1887

Journal of Medical Microbiology logo

Volume 62, Issue 4

Drug response and genetic properties of associated with endemic cholera in north-eastern Thailand, 2003–2011 Free

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.

  • Received:
  • Accepted:
  • Published Online:
© 2013 SGM
Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.053801-0
2013-04-01
2024-04-19
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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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. 4S82–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 [View Article][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 [View Article][PubMed]
     [Google Scholar]
  57. Waldor M. K., Mekalanos J. J. 1996; Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272:1910–1914 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.053801-0
Loading
Drug response and genetic properties of Vibrio cholerae associated with endemic cholera in north-eastern Thailand, 2003–2011
J. Med. Microbiol. 62, 599 (2013); https://doi.org/10.1099/jmm.0.053801-0
/content/journal/jmm/10.1099/jmm.0.053801-0
/content/journal/jmm/10.1099/jmm.0.053801-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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