1887

Abstract

Consumption of street food is considered a major health risk in the absence of public-health inspection programmes in Indonesia. It is hypothesized that ice used in street food could be one of the major sources of contamination. This study documented contamination in edible ice from different areas of Jakarta, the capital city of Indonesia, and attempted to characterize the virulence potential of the strains. A selective medium was used to isolate 98 strains and their identity was confirmed using biochemical assays. Serological tests classified the majority (78 %) in the non-O1 serogroup. Multiplex PCR was used to detect the presence of virulence genes, namely , and The and genes were detected in 75, 26, 15 and 1 % of isolates, respectively. The and genes were not detected in any of the isolates. The gene encoding the cholera toxin subunit A, which has been associated only with clinical strains of O1, here was present in both serogroups. The antibiotic-resistance profile showed that 65, 60, 52, 39, 37, 19 and 3 % of the isolates were resistant to ampicillin, streptomycin, kanamycin, sulfamethoxazole–trimethoprim, erythromycin, tetracycline and ciprofloxacin, respectively. A large proportion of isolates came from west and south Jakarta, and these strains exhibited multidrug resistance to ampicillin, streptomycin, tetracycline, erythromycin, kanamycin and sulfamethoxazole–trimethoprim. Many of these isolates from west and south Jakarta also harboured , encoding a regulator, and . The presence of multidrug-resistant with virulence genes in edible ice, which could cause a severe outbreak, reflects the poor water quality in Jakarta, and indicates an urgent need for better surveillance and management.

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2013-03-01
2020-11-30
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References

  1. 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]
  2. Bagchi K., Echeverria P., Arthur J. D., Sethabutr O., Serichantalergs O., Hoge C. W. 1993; Epidemic of diarrhea caused by Vibrio cholerae non-O1 that produced heat-stable toxin among Khmers in a camp in Thailand. J Clin Microbiol 31:1315–1317[PubMed]
    [Google Scholar]
  3. Boccia D., Tozzi A. E., Cotter B., Rizzo C., Russo T., Buttinelli G., Caprioli A., Marziano M. L., Ruggeri F. M. 2002; Waterborne outbreak of Norwalk-like virus gastroenteritis at a tourist resort, Italy. Emerg Infect Dis 8:563–568 [CrossRef][PubMed]
    [Google Scholar]
  4. Chakraborty S., Mukhopadhyay A. K., Bhadra R. K., Ghosh A. N., Mitra R., Shimada T., Yamasaki S., Faruque S. M., Takeda Y.& other authors ( 2000; Virulence genes in environmental strains of Vibrio cholerae. Appl Environ Microbiol 66:4022–4028 [CrossRef][PubMed]
    [Google Scholar]
  5. Chandralekha C., Veligandla G., Vanaja R. 2011; Emergence of Vibrio cholerae Serotype Hikojima in Northern Tamil Nadu. Indian J Community Med 36:165–166 [CrossRef][PubMed]
    [Google Scholar]
  6. Chhotray G. P., Pal B. B., Khuntia H. K., Chowdhury N. R., Chakraborty S., Yamasaki S., Ramamurthy T., Takeda Y., Bhattacharya S. K., Nair G. B. 2002; Incidence and molecular analysis of Vibrio cholerae associated with cholera outbreak subsequent to the super cyclone in Orissa, India. Epidemiol Infect 128:131–138 [CrossRef][PubMed]
    [Google Scholar]
  7. Choopun N., Louis V., Huq A., Colwell R. R. 2002; Simple procedure for rapid identification of Vibrio cholerae from the aquatic environment. Appl Environ Microbiol 68:995–998 [CrossRef][PubMed]
    [Google Scholar]
  8. Chun J., Huq A., Colwell R. R. 1999; Analysis of 16S–23S rRNA intergenic spacer regions of Vibrio cholerae and Vibrio mimicus. Appl Environ Microbiol 65:2202–2208[PubMed]
    [Google Scholar]
  9. CLSI 2005; Performance Standards for Antimicrobial Susceptibility Testing; 15th informational supplement M100–S15. Wayne, PA: Clinical and Laboratory Standards Institute;
  10. Deashinta N., Waturangi D. E., Yogiara. 2007; Antibiotic resistance and integron of Vibrio cholerae detection from school street foods in Jakarta. HAYATI J Biosci 14:71–75
    [Google Scholar]
  11. Deen J. L., Von Seidlein L., Sur D., Agtini M., Lucas M. E., Lopez A. L., Kim D. R., Ali M., Clemens J. D. 2008; The high burden of cholera in children: comparison of incidence from endemic areas in Asia and Africa. PLoS Negl Trop Dis 2:e173 [CrossRef][PubMed]
    [Google Scholar]
  12. Faruque S. M., Albert M. J., Mekalanos J. J. 1998a; Epidemiology, genetics, and ecology of toxigenic Vibrio cholerae. Microbiol Mol Biol Rev 62:1301–1314[PubMed]
    [Google Scholar]
  13. Faruque S. M., Asadulghani M. N., Saha M. N., Alim A. R., Albert M. J., Islam K. M., Mekalanos J. J. 1998b; Analysis of clinical and environmental strains of nontoxigenic Vibrio cholerae for susceptibility to CTXΦ: molecular basis for origination of new strains with epidemic potential. Infect Immun 66:5819–5825[PubMed]
    [Google Scholar]
  14. Fazil M. H., Singh D. V. 2011; Vibrio cholerae infection, novel drug targets and phage therapy. Future Microbiol 6:1199–1208 [CrossRef][PubMed]
    [Google Scholar]
  15. Graman P. S., Quinlan G. A., Rank J. A. 1997; Nosocomial legionellosis traced to a contaminated ice machine. Infect Control Hosp Epidemiol 18:637–640 [CrossRef][PubMed]
    [Google Scholar]
  16. Hill V. R., Cohen N., Kahler A. M., Jones J. L., Bopp C. A., Marano N., Tarr C. L., Garrett N. M., Boncy J.& other authors ( 2011; Toxigenic Vibrio cholerae O1 in water and seafood, Haiti. Emerg Infect Dis 17:2147–2150 [CrossRef][PubMed]
    [Google Scholar]
  17. Huang J., Zhu Y., Wen H., Zhang J., Huang S., Niu J., Li Q. 2009; Quadruplex real-time PCR assay for detection and identification of Vibrio cholerae O1 and O139 strains and determination of their toxigenic potential. Appl Environ Microbiol 75:6981–6985 [CrossRef][PubMed]
    [Google Scholar]
  18. Iwanaga M., Toma C., Miyazato T., Insisiengmay S., Nakasone N., Ehara M. 2004; Antibiotic resistance conferred by a class I integron and SXT constin in Vibrio cholerae O1 strains isolated in Laos. Antimicrob Agents Chemother 48:2364–2369 [CrossRef]
    [Google Scholar]
  19. Jagadeeshan S., Kumar P., Abraham W. P., Thomas S. 2009; Multiresistant Vibrio cholerae non-O1/non-O139 from waters in South India: resistance patterns and virulence-associated gene profiles. J Basic Microbiol 49:538–544 [CrossRef][PubMed]
    [Google Scholar]
  20. Jiang S., Chu W., Fu W. 2003; Prevalence of cholera toxin genes (ctxA and zot) among non-O1/O139 Vibrio cholerae strains from Newport Bay, California. Appl Environ Microbiol 69:7541–7544 [CrossRef][PubMed]
    [Google Scholar]
  21. John T. J., Jesudason M. V. 1995; The first epidemic of Vibrio cholerae O139. J Clin Microbiol 33:1972[PubMed]
    [Google Scholar]
  22. Kaper J. B., Morris J. G. Jr, Levine M. M. 1995; Cholera. Clin Microbiol Rev 8:48–86[PubMed]
    [Google Scholar]
  23. Kim J. K., Harrison M. A. 2008; Transfer of Escherichia coli O157 : H7 to romaine lettuce due to contact water from melting ice. J Food Prot 71:252–256[PubMed]
    [Google Scholar]
  24. Kim Y. B., Okuda J., Matsumoto C., Takahashi N., Hashimoto S., Nishibuchi M. 1999; Identification of Vibrio parahaemolyticus strains at the species level by PCR targeted to the toxR gene. J Clin Microbiol 37:1173–1177
    [Google Scholar]
  25. Kumar P., Peter W. A., Thomas S. 2008; Detection of virulence genes in Vibrio cholerae isolated from aquatic environment in Kerala, Southern India. Appl Biochem Biotechnol 151:256–262 [CrossRef][PubMed]
    [Google Scholar]
  26. Kumar P., Peter W. A., Thomas S. 2010; Rapid detection of virulence-associated genes in environmental strains of Vibrio cholerae by multiplex PCR. Curr Microbiol 60:199–202 [CrossRef][PubMed]
    [Google Scholar]
  27. Maiti D., Das B., Saha A., Nandy R. K., Nair G. B., Bhadra R. K. 2006; Genetic organization of pre-CTX and CTX prophages in the genome of an environmental Vibrio cholerae non-O1, non-O139 strain. Microbiology 152:3633–3641 [CrossRef][PubMed]
    [Google Scholar]
  28. Mandal S., Mandal M. D., Pal N. K. 2011; Cholera: a great global concern. Asian Pac J Trop Med 4:573–580 [CrossRef][PubMed]
    [Google Scholar]
  29. Mandal J., Dinoop K. P., Parija S. C. 2012; Increasing antimicrobial resistance of Vibrio cholerae O1 biotype E1 tor strains isolated in a tertiary-care centre in India. J Health Popul Nutr 30:12–16 [CrossRef]
    [Google Scholar]
  30. Miyazato T., Tamaki Y., Sithivong N., Phantouamath B., Insisiengmay S., Higa N., Toma C., Nakasone N., Iwanaga M. 2004; Antibiotic susceptibility and its genetic analysis of Vibrio cholerae non-O1, non-139 from environmental sources in Laos People’s Democratic Republic. Trop Med Health 32:245–248 [CrossRef]
    [Google Scholar]
  31. 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]
  32. Murray M. G., Thompson W. F. 1980; Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325 [CrossRef][PubMed]
    [Google Scholar]
  33. Nishibori T., De Vries G. C., Rahardjo D., Wasito E. B., De I., Kinoshita S., Hayashi Y., Hotta H., Kawabata M.& other authors ( 2011; Phenotypic and genotypic characterization of Vibrio cholerae clinically isolated in Surabaya, Indonesia. Jpn J Infect Dis 64:7–12[PubMed]
    [Google Scholar]
  34. Ogg J. E., Shrestha M. B., Poudayl L. 1978; Phage-induced changes in Vibrio cholerae: serotype and biotype conversions. Infect Immun 19:231–238[PubMed]
    [Google Scholar]
  35. Ogg J. E., Ogg B. J., Shrestha M. B., Poudayl L. 1979; Antigenic changes in Vibrio cholerae biotype El Tor serotype Ogawa after bacteriophage infection. Infect Immun 24:974–978[PubMed]
    [Google Scholar]
  36. Okuda J., Ramamurthy T., Yamasaki S. 2007; Antibacterial activity of ciprofloxacin against clinical strains of Vibrio cholerae O139 recently isolated from India. Yakugaku Zasshi 127:903–904 [CrossRef][PubMed]
    [Google Scholar]
  37. Onyemelukwe G. C., Lawande R. V. 1991; Serotype variation in Vibrio cholerae El Tor diarrhoea in northern Nigeria. Cent Afr J Med 37:186–189[PubMed]
    [Google Scholar]
  38. Ou T. Y., Liu J. W., Leu H. S. 2003; Independent prognostic factors for fatality in patients with invasive Vibrio cholerae non-O1 infections. J Microbiol Immunol Infect 36:117–122[PubMed]
    [Google Scholar]
  39. Panda S. K., Patra A. K., Kar R. N. 2012; Monitoring of multiple drug-resistant pathogens in a selected stretch of Bay of Bengal, India. Environ Monit Assess 184:193–200 [CrossRef][PubMed]
    [Google Scholar]
  40. Rahmani F., Fooladi A. A., Marashi S. M., Nourani M. R. 2012; Drug resistance in Vibrio cholerae strains isolated from clinical specimens. Acta Microbiol Immunol Hung 59:77–84 [CrossRef][PubMed]
    [Google Scholar]
  41. Ramamurthy T., Bag P. K., Pal A., Bhattacharya S. K., Bhattacharya M. K., Shimada T., Takeda T., Karasawa T., Kurazono H.& other authors ( 1993; Virulence patterns of Vibrio cholerae non-O1 strains isolated from hospitalised patients with acute diarrhoea in Calcutta, India. J Med Microbiol 39:310–317 [CrossRef][PubMed]
    [Google Scholar]
  42. Ranjbar R., Rahbar M., Naghoni A., Farshad S., Davari A., Shahcheraghi F. 2011; A cholera outbreak associated with drinking contaminated well water. Arch Iran Med 14:339–340[PubMed]
    [Google Scholar]
  43. 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]
  44. Sack D. A., Sack R. B., Nair G. B., Siddique A. K. 2004; Cholera. Lancet 363:223–233 [CrossRef][PubMed]
    [Google Scholar]
  45. Schild S., Bishop A. L., Camilli A. 2008; Ins and outs of Vibrio cholerae. Vibrio cholerae transitions between the human gut and the aquatic environment are aided by specific shifts in gene expression. Microbe 3:131–136
    [Google Scholar]
  46. Seo K. H., Valentin-Bon I. E., Brackett R. E. 2006; Detection and enumeration of Salmonella enteritidis in homemade ice cream associated with an outbreak: comparison of conventional and real-time PCR methods. J Food Prot 69:639–643[PubMed]
    [Google Scholar]
  47. Simanjuntak C. H., Larasati W., Arjoso S., Putri M., Lesmana M., Oyofo B. A., Sukri N., Nurdin D., Kusumaningrum R. P.& other authors ( 2001; Cholera in Indonesia in 1993–1999. Am J Trop Med Hyg 65:788–797[PubMed]
    [Google Scholar]
  48. Singh D. V., Isac S. R., Colwell R. R. 2002; Development of a hexaplex PCR assay for rapid detection of virulence and regulatory genes in Vibrio cholerae and Vibrio mimicus. J Clin Microbiol 40:4321–4324 [CrossRef][PubMed]
    [Google Scholar]
  49. Smith A. M., Keddy K. H., De Wee L. 2008; Characterization of cholera outbreak isolates from Namibia, December 2006 to February 2007. Epidemiol Infect 136:1207–1209 [CrossRef][PubMed]
    [Google Scholar]
  50. Stroeher U. H., Karageorgos L. E., Morona R., Manning P. A. 1992; Serotype conversion in Vibrio cholerae O1. Proc Natl Acad Sci U S A 89:2566–2570 [CrossRef][PubMed]
    [Google Scholar]
  51. Sur D., Dutta S., Sarkar B. L., Manna B., Bhattacharya M. K., Datta K. K., Saha A., Dutta B., Pazhani G. P.& other authors ( 2007; Occurrence, significance and molecular epidemiology of cholera outbreaks in West Bengal. Indian J Med Res 125:772–776[PubMed]
    [Google Scholar]
  52. Tjaniadi P., Lesmana M., Subekti D., Machpud N., Komalarini S., Santoso W., Simanjuntak C. H., Punjabi N., Campbell J. R.& other authors ( 2003; Antimicrobial resistance of bacterial pathogens associated with diarrheal patients in Indonesia. Am J Trop Med Hyg 68:666–670[PubMed]
    [Google Scholar]
  53. Villeneuve S., Boutonnier A., Mulard L. A., Fournier J. M. 1999; Immunochemical characterization of an Ogawa–Inaba common antigenic determinant of Vibrio cholerae O1. Microbiology 145:2477–2484[PubMed]
    [Google Scholar]
  54. Waldor M. K., Mekalanos J. J. 1994; ToxR regulates virulence gene expression in non-O1 strains of Vibrio cholerae that cause epidemic cholera. Infect Immun 62:72–78[PubMed]
    [Google Scholar]
  55. Waturangi D. E., Fransiska M. 2009; Rapid detection of virulence genes and class 1 integron in Vibrio cholerae from edible ice in Jakarta. Microbiol Indones J 3:133–138 [CrossRef]
    [Google Scholar]
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