Investigation of class 1 integrons and biofilm formation in multi-drug resistance uropathogenic Escherichia coli isolated from patients with urinary tract infection in Shohadaye Qom hospital, Iran



    Table of Contents ORIGINAL ARTICLE Year : 2022  |  Volume : 9  |  Issue : 1  |  Page : 47-52

Investigation of class 1 integrons and biofilm formation in multi-drug resistance uropathogenic Escherichia coli isolated from patients with urinary tract infection in Shohadaye Qom hospital, Iran

Ahmad Khorshidi1 ORC ID , Nadia Mohammad Zadeh2, Azad Khaledi1, Gholam Abbas Moosavi3, Ali Shakerimoghaddam1, Azade Matinpur1 ORC ID
1 Department of Microbiology and Immunology, Faculty of Medicine, Kashan University of Medical Science; Infectious Diseases Research Center, Kashan University of Medical Science, Kashan, Iran
2 School of Medicine, Islamic Azad University Tehran Medical Branch, Tehran, Iran
3 Department of Vital Statistics and Epidemiology, School of Health, Kashan University of Medical Sciences, Kashan, Iran

Date of Submission25-Aug-2021Date of Decision10-Jan-2022Date of Acceptance10-Jan-2022Date of Web Publication29-Mar-2022

Correspondence Address:
Dr. Azade Matinpur
Department of Microbiology and Immunology, School of Medicine, Kashan University of Medical Sciences, Kashan
Iran
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/iahs.iahs_163_21

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Aims: This study aimed to investigate class 1 integrons and biofilm formation in multi-drug resistance (MDR) Uropathogenic Escherichia coli (UPEC) isolated from patients with urinary tract infection (UTI). Materials and Methods: Three hundred and eighty positive cultures were collected from patients with UTI referred to Shohadaye Qom hospital from 2018 to 2019. Suitable tests were done to diagnose UPEC, and confirmed by usp gene polymerase chain reaction (PCR). Antibiotic susceptibility testing was performed using Kirby Bauer disk diffusion. Analysis of biofilm production was conducted using microtiter plate assay. Next, the presence of Class 1 integrons and dfr-17 gene was surveyed by PCR. Data analyzed using Chi-squared and Fisher's exact tests in SPSS software, P < 0.05 was considered statistically significant. Findings: In total, 166 isolates of UPEC were retrieved. Among them, 120 isolates were MDR. The highest resistance of MDRs was observed against ampicillin. Among MDRs, 71, 18, 15, and 16 isolates were negative, weak, moderate, and strong biofilm producers, respectively. Meanwhile, 47.5% of the isolates were positive for int-1 gene and 25.8% of the isolates were positive for dfr-17-gene cassette. Out of 57 int-1 positive MDRs, 15 isolates (26.3%) showed strong biofilm which indicated a significant correlation (P < 0.001). Furthermore, among 31 MDRs with the positive dfr-17, 8 isolates (25.8%) had strong biofilm which statistically was significant (P < 0.001). Conclusion: The present study reported a significant correlation between cassettes genes, Class 1 integrons, and biofilm formation with antibiotic resistance pattern. Hence, continuous screening for antibiotics resistance is vital for infection control and prevention.

Keywords: Antibiotic resistance, biofilm formation, integron, uropathogenic Escherichia coli


How to cite this article:
Khorshidi A, Zadeh NM, Khaledi A, Moosavi GA, Shakerimoghaddam A, Matinpur A. Investigation of class 1 integrons and biofilm formation in multi-drug resistance uropathogenic Escherichia coli isolated from patients with urinary tract infection in Shohadaye Qom hospital, Iran. Int Arch Health Sci 2022;9:47-52
How to cite this URL:
Khorshidi A, Zadeh NM, Khaledi A, Moosavi GA, Shakerimoghaddam A, Matinpur A. Investigation of class 1 integrons and biofilm formation in multi-drug resistance uropathogenic Escherichia coli isolated from patients with urinary tract infection in Shohadaye Qom hospital, Iran. Int Arch Health Sci [serial online] 2022 [cited 2022 Mar 29];9:47-52. Available from: http://www.iahs.kaums.ac.ir/text.asp?2022/9/1/47/341214   Introduction Top

Urinary tract infection (UTI) is a pathogenic invasion to urothelium alongside inflammation that includes lower and upper UTIs.[1] UTI is usually caused by Uropathogenic  Escherichia More Details coli. Seventy to ninety-nine percent high antibiotic resistance in UPEC (multidrug resistance [MDR]) leads to complications and treatment failures, recurrence, and prolonged UTI which ultimately leads to parenchymal destruction or renal failure.[2],[3]

A systematic review and meta-analysis on UTI from Iran in 2020 showed that the pooled prevalence of UTI in women and men was 65.5%, and 30.7%, respectively.[4] In addition, the same study reported the combined prevalence of MDR strains of uropathogenic E. coli (UPEC) recovered from UTI 81.1%.[4]

Integrons and genetic cassettes are key factors and important risk factors for the development of antibiotic resistance in UPEC isolates.[5] Antibiotic resistance results from these genes have raised concerns about the treatment of infections caused by UPEC MDRs.[6] Resistance genes are often spread through mobile genetic elements such as plasmids and integrons. Recent studies on UPEC have shown a strong link between the presence of integrons and antibiotic resistance in various regions of Asia, Europe, and the United States.[7] Genetic cassettes are mobile genetic elements that lack a promoter sequence in their structure; thus, expressing gene cassettes is associated with the presence of promoters in the structure of integrons. The dfra1 and dfra17, 7 genetic cassettes were recognized in 16% and 70.6% of UPEC isolates, respectively. The dfra17, 7 is highly associated with class 1 integrons.[2] This genetic cassette carries more than 40 resistance genes associated with resistance to aminoglycosides, beta-lactams, chloramphenicol, macrolides, and sulfonamides.[8] Class 1 integron (int1) is recognized in 49% of UPEC species.

Another major factor in the spread of antibiotic resistance is biofilm.[9] Infections induced by biofilm are difficult to treat. in-vitro biofilm formation ability is reported in 76.5% of UPECs. The cell proximity in the biofilm can help the exchange of mobile genetic elements and extend antibiotic resistance.[10] When microorganisms disperse in biofilm they will get vulnerable to antibiotic agents. Bacterial resistance is not acquired within the biofilm, but it happens through mutations or mobile genetic elements such as class I integrons and dfr-17 gene cassette. This fact suggests that genes associated with antibiotic resistance are involved in biofilm formation.[11] In recent years, the role of integrons as mobile genetic elements in the horizontal transmission of antibiotic resistance has been confirmed, since integrons lead to the broad spread of antibiotic resistance from one strain to another one, therefore, their identification has great importance to implement for infection control programs and prevent the spread of resistant strains.

Hence, this study aimed to investigate class 1 integrons and biofilm formation in MDR UPEC isolated from patients with UTI in Shohadaye Qom hospital from 2018 to 2019.

  Materials and Methods Top

This work was approved by the Ethics Committee of Kashan University of Medical Science; IR. KAUMS. NUHEPM. REC.1397.034.

In this cross-sectional study, 1217 urine samples were collected from patients referred to Shohadaye Qom Hospital, Qom University of Medical Sciences, Qom, Iran, for a year from 2018 to 2019. Among them, 380 (31.2%) were positive for UTI. In total, 166 UPEC isolates (43.7%) were recovered from 380 cultures through phenotypic methods. Then, UPEC isolates were confirmed by polymerase chain reaction (PCR) usp house-keeping gene.[12]

Antibiotic susceptibility testing was performed for 120 isolates using Kirby Bauer disk diffusion method according to CLSI 2018 guidelines.[13] The antibiotics used in this study were purchased from Mast Company (UK), which included: Ampicillin (10 μg), Cephalothin (30 μg), Trimethoprim, Sulfamethoxazole (23.75/1.25 μg), cefazolin (30 μg), Ceftriaxone (30 μg), Ceftizoxime (30 μg), Amikacin (30 μg), Ciprofloxacin (5 μg), Ceftazidime (30 μg), Cefotaxime (30 μg), Gentamicin (10 μg) Nitrofurantoin (300 μg), Norfloxacin (10 μg), and Imipenem (10 μg).

Biofilm formation was investigated according to Meshram method.[14] Briefly, isolates were inoculated in a 5 mL BHI medium containing 1% sucrose and incubated at 37°C for 24 h. After that, 1 mL 1% sucrose broth was added to a 2 mL BHI medium to reach 0.5 McFarland turbidity standard (1.5 × 108 colony-forming units [CFU]/mL). Two hundred microliters of dilution 1:1000 McFarland 1.5 × 108 CFU/ml were added to each well and the plates were incubated at 37°C for 24 h. The next day, the wells were washed in PBS three times, and then fixed with ethanol 96% for 15 min, as well stained with crystal violet 2%. Finally, glacial acetic acid 33% was added to each well and the absorbance was read in 492 nm using an ELISA reader; accordingly, the amount of biofilm was calculated.[15]

DNA was extracted through phenol-chloroform-isoamyl alcohol method.[16] At last, 1 mL elution buffer with pH = 7–8 was added to each microtube and put on a shaker for 2 h until the DNA is dissolved and prepared for PCR.

The PCR reaction was performed by the reaction mixture as described before.[17] Following primers were used to amplify virulence genes: F-int1: 5′-GACGATGCGTGGAGACC; R-int1: 3′-CTTGCTGCTTGGATGCC,[18] F-dfra: 5′-GTTA TGGAGCAGCAACGATGT, R-dfra: 3′-ACCACTACCG ATTACGCCAT (this study); F-usp: 5′-CCGATACGC TGCCAATCAGT; R-usp3′-ACGCAGACCGTAGG CCAGAT.[19] PCR Thermocycler program was as follows: 5 min at 94°C and 40 cycles including denaturation at 94°C for 30 s, annealing at 57°C for 30 s, extension at 72°C for 60 s and 72°C for 300 s for the final extension in a Thermal Cycler apparatus (Eppendorf master cycler, MA, Germany). The PCR product was electrophoresed on a 1.5% agarose gel in 1x TBE buffer at a voltage of 100 and 50 mA. The gel was then placed in a trans-illuminator and the picture was taken by the gel-documentation system.[17]

Statistical analysis

The analysis was performed using SPSS Statistics (IBMCorp. Released 2012. IBMSPSS Statistics for Windows, Version 16. Armonk, NY: IBM Corp). Chi-square or Fisher's exact tests were used to determine the significance of the differences. A difference was considered statistically significant if the P value was < 0.050.

  Results Top

The prevalence of UTI was 380 (31.2%). The prevalence of UTI in male and female was reported 231 (61%), and 148 (39%), respectively. In total, 166 isolates (43.7%) of UPEC were recovered. Of these, 120 isolates (72.3%) were MDR. One-hundred and fifteen isolates (95.8%) out of 120 MDR strains of E. coli were recovered from women and 5 isolates (4.2%) were from men. Most patients were over 19 years old. Five isolates (20.8%) were retrieved from patients aged ≥19 years and 95 isolates (79.2%) were recovered from patients aged >19 years.

The highest resistance of MDRs was observed against ampicillin and no resistance was reported to imipenem. Eighteen isolates showed resistance to 3 classes of antibiotics and 41 isolates showed resistance to four classes of antibiotics. The antibiotic susceptibility pattern is abstracted in [Figure 1].

Figure 1: Antibiotic susceptibility pattern of uropathogenic Escherichia coli multi-drug resistance isolates. IPM: Imipenem, FM: Nitrofurantoin, NOR: Norofloxacin, CT: Ceftizoxim, AN: Amikacin, GM: Gentamicin, CTX: Cefotaxime, CP: Ciprofloxacin, CAZ: Ceftazidime, CRO: Ceftriaxone, CZ: Cefazolin, SXT: Trimethoprim-Sulfamethoxazole, CF: Cefalotin, AM: Ampicillin

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Among MDRs, 71, 18, 15, and 16 isolates were negative (OD <0.1), weak (OD = 0.1–0.2), moderate (OD = 0.2–0.3), and strong biofilm (OD > 0.3) producers, respectively.

Of the 120 MDR isolates tested, 47.5% of them were positive for the int-1 gene [Figure 2] and [Figure 3], and 25.8% of the isolates contained the dfr-17 gene cassette [Figure 2] and [Figure 4], 20% of isolates had both genes, as well 46.7% of the isolates lacked both genes.

Figure 2: Frequency of uropathogenic Escherichia coli multi-drug resistance isolates based on type of genes

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Figure 3: Image of gel electrophoresis related to the int-1 gene. (M: 100 bp DNA Ladder, +: Positive control, -: Negative control, No. 1 and 3: Negative isolates for int-1 gene, No. 2: Positive isolate for int-1 gene

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Figure 4: Image of gel electrophoresis related to the dfr-17 gene. (M: 100 bp DNA Ladder, +: Positive control, -: Negative control, No. 2, 3 and 5: Negative isolates for dfr-17 gene, No. 1 and 4: Positive isolates for dfr-17 gene

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As shown in [Table 1], among 57 (47.5%) MDR isolates that were int-1 gene-positive, 15 isolates (93.8%) had strong biofilm which showed a statistically significant correlation between int-1 gene and biofilm formation (P < 0.001). Among 31 (25.8%) MDR isolates that were positive for dfr-17 gene, 8 (50%) isolates had strong biofilm which showed a statistically significant relationship between dfr-17 gene and biofilm (P < 0.001).

Table 1: Frequency distribution of uropathogenic multi-drug resistance isolates containing both 1 integron - and dfra-17 gene according to biofilm type

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  Discussion Top

As it was mentioned in our study, 72.3% of E. coli were MDR which was in line with a study conducted by Fallah et al. in Tehran,[20] and a study conducted by Mamani et al. in Hamedan, which reported 77.5% and 77%, respectively.[21] Other studies conducted by Iranpour et al.,[22] Shams et al.,[23] Mirzarazi et al.,[24] Babaei-Hemmati et al.,[25] and Kazemnia et al.,[26] reported the prevalence of 39.3%, 64.1%, 68%, 55%, and 27.7%, respectively. They all reported lower rates of MDR UPEC isolates than our study.

The results of antibiotic susceptibility testing for 14 antibiotics indicated that 93.3% of isolates showed resistance to ampicillin.[27] Also, Tandogdu et al., in 2003–2006 who studied antibiotic susceptibility for UPEC strains, the resistance rate against ampicillin was respectively; 34%, 35%, 40%, 43.3%, 48%, 53.9%, and 56.4 in Germany, France, Poland, Russia, Australia, Italy, Brazil, Spain, and Hungary, respectively.[28] Another antibiotic studied in our study was amikacin with a resistance of 25.7%. According to studies conducted in Iran and other parts of the world, including studies conducted by Hadifar et al.,[29] Taheri et al.,[30] Tabidehchi et al.,[31] Khoramrooz et al.,[32] and Mohajeri et al.,[33] the resistance rates to Amikacin were reported by 12.1%, 7.5%, 6.6%, 3%, and 0%, respectively. The comparison between our data with the findings of the mentioned studied shows that the level of resistance in the present study is higher.

Here, nitrofurantoin has the lowest resistance after imipenem with a resistance rate of 5% which was in line with other studies conducted in our country by Sahebnasagh et al.,[34] and Ranjbaran et al.[35] Furthermore, in our study, no antibiotic resistance was observed against imipenem. like that a study conducted by Tabidehchi et al. in Tehran in 2015,[31] Mohajeri et al. in Kermanshah in 2011,[33] and Ranjbaran et al. in Sanandaj in 2012[35] reported a low-level resistance against it, too. Therefore, imipenem still is a therapeutic choice in the treatment of UTI caused by UPEC strains. In our study among all UPEC MDRs 47.5% isolates were positive for int-1 gene and 25.8% isolates were positive for dfr-17 gene cassette. Overall, different studies worldwide showed that the prevalence of integrons in isolates cause nosocomial UTIs and even community-acquired infection was different in various geographical areas and different populations.[5] A study conducted by Bodour Al-Assil et al. in Syrian in 2013,[36] reported the prevalence rate of 54%, in contrary, we reported a higher rate.

Other studies conducted by Muhammad et al.,[7] and Ochoa et al.,[37] from 2007 to 2015 reported the prevalence of class 1 integrons between 20% and 50%. These findings indicate that antibiotic resistance by integrons is expanding and play an important role in the development of antibiotic resistance, especially through horizontal transmission.[6] The results showed that in isolates containing int-1 and a dfr-17 gene, the rate of biofilm formation was higher, which indicates a significant relationship between the presence of these genes and biofilm formation. This phenomenon is because, within the biofilm, the exchange and uptake of gene cassettes of integrons are enhanced, and also the inhibitory effect of the biofilm reduces the severity of drug penetration.[38]

In the current study, 15 (93.8%) out of 16 E. coli MDR isolates that had strong biofilm contained int-1 gene showing a statistically significant correlation between biofilm formation and int-1 gene presence (P < 0.001). Antibiotic resistance mechanisms such as efflux pumps, modifying enzymes, and target mutations do not appear to be responsible for protecting bacteria within the biofilm. On the other hand, most studies have shown that there is a relationship between efflux pumps and biofilm formation in E. coli. It has also been shown that E. coli mutants without genes encoding efflux pump formed less biofilm.[39] The current study showed the correlation between resistance genes and biofilm formation. When bacteria inside the biofilm disperse, they get quickly vulnerable to antibiotics because the bacterial resistance within the biofilm is probably due to mutations or mobile genetic elements such as class I integrons and the dfr-17 gene cassette and is not acquired. This suggests that genes associated with antibiotic resistance are involved in biofilm formation.[40] The biofilm formation has closely related to the antibiotic susceptibility pattern which is routinely used to treat UTI. The antibiotic resistance in biofilm-forming E. coli might cause chronic and recurrent UTI. In the present study, imipenem, amikacin, and Nitrofurantoin were effective against UPEC MDR isolates that were able to form biofilm. To achieve more accurate results, it is suggested to study other classes of integrons as well as their relationship with biofilm and their role in hospital infections.

  Conclusion Top

The result of this study indicated that the antibiotic resistance rate is increasing which is associated with the development of multidrug-resistant strains. Furthremore, we reported a significant correlation between cassettes genes, class 1 integrons, and biofilm formation with antibiotic resistance pattern. Thus, continuous screening for antibiotics resistance and the application of effective methods and proper therapeutic approaches is vital for infection control and prevention of its spread.

Acknowledgments

We are grateful to the laboratory personnel of Shohadaye Qom hospital for the invaluable help with gifting some isolates.

Financial support and sponsorship

This publication is based on the data achieved from an MSc degree thesis which was financially supported by Vice-Chancellor of Research, Kashan University of Medical Sciences, Kashan, Iran (Grant number: 97104).

Conflicts of interest

There are no conflicts of interest.

 

  References Top
1.Dielubanza EJ, Schaeffer AJ. Urinary tract infections in women. Med Clin North Am 2011;95:27-41.  Back to cited text no. 1
    2.Tong YQ, Sun M, Hu C, Zhao D. Plasmid transfer capacities of multi-resistant UPEC clinical isolates in biofilms. Biomed Res 2017;28:26-32.  Back to cited text no. 2
    3.Shakerimoghaddam A, Ghaemi EA. Effects of Zno nanoparticles on initial adhesion and fimH gene expression level of uropathogenic Eschercia coli. J Clin Basic Res 2017;1:25-8.  Back to cited text no. 3
    4.Mohsenzadeh M, Abtahi-Eivary SH, Pirouzi A, Khaledi A, Rahimi M. A systematic review and meta-analysis of urinary tract infection, frequency of IS elements and MDR isolates retrieved from adult patients. Gene Rep 2020;20:100707.  Back to cited text no. 4
    5.Kargar M, Mohammadalipour Z, Doosti A, Lorzadeh S, Japoni-Nejad A. High prevalence of class 1 to 3 integrons among multidrug-resistant diarrheagenic Escherichia coli in Southwest of Iran. Osong Public Health Res Perspect 2014;5:193-8.  Back to cited text no. 5
    6.Eslami G, Seyedjavadi SS, Goudarzi H, Fallah F, Goudarzi M. Distribution of integrons among multidrug resistant E. coli and klebsiella strains. Res Med 2010;34:61-5.  Back to cited text no. 6
    7.Muhammad I, Uzma M, Yasmin B, Mehmood Q, Habib B. Prevalence of antimicrobial resistance and integrons in Escherichia coli from Punjab, Pakistan. Braz J Microbiol 2011;42:462-6.  Back to cited text no. 7
    8.Stalder T, Barraud O, Casellas M, Dagot C, Ploy MC. Integron involvement in environmental spread of antibiotic resistance. Front Microbiol 2012;3:119.  Back to cited text no. 8
    9.Pavlickova S, Klancnik A, Dolezalova M, Mozina SS, Holko I. Antibiotic resistance, virulence factors and biofilm formation ability in Escherichia coli strains isolated from chicken meat and wildlife in the Czech Republic. J Environ Sci Health B 2017;52:570-6.  Back to cited text no. 9
    10.ElsayedGawad W. Study on the Prevalence of Multidrug-Resistant and In vitro Biofilm Formation among Uropathogenic Escherichia coli from Clinical Isolates. CU Theses; 2018.  Back to cited text no. 10
    11.Zhang XX, Zhang T, Zhang M, Fang HH, Cheng SP. Characterization and quantification of class 1 integrons and associated gene cassettes in sewage treatment plants. Appl Microbiol Biotechnol 2009;82:1169-77.  Back to cited text no. 11
    12.Mashayekhi F, Moghny M, Faramarzpoor M, Yahaghi E, Khodaverdi Darian E, Tarhriz V, et al. Molecular characterization and antimicrobial resistance of uropathogenic Escherichia coli. Iran J Biotechnol 2014;12:32-40.  Back to cited text no. 12
    13.Clinical and Laboratory Standards Institute [CLSI] CaL, Standards Institute.: Twenty Fourth Informational Supplement M100eS24 CLSI C, Wayne P. Performance Standards for Antimicrobial Susceptibility Testing. Elsevier: Clinical and Laboratory Standards Institute [CLSI] CaL; 2014.  Back to cited text no. 13
    14.Meshram L, Patidar RK, Khare M, Bagde S, Sahare KN, Singh V. Comparative analysis between biofilm formation of commensal and pathogenic Escherichia coli isolates. Asiat J Biotechnol Resour 2012;3:1441-6.  Back to cited text no. 14
    15.Yang X, Sha K, Xu G, Tian H, Wang X, Chen S, et al. Subinhibitory concentrations of allicin decrease uropathogenic Escherichia coli (UPEC) biofilm formation, adhesion ability, and swimming motility. Int J Mol Sci 2016;17:979.  Back to cited text no. 15
    16.Shakeri F, Shojai A, Golalipour M, Rahimi Alang S, Vaez H, Ghaemi EA. Spa diversity among MRSA and MSSA strains of Staphylococcus aureus in North of Iran. Int J Microbiol 2010;2010:351397.  Back to cited text no. 16
    17.Ebrahim-Saraie HS, Nezhad NZ, Heidari H, Motamedifar A, Motamedifar M. Detection of antimicrobial susceptibility and integrons among extended-spectrum β-lactamase producing uropathogenic Escherichia coli isolates in Southwestern Iran. Oman Med J 2018;33:218-23.  Back to cited text no. 17
    18.Asadollahi P, Akbari M, Soroush S, Taherikalani M, Asadollahi K, Sayehmiri K, et al. Antimicrobial resistance patterns and their encoding genes among Acinetobacter baumannii strains isolated from burned patients. Burns 2012;38:1198-203.  Back to cited text no. 18
    19.Osek J. Multiplex polymerase chain reaction assay for identification of enterotoxigenic Escherichia coli strains. J Vet Diagn Invest 2001;13:308-11.  Back to cited text no. 19
    20.Fallah F, Karimi A, Goudarzi M, Shiva F, Navidinia M, Jahromi MH, et al. Determination of integron frequency by a polymerase chain reaction-restriction fragment length polymorphism method in multidrug-resistant Escherichia coli, which causes urinary tract infections. Microb Drug Resist 2012;18:546-9.  Back to cited text no. 20
    21.Mamani M, Nobari N, Alikhani MY, Poorolajal J. Antibacterial susceptibility of Escherichia coli among outpatients with community-acquired urinary tract infection in Hamadan, Iran. J Glob Antimicrob Resist 2015;3:40-3.  Back to cited text no. 21
    22.Iranpour D, Hassanpour M, Ansari H, Tajbakhsh S, Khamisipour G, Najafi A. Phylogenetic groups of Escherichia coli strains from patients with urinary tract infection in Iran based on the new Clermont phylotyping method. Biomed Res Int 2015;2015:846219.  Back to cited text no. 22
    23.Shams F, Hasani A, Pormohammad A, Rezaee MA, Reza M, Nahaie AH, et al. qnrA implicated quinolone resistance in Escherichia coli and Klebsiella pneumoniae clinical isolates from a University Teaching Hospital. Life Sci J 2014;11:1032-5.  Back to cited text no. 23
    24.Mirzarazi M, Rezatofighi SE, Pourmahdi M, Mohajeri MR. Antibiotic resistance of isolated gram negative bacteria from urinary tract infections (UTIs) in Isfahan. Jundishapur J Microbiol 2013;6:1E.  Back to cited text no. 24
    25.Hemmati TB, Mehdipour Moghaddam MJ, Salehi Z, Habibzadeh SM. Prevalence of CTX-M-Type β-lactamases in multi-drug resistant Escherichia coli isolates from north of Iran, Rasht. Biol J Microorganism 2015;3:39-53.  Back to cited text no. 25
    26.Kazemnia A, Ahmadi M, Dilmaghani M. Antibiotic resistance pattern of different Escherichia coli phylogenetic groups isolated from human urinary tract infection and avian colibacillosis. Iran Biomed J 2014;18:219-24.  Back to cited text no. 26
    27.Al-Assil B, Mahfoud M, Hamzeh AR. Resistance trends and risk factors of extended spectrum β-lactamases in Escherichia coli infections in Aleppo, Syria. Am J Infect Control 2013;41:597-600.  Back to cited text no. 27
    28.Tandogdu Z, Wagenlehner FM. Global epidemiology of urinary tract infections. Curr Opin Infect Dis 2016;29:73-9.  Back to cited text no. 28
    29.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.  Back to cited text no. 29
    30.Taheri M, Saleh M, Nemati AH, Ariana M, Shojaei E, Mardani M, et al. Antibiotic resistance pattern and phylogenetic groups of the uropathogenic Escherichia coli isolates recovered from the urinary catheters of the hospitalized patients. J Med Microbiol Infect Dis 2016;4:76-82.  Back to cited text no. 30
    31.Tabidehchi S, Amini K, Moradli G. Detection of sul1, sul2, and int1 genes in the uropathogenic Escherichia coli strains by multiplex-PCR and their antibiotic susceptibility patterns. Sadra Med J 2016;4:195-204.  Back to cited text no. 31
    32.Khoramrooz SS, Sharifi A, Yazdanpanah M, Malek Hosseini SA, Emaneini M, Gharibpour F, et al. 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:e26399.  Back to cited text no. 32
    33.Mohajeri P, Rostami Z, Farahani A, Norozi B. Distribution of ESBL producing uropathogenic Escherichia coli and carriage of selected [beta]-lactamase genes in hospital and community isolates in west of Iran. Ann Trop Med Public Health 2014;7:219.  Back to cited text no. 33
  [Full text]  34.Sahebnasagh R, Saderi H, Safkhani E, Boroumandi S, Afshar R. Study of demographic characteristics of adult patients with positive urine culture in a general hospital in Tehran, Iran. J Basic Clin Pathophysiol 2015;3:7-12.  Back to cited text no. 34
    35.Ranjbaran M, Zolfaghari M, Japoni-Nejad A, Amouzandeh-Nobaveh A, Abtahi H, Nejad M, et al. Molecular investigation of integrons in Escherichia coli and Klebsiella pneumoniae isolated from urinary tract infections. J Mazandaran Univ Med Sci 2013;23:20-7.  Back to cited text no. 35
    36.Al-Assil B, Mahfoud M, Hamzeh AR. First report on class 1 integrons and trimethoprim-resistance genes from dfrA group in uropathogenic E. coli (UPEC) from the Aleppo area in Syria. Mob Genet Elements 2013;3:e25204.  Back to cited text no. 36
    37.Ochoa SA, Cruz-Córdova A, Luna-Pineda VM, Reyes-Grajeda JP, Cázares-Domínguez V, Escalona G, et al. Multidrug- and extensively drug-resistant uropathogenic Escherichia coli clinical strains: Phylogenetic groups widely associated with integrons maintain high genetic diversity. Front Microbiol 2016;7:2042.  Back to cited text no. 37
    38.Penesyan A, Gillings M, Paulsen IT. Antibiotic discovery: Combatting bacterial resistance in cells and in biofilm communities. Molecules 2015;20:5286-98.  Back to cited text no. 38
    39.Soto SM. Role of efflux pumps in the antibiotic resistance of bacteria embedded in a biofilm. Virulence 2013;4:223-9.  Back to cited text no. 39
    40.Wells R, Spurrier AJ, Linz D, Gallagher C, Mahajan R, Sanders P, et al. Postural tachycardia syndrome: Current perspectives. Vasc Health Risk Manag 2018;14:1-11.  Back to cited text no. 40
    
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