Original Article

Gene cassettes of class I integron-associated with antimicrobial resistance in isolates of Citrobacter spp. with multidrug resistance

Abstract

Background and Objectives: Integrons play a major role in the transmission and accumulation of resistance factors in multidrug resistant bacteria. This study was aimed to evaluate the gene cassettes of class I integron and antimicrobial resistance in isolates of Citrobacter with multidrug resistance (MDR).
Materials and Methods: Ninety isolates of Citrobacter spp. were collected from the largest hospital in Kermanshah, Iran. Antimicrobial resistance patterns were determined using disc diffusion method. The class I integron were detected by PCR. The integrase positive isolates were further analyzed for the presence of gene cassettes using 5' and 3' conserved sequences (CSs) primers and PCR products were sequenced. The data were analyzed using the chi-square test.
Results: Of 90 Citrobacter isolates, 46 (51.1%) were multidrug resistant. Class I integron and gene cassettes were determined in 30 isolates (65.2%). Gene cassettes were found which contained genes encoded resistance to aminoglycosides and trimethoprim and a putative gene. Gene cassettes of dfrA12-orfF-aadA2, dfrA1-aadA1, aadA1 and dfrA15-aadA2 were also found in Citrobacter isolates.
Conclusion: Our results indicate there is a high frequency of class I integron among multi-drug resistant strains of Citrobacter isolated from clinical settings. A high frequency of class I integron associated gene cassettes, in particular dfr and aadA, present in MDR strains of Citrobacter. This data indicates an important role of integrons in the creation and transmission of MDR strains in health care centers.

Nayar R, Shukla I, Sultan A. Epidemiology, prevalence and identification of Citrobacter species in clinical specimens in a tertiary care hospital in India. IJSRP 2014;4(4):1-6.

Akya A, Jafari S, Ahmadi K, Elahi A. Frequency of blaCTX-M, blaTEM and blaSHV genes in Citrobacters isolated from Imam Reza Hospital in Kermanshah. J Mazandaran Univ Med Sci 2015; 25(127): 65-73.

White PA, McIver CJ, Rawlinson WD. Integrons and gene cassettes in the Enterobacteriaceae. Antimicrob Agents Chemother 2001;45:2658-2661.

Azam H, Mikaili Ghezeljeha S, Shavandi M. Prevalence of class 1 and 2 integrons among the multidrug resistant uropathogenic strains of Escherichia coli. Asian Biomed 2015; 9:49-54.

Malek MM, Amer FA, Allam AA, El-Sokkary RH, Gheith T, Arafa MA. Occurrence of classes I and II integrons in Enterobacteriaceae collected from Zagazig University Hospitals, Egypt. Front Microbiol 2015;6:601.

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(1):e26399.

Guangchao Y, Yanmei L, Xiaochen L, Xihong Z, Yanyan L. Role of integrons in antimicrobial resistance: a review. Afr J Microbiol Res 2013;7(15):1301-1310.

El-Sokkary MMA, Abdelmegeed ES. Characterisation of class 1 integron among Escherichia coli isolated from Mansoura University Hospitals in Egypt. AiM 2015;5:269-277.

Guo X, Xia R, Han N, Xu H. Genetic diversity analyses of class 1 integrons and their associated antimicrobial resistance genes in Enterobacteriaceae strains recovered from aquatic habitats in China. Lett Appl Microbiol 2011;52:667-675.

Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing: twenty-second informational supplement M100-S22. Wayne, PA, USA: CLSI; 2012.

Mirnejad R, Mostofi S, Masjedian F. Antibiotic resistance and carriage class 1 and 2 integrons in clinical isolates of Acinetobacter baumannii from Tehran, Iran. Asian Pac J Trop Biomed 2013;3(2):140-145.

Basavaraj CM, Jyothi P. Antibiotic sensivity pattern of Citrobacter spp. Isolated from patients wirh urinary tract infections in tertiary care hospital in south india. Int J Pharm Pharm Sci 2015;7(1): 252-254.

Metri BC, Jyothi P, Peerapur BV. Antibiotic resistance in Citrobacter spp. isolated from urinary tract infection. Urol Ann 2013;5(4):312-313.

Leski TA, Taitt CR, Bangura U, Stockelman MG, Ansumana R, Cooper WH, et al. High prevalence of multidrug resistant Enterobacteriaceae isolated from outpatient urine samples but not the hospital environment in Bo, Sierra Leone. BMC Infect Dis 2016;16:167.

Mansouri S, Abbasi S. Prevalence of multiple drug resistant clinical isolates of extended-spectrum β-Lactamase producing Enterobacteriaceae in southeast Iran. IJMS 2010; 35:101-107.

Hareendranath G, Dominic RMS, Saralaya V. Clinical microbiological study of Citrobacter isolates from various clinical specimens and detection of β-lactamase production. J Int Med Dent 2015;2:36-46.

Shrestha A, Manandhar S, Pokharel P, Panthi P, Chaudhary DK. Prevalence of extended spectrum beta-Lactamase (ESBL) producing multidrug resistance gram-negative isolates causing urinary tract infection. EC Microbiol 2016;4:749-755.

Ahangarzadeh Rezaee M, Sheikhalizadeh V, Hasani A. Detection of integrons among multi-drug resistant (MDR) Escherichia coli strains isolated from clinical specimens in northern west of Iran. Braz J Microbiol 2011; 42:1308-1313.

Yu HS, Lee JC, Kang HY, Ro DW, Chung JY, Jeong YS, et al. Changes in gene cassettes of class 1 integrons among Escherichia coli isolates from urine specimens collected in Korea during the last two decades. J Clin Microbiol 2003;41:5429-5433.

Ibrahim N, Wajidi MF, Yusof MY, Tay ST. The integron prevalence of extended-spectrum beta-lactamase producing enterobacterial isolates in a Malaysian teaching hospital. Trop Biomed 2011;28:668-671.

Reyes A, Bello H, Dominguez M, Mella S, Zemelman R, Gonzalez G. Prevalence and types of class 1 integrons in aminoglycoside-resistant Enterobacteriaceae from several Chilean hospitals. J Antimicrob Chemother 2003;51:317-321.

Huan W, Fan XL. Relationship between class 1 integron and resistance in gram negative bacteria. J Dalian Med Univ 2007;29:584-586.

Martínez-Martínez L, Pascual A, Jacoby GA. Quinolone resistance from a transferable plasmid. Lancet 1998; 351:797-799.

Sallen B, Rajoharison A, Desvarenne S, Mabilat C. Molecular epidemiology of integron-associated antibiotic resistance genes in clinical isolates of Enterobacteriaceae. Microb Drug Resist 1995; 1:195-202.

Mahluji Z, Firoozeh F, Khorshidi A, Zibaei M. The frequency of class 1 integrons in multidrug resistant Klebsiella pneumoniae isolated from clinical samples using polymerase chain reaction assay. SJKU 2016;21:68-78.

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;19:233-239.

Lima AM, de Melo ME, Alves LC, Brayner FA, Lopes AC. Investigation of class 1 integrons in Klebsiella pneumoniae clinical and microbiota isolates belonging to different phylogenetic groups in Recife, State of Pernambuco. Rev Soc Bras Med Trop 2014;47:165-169.

Chang CY, Fang YT, Tsai SM, Chang LL, Yu WL. Characterization of class 1 integrons and gene cassettes in clinical isolates of Klebsiella pneumoniae from Taiwan. Diagn Microbiol Infect Dis 2009;65:214-216.

Shahcheraghi F, Rahmati Ghezelgeh F, Nobari S, Torabi E, Mousavi SF, Aslani MM, et al. Identification and characterization of class 1 integrons among atypical enteropathogenic Escherichia coli isolated from children under 5 years of age. Iran J Microbiol 2014;6:156-162.

Yan H, li L, Zong M, Alam MJ, Shinoda S, Shi L. Occurrence and characteristics of class 1 and 2 integrons in clinical bacterial isolates from patients in south china. J Health Sci 2010;56:442-450.

Chang LL, Chang TM, Chang CY. Variable gene cassette patterns of class 1 integron-associated drug-resistant Escherichia coli in Taiwan. Kaohsiung J Med Sci 2007;23:273-280.

Sung JY, Oh JE. Distribution and characterization of integrons in Enterobacteriaceae isolates from chickens in Korea. J Microbiol Biotechnol 2014;24:1008-1013.

Sunde M. Prevalence and characterization of class 1 and class 2 integrons in Escherichia coli isolated from meat and meat products of Norwegian origin. J Antimicrobial Chemother 2005;56:1019-1024.

Van Essen-Zandbergen A, Smith H, Veldman K, Mevius D. Occurrence and characteristics of class 1, 2 and 3 integrons in Escherichia coli, Salmonella and Campylobacter spp. in the Netherlands. J Antimicrob Chemother 2007;59:746-750.

Cocchi S, Grasselli E, Gutacker M, Benagli C, Convert M, Piffaretti JC. Distribution and characterization of integrons in Escherichia coli strains of animal and human origin. FEMS Immunol Med Microbiol 2007;50:126-132.

Moura A, Henriques I, Ribeiro R, Correia A. Prevalence and characterization of integrons from bacteria isolated from a slaughterhouse wastewater treatment plant. J Antimicrobial Chemother 2007;60:1243-1250.

Wang GQ, Wu CM, Du XD, Shen ZQ, Song LH, Chen X, et al. Characterization of integrons-mediated antimicrobial resistance among Escherichia coli strains isolated from bovine mastitis. Vet Microbiol 2008;127(1-2):73-78.

Waturangi DE, Suwanto A, Schwarz S, Erdelen W. Identification of class 1 integrons-associated gene cassettes in Escherichia coli isolated from Varanus spp. in Indonesia. J Antimicrob Chemother 2003;51:175-177.

Salimizand H, Shahcheraghi F, Kalantar E, Badmasti F, Mousavi SF. Molecular characterization of class 1 integrons and gene cassettes in multidrug resistant (MDR) Klebsiella spp. isolated from hospitalized and outpatients in Iran, 2009. Iran J Microbiol 2013;5:48-55.

Masoumian N, Haghi F. Analysis of integrons and associated gene cassettes in clinical isolates of Escherichia coli. J Zanjan Univ Med Sci 2015;23:74-82.

Files
IssueVol 10 No 1 (2018) QRcode
SectionOriginal Article(s)
Keywords
Citrobacter Gene cassettes Integrons Multidrug-resistant

Rights and permissions
Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
How to Cite
1.
Chegene Lorestani R, Akya A, Elahi A, Hamzavi Y. Gene cassettes of class I integron-associated with antimicrobial resistance in isolates of Citrobacter spp. with multidrug resistance. Iran J Microbiol. 2018;10(1):22-29.