Skip to main content
SpringerLink
Log in

Investigation of antibiotic resistance profile and TEM-type β-lactamase gene carriage of ampicillin-resistantEscherichia coli strains isolated from drinking water

  • Applied Microbiology
  • Original Articles
  • Published:
Annals of Microbiology Aims and scope Submit manuscript

Abstract

Fifty-five ampicillin-resistant (Ampr)Escherichia coli strains were isolated from 51 drinking water points in Rize region containing abundant fresh water sources in Turkey during the years 2000 to 2002 and from January to February 2004. The large number of organisms (nearly 57%) exhibited resistance to three or more antibiotics commonly used in human and veterinary medicine. These strains displayed a multiresistant phenotype. Nearly half of the strains (27%) expressed resistance to ceftazidime, but these strains were not an extended-spectrum β-lactamase-producer according to the results of double-disk synergy test. All isolates were then screened for the carriage of TEM-type β-lactamase gene (bla TEM) by polymerase chain reaction. TEM-type β-lactamase genes were found in six (11%) isolates. Sequence analysis showed TEM-1 type genes. However, isoelectric focusing analysis did not confirm the production of TEM-1 type β-lactamase except for one strain. Conjugation experiments showed that resistance to ampicillin, tetracycline or trimethoprim/sulfamethoxazole was transferable in six (11%) isolates. Emergence of transferable antibiotic resistance andbla TEM-1 gene inE. coli strains from public drinking waters possesses a significant public health risk.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Al-Ghazali M.R., Jazrawi S.F., Al-Doori Z.A. (1988). Antibiotic resistance among pollution indicator bacteria isolated from Al-Khair River, Baghdad. Water Res., 22: 641–644.

    Article  CAS  Google Scholar 

  • Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., and Lipman D.J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res., 25: 3389–3402.

    Article  CAS  PubMed  Google Scholar 

  • Arlet G., Philippon A. (1991). Construction by polymerase chain reaction and use of intragenic DNA probes for three main types of transferable b-lactamases (TEM, SHV, CARB). FEMS Microbiol. Lett., 82: 19–26.

    CAS  Google Scholar 

  • Arlet G., Brami G., Décrè D., Flippo A., Gaillot O., Lagrange P.H., Philippon A. (1995). Molecular chracterisation by PCR-restriction fragment length polymorphism of TEM β-lactamases. FEMS Microbiol. Lett., 134: 203–208.

    CAS  PubMed  Google Scholar 

  • Ausubel F.M., Brent R., Kingston R.E., Moore D.D., Seidman J.G., Smith J.A., Struhl K. (1995). Short Protocols in Molecular Biology, 2nd edn., John Willey & Sons, New York.

    Google Scholar 

  • Boon P.I., Cattanach M. (1999). Antibiotic resistance of native and faecal bacteria isolated from rivers, reservoirs and sewage treatment facilities in Victoria, South-Eastern Australia. Lett. Appl. Microbiol., 28: 164–168.

    Article  CAS  PubMed  Google Scholar 

  • Brenner D.J. (1986). Facultatively anaerobic Gram-negative rods. In: Krieg N.R., Holt J.G., Eds. Bergey’s Manual of Systematic Bacteriology, Vol. 1, Williams & Wilkins, Baltimore, pp. 408–516.

    Google Scholar 

  • Bush K., Jacoby G.A. (1997). Nomenclature of TEM β-lactamases. J. Antimicrob. Chemother., 39: 1–3.

    Article  CAS  PubMed  Google Scholar 

  • CLSI — Clinical and Laboratory Standards Institute (2003). Performance standards for antimicrobial disk susceptibility tests, 8th edn., Approved standard M2-A8, CLSI, Wayne, PA, USA.

    Google Scholar 

  • Col N.F., O’Connor R.W. (1987). Estimating worldwide current antibiotic usage: Report of task force I. Rev. Infect. Dis., 9: S232-S243.

    PubMed  Google Scholar 

  • Du Pont H.L., Steele J.H. (1987). Use of antimicrobial agents in animal feeds: Implications for human health. Rev. Infect. Dis., 9: 447–460.

    Google Scholar 

  • Gaur A., Ramteke P.W., Pathak S.P., Bhattacherjee J.W. (1992). Transferable antibiotic resistance among thermotolerant coliforms from rural drinking water in India. Epidemiol. Infect., 109: 113–120.

    CAS  PubMed  Google Scholar 

  • Halling-Sørensen B., Nors Nielsen S., Lanzky P.F., Ingerslev F., Holten Lützhøft H.C., Jørgensen S.E. (1998). Ocurrence, fate and effects of pharmaceutical substances in the environment-A review. Chemosphere, 36: 357–393.

    Article  PubMed  Google Scholar 

  • Harwood V.J., Whitlock J., Withington V. (2000). Classification of antibiotic resistance patterns of indicator bacteria by discriminant analysis: Use in predicting the source of fecal contamination in subtropical waters. Appl. Environ. Microbiol., 66: 3698–3704.

    Article  CAS  PubMed  Google Scholar 

  • Henriques I., Moura A., Alves A., Saavedra M.J., Correia A. (2006). Analysing diversity among β-lactamase encoding genes in aquatic environments. FEMS Microbiol. Ecol., 56: 418–429.

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann H., Sturenburg E., Heesemann J., Roggenkamp A. (2006). Prevalence of extended-spectrum β-lactamases in isolates of theEnterobacter cloacae complex from German hospitals. Clin. Microbiol. Infect., 12: 322–330.

    Article  CAS  PubMed  Google Scholar 

  • Jarlier V., Nicolas M.H., Fournier G., Philippon A. (1988). Extended broad-spectrum β-lactamases conferring transferable resistance to newer β-lactam agents inEnterobacteriaceae: hospital prevalence and susceptibility patterns. Rev. Infect. Dis., 10: 867–878.

    CAS  PubMed  Google Scholar 

  • Jones J.G., Gardener S., Simon B.M., Pickup R.W. (1986). Antibiotic resistant bacteria in Windermere and two remote upland tarns in the English Lake district. J. Appl. Bacteriol., 60: 443–453.

    CAS  PubMed  Google Scholar 

  • Krcmery V., Bajizukova A., Langsadl L., Kotuliakova M., Sobotova O. (1989). Evaluation of the resistance ofEnterobacteriaceae strains to antibiotics-comparison of strains from clinical material versus environment. J. Hyg. Epidemiol. Microbiol. Immun., 33: 299–304.

    CAS  Google Scholar 

  • Kruse H. (1999). Indirect transfer of antibiotic resistance genes to man. Acta Veter. Scand., 92 (suppl.): 59–65.

    CAS  Google Scholar 

  • Livermore D.M. (1995). β-Lactamases in laboratory and clinical resistance. Clin. Microbiol. Rev., 8: 557–584.

    CAS  PubMed  Google Scholar 

  • Livermore D.M. (1998). β-Lactamase-mediated resistance and opportunities for its control. J. Antimicrob. Chemother., 41(Suppl. D): 25–41.

    Article  CAS  PubMed  Google Scholar 

  • Martinez J.L., Cercenado E., Rodriguez-Creixems M., Vicente-Perez M.F., Delgado-Iribarren A., Baquero F. (1987). Resistance to β-lactam/clavulanate. Lancet: 1473.

  • Matthew M., Harris A.M., Marshall J.M., Ross G.W. (1975). The use of analytic isoelectric focusing for detection and identification of β-lactamases. J. Gen. Microbiol., 88: 169–178.

    Google Scholar 

  • Matyar F., Dincer S., Kaya A., Colak O. (2004). Prevalence and resistance to antibiotics in Gram negative bacteria isolated from retail fish in Turkey. Ann. Microbiol., 54: 151–160.

    CAS  Google Scholar 

  • Mendonca N., Louro D., Castro A.P., Diogo J., Canica M. (2006). CTX-M-15, OXA-30 and TEM-1-producingEscherichia coli in two Portuguese regions. J. Antimicrob. Chemother., 57: 1014–1016.

    Article  CAS  PubMed  Google Scholar 

  • Mezrioui N., Baleux B. (1994). Resistance patterns ofEscherichia coli strains isolated from domestic sewage before and after treatment in both aerobic lagoon and activated sludge. Water Res., 28: 2399–2406.

    Article  Google Scholar 

  • Misra D.S., Kumar A., Singh I.P. (1979). Antibiotic resistance and transfer factor (R+) inEscherichia coli isolated from raw sewage. Indian J. Med. Res., 70: 559–562.

    CAS  PubMed  Google Scholar 

  • Ozgumus O.B., Tosun I., Aydin F., Kilic A.O., Erturk M. (2006). Carriage of mobilizable plasmid-mediated β-lactamase gene in ampicillin-resistantEscherichia coli strains with origin of normal fecal flora. Turk. J. Med. Sci., 36: 307–314.

    CAS  Google Scholar 

  • Ozgumus, O.B., Tosun, I., Aydin, F., Kilic, A.O. (2002). Non-conjugative plasmids encoding TEM-type b-lactamase in clinical isolates ofEscherichia coli. Infek. Derg., 16: 329–333.

    Google Scholar 

  • Papandreou S., Pagonopoulou O., Vantarakis A., Papapetropoulou M. (2000). Multiantibiotic resistance of Gram-negative bacteria isolated from drinking water samples in Southwest Greece. J. Chemother., 12: 267–273.

    CAS  PubMed  Google Scholar 

  • Pathak S.P., Bhattacherjee J.W., Ray P.K. (1993). Seasonal variation in survival and antibiotic resistance among various bacterial populations in a tropical river. J. Gen. Appl. Microbiol., 39: 47–56.

    Article  Google Scholar 

  • Reinthaler F.F., Posch J., Feierl G., Wust G., Haas D., Ruckenbauer G., Mascher F., Marth E. (2003). Antibiotic resistance ofEscherichia coli in sewage and sludge. Water Res., 37: 1685–1690.

    Article  CAS  PubMed  Google Scholar 

  • Rice L.B., Willey S.H., Papanicolaou G.A., Medeiros A.A., Eliopoulos G.M., Moellering R.C. Jr., Jacoby G.A. (1990). Outbreak of ceftazidime resistance caused by extended-spectrum β-lactamases at a Massachusetts chronic care facility. Antimicrob. Agents Chemother., 34: 2193–2199.

    CAS  PubMed  Google Scholar 

  • Roe M.T., Vega E., Pillai S.D. (2003). Antimicrobial resistance markers of Class 1 and Class 2 integron bearingEscherichia coli from irrigation water and sediments. Emerg. Infect. Dis., 9: 822–826.

    CAS  PubMed  Google Scholar 

  • Schwartz T., Kohnen W., Jansen B., Obst U. (2003). Detection of antibiotic-resistant bacteria and their resistance genes in wastewater, surface water, and drinking water biofilms. FEMS Microbiol. Ecol., 43: 325–335.

    Article  CAS  PubMed  Google Scholar 

  • Sirot D., Recule C., Chaibi E.B., Bret L., Croize J., Chanal-Claris C., Labia R., Sirot J.A. (1997). Complex mutant of TEM-1 β-lactamase with mutations encountered in both IRT-4 and extended spectrum TEM-15, produced by anEscherichia coli clinical isolate. Antimicrob. Agents Chemother., 41: 1322–1325.

    CAS  PubMed  Google Scholar 

  • Tamanai-Shacoori Z., Arturo M., Pommepuy M., Mamez C., Cormier M. (1995). Conjugal transfer of natural plasmids betweenEscherichia coli strains in sterile environmental water. Cur. Microbiol., 30: 155–160.

    Article  CAS  Google Scholar 

  • Tauxe R.V. (1997). Emerging foodborne diseases: An evolving public health challenge. Emerg. Infect. Dis., 3: 425–434.

    Article  CAS  PubMed  Google Scholar 

  • Tomasz A. (1994). Multiple-antibiotic-resistant pathogenic bacteria: A report on the Rockfeller University Workshop. North. Eng. J. Med., 330: 1247–1251.

    Article  CAS  Google Scholar 

  • Toroglu S., Dincer S., Korkmaz H. (2005). Antibiotic resistance in Gram negative bacteria isolated from Aksu River in (Kahramanmaras) Turkey. Ann. Microbiol., 55: 229–233.

    CAS  Google Scholar 

  • Walia S.K., Kaiser A., Parkash M., Chaudhry G.R. (2004). Self-transmissible antibiotic resistance to ampicillin, streptomycin, and tetracycline found inEscherichia coli isolates from contaminated drinking water. J. Environ. Sci. Health Part A Tox. Hazard. Subst. Environ. Eng., 39: 651–662.

    Google Scholar 

  • Wiggins B.A., Andrews R.W., Conway R.A., Corr C.L., Dobratz E.J., Dougherty D.P., Eppard F.R., Knupp S.R., Limjoco M.C., Mettenburg J.M., Rinehardt J.M., Sonsino J., Torrijos R.L., Zimmerman M.E. (1999). Use of antibiotic resistance analysis to identify nonpoint sources of fecal pollution. Appl. Environ. Microbiol., 65: 3483–3486.

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, Faculty of Arts and Sciences, Rize University, 53100, Rize, Turkey

    Sengul Alpay-Karaoglu, Osman Birol Ozgumus, Elif Sevim, Ali Sevim & Pinar Yesilgil

  2. Department of Medical Microbiology, Faculty of Medicine, Kocaeli University, 41900, Kocaeli, Turkey

    Fetiye Kolayli

Authors
  1. Sengul Alpay-Karaoglu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Osman Birol Ozgumus
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Elif Sevim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fetiye Kolayli
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ali Sevim
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Pinar Yesilgil
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Osman Birol Ozgumus.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Alpay-Karaoglu, S., Ozgumus, O.B., Sevim, E. et al. Investigation of antibiotic resistance profile and TEM-type β-lactamase gene carriage of ampicillin-resistantEscherichia coli strains isolated from drinking water. Ann. Microbiol. 57, 281–288 (2007). https://doi.org/10.1007/BF03175221

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF03175221

Key words

Search

Navigation