@2024 Afarand., IRAN
ISSN: 2252-0805 The Horizon of Medical Sciences 2018;24(4):277-285
ISSN: 2252-0805 The Horizon of Medical Sciences 2018;24(4):277-285
A Survey of Integrons and Their Relationships with Antibiotic Resistance Among the Escherichia coli Isolates Collected from Urinary Tract Infection of Patients referred to the hospitals in Tehran, Iran
ARTICLE INFO
Article Type
Original ResearchAuthors
Habibi M. (1)Asadi Karam M.R (*)
Mohammadzadeh A. (2)
(*) Department of Molecular biology, Pasteur Institute of Iran, Tehran, Iran
(1) Department of Molecular biology, Pasteur Institute of Iran, Tehran, Iran
(2) Department of Microbiology, School of Medicine, Gonabad University of Medical Sciences, Gonabad, Iran
Correspondence
Address: Department of Molecular biology, Pasteur Institute of Iran, Tehran, IranPhone: +98 (21) 66953311
Fax: +98 (21) 66370573
m_asadi12@yahoo.com
Article History
Received: July 26, 2018Accepted: September 22, 2018
ePublished: October 10, 2018
ABSTRACT
Aims
Escherichia coli strains are the most important cause of urinary tract
infection. Integrons are considered as one of the transfer mechanisms of antibiotic
resistance. The aim of the present study was detection of integrons and their
realtionships with antibiotic resistance in Escherichia coli isolates.
Materials & Methods Totally, 150 E.coli isolates was collected from urine of patients with urinary tract infection in hospitals in Tehran, Iran. Evaluation of resistance to antibiotics and identification of isolates producing ExtendedSpectrum Beta Lactamase (ESBL) were done using the disk diffusion and combined disk diffusion tests, respectively. Amplification of integron gene class I in the isolates was performed by Polymerase Chain Reaction (PCR).
Findings The resistance rate of isolates to antibiotics was amoxicillin (71.3%), trimethoprim/sulfamethoxazole (64%), cefotaxime (55.3%), ceftazidime (52.7%), ciprofloxacin (52%), norfloxacin (46.7%), gentamicin (19.3%), meropenem (3.3%), amikacin (2%) and imipenem (0%). Seventy isolates were considered as multiple drug resistance producing isolates (MDR) and 56 (37.3%) isolates showed the ability of ESBLs production. 34 (22.7%) isolates harbored the integron class I. There was a significant relationship between the ESBL producing isolates and MDR resistance and also between the presence of integron class I and MDR resistance.
Conclusion There was a significant rate of resistance to the majority of tested antibiotics with production of ESBL that could be related to the presence of integrons class I. Thus, it suggests more studies need to be conducted to provide better conditions for prevention of antibiotic resistance.
Materials & Methods Totally, 150 E.coli isolates was collected from urine of patients with urinary tract infection in hospitals in Tehran, Iran. Evaluation of resistance to antibiotics and identification of isolates producing ExtendedSpectrum Beta Lactamase (ESBL) were done using the disk diffusion and combined disk diffusion tests, respectively. Amplification of integron gene class I in the isolates was performed by Polymerase Chain Reaction (PCR).
Findings The resistance rate of isolates to antibiotics was amoxicillin (71.3%), trimethoprim/sulfamethoxazole (64%), cefotaxime (55.3%), ceftazidime (52.7%), ciprofloxacin (52%), norfloxacin (46.7%), gentamicin (19.3%), meropenem (3.3%), amikacin (2%) and imipenem (0%). Seventy isolates were considered as multiple drug resistance producing isolates (MDR) and 56 (37.3%) isolates showed the ability of ESBLs production. 34 (22.7%) isolates harbored the integron class I. There was a significant relationship between the ESBL producing isolates and MDR resistance and also between the presence of integron class I and MDR resistance.
Conclusion There was a significant rate of resistance to the majority of tested antibiotics with production of ESBL that could be related to the presence of integrons class I. Thus, it suggests more studies need to be conducted to provide better conditions for prevention of antibiotic resistance.
CITATION LINKS
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[21]Terlizzi ME, Gribaudo G, Maffei ME. UroPathogenic Escherichia coli (UPEC) infections: Virulence factors, bladder responses, antibiotic, and non-antibiotic antimicrobial strategies. Front Microbiol. 2017;8:1566.
[22]Enne VI, Livermore DM, Stephens P, Hall LM. Persistence of sulphonamide resistance in Escherichia coli in the UK despite national prescribing restriction. Lancet. 2001;357(9265):1325-8.
[23]Mehdipour Moghaddam MJ, Mirbagheri AA, Salehi Z, Habibzade SM. Prevalence of class 1 integrons and extended spectrum beta lactamases among multi-drug resistant Escherichia coli isolates from North of Iran. Iran Biomed J. 2015;19(4):233-9.
[24]Asadi S, Kargar M, Solhjoo K, Najafi A, Ghorbani Dalini S. The association of virulence determinants of uropathogenic Escherichia coli with antibiotic resistance. Jundishapur J Microbiol. 2014;7(5):e9936.
[25]Shayan S, Bokaeian M, Shahraki S. Prevalence and molecular characterization of AmpC-producing clinical isolates of Escherichia coli from Southeastern Iran. Microb Drug Resist. 2014;20(2):104-7.
[26]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(3):193-8.
[27]Gholipour A, Soleimani N, Shokri D, Mobasherizadeh S, Kardi M, Baradaran A. Phenotypic and molecular characterization of extended-spectrum β-lactamase produced by Escherichia coli, and Klebsiella pneumoniae isolates in an educational hospital. Jundishapur J Microbiol. 2014;7(10):e11758.
[28]Dash SK, Chakraborty SP, Mandal D, Roy S. Isolation and characterization of multi drug resistant uropathogenic Escherichia coli from urine sample of Urinary tract infected patients. Int J Life Sci Pharm Res. 2012;2(1):L25-39.
[29]Sanchez GV, Baird AM, Karlowsky JA, Master RN, Bordon JM. Nitrofurantoin retains antimicrobial activity against multidrug-resistant urinary Escherichia coli from US outpatients. J Antimicrob Chemother. 2014;69(12):3259-62.
[30]Bali EB, Açık L, Sultan N. Phenotypic and molecular characterization of SHV, TEM, CTX-M and extended-spectrum β-lactamase produced by Escherichia coli, Acinobacter baumannii and Klebsiella isolates in a Turkish hospital. Afr J Microbiol Res. 2010;4(8):650-4.
[31]Sorlózano A, Gutiérrez J, Fernández F, Soto MJ, Piédrola G. A preliminary study on the presence of Extended-Spectrum Beta-Lactamases (ESBL) in clinical isolates of Escherichia coli in Granada (Spain). Ann Microbiol. 2004;54(2):99-104.
[32]Franiczek R, Dolna I, Krzyżanowska B, Szufnarowski K, Kowalska-Krochmal B. Conjugative transfer of multiresistance plasmids from ESBL-positive Escherichia coli and Klebsiella spp. clinical isolates to Escherichia coli strain K12 C600. Adv Clin Exp Med. 2007;16(2):239-47.
[33]Khoramrooz SS, Sharifi A, Yazdanpanah M, Malek Hosseini SAA, 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(1):e26399.
[34]Salem MM, Muharram M, Alhosiny IM. Distribution of classes 1 and 2 integrons among multi drug resistant E. coli isolated from hospitalized patients with urinary tract infection in Cairo, Egypt. Aust J Basic Appl Sci. 2010;4(3):398-407.
[35]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(3):e25204.
[36]Machado E, Cantón R, Baquero F, Galán JC, Rollán A, Peixe L, et al. Integron content of extended-spectrum-beta-lactamase-producing Escherichia coli strains over 12 years in a single hospital in Madrid, Spain. Antimicrob Agents Chemother. 2005;49(5):1823-9.
[37]Bonnet R. Growing group of extended-spectrum beta-lactamases: The CTX-M enzymes. Antimicrob Agents Chemother. 2004;48(1):1-14.
[38]Jacoby GA, Sutton L. Properties of plasmids responsible for production of extended-spectrum beta-lactamases. Antimicrob Agents Chemother. 1991;35(1):164-9.
[2]Gupta K, Hooton TM, Naber KG, Wullt B, Colgan R, Miller LG, et al. International clinical practice guidelines for the treatment of acute uncomplicated cystitis and pyelonephritis in women: A 2010 update by the Infectious Diseases Society of America and the European Society for Microbiology and Infectious Diseases. Clin Infect Dis. 2011;52(5):e103-20.
[3]Nicolle LE. Uncomplicated urinary tract infection in adults including uncomplicated pyelonephritis. Urol Clin North Am. 2008;35(1):1-12.
[4]Salvatore S, Salvatore S, Cattoni E, Siesto G, Serati M, Sorice P, et al. Urinary tract infections in women. Eur J Obstet Gynecol Reprod Biol. 2011;156(2):131-6.
[5]Dhakal BK, Kulesus RR, Mulvey MA. Mechanisms and consequences of bladder cell invasion by uropathogenic Escherichia coli. Eur J Clin Invest. 2008;38 Suppl 2:2-11.
[6]Vachhani AV, Barvaliya M, Naik V, Jha P, Tripathi C. Effectiveness and tolerability of short course co-trimoxazole, norfloxacin and levofloxacin in bacteriological cure of uncomplicated urinary tract infection in outpatient setting, an open label, parallel group, randomized controlled trial. Infez Med. 2015;23(2):155-60.
[7]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.
[8]Walker E, Lyman A, Gupta K, Mahoney MV, Snyder GM, Hirsch EB. Clinical management of an increasing threat: Outpatient urinary tract infections due to multidrug-resistant uropathogens. Clin Infect Dis. 2016;63(7):960-5.
[9]Sanchez GV, Babiker A, Master RN, Luu T, Mathur A, Bordon J. Antibiotic resistance among urinary isolates from female outpatients in the United States in 2003 and 2012. Antimicrob Agents Chemother. 2016;60(5):2680-3.
[10]Alizade H. Escherichia coli in Iran: An overview of antibiotic resistance, a review article. Iran J Public Health. 2018;47(1):1-12.
[11]Tong YQ, Sun M, Hu C, Zhao D. Plasmid transfer capacities of multi-resistant UPEC clinical isolates in biofilms. Biomed Res. 2017;28(5):2364-9.
[12]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(4):478-85.
[13]Kaushik M, Kumar S, Kapoor RK, Virdi JS, Gulati P. Integrons in Enterobacteriaceae: Diversity, distribution and epidemiology. Int J Antimicrob Agents. 2018;51(2):167-76.
[14]Fluit AC, Schmitz FJ. Resistance integrons and super-integrons. Clin Microbiol Infect. 2004;10(4):272-88.
[15]Mazel D. Integrons: Agents of bacterial evolution. Nat Rev Microbiol. 2006;4(8):608-20.
[16]Rowe-Magnus DA, Mazel D. Integrons: Natural tools for bacterial genome evolution. Curr Opin Microbiol. 2001;4(5):565-9.
[17]Lina TT, Khajanchi BK, Azmi IJ, Islam MA, Mahmood B, Akter M, et al. Phenotypic and molecular characterization of extended-spectrum beta-lactamase-producing Escherichia coli in Bangladesh. PLoS One. 2014;9(10):e108735.
[18]Barguigua A, El Otmani F, Talmi M, Bourjilat F, Haouzane F, Zerouali K, et al. Characterization of extended-spectrum β-lactamase-producing Escherichia coli and Klebsiella pneumoniae isolates from the community in Morocco. J Med Microbiol. 2011;60(Pt 9):1344-52.
[19]Patel JB, Cockerill III FR, Bradford PA, Eliopoulos GM, Hindler JA, Jenkins SG, et al. M100-S25: Performance standards for antimicrobial susceptibility testing, twenty-fifth informational supplement [Internet]. Wayne PA: Clinical and Laboratory Standards Institute; 2015 [cited 2017 Sep 20]. Available from: http://file.qums.ac.ir/repository/mmrc/CLSI2015.pdf
[20]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(1):19-25.
[21]Terlizzi ME, Gribaudo G, Maffei ME. UroPathogenic Escherichia coli (UPEC) infections: Virulence factors, bladder responses, antibiotic, and non-antibiotic antimicrobial strategies. Front Microbiol. 2017;8:1566.
[22]Enne VI, Livermore DM, Stephens P, Hall LM. Persistence of sulphonamide resistance in Escherichia coli in the UK despite national prescribing restriction. Lancet. 2001;357(9265):1325-8.
[23]Mehdipour Moghaddam MJ, Mirbagheri AA, Salehi Z, Habibzade SM. Prevalence of class 1 integrons and extended spectrum beta lactamases among multi-drug resistant Escherichia coli isolates from North of Iran. Iran Biomed J. 2015;19(4):233-9.
[24]Asadi S, Kargar M, Solhjoo K, Najafi A, Ghorbani Dalini S. The association of virulence determinants of uropathogenic Escherichia coli with antibiotic resistance. Jundishapur J Microbiol. 2014;7(5):e9936.
[25]Shayan S, Bokaeian M, Shahraki S. Prevalence and molecular characterization of AmpC-producing clinical isolates of Escherichia coli from Southeastern Iran. Microb Drug Resist. 2014;20(2):104-7.
[26]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(3):193-8.
[27]Gholipour A, Soleimani N, Shokri D, Mobasherizadeh S, Kardi M, Baradaran A. Phenotypic and molecular characterization of extended-spectrum β-lactamase produced by Escherichia coli, and Klebsiella pneumoniae isolates in an educational hospital. Jundishapur J Microbiol. 2014;7(10):e11758.
[28]Dash SK, Chakraborty SP, Mandal D, Roy S. Isolation and characterization of multi drug resistant uropathogenic Escherichia coli from urine sample of Urinary tract infected patients. Int J Life Sci Pharm Res. 2012;2(1):L25-39.
[29]Sanchez GV, Baird AM, Karlowsky JA, Master RN, Bordon JM. Nitrofurantoin retains antimicrobial activity against multidrug-resistant urinary Escherichia coli from US outpatients. J Antimicrob Chemother. 2014;69(12):3259-62.
[30]Bali EB, Açık L, Sultan N. Phenotypic and molecular characterization of SHV, TEM, CTX-M and extended-spectrum β-lactamase produced by Escherichia coli, Acinobacter baumannii and Klebsiella isolates in a Turkish hospital. Afr J Microbiol Res. 2010;4(8):650-4.
[31]Sorlózano A, Gutiérrez J, Fernández F, Soto MJ, Piédrola G. A preliminary study on the presence of Extended-Spectrum Beta-Lactamases (ESBL) in clinical isolates of Escherichia coli in Granada (Spain). Ann Microbiol. 2004;54(2):99-104.
[32]Franiczek R, Dolna I, Krzyżanowska B, Szufnarowski K, Kowalska-Krochmal B. Conjugative transfer of multiresistance plasmids from ESBL-positive Escherichia coli and Klebsiella spp. clinical isolates to Escherichia coli strain K12 C600. Adv Clin Exp Med. 2007;16(2):239-47.
[33]Khoramrooz SS, Sharifi A, Yazdanpanah M, Malek Hosseini SAA, 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(1):e26399.
[34]Salem MM, Muharram M, Alhosiny IM. Distribution of classes 1 and 2 integrons among multi drug resistant E. coli isolated from hospitalized patients with urinary tract infection in Cairo, Egypt. Aust J Basic Appl Sci. 2010;4(3):398-407.
[35]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(3):e25204.
[36]Machado E, Cantón R, Baquero F, Galán JC, Rollán A, Peixe L, et al. Integron content of extended-spectrum-beta-lactamase-producing Escherichia coli strains over 12 years in a single hospital in Madrid, Spain. Antimicrob Agents Chemother. 2005;49(5):1823-9.
[37]Bonnet R. Growing group of extended-spectrum beta-lactamases: The CTX-M enzymes. Antimicrob Agents Chemother. 2004;48(1):1-14.
[38]Jacoby GA, Sutton L. Properties of plasmids responsible for production of extended-spectrum beta-lactamases. Antimicrob Agents Chemother. 1991;35(1):164-9.