Incidence of extended spectrum beta-lactamase (ESBL) producing Escherichia coli isolated from women with urinary tract infections in Jordan
Abstract
Background and Objectives: Urinary tract infections are one of the world's major health problems. In addition, clinical disorders may result from the presence of bacteria or fungi in urine. The aim of this study was to isolate Escherichia coli (E. coli) strains from midstream urine samples, and to determine molecular characterization of encoded Extended Spectrum Beta-Lactamase (ESBL) genes.
Materials and Methods: Collected urine samples were streaked on MacConkey, blood and EMB agar plates, then identifying E. coli isolates by using antibiotic susceptibility tests. ESBL production was measured using double disc diffusion. Furthermore, uniplex PCR was performed to identify two ESBL genes (blaCTX and blaTEM).
Results: Among 412 isolates, 198 (48.1%) were E. coli strains, followed by Staphylococcus saprophyticus, Klebsiella sp., Serratia sp., Enterococci sp. and Proteus sp. with frequency of 132 (32.0%), 51 (12.4%), 15 (3.6%), 10 (2.4%), and 6 (1.5%) respectively. Female participants who were between the ages of 40 and 49 years old, married, and pregnant were more likely to develop urinary tract infections (UTIs). E. coli species were present in 189 (95.5) of the recurrent UTIs. Regarding antimicrobial susceptibility testing of E. coli isolates, the highest percentage of resistance and susceptible rates were found for nalidixic acid (75.8%) and gentamicin (64.1%) respectively. Among the E. coli isolates, 25 (12.6%) were ESBL-producers. The blaCTX-M gene was genetically confirmed in 20 (10.1%) of the isolates.
Conclusion: E. coli is the most common cause of UTI and ESBL production leads to increased resistance to common antibiotics and complicates treatment strategies.
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11. Lalchhandama K. History of Penicillin. WikiJ Med 2021; 8: 3.
12. Prasada S, Bhat A, Bhat S, Shenoy Mulki S, Tulasidas S. Changing antibiotic susceptibility pattern in uropathogenic Escherichia coli over a period of 5 years in a tertiary care center. Infect Drug Resist 2019; 12: 1439-1443.
13. Bajpai T, Pandey M, Varma M, Bhatambare GS. Prevalence of TEM, SHV, and CTX-M Beta-Lactamase genes in the urinary isolates of a tertiary care hospital. Avicenna J Med 2017; 7: 12-16.
14. Hayajneh WA, Hajj A, Hulliel F, Sarkis DK, Irani-Hakimeh N, Kazan L, et al. Susceptibility trends and molecular characterization of Gram-negative bacilli associated with urinary tract and intra-abdominal infections in Jordan and Lebanon: SMART 2011-2013. Int J Infect Dis 2015; 35: 56-61.
15. Husna A, Rahman MM, Badruzzaman ATM, Sikder MH, Islam MR, Rahman MT, et al. Extended-spectrum β-lactamases (ESBL): challenges and opportunities. Biomedicines 2023;11:2937.
16. Nimri LF, Azaizeh BA. First report of multidrug-resistant ESBL-producing urinary Escherichia coli in Jordan. Br Microbiol Res J 2012; 2: 71-81.
17. Tuttle AR, Trahan ND, Son MS. Growth and maintenance of Escherichia coli laboratory strains. Curr Protoc 2021; 1(1): e20.
18. Salam MA, Al-Amin MY, Pawar JS, Akhter N, Lucy IB. Conventional methods and future trends in antimicrobial susceptibility testing. Saudi J Biol Sci 2023; 30: 103582.
19. Clinical and Laboratory Standards Institute (2016). CLSI Document M100- S21. Performances standards for antimicrobial susceptibility testing. 26th Edition informational supplement, Wayne.
20. Abu-Sini M, Al-Kafaween MA, Al-Groom RM, Hilmi ABM. Comparative in vitro activity of various antibiotic against planktonic and biofilm and the gene expression profile in Pseudomonas aeruginosa. AIMS Microbiol 2023; 9: 313-331.
21. Alkafaween MA, Abu-Sini M, Al-Jamal HAN. Antibiotic susceptibility and differential expression of virulence genes in Staphylococcus aureus. Appl Environ Biotechnol 2022; 7: 6-15.
22. Mahmoud IS, Altaif KI, Sini MKA, Daoud S, Aqel NN. Determination of antimicrobial drug resistance among bacterial isolates in two hospitals of Baghdad. Jordan J Pharm Sci 2020; 13: 1-9.
23. Jarrar Y, Abudahab S, Abdul-Wahab G, Zaiter D, Madani A, Abaalkhail SJ, et al. Clinical significance of NAT2 genetic variations in type II diabetes mellitus and lipid regulation. Pharmgenomics Pers Med 2023; 16: 847-857.
24. Kristianingtyas L, Effendi MH, Tyasningsih W, Kurniawan F. Genetic identification ofblactx-M gene andblatem gene on extended spectrum beta lactamase (ESBL) producing Escherichia colifrom Dogs. Indian Vet J 2020; 97: 17-21.
25. Lorenz TC. Polymerase chain reaction: basic protocol plus troubleshooting and optimization strategies. J Vis Exp 2012; (63): e3998.
26. Dallenne C, Da Costa A, Decré D, Favier C, Arlet G. Development of a set of multiplex PCR assays for the detection of genes encoding important beta-lactamases in Enterobacteriaceae. J Antimicrob Chemother 2010; 65: 490-495.
27. Tomlekova NB, Muhovski YG, Basyirin R, Sarsu F (2017). Simple Sequence repeats protocols. http://izk-maritsa.org/wp-content/uploads/2017/05/SIMPLE-SEQUENCE-REPEATS_TomlekovaN.pdf
28. Castanheira M, Simner PJ, Bradford PA. Extended-spectrum β-lactamases: an update on their characteristics, epidemiology and detection. JAC Antimicrob Resist 2021; 3: dlab092.
29. Khan H, Bari F. Extended spectrum Beta lactamases (ESBLs): preference for age and gender; a hospital-based study. Microb Infect Dis 2021; 2: 326-332.
30. Mlugu EM, Mohamedi JA, Sangeda RZ, Mwambete KD. Prevalence of urinary tract infection and antimicrobial resistance patterns of uropathogens with biofilm forming capacity among outpatients in morogoro, Tanzania: a cross-sectional study. BMC Infect Dis 2023; 23: 660.
31. Czajkowski K, Broś-Konopielko M, Teliga-Czajkowska J. Urinary tract infection in women. Prz Menopauzalny 2021; 20: 40-47.
32. Ackerson BK, Tartof SY, Chen LH, Contreras R, Reyes IAC, Ku JH, et al. Risk factors for recurrent urinary tract infections among women in a large integrated health care Organization in the united States. J Infect Dis 2024; 230(5): e1101-e1111.
33. Murgia L, Stalio O, Arienzo A, Ferrante V, Cellitti V, Somma SD, et al (2018). Management of urinary tract infections: Problems and possible solutions. Urinary tract infection-The result of the Strength of the pathogen, or the Weakness of the host. Available from: https://ouci.dntb.gov.ua/en/works/4rAxOoJ7/
34. Al-Badr A, Al-Shaikh G. Recurrent urinary tract infections Management in women: A review. Sultan Qaboos Univ Med J 2013; 13: 359-367.
35. Odoki M, Almustapha Aliero A, Tibyangye J, Nyabayo Maniga J, Wampande E, Drago Kato C, et al. Prevalence of bacterial urinary tract infections and associated factors among patients attending hospitals in bushenyi district, uganda. Int J Microbiol 2019; 2019: 4246780.
36. Barnawi Y, Alghamdi A, Ibrahim A, Al-Anazi L, Alhumaida G, Alotaibi R, et al. Prevalence of urinary tract infections in pregnant women and antimicrobial resistance patterns in women in Riyadh, Saudi Arabia: a retrospective study. BMC Infect Dis 2024; 24: 502.
37. Ma Y, Pirolo M, Subramani P, Gehring R, Damborg P, Franzyk H, et al. Macrolide resistance and in vitro potentiation by peptidomimetics in porcine clinical Escherichia coli. mSphere 2022; 7(5): e0040222.
38. Nasrollahian S, Graham JP, Halaji M. A review of the mechanisms that confer antibiotic resistance in pathotypes of E. coli. Front Cell Infect Microbiol 2024; 14: 1387497.
39. Chaudhry WN, Badar R, Jamal M, Jeong J, Zafar J, Andleeb S. Clinico-microbiological study and antibiotic resistance profile of meca and ESBL gene prevalence in patients with diabetic foot infections. Exp Ther Med 2016; 11: 1031-1038.
40. Zhang YL, Huang FY, Gan LL, Yu X, Cai DJ, Fang J, et al. High prevalence of blaCTX-M and blaSHV among ESBL producing E. coli isolates from beef cattle in China's Sichuan-Chongqing Circle. Sci Rep 2021; 11: 13725.
2. Kaur R, Kaur R. Symptoms, risk factors, diagnosis and treatment of urinary tract infections. Postgrad Med J 2021; 97: 803-812.
3. SahuR, Sahoo RK, Prusty SK, Sahu PK. Urinary tract infection and its management. Syst Rev Pharm 2019; 10: 42-48.
4. Salari N, Khoshbakht Y, Hemmati M, Khodayari Y, Khaleghi AA, Jafari F, et al. Global prevalence of urinary tract infection in pregnant mothers: a systematic review and meta-analysis. Public Health 2023; 224: 58-65.
5. Víquez-Molina G, Aragón-Sánchez J, Pérez-Corrales C, Murillo-Vargas C, López-Valverde ME, Lipsky BA. Virulence factor genes in Staphylococcus aureus isolated from Diabetic foot soft tissue and bone infections. Int J Low Extrem Wounds 2018; 17: 36-41.
6. Corrales M, Corrales-Acosta E, Corrales-Riveros JG. Which antibiotic for urinary tract infections in pregnancy? A literature review of international guidelines. J Clin Med 2022; 11: 7226.
7. Handelsman DJ, Bacha F, DeBono M, Sleiman S, Janu MR. Sexually transmitted doping: The impact of urine contamination of semen. Drug Test Anal 2022; 14: 1623-1628.
8. Nadeem SF, Gohar UF, Tahir SF, Mukhtar H, Pornpukdeewattana S, Nukthamna P, et al. Antimicrobial resistance : more than 70 years of war between humans and bacteria. Crit Rev Microbiol 2020; 46: 578-599.
9. Rodríguez-Miranda E, Reyes-Escogido ML, Olmedo-Ramírez V, Jiménez-Garza O, López-Briones S, Hernández-Luna MA. Differential expression of fimH, ihf, upaB, and upaH genes in Biofilms- and Suspension-grown bacteria from samples of different uropathogenic strains of Escherichia coli. Int J Microbiol 2024; 2024: 5235071.
10. Bader MS, Loeb M, Leto D, Brooks AA. Treatment of urinary tract infections in the era of antimicrobial resistance and new antimicrobial agents. Postgrad Med 2020; 132: 234-250.
11. Lalchhandama K. History of Penicillin. WikiJ Med 2021; 8: 3.
12. Prasada S, Bhat A, Bhat S, Shenoy Mulki S, Tulasidas S. Changing antibiotic susceptibility pattern in uropathogenic Escherichia coli over a period of 5 years in a tertiary care center. Infect Drug Resist 2019; 12: 1439-1443.
13. Bajpai T, Pandey M, Varma M, Bhatambare GS. Prevalence of TEM, SHV, and CTX-M Beta-Lactamase genes in the urinary isolates of a tertiary care hospital. Avicenna J Med 2017; 7: 12-16.
14. Hayajneh WA, Hajj A, Hulliel F, Sarkis DK, Irani-Hakimeh N, Kazan L, et al. Susceptibility trends and molecular characterization of Gram-negative bacilli associated with urinary tract and intra-abdominal infections in Jordan and Lebanon: SMART 2011-2013. Int J Infect Dis 2015; 35: 56-61.
15. Husna A, Rahman MM, Badruzzaman ATM, Sikder MH, Islam MR, Rahman MT, et al. Extended-spectrum β-lactamases (ESBL): challenges and opportunities. Biomedicines 2023;11:2937.
16. Nimri LF, Azaizeh BA. First report of multidrug-resistant ESBL-producing urinary Escherichia coli in Jordan. Br Microbiol Res J 2012; 2: 71-81.
17. Tuttle AR, Trahan ND, Son MS. Growth and maintenance of Escherichia coli laboratory strains. Curr Protoc 2021; 1(1): e20.
18. Salam MA, Al-Amin MY, Pawar JS, Akhter N, Lucy IB. Conventional methods and future trends in antimicrobial susceptibility testing. Saudi J Biol Sci 2023; 30: 103582.
19. Clinical and Laboratory Standards Institute (2016). CLSI Document M100- S21. Performances standards for antimicrobial susceptibility testing. 26th Edition informational supplement, Wayne.
20. Abu-Sini M, Al-Kafaween MA, Al-Groom RM, Hilmi ABM. Comparative in vitro activity of various antibiotic against planktonic and biofilm and the gene expression profile in Pseudomonas aeruginosa. AIMS Microbiol 2023; 9: 313-331.
21. Alkafaween MA, Abu-Sini M, Al-Jamal HAN. Antibiotic susceptibility and differential expression of virulence genes in Staphylococcus aureus. Appl Environ Biotechnol 2022; 7: 6-15.
22. Mahmoud IS, Altaif KI, Sini MKA, Daoud S, Aqel NN. Determination of antimicrobial drug resistance among bacterial isolates in two hospitals of Baghdad. Jordan J Pharm Sci 2020; 13: 1-9.
23. Jarrar Y, Abudahab S, Abdul-Wahab G, Zaiter D, Madani A, Abaalkhail SJ, et al. Clinical significance of NAT2 genetic variations in type II diabetes mellitus and lipid regulation. Pharmgenomics Pers Med 2023; 16: 847-857.
24. Kristianingtyas L, Effendi MH, Tyasningsih W, Kurniawan F. Genetic identification ofblactx-M gene andblatem gene on extended spectrum beta lactamase (ESBL) producing Escherichia colifrom Dogs. Indian Vet J 2020; 97: 17-21.
25. Lorenz TC. Polymerase chain reaction: basic protocol plus troubleshooting and optimization strategies. J Vis Exp 2012; (63): e3998.
26. Dallenne C, Da Costa A, Decré D, Favier C, Arlet G. Development of a set of multiplex PCR assays for the detection of genes encoding important beta-lactamases in Enterobacteriaceae. J Antimicrob Chemother 2010; 65: 490-495.
27. Tomlekova NB, Muhovski YG, Basyirin R, Sarsu F (2017). Simple Sequence repeats protocols. http://izk-maritsa.org/wp-content/uploads/2017/05/SIMPLE-SEQUENCE-REPEATS_TomlekovaN.pdf
28. Castanheira M, Simner PJ, Bradford PA. Extended-spectrum β-lactamases: an update on their characteristics, epidemiology and detection. JAC Antimicrob Resist 2021; 3: dlab092.
29. Khan H, Bari F. Extended spectrum Beta lactamases (ESBLs): preference for age and gender; a hospital-based study. Microb Infect Dis 2021; 2: 326-332.
30. Mlugu EM, Mohamedi JA, Sangeda RZ, Mwambete KD. Prevalence of urinary tract infection and antimicrobial resistance patterns of uropathogens with biofilm forming capacity among outpatients in morogoro, Tanzania: a cross-sectional study. BMC Infect Dis 2023; 23: 660.
31. Czajkowski K, Broś-Konopielko M, Teliga-Czajkowska J. Urinary tract infection in women. Prz Menopauzalny 2021; 20: 40-47.
32. Ackerson BK, Tartof SY, Chen LH, Contreras R, Reyes IAC, Ku JH, et al. Risk factors for recurrent urinary tract infections among women in a large integrated health care Organization in the united States. J Infect Dis 2024; 230(5): e1101-e1111.
33. Murgia L, Stalio O, Arienzo A, Ferrante V, Cellitti V, Somma SD, et al (2018). Management of urinary tract infections: Problems and possible solutions. Urinary tract infection-The result of the Strength of the pathogen, or the Weakness of the host. Available from: https://ouci.dntb.gov.ua/en/works/4rAxOoJ7/
34. Al-Badr A, Al-Shaikh G. Recurrent urinary tract infections Management in women: A review. Sultan Qaboos Univ Med J 2013; 13: 359-367.
35. Odoki M, Almustapha Aliero A, Tibyangye J, Nyabayo Maniga J, Wampande E, Drago Kato C, et al. Prevalence of bacterial urinary tract infections and associated factors among patients attending hospitals in bushenyi district, uganda. Int J Microbiol 2019; 2019: 4246780.
36. Barnawi Y, Alghamdi A, Ibrahim A, Al-Anazi L, Alhumaida G, Alotaibi R, et al. Prevalence of urinary tract infections in pregnant women and antimicrobial resistance patterns in women in Riyadh, Saudi Arabia: a retrospective study. BMC Infect Dis 2024; 24: 502.
37. Ma Y, Pirolo M, Subramani P, Gehring R, Damborg P, Franzyk H, et al. Macrolide resistance and in vitro potentiation by peptidomimetics in porcine clinical Escherichia coli. mSphere 2022; 7(5): e0040222.
38. Nasrollahian S, Graham JP, Halaji M. A review of the mechanisms that confer antibiotic resistance in pathotypes of E. coli. Front Cell Infect Microbiol 2024; 14: 1387497.
39. Chaudhry WN, Badar R, Jamal M, Jeong J, Zafar J, Andleeb S. Clinico-microbiological study and antibiotic resistance profile of meca and ESBL gene prevalence in patients with diabetic foot infections. Exp Ther Med 2016; 11: 1031-1038.
40. Zhang YL, Huang FY, Gan LL, Yu X, Cai DJ, Fang J, et al. High prevalence of blaCTX-M and blaSHV among ESBL producing E. coli isolates from beef cattle in China's Sichuan-Chongqing Circle. Sci Rep 2021; 11: 13725.
| Files | ||
| Issue | Vol 17 No 1 (2025) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v17i1.17800 | |
| Keywords | ||
| Antibiotic resistance; blaCTX-M gene; Escherichia coli; Erythromycin; Extended-spectrum beta-lactamase; Urinary tract infections | ||
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How to Cite
1.
Al-Groom R. Incidence of extended spectrum beta-lactamase (ESBL) producing Escherichia coli isolated from women with urinary tract infections in Jordan. Iran J Microbiol. 2025;17(1):41-50.
