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Occurrence of Imipenem-Resistant Uropathogenic Escherichia coli in Pregnant Women: An Insight into Their Virulence Profile and Clonal Structure

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Abstract

Uropathogenic Escherichia coli (UPEC) is the predominant pathogen in Urinary Tract Infection (UTI) in pregnant and non-pregnant women. Limited studies were initiated to explore UPEC from pregnant women with respect to imipenem resistance, pathogenicity, and their clonal lineage. In this study, imipenem resistance, phylogenetic background, virulence-associated genes, and clonal characteristics in UPECs isolated from pregnant and non-pregnant cohorts were investigated. E. coli was identified biochemically from urine culture-positive samples from pregnant and non-pregnant women. Carbapenem (meropenem, ertapenem, imipenem) susceptibility was determined by Kirby–Bauer disk diffusion test. The pathogenic determinants were identified by PCR. MEGA 11 was used to interpret clonal lineages from MLST. GraphPad Prism 8.0 and SPSS 26.0 were used for statistical interpretation. Results indicated highest resistance against imipenem compared to meropenem and ertapenem in UPECs isolated from pregnant (UPECp; 63.89%) and non-pregnant (UPECnp; 87.88%) women. Although phylogroup E was predominant in both imipenem-resistant isolates, acquisition of virulence factors was higher among UPECnp than UPECp. Akin to this observation, the presence of PAI III536 and PAI IV536 was statistically significant (p < 0.05) in the former. MLST analysis revealed similar clonal lineages between UPECnp and UPECp, which showed an overall occurrence of ST405 followed by ST101, ST410, ST131, and ST1195 in UPECnp and ST167 in UPECp, respectively, with frequent occurrence of CC131, CC405. Therefore, imipenem-resistant UPECp although discrete with respect to their virulence determinants when compared to UPECnp shared similar STs and CCs, which implied common evolutionary history. Thus, empiric treatment must be restricted in UTIs to especially protect maternal and fetal health.

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References

  1. Matuszkiewicz-Rowińska J, Małyszko J, Wieliczko M (2015) Urinary tract infections in pregnancy: old and new unresolved diagnostic and therapeutic problems. Arch Med Sci 11(1):67–77. https://doi.org/10.5114/aoms.2013.39202

    Article  PubMed  PubMed Central  Google Scholar 

  2. Hossain M, Tabassum T, Rahman A et al (2020) Genotype–phenotype correlation of β-lactamase-producing uropathogenic Escherichia coli (UPEC) strains from Bangladesh. Sci Rep 10:14549. https://doi.org/10.1038/s41598-020-71213-5

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Terlizzi ME, Gribaudo G, Maffei ME (2017) UroPathogenic Escherichia coli (UPEC) infections: virulence factors, bladder responses, antibiotic, and non-antibiotic antimicrobial strategies. Front Microbiol 8:1566. https://doi.org/10.3389/fmicb.2017.01566

    Article  PubMed  PubMed Central  Google Scholar 

  4. Abd El Ghany M, Sharaf H, Al-agamy MH, Shibl A, Hill-Cawthrone GA, Hong PY (2018) Genomic characterization of NDM-1 and 5, and OXA-181 carbapenemases in uropathogenic Escherichia coli isolates from Riyadh Saudi Arabia. PLoS ONE 13(8):e0201613. https://doi.org/10.1371/journal.pone.0201613

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Gurung S, Kafle S, Dhungel B, Adhikari N, Shrestha UT, Adhikari B et al (2022) Detection of OXA-48 gene in carbapenem-resistant Escherichia coli and Klebsiella pneumoniae from urine samples. Infect Drug Resist 13:2311–2321. https://doi.org/10.2147/IDR.S259967

    Article  Google Scholar 

  6. Shields RK, Zhou Y, Kanakamedala H, Cai B (2021) Burden of illness in US hospitals due to carbapenem-resistant gram-negative urinary tract infections in patients with or without bacteraemia. BMC Infect Dis 21:572. https://doi.org/10.1186/s12879-021-06229-x

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Adegoke AA, Ikott WE, Okoh AI (2022) Carbapenem resistance associated with coliuria among outpatient and hospitalised urology patients. New Microbes and New Infections 48:101019. https://doi.org/10.1016/j.nmni.2022.101019

    Article  CAS  Google Scholar 

  8. Mairi A, Touati A, Bessai SA, Boutabtoub Y, Khelifi F, Sotto A, Lavigne JP, Pantel A (2018) Carbapenemase-producing Enterobacteriaceae among pregnant women and newborns in Algeria: prevalence, molecular characterization, maternal-neonatal transmission, and risk factors for carriage. Am J Infect Control 47(1):105–108. https://doi.org/10.1016/j.ajic.2018.07.009

    Article  PubMed  CAS  Google Scholar 

  9. Rezatofighi SE, Mirzarazi M, Salehi M (2021) Virulence genes and phylogenetic groups of uropathogenic Escherichia coli isolates from patients with urinary tract infection and uninfected control subjects: a case-control study. BMC Infect Dis 21(1):361. https://doi.org/10.1186/s12879-021-06036-4

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Cepas V, Soto SM (2020) Relationship between virulence and resistance among gram-negative bacteria. Antibiotics 9:719. https://doi.org/10.3390/antibiotics9100719

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Jomehzadeh N, Jahangirimehr F, Chegeni SA (2022) Virulence-associated genes analysis of carbapenemase-producing Escherichia coli isolates. PLoS ONE 17(5):e0266787. https://doi.org/10.1371/journal.pone.0266787

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Forde BM, Roberts LW, Phan MD et al (2019) Population dynamics of an Escherichia coli ST131 lineage during recurrent urinary tract infection. Nat Commun 10:3643. https://doi.org/10.1038/s41467-019-11571-5

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Jafari A, Falahatkar S, Delpasand K, Sabati H, Ebrahim-Saraie HS (2020) Emergence of Escherichia coli ST131 causing urinary tract infection in Western Asia: a systematic review and meta-analysis. Microb Drug Resist 26(11):1357–1364. https://doi.org/10.1089/mdr.2019.0312

    Article  PubMed  CAS  Google Scholar 

  14. Hussain A, Ewers C, Nandanwar N, Guenther S, Jadhav S, Wieler LH, Ahmed N (2012) 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 CTXM-15 extended-spectrum-β-lactamase-producing lineage. Antimicrob Agents Chemother 56(12):6358–6365. https://doi.org/10.1128/AAC.01099-12

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Sekar R, Srivani S, Amudhan M, Mythreyee M (2016) Carbapenem resistance in a rural part of southern India: Escherichia coli versus Klebsiella spp. Indian J Med Res 144(5):781–783. https://doi.org/10.4103/ijmr.IJMR_1035_15

    Article  PubMed  PubMed Central  Google Scholar 

  16. Jaggi N, Chatterjee N, Vyoma S, Giri SK, Dwivedi P, Panwar R, Sharma AP (2019) Carbapenem resistance in Escherichia coli and Klebsiella pneumoniae among Indian and international patients in North India. Acta Microbol Immunol Hung 66(3):367–376. https://doi.org/10.1556/030.66.2019.020

    Article  CAS  Google Scholar 

  17. Srivastava P, Bisht D, Kumar A, Tripathi A (2022) Prevalence of Carbapenem-Resistant Escherichia coli and Klebsiella pneumoniae in Rural Uttar Pradesh. J Datta Meghe Inst Med Sci Univ 17(3):584–588. https://doi.org/10.4103/jdmimsu.jdmimsu_76_22

    Article  Google Scholar 

  18. Chatterjee N, Nirwan PK, Srivastava S, Rati R, Sharma L, Sharma P, Dwivedi P, Jaggi N (2023) Trends in carbapenem resistance in Pre-COVID and COVID times in a tertiary care hospital in North India. Ann Clin Microbiol Antimicrob 22:1. https://doi.org/10.1186/s12941-022-00549-9

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Basu S, Mukherjee SK, Hazra A, Mukherjee M (2013) Molecular characterization of uropathogenic Escherichia coli : nalidixic acid and ciprofloxacin resistance, virulent factors and phylogenetic background. J Clin Diagn Res 7(12):2727–2731. https://doi.org/10.7860/JCDR/2013/6613.3744

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. 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 Phys 9(3):156–162. https://doi.org/10.4103/0974-2727.208262

    Article  CAS  Google Scholar 

  21. Vamsi KS, Moorthy SR, Murali TS, Hemiliamma M, Reddy YRR, Reddy BRC, Kumar JS (2021) Phenotypic methods for the detection of metallo-beta-lactamase production by gram-negative bacterial isolates from hospitalized patients in a tertiary care hospital in India. J Pure Appl Microbiol 15(4):2019–2026. https://doi.org/10.22207/JPAM.15.4.23

    Article  Google Scholar 

  22. Wright MH, Adelskov J, Greene AC (2017) Bacterial DNA extraction using individual enzymes and phenol/chloroform separation. J Microbiol Biol Educ https://doi.org/10.1128/jmbe.v18i2.1348

    Article  PubMed  PubMed Central  Google Scholar 

  23. Clermont O, Christenson JK, Denamur E, Gordon DM (2013) The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups: A new E. coli phylo-typing method. Environ Microbiol Rep 5:58–65. https://doi.org/10.1111/1758-2229.12019

    Article  PubMed  CAS  Google Scholar 

  24. Ghosh A, Ghosh B, Mukherjee M (2022) Epidemiologic and molecular characterization of β-lactamase-producing multidrug-resistant uropathogenic Escherichia coli isolated from asymptomatic hospitalized patients. Int Microbiol 25:27–45. https://doi.org/10.1007/s10123-021-00187-9

    Article  PubMed  CAS  Google Scholar 

  25. Wirth T, Falush D, Lan R, Colles F, Mensa P, Wieler LH et al (2006) Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol 60:1136–1151. https://doi.org/10.1111/j.1365-2958.2006.05172.x

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Wang Y, Zhou J, Li X, Ma L, Cao X, Hu W et al (2020) Genetic diversity, antimicrobial resistance and extended-spectrum β-lactamase type of Escherichia coli isolates from chicken, dog, pig and yak in Gansu and Qinghai Provinces, China. J Glob Antimicrob Res 22:726–732. https://doi.org/10.1016/j.jgar.2020.06.028

    Article  Google Scholar 

  27. Zheng B, Feng C, Xu H, Yu X, Guo L, Jiang X et al (2019) Detection and characterization of ESBL-producing Escherichia coli expressing mcr-1 from dairy cows in China. J Antimicrob Chemother 1(74):321–325. https://doi.org/10.1093/jac/dky446

    Article  CAS  Google Scholar 

  28. Loh K, Sivalingam N (2007) Urinary tract infections in pregnancy. Malays Fam phys: Off J Acad Fam Phys Malays 2(2):54–57

    Google Scholar 

  29. Vasudevan R (2014) Urinary tract infection: an overview of the infection and the associated risk factors. J Microbiol Exp 1(2):42–54. https://doi.org/10.15406/jmen.2014.01.00008

    Article  Google Scholar 

  30. Kant S, Lohiya A, Kapil A, Gupta SK (2017) Urinary Tract Infection among Pregnant Women at a Secondary Level Hospital in Northern India. Indian J Public Health 61(2):118–123. https://doi.org/10.4103/ijph.IJPH_293_15

    Article  PubMed  Google Scholar 

  31. Alemu A, Moges F, Shiferaw Y, Tafess K, Kassu A, Anagaw B et al (2012) Bacterial profile and drug susceptibility pattern of urinary tract infection in pregnant women at University of Gondar Teaching Hospital. Northwest Ethiopia BMC Res Notes 5:197. https://doi.org/10.1186/1756-0500-5-197

    Article  PubMed  Google Scholar 

  32. Johnson B, Stephen BM, Joseph N, Asiphas O, Musa K, Taseera K (2021) Prevalence and bacteriology of culture-positive urinary tract infection among pregnant women with suspected urinary tract infection at Mbarara regional referral hospital. South-Western Uganda BMC Pregnancy Childbirth 21:159. https://doi.org/10.1186/s12884-021-03641-8

    Article  PubMed  CAS  Google Scholar 

  33. Chelkeba L, Fanta K, Mulugeta T, Melaku T (2022) Bacterial profile and antimicrobial resistance patterns of common bacteria among pregnant women with bacteriuria in Ethiopia: a systematic review and meta-analysis. Arch Gynecol Obstet 306(3):663–686. https://doi.org/10.1007/s00404-021-06365-4

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Nobel FA, Akter S, Jebin RA, Sarker TC, Rahman M, Zamane SA et al (2021) Prevalence of multidrug resistance patterns of Escherichia coli from suspected urinary tract infection in Mymensingh city. Bangladesh J Adv Biotechnol Exp Ther 4(3):256–264. https://doi.org/10.5455/jabet.2021.d126

    Article  Google Scholar 

  35. Sarahi JY, Hashemi A, Ardebili A, Davoudabadi S (2021) Molecular Characteristics of antibiotic-resistant Escherichia coli and Klebsiella pneumoniae strains isolated from hospitalized patients in Tehran. Iran Ann Clin Microbiol Antimicrob 20:32. https://doi.org/10.1186/s12941-021-00437-8

    Article  CAS  Google Scholar 

  36. Manohar P, Leptihn S, Lopes BS, Nachimuthu R (2021) Dissemination of carbapenem resistance and plasmids encoding carbapenemases in Gram-negative bacteria isolated in India. JAC Antimicrob Resist https://doi.org/10.1093/jacamr/dlab015

    Article  PubMed  PubMed Central  Google Scholar 

  37. Zowawi HM, Sartor AL, Balkhy HH, Walsh TR, Johani SMA, Aljindan RY et al (2014) Molecular characterization of Carbapenemase-Producing Escherichia coli and Klebsiella pneumoniae in the Countries of the Gulf Cooperation Council: Dominance of OXA-48 and NDM producers. Antimicrob Agents Chemother 58(6):3085–3090. https://doi.org/10.1128/AAC.02050-13

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Matin FZ, Rezatofighi SE, Ardakani MR, Akhoond MR, Mahmoodi F (2021) Virulence characterization and clonal analysis of uropathogenic Escherichia coli metallo-beta-lactamase-producing isolates. Ann Clin Microbiol Antimicrob 20:50. https://doi.org/10.1186/s12941-021-00457-4

    Article  CAS  Google Scholar 

  39. Tian X, Zheng X, Sun Y, Fang R, Zhang S, Zhang X et al (2020) Molecular mechanisms and epidemiology of carbapenem-resistant Escherichia coli Isolated from Chinese patients during 2002–2017. Infection and Drug Resist 13:501–512. https://doi.org/10.2147/IDR.S232010

    Article  CAS  Google Scholar 

  40. Clermont O, Condamine B, Dion S, Gordon DM, Denamur E (2021) The E phylogroup of Escherichia coli is highly diverse and mimics the whole E. coli species population structure. Environ Microbiol 23(11):7139–7151. https://doi.org/10.1111/1462-2920.15742

    Article  PubMed  CAS  Google Scholar 

  41. Touchon M, Perrin A, De Sousa JAM, Vangchhia B, Burn S, O’Brien CL, Denamur E, Gordon D, Rocha EP (2020) Phylogenetic background and habitat drive the genetic diversification of Escherichia coli. PLoS Genet 16(6):e1008866. https://doi.org/10.1371/journal.pgen.1008866

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Ortega A, Sáez D, Bautista V, Fernández-Romero S, Lara N, Aracil B et al (2016) Carbapenemase-producing Escherichia coli is becoming more prevalent in Spain mainly because of the polyclonal dissemination of OXA-48. J Antimicrob Chemother 71:2131–2138. https://doi.org/10.1093/jac/dkw148

    Article  PubMed  Google Scholar 

  43. El-Shaer S, Abdel-Rhman SH, Barwa R, Hassan R (2021) Genetic characterization of extended-spectrum β-Lactamase- and carbapenemase-producing Escherichia coli isolated from Egyptian hospitals and environments. PLoS ONE 23(16):e0255219. https://doi.org/10.1371/journal.pone.0255219

    Article  CAS  Google Scholar 

  44. Flores-Mireles AL, Walker JN, Caparon M, Hultgren SJ (2015) Urinary tract infections: epidemiology, mechanisms of infection and treatment options. Nat Rev Microbiol 13(5):269–284. https://doi.org/10.1038/nrmicro3432

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Soto SM, Marco F, Guiral E, Vila J (2011) Biofilm formation in uropathogenic Escherichia coli strains: Relationship with urovirulence factors and antimicrobial resistance. INTECH https://doi.org/10.5772/24626

    Article  Google Scholar 

  46. Surgers L, Bleibtreu A, Burdet C, Clermont O, Laouénan C, Lefort A et al (2014) Escherichia coli bacteraemia in pregnant women is life-threatening for foetuses. Clin Microbiol Infect: Off Publ Eur Soc clin Microbiol Infect Dis 20(12):O1035–O1041. https://doi.org/10.1111/1469-0691.12742

    Article  CAS  Google Scholar 

  47. Milenkov M, Rasoanandrasana S, Rahajamanana LV, Rakotomalala RS, Razafindrakoto CA, Rafalimanana C et al (2021) Prevalence, risk factors, and genetic characterization of extended-spectrum beta-lactamase Escherichia coli Isolated from healthy pregnant women in madagaskar. Front Microbiol 12:786146. https://doi.org/10.3389/fmicb.2021.786146

    Article  PubMed  PubMed Central  Google Scholar 

  48. Hans JB, Pfenningwerth N, Neumann B, Pfeifer Y, Fischer MA, Eisfeld J et al (2023) Molecular surveillance reveals the emergence and dissemination of NDM-5-producing Escherichia coli high-risk clones in Germany, 2013 to 2019. Eurosurveillance 28(10):2200509. https://doi.org/10.2807/1560-7917.ES.2023.28.10.2200509

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Pereino G, Chen L, Nobrega D, Finn TJ, Kreiswirth BN, DeVinney R, Pitout JDD (2022) Genomic epidemiology of global carbapenemase-producing Escherichia coli, 2015–2017. Emerg Infect Dis 28(5):924–931. https://doi.org/10.3201/eid2805.212535

    Article  CAS  Google Scholar 

  50. Slown S, Walas N, Amato HK, Llyod T, Varghese V, Bender M, Pandori M, Graham J (2022) Clonal lineages and virulence factors of carbapenem Resistant E. coli in Alameda country, California 2017–2019. Antibiotics 11(12):1794. https://doi.org/10.3390/antibiotics11121794

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

The authors would like to express their sincere gratitude to the Director, Calcutta School of Tropical Medicine, Kolkata, and West Bengal, India for his kind support and cooperation. The authors would also like to thank Department of Science and Technology and Biotechnology, Government of West Bengal, India, for their funding support.

Funding

Department of Science and Technology and Biotechnology, Government of West Bengal, India (Grant no. 62(Sanc.)/BT/P/Budget/RD-60/2017).

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Authors and Affiliations

  1. Department of Biochemistry and Medical Biotechnology, School of Tropical Medicine, 108, C.R. Avenue, Kolkata, West Bengal, 700073, India

    Snehashis Koley, Arunita Ghosh & Mandira Mukherjee

  2. School of Biomedical Sciences and Pharmacy, University of Newcastle, Callaghan, NSW, Australia

    Arunita Ghosh

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Contributions

SK and MM proposed the concepts and designed the study. Data acquisition was done by SK. MLST data of eleven NP isolates were provided by AG. Data analysis, drafting, and revision of the manuscript were done by SK and MM.

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Correspondence to Mandira Mukherjee.

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The study protocol was approved by Institutional Clinical Research Ethics Committee (CREC-STM/2020-AG-13).

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Koley, S., Ghosh, A. & Mukherjee, M. Occurrence of Imipenem-Resistant Uropathogenic Escherichia coli in Pregnant Women: An Insight into Their Virulence Profile and Clonal Structure. Curr Microbiol 81, 56 (2024). https://doi.org/10.1007/s00284-023-03576-7

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