Antibiotic Susceptibility Profile and Detection of Plasmid-Mediated Quinolone Resistant Genes Among Extended Spectrum β-Lactamases (ESBL) Producing Uropathogens in Women
Abstract
Background/Aim: The most common bacterial diseases in women around the world are urinary tract infections. Aim of this study, was to evaluate the prevalence and current antibiotic resistance rate of uropathogens isolated from the female patients of a tertiary care hospital in Amritsar, Punjab, India.
Methods: Samples were collected from patients showing urinary tract infection (UTI) symptoms and analysed using microscopy, dipstick test and urine culturing followed by identification and characterisation of to identify the uropathogens. Antibiotic susceptibility test and MIC were performed.
Results: The results revealed that E coli (35.5 %) was the most prominent uropathogen followed by Klebsiella spp (21 %), Enterobacter spp (17 %), Acinetobacter (11 %), Enterococcus spp (6 %), Pseudomonas spp (4.5 %), coagulase negative Staphylococci (4 %), coagulase-positive Staphylococci (0.5 %) and Corynebacterium aurimucosum (0.5 %). The antibiotic susceptibility profile study reported eight isolates with multi-drug resistance properties. However, gentamicin, imipenem and meropenem were found to be the most effective antibiotics against the isolated uropathogens. All the extended spectrum β-lactamase (ESBL)-positive isolates possess the quinolone-resistant gene qnrB, while qnrA was absent.
Conclusion: The current study revealed that for appropriate treatment, it is crucial to be aware of the epidemiological data regarding the disease and to begin any empirical antibiotic treatment.
References
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 Feb 17;2019:4246780. doi: 10.1155/2019/4246780.
Singhal A, Sharma R, Jain M, Vyas L. Hospital and community isolates of uropathogens and their antibiotic sensitivity pattern from a tertiary care hospital in North West India. Ann Med Health Sci Res 2014 Jan;4(1):51-6.
Bischoff S, Walter T, Gerigk M, Ebert M, Vogelmann R. Empiric antibiotic therapy in urinary tract infection in patients with risk factors for antibiotic resistance in a German emergency department. BMC Infect Dis 2018 Jan 26;18(1):56. doi: 10.1186/s12879-018-2960-9.
Beahm NP, Nicolle LE, Bursey A, Smyth DJ, Tsuyuki RT. The assessment and management of urinary tract infections in adults: Guidelines for pharmacists. Can Pharm J (Ott) 2017 Jul 31;150(5):298-305.
Tandogdu Z, Wagenlehner FM. Global epidemiology of urinary tract infections. Curr Opin Infect Dis 2016 Feb;29(1):73-9.
Kaur R, Kaur R. Symptoms, risk factors, diagnosis and treatment of urinary tract infections. Postgrad Med J 2021 Dec;97(1154):803-12.
Manyi-Loh C, Mamphweli S, Meyer E, Okoh A. Antibiotic use in agriculture and its consequential resistance in environmental sources: potential public health implications. Molecules 2018 Mar 30;23(4):795. doi: 10.3390/molecules23040795.
Shaikh S, Fatima J, Shakil S, Rizvi SM, Kamal MA. Antibiotic resistance and extended spectrum beta-lactamases: Types, epidemiology and treatment. Saudi J Biol Sci 2015 Jan;22(1):90-101.
Murray CJ, Ikuta KS, Sharara F, Swetschinski L, Aguilar GR, Gray A, et al. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. The Lancet 2022 Feb 12;399(10325):629-55.
Shrivastava SR, Shrivastava PS, Ramasamy J. World health organization releases global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics. J Med Soc 2018 Jan 1;32(1):76-7.
Castanheira M, Simner PJ, Bradford PA. Extended-spectrum β-lactamases: an update on their characteristics, epidemiology and detection. JAC Antimicrob Resist 2021 Jul 16;3(3):dlab092. doi: 10.1093/jacamr/dlab092.
Kammili N, Rani M, Styczynski A, Latha M, Pavuluri PR, Reddy V, Alsan M. Plasmid-mediated antibiotic resistance among uropathogens in primigravid women-Hyderabad, India. PLoS One 2020 May 8;15(5):e0232710. doi: 10.1371/journal.pone.0232710.
Emmerson AM, Jones AM. The quinolones: decades of development and use. J Antimicrob Chemother 2003 May;51 Suppl 1:13-20.
Gibbons NE, Buchanan RE, Eds. Bergey's manual of determinative bacteriology. Philadelphia, USA: Williams & Wilkins company, 1974.
Kaur R, Singh D, Kesavan AK, Kaur R. Molecular characterization and antimicrobial susceptibility of bacterial isolates present in tap water of public toilets. Int Health 2020 Sep;12(5):472-83.
Lane DJ (1991) 16S/23S rRNA Sequencing. In: Stackebrandt E, Goodfellow M, Eds. Nucleic acid techniques in bacterial systematic. New York, USA: John Wiley and Sons, 1991; pp. 115-175.
Bauer AW, Kirby WM, Sherris JC, Turck M. Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 1966 Apr;45(4):493-6.
Wayne P. Performance standards for antimicrobial susceptibility testing; twenty-fourth informational supplement. CLSI Document M100-S24. Wayne, Pennsylvania: Clinical and Laboratory Standards Institute, 2014.
Krumperman PH. Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of foods. Appl Environ Microbiol 1983 Jul;46(1):165-70.
Kaur J, Chopra S, Sheevani, Mahajan G. Modified double disc synergy test to detect ESBL production in urinary isolates of Escherichia coli and Klebsiella pneumoniae. J Clin Diagn Res 2013 Feb;7(2):229-33.
O'Toole GA. Microtiter dish biofilm formation assay. J Vis Exp 2011 Jan 30;(47):2437. doi: 10.3791/2437.
Stepanović S, Vuković D, Dakić I, Savić B, Švabić-Vlahović M. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Methods 2000 Apr;40(2):175-9.
Hotchandani R, Aggarwal KK. Urinary tract infections in women. Indian J Clin Practice 2012;23(4):187-94.
Anejo-Okopi JA, Okojokwu OJ, Ramyil SM, Bakwet PB, Okechalu J, Agada G, et al. Bacterial and antibiotic susceptibility pattern of urinary tract infection isolated from asymptomatic and symptomatic diabetic patients attending tertiary hospital in Jos, Nigeria. Trends Med 2017 Nov 23;17(1):1-5.
Wrenn K. Dysuria, frequency, and urgency. In: Walker HK, Hall WD, Hurst JW, eds. Clinical methods: the history, physical, and laboratory examinations. 3rd edition. Boston: Butterworths, 1990; Chapter 181.
Bremnor JD, Sadovsky R. Evaluation of dysuria in adults. Am Fam Physician 2002 Apr 15;65(8):1589-96.
Kurowski K. The women with dysuria. Am Fam Physician 1998 May;57(9):2155-64.
Ainsworth JG, Weaver T, Murphy S, Renton A. General practitioners' immediate management of men presenting with urethral symptoms. Genitourin Med 1996 Dec;72(6):427-30.
Hanno P, Dmochowski R. Status of international consensus on interstitial cystitis/bladder pain syndrome/painful bladder syndrome: 2008 snapshot. Neurourol Urodyn 2009;28(4):274-86.
Hoffman RF. Acute dysuria or pyuria in men. Decision making in medicine: an algorithmic approach. St Louis, Mosby 1998:506-7.
Rao PN, Preminger GM, Kavanagh JP, eds. Urinary tract stone disease. London: Springer, 2011.
Daza R, Gutiérrez J, Piédrola G. Antibiotic susceptibility of bacterial strains isolated from patients with community-acquired urinary tract infections. Int J Antimicrob Agents 2001 Sep;18(3):211-5.
Farajnia S, Alikhani MY, Ghotaslou R, Naghili B, Nakhlband A. Causative agents and antimicrobial susceptibilities of urinary tract infections in the northwest of Iran. Int J Inf Dis 2009 Mar 1;13(2):140-4.
Foxman B. The epidemiology of urinary tract infection. Nat Rev Urol 2010 Dec;7(12):653-60.
Singhal A, Sharma R, Jain M, Vyas L. Hospital and community isolates of uropathogens and their antibiotic sensitivity pattern from a tertiary care hospital in North West India. Ann Med Health Sci Res 2014 Jan;4(1):51-6.
Fernando MM, Luke WA, Miththinda JK, Wickramasinghe RD, Sebastiampillai BS, Gunathilake MP, et al. Extended spectrum beta lactamase producing organisms causing urinary tract infections in Sri Lanka and their antibiotic susceptibility pattern–a hospital based cross sectional study. BMC Infect Dis 2017 Feb 10;17(1):138. doi: 10.1186/s12879-017-2250-y.
Gajamer VR, Bhattacharjee A, Paul D, Kapil J, Sarkar A, Singh AK, et al. The first report of phenotypic and molecular characterization of extended-spectrum beta-lactamase-producing uropathogens in Sikkim and Darjeeling hills of India. Microb Drug Resist 2018 Nov;24(9):1284-8.
Minardi D, d’Anzeo G, Cantoro D, Conti A, Muzzonigro G. Urinary tract infections in women: etiology and treatment options. Int J Gen Med 2011;4:333-43.
Sabih A, Leslie SW. Complicated urinary tract infections, 2023. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2023 Jan-. [Cited: 1-Oct_2023]. Available from: https://www.ncbi.nlm.nih.gov/books/NBK436013/.
Svanborg C, Bergsten G, Fischer H, Godaly G, Gustafsson M, Karpman D, et al. Uropathogenic Escherichia coli as a model of host–parasite interaction. Curr Opin Microbiol 2006 Feb;9(1):33-9.
Foxman B, Gillespie B, Koopman J, Zhang L, Palin K, Tallman P, et al. Risk factors for second urinary tract infection among college women. Am J Epidemiol 2000 Jun 15;151(12):1194-205.
Anejo-Okopi JA, Okojokwu OJ, Ramyil SM, Bakwet PB, Okechalu J, Agada G, et al. Bacterial and antibiotic susceptibility pattern of urinary tract infection isolated from asymptomatic and symptomatic diabetic patients attending tertiary hospital in Jos, Nigeria. Trends Med 2017 Nov 23;17(1):1-5.
Amabebe E, Anumba DO. Female gut and genital tract microbiota-induced crosstalk and differential effects of short-chain fatty acids on immune sequelae. Front Immunol 2020 Sep 10;11:2184. doi: 10.3389/fimmu.2020.02184.
Ancillotti M. Antibiotic resistance: a multimethod investigation of individual responsibility and behaviour. Digital comprehensive summaries of Uppsala dissertations from the Faculty of Medicine. Uppsala: Acta Universitatis Upsaliensis, 2021.
Elsayed TI, Ismail HA, Elgamal SA, Gad AH. The occurrence of multidrug resistant E. coli which produce ESBL and cause urinary tract infections. J Appl Microbiol Biochem 2017;1(2):8. DOI: 10.21767/2576-1412.100008.
Lerminiaux NA, Cameron ADS. Horizontal transfer of antibiotic resistance genes in clinical environments. Can J Microbiol 2019 Jan;65(1):34-44.
Baquero F, Martínez JL, Cantón R. Antibiotics and antibiotic resistance in water environments. Curr Opin Biotechnol 2008 Jun;19(3):260-5.
Canton R. Antibiotic resistance genes from the environment: a perspective through newly identified antibiotic resistance mechanisms in the clinical setting. Clin Microbiol Infect 2009 Jan;15 Suppl 1:20-5.
Ventola CL. The antibiotic resistance crisis: part 1: causes and threats. P T 2015 Apr;40(4):277-83.
Majumder MM, Mahadi AR, Ahmed T, Ahmed M, Uddin MN, Alam MZ. Antibiotic resistance pattern of microorganisms causing urinary tract infection: a 10-year comparative analysis in a tertiary care hospital of Bangladesh. Antimicrob Resist Infect Control 2022 Dec 10;11(1):156. doi: 10.1186/s13756-022-01197-6.
Kothari A, Sagar V. Antibiotic resistance in pathogens causing community-acquired urinary tract infections in India: a multicenter study. J Infect Dev Ctries 2008 Oct 1;2(5):354-8.
Gupta S, Kapur S, Padmavathi DV. Comparative prevalence of antimicrobial resistance in community-acquired urinary tract infection cases from representative States of northern and southern India. J Clin Diagn Res 2014 Sep;8(9):DC09-12.
Lakshminarayana SA, Chavan SK, Prakash R, Sangeetha S. Bacterial pathogens in urinary tract infection and antibiotic susceptibility pattern from a Teaching Hospital, Bengaluru, India. Int j Curr Microbiol Appl Sci 2015;4(11):731-6.
Patel HB, Soni ST, Bhagyalaxmi A, Patel NM. Causative agents of urinary tract infections and their antimicrobial susceptibility patterns at a referral centre in Western India: An audit to help clinicians prevent antibiotic misuse. J Family Med Prim Care 2019 Jan;8(1):154-9.
Oberoi L, Singh N, Sharma P, Aggarwal A. ESBL, MBL and Ampc β Lactamases Producing Superbugs - Havoc in the Intensive Care Units of Punjab India. J Clin Diagn Res 2013 Jan;7(1):70-3.
Ojdana D, Sacha P, Wieczorek P, Czaban S, Michalska A, Jaworowska J, et al. 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 Antib 2014:935842. Doi:10.1155/2014/935842.
Gajamer VR, Bhattacharjee A, Paul D, Ingti B, Sarkar A, Kapil J, et al. High prevalence of carbapenamase genes, AmpC genes and aminoglycoside resistance genes in extended spectrum β-lactamase positive uropathogens from Northern India. J Glob Antimicrob Resist 2020 Mar;20:197-203.
Malekzadegan Y, Rastegar E, Moradi M, Heidari H, Ebrahim-Saraie HS. Prevalence of quinolone-resistant uropathogenic Escherichia coli in a tertiary care hospital in south Iran. Infect Drug Resist 2019 Jun 19;12:1683-9.
Tayebi Z, Heidari H, Kazemian H, Ghafoori SM, Boroumandi S, Houri H. Comparison of quinolone and beta-lactam resistance among Escherichia coli strains isolated from urinary tract infections. Infez Med 2016 Dec 1;24(4):326-30.
Eberly A, Floyd K, Beebout C, Colling S, Fitzgerald M, Stratton C, et al. Biofilm formation by uropathogenic Escherichia coli is favored under oxygen conditions that mimic the bladder environment. Int J Mol Sci 2017 Sep 30;18(10):2077. doi: 10.3390/ijms18102077.
Zheng JX, Bai B, Lin ZW, Pu ZY, Yao WM, Chen Z, et al. Characterization of biofilm formation by Enterococcus faecalis isolates derived from urinary tract infections in China. J Med Microbiol 2018 Jan;67(1):60-7.
Alves MJ, Barreira J, Carvalho I, Trinta L, Pereira L, Ferreira IC, et al. Propensity for biofilm formation by clinical isolates from urinary tract infections: developing a multifactorial predictive model to improve the antibiotherapy. J Med Microbiol 2014;63:471-7.
Tayal RA, Baveja SM, De Anuradha S. Analysis of biofilm formation and antibiotic susceptibility pattern of uropathogens in patients admitted in a tertiary care hospital in India. Int J Health Allied Sci 2015 Oct 1;4(4):247-52.
Karigoudar RM, Karigoudar MH, Wavare SM, Mangalgi SS. Detection of biofilm among uropathogenic Escherichia coli and its correlation with antibiotic resistance pattern. J Lab Physicians 2019 Jan-Mar;11(1):17-22.
Ahmed OI, El-Hady SA, Ahmed TM, Ahmed IZ. Detection of bla SHV and bla CTX-M genes in ESBL producing Klebsiella pneumoniae isolated from Egyptian patients with suspected nosocomial infections. Egyptian J Med Human Gen 2013 Jul 9;14(3):277-83.
Grover SS, Sharma M, Chattopadhya D, Kapoor H, Pasha ST, Singh G. Phenotypic and genotypic detection of ESBL mediated cephalosporin resistance in Klebsiella pneumoniae: emergence of high resistance against cefepime, the fourth generation cephalosporin. J Infect 2006 Oct;53(4):279-88.
Schwartz T, Kohnen W, Jansen B, Obst U. Detection of antibiotic-resistant bacteria and their resistance genes in wastewater, surface water, and drinking water biofilms. FEMS Microbiol Ecol 2003 Apr 1;43(3):325-35.
Wu JJ, Ko WC, Tsai SH, Yan JJ. Prevalence of plasmid-mediated quinolone resistance determinants QnrA, QnrB, and QnrS among clinical isolates of Enterobacter cloacae in a Taiwanese hospital. Antimicrob Agents Chemother 2007 Apr;51(4):1223-7.
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