Abstract
Owing to the scarce evidence about the multidrug-resistant (MDR) beta-lactamase-producing Shigella isolates in Iran, this study aimed to evaluate the occurrence of extended-spectrum beta-lactamases (ESBL) and AmpC β-lactamases in Shigella species collected in the southwest of Iran. This study was conducted on Shigella species isolated from stool samples of pediatric patients aged less than 15 years suffering from diarrhea. These isolates were identified by bacteriology tests, serotyping, and polymerase chain reaction (PCR). The antibiotic resistance was determined by disc diffusion. The production of ESBLs and AmpC was investigated by phenotypic confirmatory tests and PCR. In total, 79 Shigella isolates, including 46.8% (n = 37) of S. flexneri and 53.2% (n = 42) of S. sonnei, were isolated, respectively. The most effective antibiotic was imipenem with 93.7% of susceptibility followed by ampicillin (29.1%), and cotrimoxazole (30.4%).The resistance rates of ceftriaxone, ceftazidime, and cefotaxime were 41.8%, 34.2%, and 41.8%, respectively. Also, a total of 57 (72.2%) isolates showed MDR profiles. The phenotypic tests showed that 43.0% (34/79) of isolates can produce ESBLs, and no one was positive for ApmC. The frequency of blaTEM and blaCTX-M were 30.4% and 32.9%, respectively, while the blaPER, blaSHV, and AmpC genes were not detected. The ESBL-producing isolates had a significant (p-value ˂ 0.05) resistance rate against ceftriaxone, ceftazidime, cefotaxime, cefepime, erythromycin, and amikacin. The significant prevalence of MDR Shigella isolates harboring ESBL genes highlights the need for effective surveillance measures to prevent the more spread of drug resistance among species.
Similar content being viewed by others
Data availability
All data are presented in the manuscript.
References
Moosavian M, Seyed-Mohammadi S, Sheikh AF, Khoshnood S, Dezfuli AA, Saki M et al (2019) Prevalence of enterotoxin-encoding genes among diverse Shigella strains isolated from patients with diarrhea, southwest Iran. Acta Microbiol Immunol Hung 66(1):91–101
Sheikh AF, Moosavian M, Abdi M, Heidary M, Shahi F, Jomehzadeh N et al (2019) Prevalence and antimicrobial resistance of Shigella species isolated from diarrheal patients in Ahvaz, southwest Iran. Infect Drug Resist 12:1535–1544
Kahbazi M, Ebrahimi M, Zarinfar N, Arjomandzadegan M, Fereydouni T, Karimi F et al (2016) Efficacy of synbiotics for treatment of bacillary dysentery in children: A double-blind, randomized, placebo-controlled study. Adv Med 2016:3194010
Khalil IA, Troeger C, Blacker BF, Rao PC, Brown A, Atherly DE et al (2018) Morbidity and mortality due to Shigella and enterotoxigenic Escherichia coli diarrhoea: the global burden of disease study 1990–2016. Lancet Infect Dis 18(11):1229–1240
Li R, Lai Y, Feng C, Dev R, Wang Y, Hao Y (2020) Diarrhea in under five year-old children in Nepal: A spatiotemporal analysis based on demographic and health survey data. Int J Environ Res Public Health 17(6):2140
Yang C, Li P, Zhang X, Ma Q, Cui X, Li H et al (2016) Molecular characterization and analysis of high-level multidrug-resistance of Shigella flexneri serotype 4s strains from China. Sci Rep 6:29124
Abbasi E, Abtahi H, van Belkum A, Ghaznavi-Rad E (2019) Multidrug-resistant Shigella infection in pediatric patients with diarrhea from central Iran. Infect Drug Resist 12:1535–1544
Rodríguez-Baño J, Gutiérrez-Gutiérrez B, Machuca I, Pascual A (2018) Treatment of infections caused by extended-spectrum-beta-lactamase-, AmpC-, and carbapenemase-producing Enterobacteriaceae. Clin Microbiol Rev 31(2):e00079–e117
Ur Rahman S, Ali T, Ali I, Khan NA, Han B, Gao J (2018) The growing genetic and functional diversity of extended-spectrum beta-lactamases. BioMed Res Int 2018:9519718
Yazdansetad S, Alkhudhairy MK, Najafpour R, Farajtabrizi E, Al-Mosawi RM, Saki M et al (2019) Preliminary survey of extended-spectrum β-lactamases (ESBLs) in nosocomial uropathogen Klebsiella pneumoniae in north-central Iran. Heliyon 5(9):e02349
Ejikeugwu C, Saki M, Nwakaeze E, Eze P, Chinedu O, Carissa D et al (2019) Characterization of metallo-β-lactamases-encoding genes blaIMP-1 and blaVIM-1 amongst Klebsiella pneumoniae from abattoir samples of Ebonyi state, southeastern Nigeria. Gene Rep 16:100428
Liu Y, Cheng Y, Yang H, Hu L, Cheng J, Ye Y et al (2017) Characterization of extended-spectrum β-lactamase genes of Shigella flexneri isolates with fosfomycin resistance from patients in China. Ann Lab Med 37(5):415–419
Mook P, McCormick J, Bains M, Cowley LA, Chattaway MA, Jenkins C et al (2015) (2015) ESBL-producing and macrolide-resistant Shigella sonnei infections among men who have sex with men, England. Emerg Infect Dis 22(11):1948–1952
Yilmaz NO, Agus N, Bozcal E, Oner O, Uzel AT (2013) Detection of plasmid-mediated AmpC β-lactamase in Escherichia coli and Klebsiella pneumoniae. Indian J Med Microbiol 31(1):53–59
Ejikeugwu C, Hasson SO, Al-Mosawi RM, Alkhudhairy MK, Saki M, Ezeador C et al (2020) Occurrence of FOX AmpC gene among Pseudomonas aeruginosa isolates in abattoir samples from south-eastern Nigeria. Rev Med Microbiol 31(2):99–103
Puzari M, Sharma M, Chetia P (2018) Emergence of antibiotic resistant Shigella species: a matter of concern. J Infect Public Heal 11(4):451–454
Abbasi-Montazeri E, Seyed-Mohammadi S, Asarehzadegan-Dezfuli A, Khosravi AD, Dastoorpoor M, Roointan M, Saki M (2020) Investigation of SCCmec types I-IV in clinical isolates of methicillin-resistant coagulase-negative Staphylococci in Ahvaz, southwest Iran. Biosci Rep 40(5):BSR20200847
Abbasi Montazeri E, Khosravi AD, Saki M, Sirous M, Keikhaei B, Seyed-Mohammadi S (2020) Prevalence of extended-spectrum beta-lactamase-producing Enterobacteriaceae causing bloodstream infections in cancer patients from southwest of Iran. Infect Drug Resist 2020:1319–1326
Wayne PE (2019) Performance standards for antimicrobial susceptibility testing. Twenty-ninth informational supplement. CLSI document M100-S29. Clinical and Laboratory Standards Institute, Wayne
Amin M, Sirous M, Javaherizadeh H, Motamedifar M, Saki M, Veisi H et al (2018) Antibiotic resistance pattern and molecular characterization of extended-spectrum β-lactamase producing enteroaggregative Escherichia coli isolates in children from southwest Iran. Infect Drug Resist 11:1097–1104
Ibrahim ME, Abbas M, Al-Shahrai AM, Elamin BK (2019) Phenotypic characterization and antibiotic resistance patterns of extended-spectrum β-lactamase-and AmpC β-lactamase-producing Gram-negative bacteria in a referral hospital, Saudi Arabia. Can J Infect Dis Med Microbiol 2019:6054694
Lan NP, Hien NH, Phuong TL, Thanh DP, Thieu NT, Ngoc DT et al (2017) Phenotypic and genotypic characteristics of ESBL and AmpC producing organisms associated with bacteraemia in Ho Chi Minh City. Vietnam Antimicrob Resist Infect Control 6(1):105
Delfino Vubil SA, Quintò L, Ballesté-Delpierre C, Nhampossa T, Kotloff K, Levine MM et al (2018) Clinical features, risk factors, and impact of antibiotic treatment of diarrhea caused by Shigella in children less than 5 years in Manhiça District, rural Mozambique. Infect Drug Resist 11:2095–2106
Soltan Dallal MM, Ranjbar R, Yaghoubi S, Rajabi Z, Aminharati F, Adeli Behrooz H (2018) Molecular epidemiology and genetic characterization of Shigella in pediatric patients in Iran. Infez Med 26(4):321–328
Mamishi S, Arab Yazdi Z, Mahmoudi S, Moradzadeh M, Taghi Haghi Ashtiani M, Pourakbari B (2019) Antimicrobial-resistance pattern of Shigella species in children: a six-year study in an Iranian referral Hospital. Ann Ig 31(4):356–364
Nikfar R, Shamsizadeh A, Darbor M, Khaghani S, Moghaddam M (2017) A study of prevalence of Shigella species and antimicrobial resistance patterns in paediatric medical center, Ahvaz. Iran Iran J Microbiol 9(5):277–283
Tosisa W, Mihret A, Ararsa A, Eguale T, Abebe T (2020) Prevalence and antimicrobial susceptibility of Salmonella and Shigella species isolated from diarrheic children in Ambo town. BMC Pediatr 20(1):91
Lluque A, Mosquito S, Gomes C, Riveros M, Durand D, Tilley DH et al (2015) Virulence factors and mechanisms of antimicrobial resistance in Shigella strains from periurban areas of Lima (Peru). Int J Med Microbiol 305:480–490
Terfassa A (2018) Jida M (2018) Prevalence and antibiotics susceptibility pattern of Salmonella and Shigella species among diarrheal patients attending Nekemte Referral Hospital, Oromia, Ethiopia. Int J Microbiol 2018:9214689
Beyene G, Tasew H (2014) Prevalence of intestinal parasite, Shigella and Salmonella species among diarrheal children in Jimma health center, Jimma southwest Ethiopia: a cross sectional study. Ann Clin Microbiol Antimicrob 13:10
Sati HF, Bruinsma N, Galas M, Hsieh J, Sanhueza A, Ramon Pardo P et al (2019) Characterizing Shigella species distribution and antimicrobial susceptibility to ciprofloxacin and nalidixic acid in Latin America between 2000–2015. PLoS ONE 14(8):e0220445
Chung The H, Rabaa MA, Pham Thanh D, De Lappe N, Cormican M, Valcanis M et al (2016) South Asia as a reservoir for the global spread of ciprofloxacin-resistant Shigella sonnei: a cross-sectional study. PLoS Med 13(8):e1002055
Zamanlou S, Ahangarzadeh Rezaee M, Aghazadeh M, Ghotaslou R, Babaie F, Khalili Y (2018) Characterization of integrons, extended-spectrum β-lactamases, AmpC cephalosporinase, quinolone resistance, and molecular typing of Shigella spp. from Iran. Infect Dis 50(8):616–624
Bian F, Yao M, Fu H, Yuan G, Wu S, Sun Y (2019) Resistance characteristics of CTX-M type Shigella flexneri in China. Biosci Rep 39(9):BSR20191741
Liu G, Qian H, Tang B, Chen Y, Kang H, Jiang F et al (2018) Prevalence and characterization of third-generation cephalosporin-resistant Shigella flexneri isolates from Jiangsu Province, China, 2013–2015. J Glob Antimicrob Resist 15:283–287
Gu B, Zhou M, Ke X, Pan S, Cao Y, Huang Y et al (2015) Comparison of resistance to third-generation cephalosporins in Shigella between Europe-America and Asia-Africa from 1998 to 2012. Epidemiol Infect 143(13):2687–2699
Bialvaei AZ, Kafil HS, Asgharzadeh M, Aghazadeh M, Yousefi M (2016) CTX-M extended-spectrum β-lactamase-producing Klebsiella spp, Salmonella spp., Shigella spp. and Escherichia coli isolates in Iranian hospitals. Braz J Microbiol 47(3):706–711
Dhital S, Sherchand JB, Pokharel BM, Parajuli K, Mishra SK, Sharma S et al (2017) Antimicrobial susceptibility pattern of Shigella spp. isolated from children under 5 years of age attending tertiary care hospitals, Nepal along with first finding of ESBL-production. BMC Res Notes 10(1):1–5
Tajbakhsh M, García Migura L, Rahbar M, Svendsen CA, Mohammadzadeh M, Zali MR et al (2012) Antimicrobial-resistant Shigella infections from Iran: an overlooked problem? J Antimicrob Chemother 67:1128–1133
Acknowledgements
This research was a part of the MSc. thesis of Maryam Moradi Bandbal, which was approved in the Infectious and Tropical Diseases Research Center, and was financially supported by a grant from Research Affairs, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran. We would like to thank all staff of the Microbiology Ward of the laboratorie of Golestan, Razi, and Abuzar hospitals for their significant assistance in collecting the samples.
Funding
Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran (Grant no: OG-9825).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethics approval
The current study was conducted according to the Declaration of Helsinki and obtained approval from the Ethics Committee of Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran (IR.AJUMS.MEDICINE.REC.1398.014). Written informed consent was obtained from all patients or their parents/guardians.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Farajzadeh Sheikh, A., Moradi Bandbal, M. & Saki, M. Emergence of multidrug-resistant Shigella species harboring extended-spectrum beta-lactamase genes in pediatric patients with diarrhea from southwest of Iran. Mol Biol Rep 47, 7097–7106 (2020). https://doi.org/10.1007/s11033-020-05776-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11033-020-05776-x