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BMC Infectious Diseases

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Open Access 01-12-2018 | Research article

Distribution of virulence genes and their association with antimicrobial resistance among uropathogenic Escherichia coli isolates from Iranian patients

Authors: Yalda Malekzadegan, Reza Khashei, Hadi Sedigh Ebrahim-Saraie, Zahra Jahanabadi

Published in: BMC Infectious Diseases | Issue 1/2018

Abstract

Background

Urinary tract infections (UTIs) are one of the most frequent diseases encountered by humans worldwide. The presence of multidrug-resistant (MDR) uropathogenic Escherichia coli (UPEC) harboring several virulence factors, is a major risk factor for inpatients. We sought to investigate the rate of antibiotic resistance and virulence-associated genes among the UPECs isolated from an Iranian symptomatic population.

Methods

A total of 126 isolates from inpatients with UTI from different wards were identified as UPEC using the conventional microbiological tests. After identification of UPECs, all the isolates were subjected to antimicrobial susceptibility test and polymerase chain reaction (PCR) to identify the presence of 9 putative virulence genes and their association with the clinical outcomes or antimicrobial resistance.

Results

The data showed that the highest and the lowest resistance rates were observed against ampicillin (88.9%), and imipenem (0.8%), respectively. However, the frequency of resistance to ciprofloxacin was found to be 55.6%. High prevalence of MDR (77.8%) and extended-spectrum β-lactamase (ESBL) (54.8%) were substantial. PCR results revealed the frequency of virulence genes ranged from 0 to 99.2%. Among 9 evaluated genes, the frequency of 4 genes (fimH, sfa, iutA, and PAI marker) was > 50% among all the screened isolates. The iutA, pap GII, and hlyA genes were more detected in the urosepsis isolates with significantly different frequencies. The different combinations of virulence genes were characterized as urovirulence patterns. The isolates recovered from pyelonephritis, cystitis, and urosepsis cases revealed 27, 22, and 6 virulence patterns, respectively. A significant difference was determined between ESBL production with pap GII, iutA, and PAI marker genes.

Conclusions

Our study highlighted the MDR UPEC with high heterogeneity of urovirulence genes. Considering the high rate of ciprofloxacin resistance, alternative drugs and monitoring of the susceptibility profile for UPECs are recommended.

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Lee JH, Subhadra B, Son YJ, Kim DH, Park HS, Kim JM, et al. Phylogenetic group distributions, virulence factors and antimicrobial resistance properties of uropathogenic Escherichia coli strains isolated from patients with urinary tract infections in South Korea. Lett Appl Microbiol. 2016;62:84–90. https://doi.org/10.1111/lam.12517.CrossRefPubMed

Lai YM, Zaw MT, Shamsudin SB, Lin Z. Evaluation of PAIusp subtyping to characterize uropathogenic E. coli isolates. J Infect Dev Ctries. 2016;10:1053–8. https://doi.org/10.3855/jidc.6944.CrossRefPubMed

Morales-Espinosa R, Hernandez-Castro R, Delgado G, Mendez JL, Navarro A, Manjarrez A, et al. UPEC strain characterization isolated from Mexican patients with recurrenturinary infections. J Infect Dev Ctries. 2016;10:317–28. https://doi.org/10.3855/jidc.6652.CrossRefPubMed

Singh SK, Seema K, Gupta M. Detection of AmpC b-lactamase and adherence factors in uropathogenic Escherichia coli isolated from aged patients. Microb Pathog. 2016;100:293–8. https://doi.org/10.1016/j.micpath.2016.10.010.CrossRefPubMed

Gao Q, Zhang D, Ye Z, Zhu X, Yang W, Dong L, et al. Virulence traits and pathogenicity of uropathogenic Escherichia coli isolates with common and uncommon O serotypes. Microb Pathog. 2017;104:217–24. https://doi.org/10.1016/j.micpath.2017.01.027.CrossRefPubMed

Alteri CJ, Mobley HL. Metabolism and fitness of urinary tract pathogens. Microbiol Spectr. 2015;3(3). https://doi.org/10.1128/microbiolspec.

Yun KW, Kim HY, Park HK, Kim W, Lim IS. Virulence factors of uropathogenic Escherichia coli of urinary tract infections and asymptomatic bacteriuria in children. J Microbiol Immunol Infect. 2014;47:455–61. https://doi.org/10.1016/j.jmii.2013.07.010.CrossRefPubMed

Flokas ME, Detsis M, Ml A, Mylonakis E. Prevalence of ESBL-producing Enterobacteriaceae in paediatric urinary tract infections: a systematic review and meta-analysis. J Inf Secur. 2016;73:547–57. https://doi.org/10.1016/j.jinf.2016.07.014.CrossRef

Hadifar S, Moghoofei M, Nematollahi S, Ramazanzadeh R, Sedighi M, Salehi-Abargouei A, et al. Epidemiology of multidrug resistant uropathogenic Escherichia coli in Iran: a systematic review and meta-analysis. Jpn J Infect Dis. 2017;70:19–25. https://doi.org/10.7883/yoken.JJID.2015.652.CrossRefPubMed

10.

Walker KE, Mahon CR, Lehman D, Manuselis G. Enterobacteriaceae. In: Mahon CR, Lehman D, Manuselis G, editors. Textbook of diagnostic microbiology. 5th ed. New York: W. B. Saunders Company; 2015. p. 420–54.

11.

Wayne PA. Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing 2015; 25th informational supplement. M100-S25.

12.

Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012;18:268–81. https://doi.org/10.1111/j.1469-0691.2011.03570.x.CrossRefPubMed

13.

Oktem IM, Gulay Z, Bicmen M, Gur D. HITIT project study group. qnrA prevalence in extended-spectrum beta-lactamase-positive Enterobacteriaceae isolates from Turkey. Jpn J Infect Dis. 2008;61:13–7.PubMed

14.

Chapman TA, Wu XY, Barchia I, Bettelheim KA, Driesen S, Trott D, et al. Comparison of virulence gene profiles of Escherichia coli strains isolated from healthy and diarrheic swine. Appl Environ Microbiol. 2006;72:4782–95.CrossRef

15.

Paniagua-Contreras GL, Monroy-Pérez E, Rodríguez-Moctezuma JR, Domínguez-Trejo P, Vaca-Paniagua F, Vaca S. Virulence factors, antibiotic resistance phenotypes and O-serogroups of Escherichia coli strains isolated from community-acquired urinary tract infection patients in Mexico. J Microbiol Immunol Infect. 2017;50:478–85. https://doi.org/10.1016/j.jmii.2015.08.005.CrossRefPubMed

16.

Narciso A, Nunes F, Amores T, Lito L, Melo-Cristino J, Duarte A. Persistence of uropathogenic Escherichia coli strains in the host for long periods of time: relationship between phylogenetic groups and virulence factors. Eur J Clin Microbiol Infect Dis. 2012;31:1211–7. https://doi.org/10.1007/s10096-011-1431-7.CrossRefPubMed

17.

Rahdar M, Rashki A, Miri HR, Rashki Ghalehnoo M. Detection of pap, sfa, afa, foc, and fim adhesin-encoding operons in uropathogenic Escherichia coli isolates collected from patients with urinary tract infection. Jundishapur J Microbiol. 2015;8:e22647. https://doi.org/10.5812/jjm.22647.CrossRefPubMedPubMedCentral

18.

Qin X, Hu F, Wu S, Ye X, Zhu D, Zhang Y, et al. Comparison of adhesin genes and antimicrobial susceptibilities between uropathogenic and intestinal commensal Escherichia coli strains. PLoS One. 2013;8:e61169. https://doi.org/10.1371/journal.pone.0061169.CrossRefPubMedPubMedCentral

19.

Tarchouna M, Ferjani A, Ben-Selma W, Boukadida J. Distribution of uropathogenic virulence genes in Escherichia coli isolated from patients with urinary tract infection. Int J Infect Dis. 2013;17:e450–3. https://doi.org/10.1016/j.ijid.2013.01.025.CrossRefPubMed

20.

Tabasi M, Asadi Karam MR, Habibi M, Yekaninejad MS, Bouzari S. Phenotypic assays to determine virulence factors of uropathogenic Escherichia coli (UPEC) isolates and their correlation with antibiotic resistance pattern. Osong Public Health Res Perspect. 2015;6:261–8. https://doi.org/10.1016/j.phrp.2015.08.002.CrossRefPubMedPubMedCentral

21.

Mohajeri P, Khademi H, Ebrahimi R, Farahani A, Rezaei M. Frequency distribution of virulence factors in uropathogenic Escherichia coli isolated from Kermanshah in 2011-2012. Int J Appl Basic Med Res. 2014;4:111–6. https://doi.org/10.4103/2229-516X.136794.CrossRefPubMedPubMedCentral

22.

Santo E, Macedo C, Marin JM. Virulence factors of uropathogenic Escherichia coli from a university hospital in Ribeirão Preto, São Paulo, Brazil. Rev Inst Med Trop Sao Paulo. 2006;48:185–8.CrossRef

23.

Firoozeh F, Saffari M, Neamati F, Zibaei M. Detection of virulence genes in Escherichia coli isolated from patients with cystitis and pyelonephritis. Int J Infect Dis. 2014;29:219–22. https://doi.org/10.1016/j.ijid.2014.03.1393.CrossRefPubMed

24.

Oliveira FA, Paludo KS, Arend LN, Farah SM, Pedrosa FO, Souza EM, et al. Virulence characteristics and antimicrobial susceptibility of uropathogenic Escherichia coli strains. Genet Mol Res. 2011;10:4114–25. https://doi.org/10.4238/2011. CrossRefPubMed

25.

Samei A, Haghi F, Zeighami H. Distribution of pathogenicity island markers in commensal and uropathogenic Escherichia coli isolates. Folia Microbiol (Praha). 2016;61:261–8. https://doi.org/10.1007/s12223-015-0433-8.CrossRef

26.

Firoozeh F, Soleimani-Moorchekhorti L, Zibaei M. Evaluation of pathogenicity islands in uropathogenic Escherichia coli isolated from patients with urinary catheters. J Infect Dev Ctries. 2017;11:557–62. https://doi.org/10.3855/jidc.8660.CrossRef

27.

Navidinia M, Najar Peerayeh S, Fallah F, Bakhshi B. Phylogenetic groups and pathogenicity island markers in Escherichia coli isolated from children. Jundishapur J Microbiol. 2013;6:e8362. https://doi.org/10.5812/jjm.8362.CrossRef

28.

Yahiaoui M, Robin F, Bakour R, Hamidi M, Bonnet R, Messai Y. Antibiotic resistance, virulence, and genetic background of community-acquired uropathogenic Escherichia coli from Algeria. Microb Drug Resist. 2015;21:516–26. https://doi.org/10.1089/mdr.2015.0045.CrossRefPubMed

29.

Chiu CC, Lin TC, Wu RX, Yang YS, Hsiao PJ, Lee Y, et al. Etiologies of community-onset urinary tract infections requiring hospitalization and antimicrobial susceptibilities of causative microorganisms. J Microbiol Immunol Infect. 2017;50:879–85. https://doi.org/10.1016/j.jmii.2016.08.008.CrossRefPubMed

30.

Neamati F, Firoozeh F, Saffari M, Zibaei M. Virulence genes and antimicrobial resistance pattern in uropathogenic Escherichia coli isolated from hospitalized patients in Kashan, Iran. Jundishapur J Microbiol. 2015;8:e17514. https://doi.org/10.5812/jjm.17514.CrossRefPubMedPubMedCentral

31.

Tandogdu Z, Wagenlehner FM. Global epidemiology of urinary tract infections. Curr Opin Infect Dis. 2016;29:73–9. https://doi.org/10.1097/QCO.0000000000000228.CrossRefPubMed

32.

Stultz JS, Doern CD, Godbout E. Antibiotic resistance in pediatric urinary tract infections. Curr Infect Dis Rep. 2016;18:40.CrossRef

33.

Fasugba O, Gardner A, Mitchell BG, Mnatzaganian G. Ciprofloxacin resistance in community- and hospital-acquired Escherichia coli urinary tract infections: a systematic review and meta-analysis of observational studies. BMC Infect Dis. 2015;15:545. https://doi.org/10.1186/s12879-015-1282-4.CrossRefPubMedPubMedCentral

34.

Haghighatpanah M, Mozaffari Nejad AS, Mojtahedi A, Amirmozafari N, Zeighami H. Detection of extended-spectrum β-lactamase (ESBL) and plasmid-borne blaCTX-M and blaTEM genes among clinical strains of Escherichia coli isolated from patients in the north of Iran. J Glob Antimicrob Resist. 2016;7:110–3. https://doi.org/10.1016/j.jgar.2016.08.005. CrossRefPubMed

35.

Farshad S, Japoni A, Hosseini M. Low distribution of integrons among multidrug resistant E. coli strains isolated from children with community-acquired urinary tract infections in shiraz, Iran. Pol J Microbiol. 2008;57:193–8.PubMed

36.

Stock I. Nitrofurantoin--clinical relevance in uncomplicated urinary tract infections. Med Monatsschr Pharm. 2014;37:242–8.PubMed

37.

El Sakka N, Gould IM. Role of old antimicrobial agents in the management of urinary tract infection. Expert Rev Clin Pharmacol. 2016;9:1047–56. https://doi.org/10.1080/17512433.2016.1189325.CrossRefPubMed

38.

Ramos NL, Dzung DT, Stopsack K, Jankó V, Pourshafie MR, Katouli M, et al. Characterisation of uropathogenic Escherichia coli from children with urinary tract infection in different countries. Eur J Clin Microbiol Infect Dis. 2011;30:1587–93. https://doi.org/10.1007/s10096-011-1264-4.CrossRefPubMed

39.

Asgharzadeh Kangachar S, Mojtahedi A. The presence of extended-spectrum β-lactamase as a risk factor for MDR in clinical isolation of Escherichia coli. Trop Biomed. 2017;34:1–12.

40.

Ghadiri H, Vaez H, Razavi-Azarkhiavi K, Rezaee R, Haji-Noormohammadi M, Rahimi AA, et al. Prevalence and antibiotic susceptibility patterns of extended-spectrum ß-lactamase and metallo-ß-lactamase-producing uropathogenic Escherichia coli isolates. Lab Med. 2014;45:291–6. https://doi.org/10.1309/LMHEP4VQHEY2POOK.CrossRefPubMed

Title: Distribution of virulence genes and their association with antimicrobial resistance among uropathogenic Escherichia coli isolates from Iranian patients
Authors: Yalda Malekzadegan
Reza Khashei
Hadi Sedigh Ebrahim-Saraie
Zahra Jahanabadi
Publication date: 01-12-2018
Publisher: BioMed Central
Published in: BMC Infectious Diseases / Issue 1/2018
Electronic ISSN: 1471-2334
DOI: https://doi.org/10.1186/s12879-018-3467-0

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