Abstract
Urinary tract infection (UTI) is regarded one of the most frequent bacterial infections in women. Accordingly, the aim of the current study was to determine the prevalence of extended-spectrum beta-lactamase (ESBL), as well as the degree of antimicrobial resistance among premenopausal (n = 44) and postmenopausal (n = 49) women suffering from uncomplicated UTI. Urinary samples (n = 93) collected from women with UTI were tested for their antimicrobial sensitivity and assessed for ESBL production by both phenotypic and genotypic methods. Phenotypically, the presence of ESBL was observed in 64 isolates, while polymerase chain reaction detected ESBL-encoding genes in 57 isolates. The CTX-M gene was the most predominant (51.6%), followed by TEM (46.2%), and the SHV gene (17.2%). Surprisingly, all ESBL-producing Escherichia coli isolates were multidrug-resistant (MDR). To the best of our knowledge, this is the first study conducted in Egypt showing significant correlation between ESBL production, multidrug resistance and menopausal state in women. The results demonstrate alarming signal for the dissemination of ESBL genes among uropathogenic E. coli that are MDR in Egypt.
Similar content being viewed by others
References
Fatima S, Muhammad IN, Usman S, Jamil S, Khan MN, Khan SI (2018) Incidence of multidrug resistance and extended-spectrum beta-lactamase expression in community-acquired urinary tract infection among different age groups of patients. Indian J Pharmacol 50(2):69–74. https://doi.org/10.4103/ijp.IJP_200_17
Genovese C, Davinelli S, Mangano K, Tempera G, Nicolosi D, Corsello S, Vergalito F, Tartaglia E, Scapagnini G, Di Marco R (2018) Effects of a new combination of plant extracts plus d-mannose for the management of uncomplicated recurrent urinary tract infections. J Chemother 30(2):107–114. https://doi.org/10.1080/1120009x.2017.1393587
Nicolosi D, Tempera G, Genovese C, Furneri PM (2014) Anti-adhesion activity of A2-type proanthocyanidins (a cranberry major component) on uropathogenic E. coli and P. mirabilis strains. Antibiotics (Basel) 3(2):143–154. https://doi.org/10.3390/antibiotics3020143
Foxman B (2014) Urinary tract infection syndromes: occurrence, recurrence, bacteriology, risk factors, and disease burden. Infect Dis Clin North Am 28(1):1–13. https://doi.org/10.1016/j.idc.2013.09.003
Miotla P, Romanek-Piva K, Bogusiewicz M, Markut-Miotla E, Adamiak A, Wróbel A, Zebrowska M, Wawrysiuk S, Mendyk K, Rechberger E, Jakubczak A, Rechberger T (2017) Antimicrobial resistance patterns in women with positive urine culture: does menopausal status make a significant difference? BioMed Res Int 2017:4192908. https://doi.org/10.1155/2017/4192908
Bubpamala J, Khuntayaporn P, Thirapanmethee K, Montakantikul P, Santanirand P, Chomnawang MT (2018) Phenotypic and genotypic characterizations of extended-spectrum beta-lactamase-producing Escherichia coli in Thailand. Infect Drug Resist 11:2151–2157. https://doi.org/10.2147/IDR.S174506
Chen LF, Chopra T, Kaye KS (2009) Pathogens resistant to antibacterial agents. Infect Dis Clin North Am 23(4):817–845. https://doi.org/10.1016/j.idc.2009.06.002
Ghafourian S, Sadeghifard N, Soheili S, Sekawi Z (2015) Extended spectrum beta-lactamases: definition, classification and epidemiology. Curr Issues Mol Biol 17:11–21
Shaikh S, Fatima J, Shakil S, Rizvi SM, Kamal MA (2015) Antibiotic resistance and extended spectrum beta-lactamases: types, epidemiology and treatment. Saudi J Biol Sci 22(1):90–101. https://doi.org/10.1016/j.sjbs.2014.08.002
Meier S, Weber R, Zbinden R, Ruef C, Hasse B (2011) Extended-spectrum beta-lactamase-producing gram-negative pathogens in community-acquired urinary tract infections: an increasing challenge for antimicrobial therapy. Infection 39(4):333–340. https://doi.org/10.1007/s15010-011-0132-6
Laupland KB, Church DL, Vidakovich J, Mucenski M, Pitout JD (2008) Community-onset extended-spectrum beta-lactamase (ESBL) producing Escherichia coli: importance of international travel. J Infect 57(6):441–448. https://doi.org/10.1016/j.jinf.2008.09.034
Tharwat N, El-Sherif R, Elnagdy S, Marzaban R, Amer S (2019) Virulent Escherichia coli strains among Egyptian patients with acute diarrhoea versus urinary tract infection, and their antibiotic susceptibility. Arab J Gastroenterol 20(2):74–80. https://doi.org/10.1016/j.ajg.2019.01.003
Gawad W, Helmy O, Tawakkol W, Hashem A (2018) Antimicrobial resistance, biofilm formation, and phylogenetic grouping of uropathogenic Escherichia coli isolates in Egypt: the role of efflux pump-mediated resistance Jundishapur. J Microbiol 11(2):e14444. https://doi.org/10.5812/jjm.14444
Alabsi MS, Ghazal A, Sabry SA, Alasaly MM (2014) Association of some virulence genes with antibiotic resistance among uropathogenic Escherichia coli isolated from urinary tract infection patients in Alexandria, Egypt: a hospital-based study. J Glob Antimicrob Resist 2(2):83–86. https://doi.org/10.1016/j.jgar.2014.01.003
Al-Mayahie SM (2013) Phenotypic and genotypic comparison of ESBL production by vaginal Escherichia coli isolates from pregnant and non-pregnant women. Ann Clin Microbiol Antimicrob 12:7. https://doi.org/10.1186/1476-0711-12-7
Bergey’s manual of determinative bacteriology identification flow charts (2015). https://static1.squarespace.com/static/54c7f25fe4b0447c7f8aed4b/t/5504c972e4b06ae7c7462e69/1426377074561/IDFlowcharts.pdf. Accessed 26 May 2019
Clinical and Laboratory Standards Institute (CLSI) (2016) Performance standards for antimicrobial susceptibility testing: CLSI supplement M100S, 26th edn. Clinical and Laboratory Standards Institute, Wayne
MacFadden JF (2000) Biochemical tests for identification of medical bacteria, 3rd edn. The Williams & Wilkins Co, USA
Bauer AW, Kirby WM, Sherris JC, Turck M (1966) Antibiotic susceptibility testing by a standardized single disk method. Tech Bull Regist Med Technol 36:49–52
The European Committee on Antimicrobial Susceptibility Testing (EUCAST) (2021) Clinical breakpoints - breakpoints and guidance. https://www.eucast.org/clinical_breakpoints/. Accessed 6 Jan 2021
Garrec H, Drieux-Rouzet L, Golmard JL, Jarlier V, Robert J (2011) Comparison of nine phenotypic methods for detection of extended-spectrum beta-lactamase production by Enterobacteriaceae. J Clin Microbiol 49(3):1048–1057. https://doi.org/10.1128/jcm.02130-10
Wayne PA (2008) Performance standards for antimicrobial susceptibility testing. 18th informational supplement: M100–S18. Clinical and Laboratory Standards Institute, Pennsylvania
Sambrook J, Russell DW (2011) Molecular cloning: laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New York
Machado E, Cantón R, Baquero F, Galán JC, Rollán A, Peixe L, Coque TM (2005) Integron content of extended-spectrum-beta-lactamase-producing Escherichia coli strains over 12 years in a single hospital in Madrid Spain. Antimicrob Agents Chemother 49(5):1823–1829. https://doi.org/10.1128/aac.49.5.1823-1829.2005
Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, Harbarth S, Hindler JF, Kahlmeter G, Olsson-Liljequist B, Paterson DL, Rice LB, Stelling J, Struelens MJ, Vatopoulos A, Weber JT, Monnet DL (2012) Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 18(3):268–281. https://doi.org/10.1111/j.1469-0691.2011.03570.x
Shamsrizi P, Gladstone BP, Carrara E, Luise D, Cona A, Bovo C, Tacconelli E (2020) Variation of effect estimates in the analysis of mortality and length of hospital stay in patients with infections caused by bacteria-producing extended-spectrum beta-lactamases: a systematic review and meta-analysis. BMJ Open 10(1):e030266. https://doi.org/10.1136/bmjopen-2019-030266
Abayneh M, Tesfaw G, Abdissa A (2018) Isolation of extended-spectrum β-lactamase- (ESBL-) producing Escherichia coli and Klebsiella pneumoniae from patients with community-onset urinary tract infections in Jimma university specialized hospital, Southwest Ethiopia. Can J Infect Dis Med Microbiol 2018:4846159. https://doi.org/10.1155/2018/4846159
Falgenhauer L, Imirzalioglu C, Oppong K, Akenten CW, Hogan B, Krumkamp R, Poppert S, Levermann V, Schwengers O, Sarpong N, Owusu-Dabo E, May J, Eibach D (2019) Detection and characterization of ESBL-producing Escherichia coli from humans and poultry in Ghana. Front Microbiol 9:3358. https://doi.org/10.3389/fmicb.2018.03358
Chong Y, Shimoda S, Shimono N (2018) Current epidemiology, genetic evolution and clinical impact of extended-spectrum β-lactamase-producing Escherichia coli and Klebsiella pneumoniae. Infect Genet Evol 61:185–188. https://doi.org/10.1016/j.meegid.2018.04.005
World Health Organization (WHO) (2014) Antimicrobial resistance: global report on surveillance. WHO Library Cataloguing-in-Publication, Geneva
Esteve-Palau E, Solande G, Sanchez F, Sorli L, Montero M, Guerri R, Villar J, Grau S, Horcajada JP (2015) Clinical and economic impact of urinary tract infections caused by ESBL-producing Escherichia coli requiring hospitalization: a matched cohort study. J Infect 71(6):667–674. https://doi.org/10.1016/j.jinf.2015.08.012
Lee DS, Lee S-J, Choe H-S (2018) Community-acquired urinary tract infection by Escherichia coli in the era of antibiotic resistance. BioMed Res Int 2018:7656752. https://doi.org/10.1155/2018/7656752
Al-Subol I, Youssef N (2015) Prevalence of CTX-M, TEM and SHV beta-lactamases in clinical isolates of Escherichia coli and Klebsiella pneumoniae isolated from Aleppo university hospitals, Aleppo. Syria Arch Clin Infect Dis 10(2):e22540. https://doi.org/10.5812/archcid.22540
Alqasim A, Abu Jaffal A, Alyousef AA (2018) Prevalence of multidrug resistance and extended-spectrum β-lactamase carriage of clinical uropathogenic Escherichia coli isolates in Riyadh. Saudi Arabia Int J Microbiol 2018:3026851. https://doi.org/10.1155/2018/3026851
Rajapandiyan K, Shanthi S, Vijayalakshmi P, Daisy P, Murugan M, Ranjitsingh AJ (2014) Prevalence of extended-spectrum beta-lactamase-producing multidrug-resistant Escherichia coli among isolates from community-acquired infections and in silico structural modeling of an ESBL protein. Microb Drug Resist 20(2):170–176. https://doi.org/10.1089/mdr.2013.0088
Ramírez Castillo F, Moreno Flores A, González F, Díaz F, Harel J, Guerrero-Barrera A (2018) An evaluation of multidrug-resistant Escherichia coli isolates in urinary tract infections from Aguascalientes, Mexico: cross-sectional study. Ann Clin Microbiol Antimicrob 17:34. https://doi.org/10.1186/s12941-018-0286-5
Moini AS, Soltani B, Taghavi Ardakani A, Moravveji A, Erami M, Haji Rezaei M, Namazi M (2015) Multidrug-resistant Escherichia coli and Klebsiella pneumoniae isolated from patients in Kashan. Iran Jundishapur J Microbiol 8(10):e27517. https://doi.org/10.5812/jjm.27517
Dehbanipour R, Rastaghi S, Sedighi M, Maleki N, Faghri J (2016) High prevalence of multidrug-resistance uropathogenic Escherichia coli strains, Isfahan. Iran J Nat Sci Biol Med 7:22. https://doi.org/10.4103/0976-9668.175020
Pandit R, Awal B, Shrestha SS, Joshi G, Rijal BP, Parajuli NP (2020) Extended-spectrum β-lactamase (ESBL) genotypes among multidrug-resistant uropathogenic Escherichia coli clinical isolates from a teaching hospital of Nepal. Interdiscip Perspect Infect Dis 2020:6525826. https://doi.org/10.1155/2020/6525826
Ahmed O, Omar A, Asghar A, El hassan M (2013) Prevalence of TEM, SHV and CTX-M genes in Escherichia coli and Klebsiella spp. urinary isolates from Sudan with confirmed ESBL phenotype. Life Sci J 10:191–195
Hassuna NA, Khairalla AS, Farahat EM, Hammad AM, Abdel-Fattah M (2020) Molecular characterization of extended-spectrum beta lactamase- producing E. coli recovered from community-acquired urinary tract infections in Upper Egypt. Sci Rep 10(1):2772. https://doi.org/10.1038/s41598-020-59772-z
Ouchar Mahamat O, Lounnas M, Hide M, Dumont Y, Tidjani A, Kamougam K, Abderrahmane M, Benavides J, Solassol J, Bañuls A-L, Jean-Pierre H, Carrière C, Godreuil S (2019) High prevalence and characterization of extended-spectrum ß-lactamase producing enterobacteriaceae in Chadian hospitals. BMC Infect Dis 19(1):205. https://doi.org/10.1186/s12879-019-3838-1
Al-agamy M, Shibl A, Hafez M, Al-Ahdal M, Memish Z, Khubnani H (2014) Molecular characteristics of extended-spectrum β-lactamase-producing Escherichia coli in riyadh: emergence of CTX-M-15-producing E. coli ST131. Ann Clin Microbiol Antimicrob 13:4. https://doi.org/10.1186/1476-0711-13-4
Valenza G, Nickel S, Pfeifer Y, Eller C, Krupa E, Lehner-Reindl V, Höller C (2014) Extended-spectrum-β-lactamase-producing Escherichia coli as intestinal colonizers in the German community. Antimicrob Agents Chemother 58(2):1228–1230. https://doi.org/10.1128/aac.01993-13
Livermore DM (2012) Current epidemiology and growing resistance of gram-negative pathogens. Korean J Intern Med 27(2):128–142. https://doi.org/10.3904/kjim.2012.27.2.128
Pitout JD, Gregson DB, Campbell L, Laupland KB (2009) Molecular characteristics of extended-spectrum-beta-lactamase-producing Escherichia coli isolates causing bacteremia in the calgary health region from 2000 to 2007: emergence of clone ST131 as a cause of community-acquired infections. Antimicrob Agents Chemother 53(7):2846–2851. https://doi.org/10.1128/AAC.00247-09
Ojdana D, Sacha P, Wieczorek P, Czaban S, Michalska A, Jaworowska J, Jurczak A, Poniatowski B, Tryniszewska E (2014) The occurrence of blaCTX-M, blaSHV, and blaTEM genes in extended-spectrum β-lactamase-positive strains of Klebsiella pneumoniae, Escherichia coli, and proteus mirabilis in Poland. Int J Antibiotic 2014:935842. https://doi.org/10.1155/2014/935842
Sepp E, Andreson R, Balode A, Bilozor A, Brauer A, Egorova S, Huik K, Ivanova M, Kaftyreva L, Kõljalg S, Kõressaar T, Makarova M, Miciuleviciene J, Pai K, Remm M, Rööp T, Naaber P (2019) Phenotypic and molecular epidemiology of ESBL-, AmpC-, and carbapenemase-producing Escherichia coli in Northern and Eastern Europe. Front Microbiol 10:2465. https://doi.org/10.3389/fmicb.2019.02465
Kjeldsen TS, Overgaard M, Nielsen SS, Bortolaia V, Jelsbak L, Sommer M, Guardabassi L, Olsen JE (2015) CTX-M-1 β-lactamase expression in Escherichia coli is dependent on cefotaxime concentration, growth phase and gene location. J Antimicrob Chemother 70(1):62–70. https://doi.org/10.1093/jac/dku332
Pitout JD (2010) Infections with extended-spectrum beta-lactamase-producing enterobacteriaceae: changing epidemiology and drug treatment choices. Drugs 70(3):313–333. https://doi.org/10.2165/11533040-000000000-00000
Mody L, Juthani-Mehta M (2014) Urinary tract infections in older women: a clinical review. JAMA 311(8):844–854. https://doi.org/10.1001/jama.2014.303
Hooton T (2001) Recurrent urinary tract infection in women (review). Int J Antimicrob Agents 17:259–268. https://doi.org/10.1016/s0924-8579(00)00350-2
Al-Badr A, Al-Shaikh G (2013) Recurrent urinary tract infections management in women: a review. Sultan Qaboos Univ Med J 13(3):359–367. https://doi.org/10.12816/0003256
Acknowledgements
The author thanks Pharos University in Alexandria and Medical technology center for their technical support.
Author information
Authors and Affiliations
Contributions
GHA and MAY designed and performed the experiments. GHA wrote the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Ethical Approval
Regarding ethical clarification required concerning the isolation of bacterial isolates form clinical specimens, this was carried out by nurses and technicians in the hospitals not by us. We only collected the subcultured isolates from the microbiology laboratories in these hospitals. Privacy and confidentiality of all patients’ information was anonymized. Therefore, no need for ethical approval or consent.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ali, G.H., Yakout, M.A. Comparative Study of ESBL Production Among Uropathogenic Escherichia coli Clinical Isolates from Pre- and Post-menopausal Women in Egypt. Curr Microbiol 78, 3516–3525 (2021). https://doi.org/10.1007/s00284-021-02599-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00284-021-02599-2