Molecular Characterization of Extended-Spectrum β-Lactamase Enterobacteriaceae Isolated from Egyptian Patients with Community- and Hospital-Acquired Urinary Tract Infection

Rania Y. Shash Medical Microbiology and Immunology Department, Faculty of Medicine, Cairo University, Cairo, Egypt;

Search for other papers by Rania Y. Shash in
Current site
Google Scholar
PubMed
Close
,
Amal A. Elshimy Medical Microbiology and Immunology Department, Faculty of Medicine, Cairo University, Cairo, Egypt;
Medical Microbiology and Immunology Department, Faculty of Medicine, New Giza University, Giza, Egypt;

Search for other papers by Amal A. Elshimy in
Current site
Google Scholar
PubMed
Close
,
Mohammed Y. Soliman Medical Microbiology and Immunology Department, Faculty of Medicine, Cairo University, Cairo, Egypt;

Search for other papers by Mohammed Y. Soliman in
Current site
Google Scholar
PubMed
Close
, and
Ashraf A. Mosharafa Urology Department, Faculty of Medicine, Cairo University, Cairo, Egypt

Search for other papers by Ashraf A. Mosharafa in
Current site
Google Scholar
PubMed
Close
Restricted access

Extended-spectrum β-lactamases (ESβLs) pose a serious problem in the treatment of urinary tract infections (UTIs). The ESβL-producing organism is an expanding global health problem. Therefore, screening for ESβL, detection of their drug-resistance pattern, and molecular characterization should be a continuous process. The present study was performed to determine the antibiotic resistance profile and the genetic characterization of ESβL isolates from hospital- and community-acquired UTIs. Two hundred fifty Enterobacteriaceae isolates were obtained from urine samples of outpatient clinic attendants and hospitalized patients at Kasr Al-Aini Hospital. By phenotypic screening tests, 100 ESβL isolates were detected among the studied groups. Furthermore, detection of beta-lactamase (bla) cefotaxime (CTX)-M, sulfhydryl variable, and temoneira ESβL genes was investigated by polymerase chain reaction. A subset of 25 CTX-M–positive isolates was further identified by gene sequencing technology. Among the 100 ESβL isolates, 66% were Escherichia coli and 34% were Klebsiella spp. There was no statistical difference in the prevalence of ESβL Enterobacteriaceae in community-acquired versus hospital-acquired UTIs. The susceptibility of all ESβL isolates to carbapenems was the most prevalent finding. In addition, all ESβL E. coli isolates were susceptible to fosfomycin, whereas all community-acquired ESβL isolates were susceptible to nitrofurantoin. A total of 98% of the ESβL isolates harbored bla-CTX-M genes, with CTX-M-15 being the most prevalent. It could be concluded that ESβL production is present at a high rate among Egyptian patients with hospital- and community-acquired UTI. The high prevalence of bla-CTX-M may suggest it as a candidate for molecular screening of ESβL.

Author Notes

Address correspondence to Amal A. Elshimy, Medical Microbiology and Immunology Department, Faculty of Medicine, Cairo University, Kasr Al-Aini Hospital, Cairo, Egypt. E-mail: aelshimy@ngu.edu.eg

Authors’ addresses: Rania Y. Shash and Mohammed Y. Soliman, Medical Microbiology and Immunology Department, Faculty of Medicine, Cairo University, Cairo, Egypt, E-mails: raniayahiashash@hotmail.com and ysnassar@hotmail.com. Amal A. Elshimy, Medical Microbiology and Immunology Department, Faculty of Medicine, Cairo University, Cairo, Egypt, and Medical Microbiology and Immunology Department, Faculty of Medicine, New Giza University, Egypt, E-mail: aelshimy@ngu.edu.eg. Ashraf A. Mosharafa, Urology Department, Faculty of Medicine, Cairo University, Cairo, Egypt, E-mail: ashraf.mosharafa@kasralainy.edu.eg.

  • 1.

    Gupta K et al. 2011. International clinical practice guidelines for the treatment of acute uncomplicated cystitis and pyelonephritis in women: a 2010 update by the Infectious Diseases Society of America and the European Society for Microbiology and Infectious Diseases. Clin Infect Dis 52: e103e120.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2.

    Carlet J, Pittet D, 2013. Access to antibiotics: a safety and equity challenge for the next decade. Antimicrob Resist Infect Control 2: 1.

  • 3.

    Masud MR, Afroz H, Fakruddin M, 2014. Prevalence of extended-spectrum β-lactamase positive bacteria in radiologically positive urinary tract infection. Springerplus 3: 216.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Biehl LM, Schmidt-Hieber M, Liss B, Cornely OA, 2014. Colonization and infection with extended-spectrum beta-lactamase producing-Enterobacteriaceae in high-risk patients-review of the literature from a clinical perspective. Crit Rev Microbiol 42: 116.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Morosini MI, García-Castillo M, Coque TM, Valverde A, Novais A, Loza E, Baquero F, Cantón R, 2006. Antibiotic co-resistance in extended-spectrum-beta-lactamase-producing Enterobacteriaceae and invitro activity of tigecycline. Antimicrob Agents Chemother 50: 26952699.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Manyahi J, Moyo SJ, Tellevik MG, Ndugulile F, Urassa W, Blomberg B, Langeland N, 2017. Detection of CTX-M-15 beta-lactamases in Enterobacteriaceae causing hospital-and community-acquired urinary tract infections as early as 2004, in Dar es Salaam, Tanzania. BMC Infect Dis 17: 282.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Moghaddam MN, Beidokhti MH, Jamadar SA, Ghahraman M, 2014. Genetic properties of bla CTX-M and bla PER–beta-lactamase genes in clinical isolates of Enterobacteriaceae by polymerase chain reaction. Iran J Basic Med Sci 17: 378383.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Nisha KV, Veena SA, Rathika SD, Vijaya SM, Avinash SK, 2017. Antimicrobial susceptibility, risk factors, and prevalence of bla cefotaximase, temoneira, and sulfhydryl variable genes among Escherichia coli in community-acquired pediatric urinary tract infection. J Lab Physicians 9: 156162.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Djuikoue IC, Njajou O, Gonsu KH, Fokunang C, Bongo A, Bruno EO, Tanjung P, Linjouom A, Kakam C, Ngogang J, 2017. Prevalence of CTX-M beta-lactamases in Escherichia coli from community-acquired urinary tract infections and associated risk factors among women in Cameroon. J Epidemiol Res 3: 5156.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    De Oliveira CF, Salla A, Lara VM, Rieger A, Horta JA, Alves SH, 2010. Prevalence of extended-spectrum beta-lactamases-producing microorganisms in nosocomial patients and molecular characterization of the SHV-type isolates. Braz J Microbiol 41: 278282.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Salah M, Azab M, Halaby H, Hanora A, 2016. Mutations in β-lactamases detected in multidrug-resistant gram-negative bacteria isolated from community-acquired urinary tract infections in Assiut, Egypt. Afr J Microbiol Res 10: 19381943.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Ramadan DS, Bassyoni EA, Amer MM, Emam SM, 2016. Detection of ESBL producing bacteria in cases of urinary tract infection in pediatric department at Benha University Hospital. Egypt J Med Microbiol 25: 7784.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Valverde A, Coque TM, Sanchez-Moreno MP, Rollán A, Baquero F, Cantón R, 2004. The dramatic increase in the prevalence of fecal carriage of extended-spectrum-beta-lactamase-producing-Enterobacteriaceae during non-outbreak situations in Spain. J Clin Microbiol 42: 47694775.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Rodriguez-Bano J, Lopez-Cerero L, Navarro MD, Pascual A, 2008. Faecal carriage of extended-spectrum beta-lactamase-producing Escherichia coli: prevalence, risk factors and molecular epidemiology. J Antimicrob Chemother 62: 11421149.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Sullivan R, Schaus D, John M, Delport JA, 2015. Extended spectrum beta-lactamases: a mini review of clinical relevant groups. J Med Microb Diagn 4: 203.

  • 16.

    Cheesbrough M, 2006. Examination of urine. District Laboratory Practice in Tropical Countries , Part 2, 2nd edition. Cambridge University Press, 105115.

  • 17.

    Clinical and Laboratory Standards Institute, 2014. Performance Standards for Antimicrobial Susceptibility Testing: Twenty-Fourth Informational Supplement. Wayne, PA: CLSI M100-S24.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Koneman EW, Allen SD, Janda WM, Schreckenberger PC, Winn WC, 1997. Color Atlas and Textbook of Diagnostic Microbiology, 5th edition. Philadelphia, PA: J.B. Lippincott Company Press, 110145.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Heffernan H, Pope C, Carter P, 2007. Identification of Extended Spectrum Β-Lactamase Types, Plasmid-Mediated AmpC Β-Lactamases and Strains Among Urinary Escherichia coli and Klebsiella in New Zeland in 2006. Communicable Disease Group, Environmental Science and Research, FW07103.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Paterson DL, Bonomo RA, 2005. Extended spectrum β-lactamases: a clinical update. Clin Microbiol Rev 18: 657686.

  • 21.

    Chan YH, 2003a. Biostatistics102: quantitative data–parametric & non-parametric tests. Singapore Med J 44: 391396.

  • 22.

    Chan YH, 2003b. Biostatistics 103: qualitative data–tests of independence. Singapore Med J 44: 498503.

  • 23.

    Osthoff M, McGuinness SL, Wagen AZ, Eisen DP, 2015. Urinary tract infections due to extended-spectrum beta-lactamase-producing Gram-negative bacteria: identification of risk factors and outcome predictors in an Australian tertiary referral hospital. Int J Infect Dis 34: 7983.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Lee DS, Lee CB, Lee SJ, 2010. Prevalence and risk factors for extended spectrum beta-lactamase-producing uropathogens in patients with urinary tract infection. Korean J Urol 51: 492497.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Labah EA, Afifi IK, Ahmed LM, 2009. Community-acquired urinary tract infections in Tanta, Egypt: aetiology and antibiotics resistance pattern. Egypt J Med Microbiol 18: 179190.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Ibrahim MA, Agban MN, Thabit AG, El-Khamissy TR, Attia AE, 2014. Prevalence of extended-spectrum B-lactamase producing Klebsiella pneumoniae by phenotypic and genotypic methods in Assiut University Hospital. Egypt J Med Microbiol 23: 6170.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    El Bouamri MC, Arsalane L, Zerouali K, Kathy K, El Kamouni Y, Zouhair S, 2015. Molecular characterization of extended spectrum B-lactamase-producing Escherichia coli in a university hospital in Morocco, North Africa. Afr J Urol 21: 161166.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Kandeel A, 2014. Prevalence and risk factors of extended-spectrum β-lactamases producing Enterobacteriaceae in a general hospital in Saudi Arabia. J Microbiol Infect Dis 4: 5054.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Fadil AA, Hakeem MA, Abdelraheem AR, 2017. Esβl-producing E. coli and Klebsiella among patients treated at Minia University Hospitals. J Infect Dis Preve Med 5: 156163.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Al-Agamy MH, Shibil AM, Hafez MM, Al-Ahdal MN, Memish ZA, Khubnani H, 2014. Molecular characteristics of extended-spectrum-beta-lactamase-producing Escherichia coli in Riyadh: the emergence of CTX-M-15-producing E. coli ST131. Ann Clin Microbiol Antimicrob 13: 48.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Chandramohan L, Revell PA, 2012. Prevalence and molecular characterization of extended-spectrum—beta-lactamase—producing Enterobacteriaceae in a pediatric patient population. Antimicrob Agents Chemother 56: 47654770.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Ho PL, Yip KS, Chow KH, Lo JYC, Que TL, Yuen KY, 2010. Antimicrobial resistance among uropathogens that cause acute uncomplicated cystitis in women in Hong Kong: a prospective multicenter study from 2006 to 2008. Diagn Microbiol Infect Dis 66: 8793.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Antibiotic Expert Group, 2010. Therapeutic Guidelines: Antibiotic. Version 14. Melbourne, Australia: Therapeutic Guidelines Limited.

  • 34.

    Onnberg A, Mölling P, Zimmermann J, Söderquist B, 2011. Molecular and phenotypic characterization of Escherichia coli and Klebsiella pneumoniae producing extended-spectrum β-lactamases with focus on CTX-M in a low-endemic area in Sweden. APMIS 119: 287295.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35.

    Rezai MS, Salehifar E, Rafiei A, Langaee T, Rafati M, Shafahi K, 2015. Characterization of multidrug-resistant extended-spectrum beta-lactamase-producing Escherichia coli among uropathogens of pediatrics in north of Iran. Biomed Res Int 2015: 309478.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Bajpai T, Pandey M, Varma M, Bhatambare GS, 2017. Prevalence of TEM, SHV, and CTX-M Beta-Lactamase genes in the urinary isolates of a tertiary care hospital. Avicenna J Med 7: 1216.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Moubareck C, Daoud Z, Hakime NI, Hamze M, Mangeney N, Matta H, Mokhbat JE, Rohban R, Sarkis DK, Populaire FD, 2005. Countrywide spread of community-and the hospital-acquired extended-spectrum beta-lactamase (CTX-M-15)-producing Enterobacteriaceae in Lebanon. J Clin Microbiol 43: 33093313.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Livermore DM et al. 2007. CTX-M; changing the face of ESβLs in Europe. J Antimicrob Chemother 59: 165174.

  • 39.

    Rubio-Perez I, Martin-Perez E, Garcia DD, Calvo ML, Barrera EL, 2012. Extended-spectrum β lactamase producing bacteria in a tertiary care hospital in Madrid: epidemiology, risk factors, and antimicrobial susceptibility patterns. Emerg Health Threats J 5: 11589.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40.

    Hernandez E, Araque M, Millan Y, Millan B, Vielmas S, 2014. Prevalence of beta-lactamase CTX-M-15 in phylogenetic groups of uropathogenic Escherichia coli isolated from patients in the community of Merida, Venezuela. Invest Clin 55: 3243.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41.

    Rogers BA, Sidjabat HE, Paterson DL, 2011. Escherichia coli O25b-ST131: a pandemic, multi-resistant, community-associated strain. J Antimicrob Chemother 66: 114.

  • 42.

    Dutour C, Bonnet R, Marchandin H, Boyer M, Chanal C, Sirot D, Sirot J, 2002. CTX-M-1, CTX-M-3, and CTX-M-14β-lactamases from Enterobacteriaceae isolated in France. Antimicrob Agents Chemother 46: 534537.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43.

    Mavroidi A, Tzelepi E, Miriagou V, Gianneli D, Legakis NJ, Tzouvelekis LS, 2002. CTX-M-3 β-lactamase—producing Escherichia coli from Greece. Microb Drug Resist 8: 3537.

  • 44.

    Yu WL, Winokur PL, Von Stein DL, Pfaller MA, Wang JH, Jones RN, 2002. The first description of Klebsiella pneumoniae harboring CTX-M β-lactamases (CTX-M-14 and CTX-M-3) in Taiwan. Antimicrob Agents Chemother 46: 10981100.

    • PubMed
    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 611 333 116
Full Text Views 1093 10 0
PDF Downloads 319 5 0
 

 

 

 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save