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Journal of Medical Microbiology logo Journal of Medical Microbiology

Volume 64, Issue 10

Comparative analysis of virulence determinants, antibiotic susceptibility patterns and serogrouping of atypical enteropathogenic versus typical enteropathogenic in India No Access

Abstract

The epidemiology of enteropathogenic (EPEC) and the significance of isolation of atypical EPEC (aEPEC) in childhood diarrhoea have not been well studied in an Indian context. A comparative study was undertaken to investigate virulence determinants, antibiotic susceptibility patterns and serogrouping of typical EPEC (tEPEC) versus aEPEC causing diarrhoea in children. A total of 400 prospective and 500 retrospective isolates were included. PCR was performed for , , , , , , and genes. The Clinical and Laboratory Standards Institute's disc diffusion test was used to determine the antimicrobial susceptibility. Phenotypic screening of extended spectrum β-lactamases (ESBLs), AmpC and carbapenemase (KPC) production, and molecular detection of , , , and were performed. aEPEC (57.6 %) were more common as compared with tEPEC (42.3 %). The occurrence of virulence genes was observed to be three times higher in aEPEC as compared with tEPEC, (14.7 % of aEPEC, 4 % of tEPEC) being the most common. Most of the isolates did not belong to the classical EPEC O-serogroups. The highest resistance was observed against amoxicillin (93.22 %) followed by quinolones (83 %), cephalosporins (37.28 %), cotrimoxazole (35.59 %) and carbapenems (30.5 %). Overall equal numbers of aEPEC (41.17 %) and tEPEC (40 %) were observed to be multidrug-resistant. Fifteen EPEC strains demonstrated presence of ESBLs, five produced AmpC and four each produced metallo-β-lactamases and KPC-type carbapenemases; eight, seven and one isolate(s) each were positive for , and , respectively. Here, to the best of our knowledge, we report for the first time on carbapenem resistance and the presence of and in EPEC isolates from India.

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© 2015 The Authors
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2015-10-01
2025-12-16

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References

  1. Afset J. E., Bruant G., Brousseau R., Harel J., Anderssen E., Bevanger L., Bergh K. 2006; Identification of virulence genes linked with diarrhea due to atypical enteropathogenic Escherichia coli by DNA microarray analysis and PCR. J Clin Microbiol 44:3703–3711 [View Article][PubMed]
     [Google Scholar]
  2. Albert M. J., Rotimi V. O., Dhar R., Silpikurian S., Pacsa A. S., Molla A. M., Szucs G. 2009; Diarrhoeagenic Escherichia coli are not a significant cause of diarrhoea in hospitalised children in Kuwait. BMC Microbiol 9:62 [View Article][PubMed]
     [Google Scholar]
  3. Aranda K. R. S., Fagundes-Neto U., Scaletsky I. C. A. 2004; Evaluation of multiplex PCRs for diagnosis of infection with diarrheagenic Escherichia coli and Shigella spp. J Clin Microbiol 42:5849–5853 [View Article][PubMed]
     [Google Scholar]
  4. Batisson I., Guimond M. P., Girard F., An H., Zhu C., Oswald E., Fairbrother J. M., Jacques M., Harel J. 2003; Characterization of the novel factor paa involved in the early steps of the adhesion mechanism of attaching and effacing Escherichia coli. Infect Immun 71:4516–4525 [View Article][PubMed]
     [Google Scholar]
  5. Black J. A., Moland E. S., Thomson K. S. 2005; AmpC disk test for detection of plasmid-mediated AmpC β-lactamases in Enterobacteriaceae lacking chromosomal AmpC β-lactamases. J Clin Microbiol 43:3110–3113 [View Article][PubMed]
     [Google Scholar]
  6. Bouzari S., Varghese A. 1990; Cytolethal distending toxin (CLDT) production by enteropathogenic Escherichia coli (EPEC). FEMS Microbiol Lett 71:193–198 [View Article][PubMed]
     [Google Scholar]
  7. Brian M. J., Frosolono M., Murray B. E., Miranda A., Lopez E. L., Gomez H. F., Cleary T. G. 1992; Polymerase chain reaction for diagnosis of enterohemorrhagic Escherichia coli infection and hemolytic-uremic syndrome. J Clin Microbiol 30:1801–1806[PubMed]
     [Google Scholar]
  8. CLSI 2011 Performance Standards for Antimicrobial Susceptibility Testing 21st Informational Supplement M100-S21 Wayne, PA: Clinical and Laboratory Standards Institute;
     [Google Scholar]
  9. Cortes-Bratti X., Chaves-Olarte E., Lagergård T., Thelestam M. 1999; The cytolethal distending toxin from the chancroid bacterium Haemophilus ducreyi induces cell-cycle arrest in the G2 phase. J Clin Invest 103:107–115 [View Article][PubMed]
     [Google Scholar]
  10. Croxen M. A., Law R. J., Scholz R., Keeney K. M., Wlodarska M., Finlay B. B. 2013; Recent advances in understanding enteric pathogenic Escherichia coli. Clin Microbiol Rev 26:822–880 [View Article][PubMed]
     [Google Scholar]
  11. Ellington M. J., Kistler J., Livermore D. M., Woodford N. 2007; Multiplex PCR for rapid detection of genes encoding acquired metallo-β-lactamases. J Antimicrob Chemother 59:321–322 [View Article][PubMed]
     [Google Scholar]
  12. Estrada-García T., Cerna J. F., Paheco-Gil L., Velázquez R. F., Ochoa T. J., Torres J., DuPont H. L. 2005; Drug-resistant diarrheogenic Escherichia coli, Mexico. Emerg Infect Dis 11:1306–1308 [View Article][PubMed]
     [Google Scholar]
  13. Gannon V. P., Rashed M., King R. K., Thomas E. J. 1993; Detection and characterization of the eae gene of Shiga-like toxin-producing Escherichia coli using polymerase chain reaction. J Clin Microbiol 31:1268–1274[PubMed]
     [Google Scholar]
  14. Ghosh P. K., Ali A. 2010; Isolation of atypical enteropathogenic Escherichia coli from children with and without diarrhoea in Delhi and the National Capital Region, India. J Med Microbiol 59:1156–1162 [View Article][PubMed]
     [Google Scholar]
  15. Giammanco A., Maggio M., Giammanco G., Morelli R., Minelli F., Scheutz F., Caprioli A. 1996; Characteristics of Escherichia coli strains belonging to enteropathogenic E. coli serogroups isolated in Italy from children with diarrhea. J Clin Microbiol 34:689–694[PubMed]
     [Google Scholar]
  16. Gunzburg S. T., Tornieporth N. G., Riley L. W. 1995; Identification of enteropathogenic Escherichia coli by PCR-based detection of the bundle-forming pilus gene. J Clin Microbiol 33:1375–1377[PubMed]
     [Google Scholar]
  17. Guth B. E., Giraldi R., Gomes T. A., Marques L. R. 1994; Survey of cytotoxin production among Escherichia coli strains characterized as enteropathogenic (EPEC) by serotyping and presence of EPEC adherence factor (EAF) sequences. Can J Microbiol 40:341–344 [View Article][PubMed]
     [Google Scholar]
  18. Hernandes R. T., Elias W. P., Vieira M. A. M., Gomes T. A. T. 2009; An overview of atypical enteropathogenic Escherichia coli. FEMS Microbiol Lett 297:137–149 [View Article][PubMed]
     [Google Scholar]
  19. Iroha I. R., Esimone C. O., Neumann S., Marlinghaus L., Korte M., Szabados F., Gatermann S., Kaase M. 2012; First description of Escherichia coli producing CTX-M-15-extended spectrum beta lactamase (ESBL) in out-patients from south eastern Nigeria. Ann Clin Microbiol Antimicrob 11:19 [View Article][PubMed]
     [Google Scholar]
  20. Isenberg H. D.editor 2004 Clinical Microbiology Procedures Handbook Washington, DC: American Society for Microbiology;
     [Google Scholar]
  21. Johnson W. M., Lior H. 1987; Response of Chinese hamster ovary cells to a cytolethal distending toxin (CDT) of Escherichia coli and possible misinterpretation as heat-labile (LT) enterotoxin. FEMS Microbiol Lett 43:19–23 [View Article]
     [Google Scholar]
  22. Kelly M., Hart E., Mundy R., Marchès O., Wiles S., Badea L., Luck S., Tauschek M., Frankel G., other authors. 2006; Essential role of the type III secretion system effector NleB in colonization of mice by Citrobacter rodentium. Infect Immun 74:2328–2337 [View Article][PubMed]
     [Google Scholar]
  23. Kim J. H., Kim J. C., Choo Y. A., Jang H. C., Choi Y. H., Chung J. K., Cho S. H., Park M. S., Lee B. K. 2009; Detection of cytolethal distending toxin and other virulence characteristics of enteropathogenic Escherichia coli isolates from diarrheal patients in Republic of Korea. J Microbiol Biotechnol 19:525–529 [View Article][PubMed]
     [Google Scholar]
  24. Lee K., Lim Y. S., Yong D., Yum J. H., Chong Y. 2003; Evaluation of the Hodge test and the imipenem-EDTA double-disk synergy test for differentiating metallo-β-lactamase-producing isolates of Pseudomonas spp. and Acinetobacter spp. J Clin Microbiol 41:4623–4629 [View Article][PubMed]
     [Google Scholar]
  25. Levine M. M., Ferreccio C., Prado V., Cayazzo M., Abrego P., Martinez J., Maggi L., Baldini M. M., Martin W., other authors. 1993; Epidemiologic studies of Escherichia coli diarrheal infections in a low socioeconomic level peri-urban community in Santiago, Chile. Am J Epidemiol 138:849–869[PubMed]
     [Google Scholar]
  26. Lietzau S., Raum E., von Baum H., Marre R., Brenner H. 2007; Household contacts were key factor for children's colonization with resistant Escherichia coli in community setting. J Clin Epidemiol 60:1149–1155 [View Article][PubMed]
     [Google Scholar]
  27. Morabito S., Tozzoli R., Oswald E., Caprioli A. 2003; A mosaic pathogenicity island made up of the locus of enterocyte effacement and a pathogenicity island of Escherichia coli O157 : H7 is frequently present in attaching and effacing E. coli. Infect Immun 71:3343–3348 [View Article][PubMed]
     [Google Scholar]
  28. Nakhjavani F. A., Emaneini M., Hosseini H., Iman-Eini H., Aligholi M., Jabalameli F., Haghi-Ashtiani M. T., Taherikalani M., Mirsalehian A. 2013; Molecular analysis of typical and atypical enteropathogenic Escherichia coli (EPEC) isolated from children with diarrhoea. J Med Microbiol 62:191–195 [View Article][PubMed]
     [Google Scholar]
  29. Nguyen T. V., Le Van P., Le Huy C., Gia K. N., Weintraub A. 2005; Detection and characterization of diarrheagenic Escherichia coli from young children in Hanoi, Vietnam. J Clin Microbiol 43:755–760 [View Article][PubMed]
     [Google Scholar]
  30. Nicholls L., Grant T. H., Robins-Browne R. M. 2000; Identification of a novel genetic locus that is required for in vitro adhesion of a clinical isolate of enterohaemorrhagic Escherichia coli to epithelial cells. Mol Microbiol 35:275–288 [View Article][PubMed]
     [Google Scholar]
  31. Ochoa T. J., Contreras C. A. 2011; Enteropathogenic Escherichia coli infection in children. Curr Opin Infect Dis 24:478–483 [View Article][PubMed]
     [Google Scholar]
  32. Ochoa T. J., Barletta F., Contreras C., Mercado E. 2008; New insights into the epidemiology of enteropathogenic Escherichia coli infection. Trans R Soc Trop Med Hyg 102:852–856 [View Article][PubMed]
     [Google Scholar]
  33. Okuda J., Kurazono H., Takeda Y. 1995; Distribution of the cytolethal distending toxin A gene (cdtA) among species of Shigella and Vibrio, and cloning and sequencing of the cdt gene from Shigella dysenteriae. Microb Pathog 18:167–172 [View Article][PubMed]
     [Google Scholar]
  34. Poirel L., Walsh T. R., Cuvillier V., Nordmann P. 2011; Multiplex PCR for detection of acquired carbapenemase genes. Diagn Microbiol Infect Dis 70:119–123 [View Article][PubMed]
     [Google Scholar]
  35. Ratchtrachenchai O. A., Subpasu S., Hayashi H., Ba-Thein W. 2004; Prevalence of childhood diarrhoea-associated Escherichia coli in Thailand. J Med Microbiol 53:237–243 [View Article][PubMed]
     [Google Scholar]
  36. Rosa A. C. P., Mariano A. T., Pereira A. M. S., Tibana A., Gomes T. A. T., Andrade J. R. C. 1998; Enteropathogenicity markers in Escherichia coli isolated from infants with acute diarrhoea and healthy controls in Rio de Janeiro, Brazil. J Med Microbiol 47:781–790 [View Article][PubMed]
     [Google Scholar]
  37. Rothbaum R. J., Partin J. C., Saalfield K., McAdams A. J. 1983; An ultrastructural study of enteropathogenic Escherichia coli infection in human infants. Ultrastruct Pathol 4:291–304 [View Article][PubMed]
     [Google Scholar]
  38. Scotland S. M., Smith H. R., Cheasty T., Said B., Willshaw G. A., Stokes N., Rowe B. 1996; Use of gene probes and adhesion tests to characterise Escherichia coli belonging to enteropathogenic serogroups isolated in the United Kingdom. J Med Microbiol 44:438–443 [View Article][PubMed]
     [Google Scholar]
  39. Shetty V. A., Kumar S. H., Shetty A. K., Karunasagar I., Karunasagar I. 2012; Prevalence and characterization of diarrheagenic Escherichia coli isolated from adults and children in Mangalore, India. J Lab Physicians 4:24–29 [View Article][PubMed]
     [Google Scholar]
  40. Thorén A., Wolde-Mariam T., Stintzing G., Wadström T., Habte D. 1980; Antibiotics in the treatment of gastroenteritis caused by enteropathogenic Escherichia coli. J Infect Dis 141:27–31 [View Article][PubMed]
     [Google Scholar]
  41. Tilak G. P., Mudaliar J. L. 2012; Role of enteropathogenic Escherichia coli in paediatric diarrhoeas in South India. Mater Sociomed 24:178–181 [View Article][PubMed]
     [Google Scholar]
  42. Toma C., Martínez Espinosa E., Song T., Miliwebsky E., Chinen I., Iyoda S., Iwanaga M., Rivas M. 2004; Distribution of putative adhesins in different seropathotypes of Shiga toxin-producing Escherichia coli. J Clin Microbiol 42:4937–4946 [View Article][PubMed]
     [Google Scholar]
  43. Trabulsi L. R., Keller R., Tardelli Gomes T. A. 2002; Typical and atypical enteropathogenic Escherichia coli. Emerg Infect Dis 8:508–513 [View Article][PubMed]
     [Google Scholar]
  44. Vieira M. A. M., Salvador F. A., Silva R. M., Irino K., Vaz T. M. I., Rockstroh A. C., Guth B. E. C., Gomes T. A. T. 2010; Prevalence and characteristics of the O122 pathogenicity island in typical and atypical enteropathogenic Escherichia coli strains. J Clin Microbiol 48:1452–1455 [View Article][PubMed]
     [Google Scholar]
  45. Wani S. A., Nabi A., Fayaz I., Ahmad I., Nishikawa Y., Qureshi K., Khan M. A., Chowdhary J. 2006; Investigation of diarrhoeic faecal samples for enterotoxigenic, Shiga toxin-producing and typical or atypical enteropathogenic Escherichia coli in Kashmir, India. FEMS Microbiol Lett 261:238–244 [View Article][PubMed]
     [Google Scholar]
  46. WHO/UNICEF 2009; Diarrhoea: why children are still dying and what can be done.. http://www.unicef.org/media/files/Final_Diarrhoea_Report_October_2009_final.pdf
  47. Zurawski D. V., Mumy K. L., Badea L., Prentice J. A., Hartland E. L., McCormick B. A., Maurelli A. T. 2008; The NleE/OspZ family of effector proteins is required for polymorphonuclear transepithelial migration, a characteristic shared by enteropathogenic Escherichia coli and Shigella flexneri infections. Infect Immun 76:369–379 [View Article][PubMed]
     [Google Scholar]
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Comparative analysis of virulence determinants, antibiotic susceptibility patterns and serogrouping of atypical enteropathogenic Escherichia coli versus typical enteropathogenic E. coli in India
J. Med. Microbiol. 64, 1208 (2015); https://doi.org/10.1099/jmm.0.000131
/content/journal/jmm/10.1099/jmm.0.000131
/content/journal/jmm/10.1099/jmm.0.000131
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