1887

Abstract

Cholera, caused by , results in significant morbidity and mortality worldwide, including Thailand. Representative strains associated with endemic cholera ( = 32), including strains ( = 3) from surface water sources, in Khon Kaen, Thailand (2003–2011), were subjected to microbiological, molecular and phylogenetic analyses. According to phenotypic and related genetic data, all tested strains belonged to serogroup O1, biotype El Tor (ET), Inaba (IN) or Ogawa (OG). All of the strains were sensitive to gentamicin and ciprofloxacin, while multidrug-resistant (MDR) strains showing resistance to erythromycin, tetracycline, trimethoprim/sulfamethoxazole and ampicillin were predominant in 2007. isolated before and after 2007 were non-MDR. All except six diarrhoeal strains possessed and genes and were toxigenic altered ET, confirmed by MAMA-PCR and DNA sequencing. Year-wise data revealed that INET strains isolated between 2003 and 2004, plus one strain isolated in 2007, lacked the RS1 sequence () and toxin-linked cryptic plasmid (TLC)-specific genetic marker, but possessed CTX prophage genes and . A sharp genetic transition was noted, namely the majority of strains in 2007 and all in 2010 and 2011 were not repressor genotype but instead were , and all strains possessed RS1 and TLC-specific genetic markers. DNA sequencing data revealed that strains isolated since 2007 had a mutation in the gene at amino acid position 64 (N→S). Four clonal types, mostly of environmental origin, including subtypes, reflected genetic diversity, while distinct signatures were observed for clonally related, altered ET from Thailand, Vietnam and Bangladesh, confirmed by distinct subclustering patterns observed in the PFGE (I)-based dendrogram, suggesting that endemic cholera is caused by indigenous to Khon Kaen.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.053801-0
2013-04-01
2019-10-15
Loading full text...

Full text loading...

/deliver/fulltext/jmm/62/4/599.html?itemId=/content/journal/jmm/10.1099/jmm.0.053801-0&mimeType=html&fmt=ahah

References

  1. 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. [CrossRef][PubMed]
    [Google Scholar]
  2. 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. [CrossRef][PubMed]
    [Google Scholar]
  3. Ang G. Y., Yu C. Y., Balqis K., Elina H. T., Azura H., Hani M. H., Yean C. Y.. ( 2010;). Molecular evidence of cholera outbreak caused by a toxigenic Vibrio cholerae O1 El Tor variant strain in Kelantan, Malaysia. . J Clin Microbiol 48:, 3963–3969. [CrossRef][PubMed]
    [Google Scholar]
  4. Ansaruzzaman M., Bhuiyan N. A., Nair B. G., Sack D. A., Lucas M., Deen J. L., Ampuero J., Chaignat C. L..Mozambique Cholera Vaccine Demonstration Project Coordination Group ( 2004;). Cholera in Mozambique, variant of Vibrio cholerae. . Emerg Infect Dis 10:, 2057–2059. [CrossRef][PubMed]
    [Google Scholar]
  5. Ansaruzzaman M., Bhuiyan N. A., Safa A., Sultana M., McUamule A., Mondlane C., Wang X. Y., Deen J. L., von Seidlein L., Clemens J.. ( 2007;). Genetic diversity of El Tor strains of Vibrio cholerae O1 with hybrid traits isolated from Bangladesh and Mozambique. . Int J Med Microbiol 297:, 443–449. [CrossRef][PubMed]
    [Google Scholar]
  6. 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]
  7. Beltrán P., Delgado G., Navarro A., Trujillo F., Selander R. K., Cravioto A.. ( 1999;). Genetic diversity and population structure of Vibrio cholerae. . J Clin Microbiol 37:, 581–590.[PubMed]
    [Google Scholar]
  8. Blake P. A.. ( 1994;). Endemic cholera in Australia and United States. . In Vibrio cholerae and Cholera: Molecular to Global Perspectives, pp. 309–319. Edited by Wachsmuth I. K., Blake P. A., Olsvik O... Washington, DC:: American Society for Microbiology;.
    [Google Scholar]
  9. Bureau of Epidemiology (2010). Annual epidemiological surveillance report. Nonthaburi, Thailand: Department of Disease Control, Ministry of Public Health
  10. Cameron D. N., Khambaty F. M., Wachsmuth I. K., Tauxe R. V., Barrett T. J.. ( 1994;). Molecular characterization of Vibrio cholerae O1 strains by pulsed-field gel electrophoresis. . J Clin Microbiol 32:, 1685–1690.[PubMed]
    [Google Scholar]
  11. 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. [CrossRef][PubMed]
    [Google Scholar]
  12. Choi S. Y., Lee J. H., Jeon Y. S., Lee H. R., Kim E. J., Ansaruzzaman M., Bhuiyan N. A., Endtz H. P., Niyogi S. K.. & other authors ( 2010;). Multilocus variable-number tandem repeat analysis of Vibrio cholerae O1 El Tor strains harbouring classical toxin B. . J Med Microbiol 59:, 763–769. [CrossRef][PubMed]
    [Google Scholar]
  13. 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. [CrossRef][PubMed]
    [Google Scholar]
  14. 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. [CrossRef][PubMed]
    [Google Scholar]
  15. CLSI ( 2010;). Methods for Antimicrobial Dilution and Disc 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.
  16. Dalsgaard A., Skov M. N., Serichantalergs O., Echeverria P., Meza R., Taylor D. N.. ( 1997;). Molecular evolution of Vibrio cholerae O1 strains isolated in Lima, Peru, from 1991 to 1995. . J Clin Microbiol 35:, 1151–1156.[PubMed]
    [Google Scholar]
  17. 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. [CrossRef][PubMed]
    [Google Scholar]
  18. Faruque S. M., Tam V. C., Chowdhury N., Diraphat P., Dziejman M., Heidelberg J. F., Clemens J. D., Mekalanos J. J., Nair G. B.. ( 2007;). Genomic analysis of the Mozambique strain of Vibrio cholerae O1 reveals the origin of El Tor strains carrying classical CTX prophage. . Proc Natl Acad Sci U S A 104:, 5151–5156. [CrossRef][PubMed]
    [Google Scholar]
  19. 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. [CrossRef][PubMed]
    [Google Scholar]
  20. Goel A. K., Jain M., Kumar P., Sarguna P., Bai M., Ghosh N., Gopalan N.. ( 2011;). Molecular characterization reveals involvement of altered El Tor biotype Vibrio cholerae O1 strains in cholera outbreak at Hyderabad, India. . J Microbiol 49:, 280–284. [CrossRef][PubMed]
    [Google Scholar]
  21. 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. [CrossRef][PubMed]
    [Google Scholar]
  22. Hasan N. A., Choi S. Y., Eppinger M., Clark P. W., Chen A., Alam M., Haley B. J., Taviani E., Hine E.. & other authors ( 2012;). Genomic diversity of 2010 Haitian cholera outbreak strains. . Proc Natl Acad Sci U S A 109:, E2010–E2017. [CrossRef][PubMed]
    [Google Scholar]
  23. 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. [CrossRef][PubMed]
    [Google Scholar]
  24. Ibarra J. O., Alvarado D. E.. ( 2007;). Antimicrobial resistance of clinical and environmental strains of Vibrio cholerae isolated in Lima-Peru during epidemics of 1991 and 1998. . Braz J Infect Dis 11:, 100–105. [CrossRef][PubMed]
    [Google Scholar]
  25. 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. [CrossRef][PubMed]
    [Google Scholar]
  26. Kaper J. B., Morris J. G. Jr, Levine M. M.. ( 1995;). Cholera. . Clin Microbiol Rev 8:, 48–86.[PubMed]
    [Google Scholar]
  27. Karaolis D. K. R., Somara S., Maneval D. R. Jr, Johnson J. A., Kaper J. B.. ( 1999;). A bacteriophage encoding a pathogenicity island, a type-IV pilus and a phage receptor in cholera bacteria. . Nature 399:, 375–379. [CrossRef][PubMed]
    [Google Scholar]
  28. Kumar P., Wilson P. A., Bhai R., Thomas S.. ( 2010a;). Characterization of an SXT variant Vibrio cholerae O1 Ogawa isolated from a patient in Trivandrum, India. . FEMS Microbiol Lett 303:, 132–136. [CrossRef][PubMed]
    [Google Scholar]
  29. Kumar P., Peter W. A., Thomas S.. ( 2010b;). Rapid detection of virulence-associated genes in environmental strains of Vibrio cholerae by multiplex PCR. . Curr Microbiol 60:, 199–202. [CrossRef][PubMed]
    [Google Scholar]
  30. Lindenbaum J., Greenough W. B., Islam M. R.. ( 1967;). Antibiotic therapy of cholera. . Bull World Health Organ 36:, 871–883.[PubMed]
    [Google Scholar]
  31. Mandomando I., Espasa M., Vallès X., Sacarlal J., Sigaúque B., Ruiz J., Alonso P.. ( 2007;). Antimicrobial resistance of Vibrio cholerae O1 serotype Ogawa isolated in Manhiça District Hospital, southern Mozambique. . J Antimicrob Chemother 60:, 662–664. [CrossRef][PubMed]
    [Google Scholar]
  32. 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. [CrossRef][PubMed]
    [Google Scholar]
  33. Morita M., Ohnishi M., Arakawa E., Bhuiyan N. A., Nusrin S., Alam M., Siddique A. K., Qadri F., Izumiya H.. & other authors ( 2008;). Development and validation of a mismatch amplification mutation PCR assay to monitor the dissemination of an emerging variant of Vibrio cholerae O1 biotype El Tor. . Microbiol Immunol 52:, 314–317. [CrossRef][PubMed]
    [Google Scholar]
  34. Morita M., Ohnishi M., Arakawa E., Yamamoto S., Nair G. B., Matsushita S., Yokoyama K., Kai A., Seto K.. & other authors ( 2010;). Emergence and genetic diversity of El Tor Vibrio cholerae O1 that possess classical biotype ctxB among travel-associated cases of cholera in Japan. . J Med Microbiol 59:, 708–712. [CrossRef][PubMed]
    [Google Scholar]
  35. Mwansa J. C. L., Mwaba J., Lukwesa C., Bhuiyan N. A., Ansaruzzaman M., Ramamurthy T., Alam M., Balakrish Nair G.. ( 2007;). Multiply antibiotic-resistant Vibrio cholerae O1 biotype El Tor strains emerge during cholera outbreaks in Zambia. . Epidemiol Infect 135:, 847–853. [CrossRef][PubMed]
    [Google Scholar]
  36. Na-Ubol M., Srimanote P., Chongsa-Nguan M., Indrawattana N., Sookrung N., Tapchaisri P., Yamazaki S., Bodhidatta L., Eampokalap B.. & other authors ( 2011;). Hybrid & El Tor variant biotypes of Vibrio cholerae O1 in Thailand. . Indian J Med Res 133:, 387–394.[PubMed]
    [Google Scholar]
  37. Nair G. B., Qadri F., Holmgren J., Svennerholm A. M., Safa A., Bhuiyan N. A., Ahmad Q. S., Faruque S. M., Faruque A. S. G.. & other authors ( 2006;). Cholera due to altered El Tor strains of Vibrio cholerae O1 in Bangladesh. . J Clin Microbiol 44:, 4211–4213. [CrossRef][PubMed]
    [Google Scholar]
  38. Nandi B., Nandy R. K., Mukhopadhyay S., Nair G. B., Shimada T., Ghose A. C.. ( 2000;). Rapid method for species-specific identification of Vibrio cholerae using primers targeted to the gene of outer membrane protein OmpW. . J Clin Microbiol 38:, 4145–4151.[PubMed]
    [Google Scholar]
  39. Nguyen B. M., Lee J. H., Cuong N. T., Choi S. Y., Hien N. T., Anh D. D., Lee H. R., Ansaruzzaman M., Endtz H. P.. & other authors ( 2009;). Cholera outbreaks caused by an altered Vibrio cholerae O1 El Tor biotype strain producing classical cholera toxin B in Vietnam in 2007 to 2008. . J Clin Microbiol 47:, 1568–1571. [CrossRef][PubMed]
    [Google Scholar]
  40. Nusrin S., Gil A. I., Bhuiyan N. A., Safa A., Asakura M., Lanata C. F., Hall E., Miranda H., Huapaya B.. & other authors ( 2009;). Peruvian Vibrio cholerae O1 El Tor strains possess a distinct region in the Vibrio seventh pandemic island-II that differentiates them from the prototype seventh pandemic El Tor strains. . J Med Microbiol 58:, 342–354. [CrossRef][PubMed]
    [Google Scholar]
  41. O’Shea Y. A., Reen F. J., Quirke A. M., Boyd E. F.. ( 2004;). Evolutionary genetic analysis of the emergence of epidemic Vibrio cholerae isolates on the basis of comparative nucleotide sequence analysis and multilocus virulence gene profiles. . J Clin Microbiol 42:, 4657–4671. [CrossRef][PubMed]
    [Google Scholar]
  42. Okada K., Chantaroj S., Roobthaisong A., Hamada S., Sawanpanyalert P.. ( 2010;). A cholera outbreak of the Vibrio cholerae O1 El Tor variant carrying classical CtxB in northeastern Thailand in 2007. . Am J Trop Med Hyg 82:, 875–878. [CrossRef][PubMed]
    [Google Scholar]
  43. Okada K., Roobthaisong A., Nakagawa I., Hamada S., Chantaroj S.. ( 2012;). Genotypic and PFGE/MLVA analyses of Vibrio cholerae O1: geographical spread and temporal changes during the 2007–2010 cholera outbreaks in Thailand. . PLoS ONE 7:, e30863. [CrossRef][PubMed]
    [Google Scholar]
  44. 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]
  45. Popovic T., Bopp C., Olsvik O., Wachsmuth K.. ( 1993;). Epidemiologic application of a standardized ribotype scheme for Vibrio cholerae O1. . J Clin Microbiol 31:, 2474–2482.[PubMed]
    [Google Scholar]
  46. 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. [CrossRef][PubMed]
    [Google Scholar]
  47. Raychoudhuri A., Mukhopadhyay A. K., Ramamurthy T., Nandy R. K., Takeda Y., Nair G. B.. ( 2008;). Biotyping of Vibrio cholerae O1: time to redefine the scheme. . Indian J Med Res 128:, 695–698.[PubMed]
    [Google Scholar]
  48. Reimer A. R., Van Domselaar G., Stroika S., Walker M., Kent H., Tarr C., Talkington D., Rowe L., Olsen-Rasmussen M.. & other authors ( 2011;). Comparative genomics of Vibrio cholerae from Haiti, Asia, and Africa. . Emerg Infect Dis 17:, 2113–2121. [CrossRef][PubMed]
    [Google Scholar]
  49. Rivera I. N. G., Chun J., Huq A., Sack R. B., Colwell R. R.. ( 2001;). Genotypes associated with virulence in environmental isolates of Vibrio cholerae. . Appl Environ Microbiol 67:, 2421–2429. [CrossRef][PubMed]
    [Google Scholar]
  50. Safa A., Nair G. B., Kong R. Y. C.. ( 2010;). Evolution of new variants of Vibrio cholerae O1. . Trends Microbiol 18:, 46–54. [CrossRef][PubMed]
    [Google Scholar]
  51. 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. [CrossRef][PubMed]
    [Google Scholar]
  52. 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. [CrossRef][PubMed]
    [Google Scholar]
  53. Supawat K., Huttayananont S., Sawanpanyalert P., Aswapokee N., Mootsikapun P.. ( 2009;). Antimicrobial resistance surveillance of Vibrio cholerae in Thailand from 2000 to 2004. . J Med Assoc Thai 92: (Suppl. 4), S82–S86.[PubMed]
    [Google Scholar]
  54. Tangkanakul W., Hanpanjakit C.. ( 2007;). Weekly Epidemiological Surveillance Report. Bangkok. Bangkok, Thailand:: Bureau of Epidemiology, Department of Disease Control, Ministry of Public Health;.
    [Google Scholar]
  55. Taylor R. K., Miller V. L., Furlong D. B., Mekalanos J. J.. ( 1987;). Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. . Proc Natl Acad Sci U S A 84:, 2833–2837. [CrossRef][PubMed]
    [Google Scholar]
  56. Tran H. D., Alam M., Trung N. V., Kinh N. V., Nguyen H. H., Pham V. C., Ansaruzzaman M., Rashed S. M., Bhuiyan N. A.. & other authors ( 2012;). Multi-drug resistant Vibrio cholerae O1 variant El Tor isolated in northern Vietnam between 2007 and 2010. . J Med Microbiol 61:, 431–437. [CrossRef][PubMed]
    [Google Scholar]
  57. Waldor M. K., Mekalanos J. J.. ( 1996;). Lysogenic conversion by a filamentous phage encoding cholera toxin. . Science 272:, 1910–1914. [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.053801-0
Loading
/content/journal/jmm/10.1099/jmm.0.053801-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error