vibrio cholerae cholera toxin. J Clin Microbiol. 1992 Sep;30(9):2302–2306. [PMC free article] [PubMed]
  • Yamamoto K, Al-Omani M, Honda T, Takeda Y, Miwatani T. Non-O1 Vibrio cholerae hemolysin: purification, partial characterization, and immunological relatedness to El Tor hemolysin. Infect Immun. 1984 Jul;45(1):192–196. [PMC free article] [PubMed]
  • Yamamoto K, Takeda Y, Miwatani T, Craig JP. Evidence that a non-O1 Vibrio cholerae produces enterotoxin that is similar but not identical to cholera enterotoxin. Infect Immun. 1983 Sep;41(3):896–901. [PMC free article] [PubMed]
  • Yoh M, Honda T, Miwatani T. Purification and partial characterization of a non-O1 Vibrio cholerae hemolysin that cross-reacts with thermostable direct hemolysin of Vibrio parahaemolyticus. Infect Immun. 1986 Apr;52(1):319–322. [PMC free article] [PubMed]

Articles from Journal of Clinical Microbiology are provided here courtesy of American Society for Microbiology (ASM)


Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...


Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...