1887

Abstract

O1 biotype El Tor (ET), causing the seventh cholera pandemic, was recently replaced in Bangladesh by an altered ET possessing of the Classical (CL) biotype, which caused the first six cholera pandemics. In the present study, O1 strains associated with endemic cholera in Dhaka between 2006 and 2011 were analysed for major phenotypic and genetic characteristics. Of 54 representative isolates tested, all were phenotypically ET and showed uniform resistance to trimethoprim/sulfamethoxazole (SXT) and furazolidone (FR). Resistance to tetracycline (TE) and erythromycin (E) showed temporal fluctuation, varying from year to year, while all isolates were susceptible to gentamicin (CN) and ciprofloxacin (CIP). Year-wise data revealed erythromycin resistance to be 33.3 % in 2006 and 11 % in 2011, while tetracycline resistance accounted for 33, 78, 0, 100 and 27 % in 2006, 2007, 2008, 2009 and 2010, respectively; interestingly, all isolates tested were sensitive to TE in 2011, as observed in 2008. All isolates tested possessed genetic elements such as SXT, , , and ; none had I (Integron I). Double mismatch amplification mutation assay (DMAMA)-PCR followed by DNA sequencing and analysis of the gene revealed a point mutation at position 58 (C→A), which has resulted in an amino acid substitution from histidine (H) to asparagine (N) at position 20 (genotype 7) since 2008. Although the multi-resistant strains having tetracycline resistance showed minor genetic divergence, strains were clonal, as determined by a PFGE (I)-based dendrogram. This study shows 2008–2010 to be the time of transition from genotype 1 to genotype 7 in ET causing endemic cholera in Dhaka, Bangladesh.

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2012-12-01
2024-03-29
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References

  1. Alam M., Hasan N. A., Sadique A., Bhuiyan N. A., Ahmed K. U., Nusrin S., Nair G. B., Siddique A. K., Sack R. B. other authors 2006; Seasonal cholera caused by Vibrio cholerae serogroups O1 and O139 in the coastal aquatic environment of Bangladesh. Appl Environ Microbiol 72:4096–4104 [View Article][PubMed]
    [Google Scholar]
  2. Alam M., Sultana M., Nair G. B., Siddique A. K., Hasan N. A., Sack R. B., Sack D. A., Ahmed K. U., Sadique A. other authors 2007; Viable but nonculturable Vibrio cholerae O1 in biofilms in the aquatic environment and their role in cholera transmission. Proc Natl Acad Sci U S A 104:17801–17806 [View Article][PubMed]
    [Google Scholar]
  3. Alam M., Nusrin S., Islam A., Bhuiyan N. A., Rahim N., Delgado G., Morales R., Mendez J. L., Navarro A. other authors 2010; Cholera between 1991 and 1997 in Mexico was associated with infection by classical, El Tor, and El Tor variants of Vibrio cholerae . J Clin Microbiol 48:3666–3674 [View Article][PubMed]
    [Google Scholar]
  4. Bauer A. W., Kirby W. M., Sherris J. C., Turck M. 1966; Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 45:493–496[PubMed]
    [Google Scholar]
  5. Chin C. S., Sorenson J., Harris J. B., Robins W. P., Charles R. C., Jean-Charles R. R., Bullard J., Webster D. R., Kasarskis A. other authors 2011; The origin of the Haitian cholera outbreak strain. N Engl J Med 364:33–42 [View Article][PubMed]
    [Google Scholar]
  6. Cholera working group 1993; Large epidemic of cholera-like disease in Bangladesh caused by Vibrio cholerae O139 synonym Bengal. Lancet 342:387–390 [View Article][PubMed]
    [Google Scholar]
  7. Chow K. H., Ng T. K., Yuen K. Y., Yam W. C. 2001; Detection of RTX toxin gene in Vibrio cholerae by PCR. J Clin Microbiol 39:2594–2597 [View Article][PubMed]
    [Google Scholar]
  8. Chun J., Grim C. J., Hasan N. A., Lee J. H., Choi S. Y., Haley B. J., Taviani E., Jeon Y. S., Kim D. W. other authors 2009; Comparative genomics reveals mechanism for short-term and long-term clonal transitions in pandemic Vibrio cholerae . Proc Natl Acad Sci U S A 106:15442–15447 [View Article][PubMed]
    [Google Scholar]
  9. CLSI 2010; Methods for antimicrobial dilution and disk susceptibility testing of infrequently isolated or fastidious bacteria. Approved Guideline 2nd edn, document M45–A2 (ISBN 1–56238–732–4) Wayne, PA: Clinical and Laboratory Standards Institute;
    [Google Scholar]
  10. Cooper K. L., Luey C. K., Bird M., Terajima J., Nair G. B., Kam K. M., Arakawa E., Safa A., Cheung D. T. other authors 2006; Development and validation of a PulseNet standardized pulsed-field gel electrophoresis protocol for subtyping of Vibrio cholerae . Foodborne Pathog Dis 3:51–58 [View Article][PubMed]
    [Google Scholar]
  11. Dziejman M., Balon E., Boyd D., Fraser C. M., Heidelberg J. F., Mekalanos J. J. 2002; Comparative genomic analysis of Vibrio cholerae: genes that correlate with cholera endemic and pandemic disease. Proc Natl Acad Sci U S A 99:1556–1561 [View Article][PubMed]
    [Google Scholar]
  12. Faruque A. S. G., Salam M. A., Faruque S. M., Fuchs G. J. 1998; Aetiological, clinical and epidemiological characteristics of a seasonal peak of diarrhoea in Dhaka, Bangladesh. Scand J Infect Dis 30:393–396 [View Article][PubMed]
    [Google Scholar]
  13. Faruque A. S. G., Alam K., Malek M. A., Khan M. G., Ahmed S., Saha D., Khan W. A., Nair G. B., Salam M. A. other authors 2007; Emergence of multidrug-resistant strain of Vibrio cholerae O1 in Bangladesh and reversal of their susceptibility to tetracycline after two years. J Health Popul Nutr 25:241–243[PubMed]
    [Google Scholar]
  14. Glass R. I., Huq I., Alim A. R. M. A., Yunus M. 1980; Emergence of multiply antibiotic-resistant Vibrio cholerae in Bangladesh. J Infect Dis 142:939–942 [View Article][PubMed]
    [Google Scholar]
  15. Glass R. I., Huq M. I., Lee J. V., Threlfall E. J., Khan M. R., Alim A. R., Rowe B., Gross R. J. 1983; Plasmid-borne multiple drug resistance in Vibrio cholerae serogroup O1, biotype El Tor: evidence for a point-source outbreak in Bangladesh. J Infect Dis 147:204–209 [View Article][PubMed]
    [Google Scholar]
  16. Goel A. K., Jiang S. C. 2010; Genetic determinants of virulence, antibiogram and altered biotype among the Vibrio cholerae O1 isolates from different cholera outbreaks in India. Infect Genet Evol 10:815–819 [View Article][PubMed]
    [Google Scholar]
  17. Greenough W. B. III, Gordon R. S. Jr, Rosenberg I. S., Davies B. I., Benenson A. S. 1964; Tetracycline in the treatment of cholera. Lancet 1:355–357 [View Article][PubMed]
    [Google Scholar]
  18. Hoshino K., Yamasaki S., Mukhopadhyay A. K., Chakraborty S., Basu A., Bhattacharya S. K., Nair G. B., 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 20:201–207 [View Article][PubMed]
    [Google Scholar]
  19. Jain M., Goel A. K., Bhattacharya P., Ghatole M., Kamboj D. V. 2011; Multidrug resistant Vibrio cholerae O1 El Tor carrying classical ctxB allele involved in a cholera outbreak in South Western India. Acta Trop 117:152–156 [View Article][PubMed]
    [Google Scholar]
  20. Jesudason M. V., John T. J. 1990; Transferable trimethoprim resistance of Vibrio cholerae O1 encountered in southern India. Trans R Soc Trop Med Hyg 84:136–137 [View Article][PubMed]
    [Google Scholar]
  21. Kaper J. B., Morris J. G. Jr, Levine M. M. 1995; Cholera. Clin Microbiol Rev 8:48–86[PubMed]
    [Google Scholar]
  22. Kimsey H. H., Nair G. B., Ghosh A., Waldor M. K. 1998; Diverse CTXϕs and evolution of new pathogenic Vibrio cholerae . Lancet 352:457–458 [View Article][PubMed]
    [Google Scholar]
  23. Kumar P., Jain M., Goel A. K., Bhadauria S., Sharma S. K., Kamboj D. V., Singh L., Ramamurthy T., Nair G. B. 2009; A large cholera outbreak due to a new cholera toxin variant of the Vibrio cholerae O1 El Tor biotype in Orissa, Eastern India. J Med Microbiol 58:234–238 [View Article][PubMed]
    [Google Scholar]
  24. Kumar P., Wilson P. A., Bhai R., Thomas S. 2010; Characterization of an SXT variant Vibrio cholerae O1 Ogawa isolated from a patient in Trivandrum, India. FEMS Microbiol Lett 303:132–136 [View Article][PubMed]
    [Google Scholar]
  25. Lindenbaum J., Greenough W. B., Islam M. R. 1967; Antibiotic therapy of cholera. Bull World Health Organ 36:871–883[PubMed]
    [Google Scholar]
  26. Maimone F., Coppo A., Pazzani C., Ismail S. O., Guerra R., Procacci P., Rotigliano G., Omar K. H. 1986; Clonal spread of multiply resistant strains of Vibrio cholerae O1 in Somalia. J Infect Dis 153:802–803 [View Article][PubMed]
    [Google Scholar]
  27. Marin M. A., Vicente A. C. 2012; Variants of Vibrio cholerae O1 El Tor from Zambia showed new genotypes of ctxB . Epidemiol Infect 140:1386–1387, author reply 1387–1388[PubMed] [CrossRef]
    [Google Scholar]
  28. Mhalu F. S., Mmari P. W., Ijumba J. 1979; Rapid emergence of El Tor Vibrio cholerae resistant to antimicrobial agents during first six months of fourth cholera epidemic in Tanzania. Lancet 1:345–347 [View Article][PubMed]
    [Google Scholar]
  29. Mutreja A., Kim D. W., Thomson N. R., Connor T. R., Lee J. H., Kariuki S., Croucher N. J., Choi S. Y., Harris S. R. other authors 2011; Evidence for several waves of global transmission in the seventh cholera pandemic. Nature 477:462–465 [View Article][PubMed]
    [Google Scholar]
  30. Naha A., Pazhani G. P., Ganguly M., Ghosh S., Ramamurthy T., Nandy R. K., Nair G. B., Takeda Y., Mukhopadhyay A. K. 2012; Development and evaluation of a PCR assay for tracking the emergence and dissemination of Haitian variant ctxB in Vibrio cholerae O1 strains isolated from Kolkata, India. J Clin Microbiol 50:1733–1736 [View Article][PubMed]
    [Google Scholar]
  31. Nair G. B., Faruque S. M., Bhuiyan N. A., Kamruzzaman M., Siddique A. K., Sack D. A. 2002; 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 40:3296–3299 [View Article][PubMed]
    [Google Scholar]
  32. Nair G. B., Qadri F., Holmgren J., Svennerholm A. M., Safa A., Bhuiyan N. A., Ahmad Q. S., Faruque S. M., Faruque A. S. other authors 2006; Cholera due to altered El Tor strains of Vibrio cholerae O1 in Bangladesh. J Clin Microbiol 44:4211–4213 [View Article][PubMed]
    [Google Scholar]
  33. Olsvik O., Wahlberg J., Petterson B., Uhlén M., Popovic T., Wachsmuth I. K., Fields P. I. 1993; Use of automated sequencing of polymerase chain reaction-generated amplicons to identify three types of cholera toxin subunit B in Vibrio cholerae O1 strains. J Clin Microbiol 31:22–25[PubMed]
    [Google Scholar]
  34. Politzer R. 1959 Cholera pp. 11–50 Geneva, Switzerland: World Health Organization;
    [Google Scholar]
  35. Quilici M. L., Massenet D., Gake B., Bwalki B., Olson D. M. 2010; Vibrio cholerae O1 variant with reduced susceptibility to ciprofloxacin, Western Africa. Emerg Infect Dis 16:1804–1805 [View Article][PubMed]
    [Google Scholar]
  36. Ramamurthy T., Garg S., Sharma R., Bhattacharya S. K., Nair G. B., Shimada T., Takeda T., Karasawa T., Kurazano H. other authors 1993; Emergence of novel strain of Vibrio cholerae with epidemic potential in southern and eastern India. Lancet 341:703–704 [View Article][PubMed]
    [Google Scholar]
  37. Sack D. A., Sack R. B., Nair G. B., Siddique A. K. 2004; Cholera. Lancet 363:223–233 [View Article][PubMed]
    [Google Scholar]
  38. Safa A., Sultana J., Dac Cam P., Mwansa J. C., Kong R. Y. 2008; Vibrio cholerae O1 hybrid El Tor strains, Asia and Africa. Emerg Infect Dis 14:987–988 [View Article][PubMed]
    [Google Scholar]
  39. Saha D., Karim M. M., Khan W. A., Ahmed S., Salam M. A., Bennish M. L. 2006; Single-dose azithromycin for the treatment of cholera in adults. N Engl J Med 354:2452–2462 [View Article][PubMed]
    [Google Scholar]
  40. Siddique A. K., Nair G. B., Alam M., Sack D. A., Huq A., Nizam A., Longini I. M. Jr, Qadri F., Faruque S. M. other authors 2010; El Tor cholera with severe disease: a new threat to Asia and beyond. Epidemiol Infect 138:347–352 [View Article][PubMed]
    [Google Scholar]
  41. Taneja N., Samanta P., Mishra A., Sharma M. 2010; Emergence of tetracycline resistance in Vibrio cholerae O1 biotype El Tor serotype Ogawa from north India. Indian J Pathol Microbiol 53:865–866 [View Article][PubMed]
    [Google Scholar]
  42. Thungapathra M., Amita, Sinha K. K., Chaudhuri S. R., Garg P., Ramamurthy T., Nair G. B., Ghosh A. 2002; Occurrence of antibiotic resistance gene cassettes aac(6′)-Ib, dfrA5, dfrA12, and ereA2 in class I integrons in non-O1, non-O139 Vibrio cholerae strains in India. Antimicrob Agents Chemother 46:2948–2955 [View Article][PubMed]
    [Google Scholar]
  43. Waldor M. K., Tschäpe H., Mekalanos J. J. 1996; A new type of conjugative transposon encodes resistance to sulfamethoxazole, trimethoprim, and streptomycin in Vibrio cholerae O139. J Bacteriol 178:4157–4165[PubMed]
    [Google Scholar]
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