Distribution of ciprofloxacin-resistance genes among ST131 and non-ST131 clones of Escherichia coli isolates with ESBL phenotypes isolated from women with urinary tract infection
-
Masoumeh Rasoulinasab
,
Fereshteh Shahcheraghi
,
Mohammad Mehdi Feizabadi
,
Bahram Nikmanesh
,
Azade Hajihasani
,
Mohammad Mehdi Aslani
Abstract
Background and Objectives: Escherichia coli (E. coli) sequence type 131 (ST131) is associated with extended-spectrum beta-lactamase (ESBL) production and fluoroquinolone resistance. This study aimed to investigate the prevalence of ST131, ESBL, and plasmid-mediated quinolone resistance (PMQR) genes in the ciprofloxacin-resistant (CIPR) and ESBL producers from women with UTI.
Materials and Methods: The CIP-resistant ESBL producing (CIPR/ESBL+) E. coli isolates were screened for ST131-by specific PCR of mdh and gyrB. The ESBL and PMQR genes were screened by single PCR. The ST131 and non-ST131 isolates were selected to determine the mutations of gyrA and parC using PCR and sequencing, and also their genetic background by the Pasteur-MLST scheme.
Results: Overall, 55% (33/60) CIPR/ESBL+ isolates were identified as ST131 (94% O25b-ST131). Resistance rate to ampicillin-sulbactam (70%), aztreonam (97%) and gentamicin (61%), the prevalence of aac(6′)-Ib-cr (66%), blaCTX-M-15 (82%), the profile of qnrS+aac(6′)-Ib-cr (30%), and the double mutation in the parC was significantly higher in ST131 than non-ST131 isolates. The coexistence of PMQR and ESBL genes was found in more than 50% of ST131 and non-ST131 isolates. ST131 isolates differentiated into PST43 and PST506.
Conclusion: Management of women with UTI caused by the CIPR/ESBL+ isolates (ST131) co-harbored PMQR, ESBL, and chromosomal mutations, is important for their effective therapy.
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15. Weill FX, Demartin M, Tandé D, Espié E, Rakotoarivony I, Grimont PA. SHV-12-like extended-spectrum-β-lactamase-producing strains of Salmonella enterica serotypes babelsberg and enteritidis isolated in France among infants adopted from Mali. J Clin Microbiol 2004; 42:2432-2437.
16. Cattoir V, Poirel L, Rotimi V, Soussy CJ, Nordmann P. Multiplex PCR for detection of plasmid-mediated quinolone resistance qnr genes in ESBL-producing enterobacterial isolates. J Antimicrob Chemother 2007; 60:394-397.
17. Chen X, Zhang W, Pan W, Yin J, Pan Z, Gao S, et al. Prevalence of qnr, aac (6′)-Ib-cr, qepA, and oqxAB in Escherichia coli isolates from humans, animals, and the environment. Antimicrob Agents Chemother 2012; 56:3423-3427.
18. Platell JL, Cobbold RN, Johnson JR, Heisig A, Heisig P, Clabots C, et al. Commonality among fluoroquinolone-resistant sequence type ST131 extraintestinal Escherichia coli isolates from humans and companion animals in Australia. Antimicrob Agents Chemother 2011; 55:3782-3787.
19. Zhao L, Zhang J, Zheng B, Wei Z, Shen P, Li S, et al. Molecular epidemiology and genetic diversity of fluoroquinolone-resistant Escherichia coli isolates from patients with community-onset infections in 30 Chinese county hospitals. J Clin Microbiol 2015; 53:766-770.
20. Clinical and Laboratory Standards Institute (2018). Performance standards for antimicrobial disk susceptibility tests, CLSI standard M02. 13th ed. Wayne, PA. USA.
21. Shahcheraghi F, Nobari S, Rahmati Ghezelgeh F, Nasiri S, Owlia P, Nikbin VS, et al. First report of New Delhi metallo-beta-lactamase-1-producing Klebsiella pneumoniae in Iran. Microb Drug Resist 2013; 19:30-36.
22. Rogers BA, Sidjabat HE, Paterson DL. Escherichia coli O25b-ST131: a pandemic, multiresistant, community-associated strain. J Antimicrob Chemother 2011; 66:1-14.
23. Zhong YM, Liu WE, Meng Q, Li Y. Escherichia coli O25b-ST131 and O16-ST131 causing urinary tract infection in women in Changsha, China: molecular epidemiology and clinical characteristics. Infect Drug Resist 2019; 12:2693-2702.
24. Banerjee R, Johnston B, Lohse C, Porter SB, Clabots C, Johnson JR. Escherichia coli sequence type 131 is a dominant, antimicrobial-resistant clonal group associated with healthcare and elderly hosts. Infect Control Hosp Epidemiol 2013; 34:361-369.
25. Yeganeh-Sefidan F, Ghotaslou R, Akhi MT, Sadeghi MR, Mohammadzadeh-Asl Y, Bannazadeh Baghi H. Fosfomycin, interesting alternative drug for treatment of urinary tract infections created by multiple drug resistant and extended spectrum β-lactamase producing strains. Iran J Microbiol 2016; 8:125-131.
26. Rezazadeh M, Baghchesaraei H, Peymani A. Plasmid-Mediated quinolone-resistance (qnr) genes in clinical isolates of Escherichia coli collected from several hospitals of Qazvin and Zanjan provinces, Iran. Osong Public Health Res Perspect 2016; 7:307-312.
27. Yang HY, Nam YS, Lee HJ. Prevalence of plasmid-mediated quinolone resistance genes among ciprofloxacin-nonsusceptible Escherichia coli and Klebsiella pneumoniae isolated from blood cultures in Korea. Can J Infect Dis Med Microbiol 2014; 25:163-169.
28. Park CH, Robicsek A, Jacoby GA, Sahm D, Hooper DC. Prevalence in the United States of aac(6′)-Ib-cr encoding a ciprofloxacin-modifying enzyme. Antimicrob Agents Chemother 2006; 50:3953-3955.
29. Hussain A, Ewers C, Nandanwar N, Guenther S, Jadhav S, Wieler LH, et al. Multiresistant uropathogenic Escherichia coli from a region in India where urinary tract infections are endemic: genotypic and phenotypic characteristics of sequence type 131 isolates of the CTX-M-15 extended-spectrum-β-lactamase-producing lineage. Antimicrob Agents Chemother 2012; 56:6358-6365.
30. Johnning A, Kristiansson E, Fick J, Weijdegård B, Larsson D. Resistance mutations in gyrA and parC are common in Escherichia communities of both fluoroquinolone-polluted and uncontaminated aquatic environments. Front Microbiol 2015; 6:1355.
31. Kotb DN, Mahdy WK, Mahmoud MS, Khairy RMM. Impact of co-existence of PMQR genes and QRDR mutations on fluoroquinolones resistance in Enterobacteriaceae strains isolated from community and hospital acquired UTIs. BMC Infect Dis 2019; 19: 979.
32. Paltansing S, Kraakman M, Ras J, Wessels E, Bernards A. Characterization of fluoroquinolone and cephalosporin resistance mechanisms in Enterobacteriaceae isolated in a Dutch teaching hospital reveals the presence of an Escherichia coli ST131 clone with a specific mutation in parE. J Antimicrob Chemother 2013; 68:40-45.
33. Johnson JR, Clermont O, Johnston B, Clabots C, Tchesnokova V, Sokurenko E, et al. Rapid and specific detection, molecular epidemiology, and experimental virulence of the O16 subgroup within Escherichia coli sequence type 131. J Clin Microbiol 2014; 52:1358-1365.
34. Kim H, Kim YA, Park YS, Choi MH, Lee GI, Lee K. Risk factors and molecular features of sequence type (ST) 131 extended-spectrum β-lactamase-producing Escherichia coli in community-onset bacteremia. Sci Rep 2017; 7:14640.
2. Pujades-Rodriguez M, West RM, Wilcox MH, Sandoe J. Lower urinary tract infections: management, outcomes and risk factors for antibiotic re-prescription in primary care. EClinicalMedicine 2019; 14:23-31.
3. Mansury D, Motamedifar M, Sarvari J, Shirazi B, Khaledi A. Antibiotic susceptibility pattern and identification of extended spectrum β-lactamases (ESBLs) in clinical isolates of Klebsiella pneumoniae from Shiraz, Iran. Iran J Microbiol 2016; 8:55-61.
4. Nicolas-Chanoine MH, Bertrand X, Madec JY. Escherichia coli ST131, an intriguing clonal group. Clin Microbiol Rev 2014; 27:543-574.
5. Johnson JR, Porter S, Thuras P, Castanheira M. Epidemic emergence in the United States of Escherichia coli sequence type 131-H30 (ST131-H30), 2000 to 2009. Antimicrob Agents Chemother 2017; 61(8):e00732-17.
6. Kim YA, Park YS, Youk T, Lee H, Lee K. Trends in South Korean antimicrobial use and association with changes in Escherichia coli resistance rates: 12-year ecological study using a nationwide surveillance and antimicrobial prescription database. PloS One 2018; 13(12):e0209580.
7. Hooper DC, Jacoby GA. Mechanisms of drug resistance: quinolone resistance. Ann N Y Acad Sci 2015; 1354:12-31.
8. Pham TDM, Ziora ZM, Blaskovich MAT. Quinolone antibiotics. MedChemComm 2019; 10:1719-1739.
9. Yanat B, Rodríguez-Martínez JM, Touati A. Plasmid-mediated quinolone resistance in Enterobacteriaceae: a systematic review with a focus on Mediterranean countries. Eur J Clin Microbiol Infect Dis 2017; 36:421-435.
10. Cappuccino JG, Welsh C (2017). Microbiology: A Laboratory Manual. 11th Edition. Pearson Press. Harlow, England.
11. Johnson JR, Menard M, Johnston B, Kuskowski MA, Nichol K, Zhanel GG. Epidemic clonal groups of Escherichia coli as a cause of antimicrobial-resistant urinary tract infections in Canada, 2002 to 2004. Antimicrob Agents Chemother 2009; 53:2733-2739.
12. Clermont O, Dhanji H, Upton M, Gibreel T, Fox A, Boyd D, et al. Rapid detection of the O25b-ST131 clone of Escherichia coli encompassing the CTX-M-15-producing strains. J Antimicrob Chemother 2009; 64:274-277.
13. Muzaheed AR, Doi Y, Adams-Haduch JM, Endimiani A, Sidjabat HE, Gaddad SM, et al. High prevalence of CTX-M-15-producing Klebsiella pneumoniae among inpatients and outpatients with urinary tract infection in Southern India. J Antimicrob Chemother 2008; 61:1393-1394.
14. Hosoglu S, Gundes S, Kolayli F, Karadenizli A, Demirdag K, Gunaydin M, et al. Extended-spectrum beta-lactamases in ceftazidime-resistant Escherichia coli and Klebsiella pneumoniae isolates in Turkish hospitals. Indian J Med Microbiol 2007; 25:346-350.
15. Weill FX, Demartin M, Tandé D, Espié E, Rakotoarivony I, Grimont PA. SHV-12-like extended-spectrum-β-lactamase-producing strains of Salmonella enterica serotypes babelsberg and enteritidis isolated in France among infants adopted from Mali. J Clin Microbiol 2004; 42:2432-2437.
16. Cattoir V, Poirel L, Rotimi V, Soussy CJ, Nordmann P. Multiplex PCR for detection of plasmid-mediated quinolone resistance qnr genes in ESBL-producing enterobacterial isolates. J Antimicrob Chemother 2007; 60:394-397.
17. Chen X, Zhang W, Pan W, Yin J, Pan Z, Gao S, et al. Prevalence of qnr, aac (6′)-Ib-cr, qepA, and oqxAB in Escherichia coli isolates from humans, animals, and the environment. Antimicrob Agents Chemother 2012; 56:3423-3427.
18. Platell JL, Cobbold RN, Johnson JR, Heisig A, Heisig P, Clabots C, et al. Commonality among fluoroquinolone-resistant sequence type ST131 extraintestinal Escherichia coli isolates from humans and companion animals in Australia. Antimicrob Agents Chemother 2011; 55:3782-3787.
19. Zhao L, Zhang J, Zheng B, Wei Z, Shen P, Li S, et al. Molecular epidemiology and genetic diversity of fluoroquinolone-resistant Escherichia coli isolates from patients with community-onset infections in 30 Chinese county hospitals. J Clin Microbiol 2015; 53:766-770.
20. Clinical and Laboratory Standards Institute (2018). Performance standards for antimicrobial disk susceptibility tests, CLSI standard M02. 13th ed. Wayne, PA. USA.
21. Shahcheraghi F, Nobari S, Rahmati Ghezelgeh F, Nasiri S, Owlia P, Nikbin VS, et al. First report of New Delhi metallo-beta-lactamase-1-producing Klebsiella pneumoniae in Iran. Microb Drug Resist 2013; 19:30-36.
22. Rogers BA, Sidjabat HE, Paterson DL. Escherichia coli O25b-ST131: a pandemic, multiresistant, community-associated strain. J Antimicrob Chemother 2011; 66:1-14.
23. Zhong YM, Liu WE, Meng Q, Li Y. Escherichia coli O25b-ST131 and O16-ST131 causing urinary tract infection in women in Changsha, China: molecular epidemiology and clinical characteristics. Infect Drug Resist 2019; 12:2693-2702.
24. Banerjee R, Johnston B, Lohse C, Porter SB, Clabots C, Johnson JR. Escherichia coli sequence type 131 is a dominant, antimicrobial-resistant clonal group associated with healthcare and elderly hosts. Infect Control Hosp Epidemiol 2013; 34:361-369.
25. Yeganeh-Sefidan F, Ghotaslou R, Akhi MT, Sadeghi MR, Mohammadzadeh-Asl Y, Bannazadeh Baghi H. Fosfomycin, interesting alternative drug for treatment of urinary tract infections created by multiple drug resistant and extended spectrum β-lactamase producing strains. Iran J Microbiol 2016; 8:125-131.
26. Rezazadeh M, Baghchesaraei H, Peymani A. Plasmid-Mediated quinolone-resistance (qnr) genes in clinical isolates of Escherichia coli collected from several hospitals of Qazvin and Zanjan provinces, Iran. Osong Public Health Res Perspect 2016; 7:307-312.
27. Yang HY, Nam YS, Lee HJ. Prevalence of plasmid-mediated quinolone resistance genes among ciprofloxacin-nonsusceptible Escherichia coli and Klebsiella pneumoniae isolated from blood cultures in Korea. Can J Infect Dis Med Microbiol 2014; 25:163-169.
28. Park CH, Robicsek A, Jacoby GA, Sahm D, Hooper DC. Prevalence in the United States of aac(6′)-Ib-cr encoding a ciprofloxacin-modifying enzyme. Antimicrob Agents Chemother 2006; 50:3953-3955.
29. Hussain A, Ewers C, Nandanwar N, Guenther S, Jadhav S, Wieler LH, et al. Multiresistant uropathogenic Escherichia coli from a region in India where urinary tract infections are endemic: genotypic and phenotypic characteristics of sequence type 131 isolates of the CTX-M-15 extended-spectrum-β-lactamase-producing lineage. Antimicrob Agents Chemother 2012; 56:6358-6365.
30. Johnning A, Kristiansson E, Fick J, Weijdegård B, Larsson D. Resistance mutations in gyrA and parC are common in Escherichia communities of both fluoroquinolone-polluted and uncontaminated aquatic environments. Front Microbiol 2015; 6:1355.
31. Kotb DN, Mahdy WK, Mahmoud MS, Khairy RMM. Impact of co-existence of PMQR genes and QRDR mutations on fluoroquinolones resistance in Enterobacteriaceae strains isolated from community and hospital acquired UTIs. BMC Infect Dis 2019; 19: 979.
32. Paltansing S, Kraakman M, Ras J, Wessels E, Bernards A. Characterization of fluoroquinolone and cephalosporin resistance mechanisms in Enterobacteriaceae isolated in a Dutch teaching hospital reveals the presence of an Escherichia coli ST131 clone with a specific mutation in parE. J Antimicrob Chemother 2013; 68:40-45.
33. Johnson JR, Clermont O, Johnston B, Clabots C, Tchesnokova V, Sokurenko E, et al. Rapid and specific detection, molecular epidemiology, and experimental virulence of the O16 subgroup within Escherichia coli sequence type 131. J Clin Microbiol 2014; 52:1358-1365.
34. Kim H, Kim YA, Park YS, Choi MH, Lee GI, Lee K. Risk factors and molecular features of sequence type (ST) 131 extended-spectrum β-lactamase-producing Escherichia coli in community-onset bacteremia. Sci Rep 2017; 7:14640.
| Files | ||
| Issue | Vol 13 No 3 (2021) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v13i3.6389 | |
| Keywords | ||
| Urinary tract infections; Uropathogenic Escherichia coli; Fluoroquinolones; Beta-lactamase CTX-M-15; Multilocus sequence typing | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Rasoulinasab M, Shahcheraghi F, Feizabadi MM, Nikmanesh B, Hajihasani A, Aslani MM. Distribution of ciprofloxacin-resistance genes among ST131 and non-ST131 clones of Escherichia coli isolates with ESBL phenotypes isolated from women with urinary tract infection. Iran J Microbiol. 2021;13(3):294-302.
