Characterization of Uropathogenic <i>Escherichia coli</i> by Phylogenetic Grouping, Integron, and Antibiotic Resistance Properties

Suhad H. Nasif; Munim R. Ali; Ali H. Alsakini

doi:10.26538/tjnpr/v8i4.41

Authors

Suhad H. Nasif Department of Biology, College of Science, Mustansiriyah University, Baghdad, Iraq
Munim R. Ali Department of Biology, College of Science, Mustansiriyah University, Baghdad, Iraq
Ali H. Alsakini Department of Biology, College of Science, Mustansiriyah University, Baghdad, Iraq

DOI:

https://doi.org/10.26538/tjnpr/v8i4.41%20

Keywords:

Urinary tract infections, Phylogenetic group, Integrons, Extensively-drug resistant, Escherichia coli

Abstract

Multidrug-resistant phenotypes in clinically important Gram-negative bacteria are a major medical issue worldwide. The presence of integrons from classes 1 and 2 (intl1 and intl2) and their phylogenetic correlations with antibiotic resistance in UPEC clinical isolates were examined in this investigation. Midstream urine samples from urinary tract infection outpatients in multiple Baghdad hospitals yielded 100 highly resistant E. coli bacteria. The automated VITEK system recognized typical E. coli colonies. Disk diffusion was used to investigate antibiotic susceptibility for the most frequent phylogroups. PCR was utilized to detect and characterize integrons and antibiotic resistance genes. The most common phylogroups were F (36.66%) and C (23.33%). UPEC isolates were detected in all phylogroups except six untyped ones. Integrons were found in 74.4% of isolates (61.4% intI1 and 13.3% intI2). The highest integron rate (85.71%) was in phylogroup C isolates. Integrons were linked to multidrug resistance in 60% of phylogroup F and C isolates. Nearly half of these isolates had multidrug resistance. This study found that phylogroup F dominates E. coli isolates due to a complex set of variables that support its expansion and persistence. Enhanced fitness, pathogenicity, and antibiotic resistance make these strains a public health threat. This study shows that clinically mobile Class 1 integrons attract more mobile genomic components. This may affect the establishment of complex, horizontally moving multidrug-resistant units, complicating antibiotic therapy.

References

Abed SY, Alsakini AH, Mohammad MK, Mohammed SQ, Kaabi SA. A Novel Broad-Host-Range Phage for Treatment of Mouse Model of Escherichia Coli Urinary Tract Infection. Trop J Nat Prod Res. 2022; 6(4): 488-493.

Dormanesh B, Dehkordi FS, Hosseini S, Momtaz H, Mirnejad R, Hoseini MJ, Yahaghi E, Tarhriz V, Darian EK. Virulence factors and o-serogroups profiles of uropathogenic Escherichia coli isolated from Iranian pediatric patients. Iran Red Crescent Med J. 2014; 16(2):e26399.

Mohsin MR, Al-Rubaii BA. Bacterial growth and antibiotic sensitivity of Proteus mirabilis treated with anti-inflammatory and painkiller drugs. Biomedicine (India), 2023; 43(2):728–734.

Clermont O, Christenson JK, Denamur E, Gordon DM. The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups. Environ Microbiol Rep. 2013; 5(1):58-65.

Heidari H, Hasanpour S, Ebrahim-Saraie HS, Motamedifar M. High incidence of virulence factors among clinical Enterococcus faecalis isolates in Southwestern Iran. Infect Chemother .2018; 49(1):51-56.

Kaushik M, Khare N, Kumar S, Gulati P. High Prevalence of Antibiotic Resistance and Integrons in Escherichia coli Isolated from Urban River Water, India. Microb Drug Resist. 2019; 25(3), 359–370.

Atlas RM, Alfred EB, Lawrence CP. Laboratory manual experimental microbiology. 1995. Mosby-year, Inc.

Clinical and Laboratory Standard Institute, Performance Standards for Antimicrobial Susceptibility Testing; Twenty-eight Informational Supplement. Document M100-S28,Wayne, PA, USA, 28th edition, 2021.

Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, Harbarth S, Hindler JF, Kahlmeter G, Olsson-Liljequist B, Paterson DL. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect.2012; 18(3), 268–281.

Tewawong N, Kowaboot S, Pimainog Y, Watanagul N, Thongmee T, Poovorawan Y. Distribution of phylogenetic groups, adhesin genes, biofilm formation, and antimicrobial resistance of uropathogenic Escherichia coli isolated from hospitalized patients in Thailand. Peer J. 2020; 8: e10453.

Ali MR and Khudhair AM. Detection of Colony Adhesion Factors and Genetic Background of Adhesion Genes among Multidrug-Resistant Uropathogenic Escherichia coli Isolated in Iraq. J Pure Appl Microbiol. 2018; 12(4):2017-2025.

Mobasseri P, Harsini MJ, Mehrabian S, Amini K. Detection of Different Types of Class 1, 2 and 3 Integrons among Pseudomonas aeruginosa Isolates from Raw Milks. J Med Bacteriol. 2021; 10(4), 11-18.

Vignoli R, Cordeiro N, Seija V, Schelotto F, Radice M, Ayala J, Power P, Gutkind G. Genetic environment of CTX-M-2 in Klebsiella pneumoniae isolates from hospitalized patients in Uruguay. Rev Argent Microbiol. 2006; 38(2), 84–88.

Clermont O, Gordon D, Denamur E. Guide to the various phylogenetic classification schemes for Escherichia coli and the correspondence among schemes. Microbiology.2015; 161(5), 980-988.

Mohsin AS, Alsakini AH, Ali MR. Outbreak of drug resistance Escherichia coli phylogenetic F group associated urinary tract infection. Iran J Microbiol. 2022; 14 (3): 341-350.

Fiore DC, Fox CL. Urology and nephrology update: recurrent urinary tract infection. FP Essent. 2014; 416, 30–37.

Nuutinen M, Uhari M. Recurrence and follow-up after urinary tract infection under the age of 1 year. Pediatr Nephrol.2001; 16(1), 69-72.

Silverman JA, Schreiber HL, Hooton TM, Hultgren SJ. From physiology to pharmacy: developments in the pathogenesis and treatment of recurrent urinary tract infections. Curr Urol Rep. 2013; 14, 448–456.

Milart P, Woźniakowska E, Woźniak S, Palacz T, Czuczwar P, Wrona W, Szkodziak P, Paszkowski M, Paszkowski T. Urinary tract infections in the menopausal period: optimal management. Prz Menopauzalny.2013; 12:23–28.

Arnold JJ, Hehn LE, Klein DA. Common questions about recurrent urinary tract infections in women. Am Fam Physician. 2016; 93:560–569.

Mohsin AS, Alsakini AH, Ali MR. Molecular characterization of Dr/Afa genes prevalent among multi drug resistant Escherichia coli isolated from urinary tract infections. Biomedicine .2022; 42(3):523-529.

Ali MR, Al-Taai HR, Al-Nuaeyme HA, Khudhair AM. Molecular study of genetic diversity in Escherichia coli isolated from different clinical sources. Biochem Cell Arch. 2018; 18(2): 2553-2560.

Maleki N, Kashanian S, Maleki E, Nazari M. A novel enzyme based biosensor for catechol detection in water samples using artificial neural network. Biochem Eng J. 2017; 128: 1-11.

Shah C, Baral R, Bartaula B, Shrestha LB. Virulence factors of uropathogenic Escherichia coli (UPEC) and correlation with antimicrobial resistance. BMC Microbiol. 2019; 19(1):1-6.

Abernethy J, Guy R, Sheridan EA, Hopkins S, Kiernan M, Wilcox MH, Johnson AP, Hope R, Sen RA, Mifsud A, O'Driscoll J. Epidemiology of Escherichia coli bacteraemia in England: results of an enhanced sentinel surveillance programme. J Hosp Infect .2017; 95(4): 365–375.

AL-Shuwaikh AM, Ibrahim IA, Al- Shwaikh RM. Detection of E. coli and rotavirus in diarrhea among children under five years old.. Iraqi J Biotechnol. 2015; 14(1):85-92.

Ciontea AS, Cristea D, Andrei MM, Popa A, Usein CR. In vitro antimicrobial resistance of urinary Escherichia coli isolates from outpatients collected in a laboratory during two years, 2015–2017. Roum Arch Microbiol Immunol. 2018; 77(1):28–32.

Husain AG, Alrubaii BA. Molecular detection and expression of virulence factor encoding genes of Pseudomonas aeruginosa isolated from clinical samples. Biomedicine (India), 2023; 43(5):1514-1519.

Al-Saadi HK, Awad HA, Saltan ZS, Hasoon BA, Abdulwahab AI, Al-Azawi KF, Al-Rubaii BA. Antioxidant and Antibacterial Activities of Allium sativum Ethanol Extract and Silver Nanoparticles. Trop J Nat Prod Res. 2023; 7(6): 3105–3110.

Khoramrooz SS, Sharifi A, Yazdanpanah M, Hosseini SA, Emaneini M, Gharibpour F, Parhizgari N, Mirzaii M, Zoladl M, Khosravani SA. High frequency of class 1 integrons in Escherichia coli isolated from patients with urinary tract infections in Yasuj, Iran. Iran Red Crescent Med J. 2016; 18(1):e26399.

Partridge SR, Kwong SM, Firth N, Jensen SO. Mobile Genetic Elements Associated with Antimicrobial Resistance. Clin Microbiol Rev.2018; 31(4):e00088.

Sütterlin S, Bray JE, Miaden MCJ, Tano E. Distribution of class 1 integrons in historic and contemporary collections of human pathogenic Escherichia coli. PLoS One. 2020; 15:e0233315.

Kubomura A, Sekizuka T, Onozuka D, Murakami K, Kimura H, Sakaguchi M, Oishi K, Hirai S, Kuroda M, Okabe N. Truncated class 1 integron gene cassette arrays contribute to antimicrobial resistance of diarrheagenic Escherichia coli. Biomed Res Int. 2020; 1-9.

Gaze WH, Abdouslam N, Hawkey PM, Wellington EM. Incidence of class 1 integrons in a quaternary ammonium compound-polluted environment. Antimicrob Agents Chemother. 2005; 49(5), 1802–1807.

Phongpaichit S, Wuttananupan K, Samasanti W. Class 1 integrons and multidrug resistance among Escherichia coli isolates from human stools. Southeast Asian J Trop Med Public Health. 2008; 39(2):279-278.

Momtaz H, Dehkordi FS, Hosseini MJ, Sarshar M, Heidari M. Serogroups, virulence genes and antibiotic resistance in Shiga toxin-producing Escherichia coli isolated from diarrheic and non-diarrheic pediatric patients in Iran. Gut pathogens.2013; 5(1):1-10.

Partridge SR, Kwong SM, Firth N, Jensen SO. Mobile genetic elements associated with antimicrobial resistance. Clin Microbiol Rev. 2018; 31(4):10-128.