Objectives
Plasmid-mediated AmpC β-lactamases (PMABLs) and carbapenemases are emerging groups of antimicrobial-resistance determinants. The aims of the study were to evaluate the occurrence of PMABLs and carbapenemases in clinical isolates of Klebsiella pneumoniae and compare the test performance of various phenotypic methods for detection of these enzymes in Iran. Methods
A total of 100 K. pneumoniae isolates were collected from clinical specimens obtained in Valiasr Hospital. AmpC production in all isolates was determined using the AmpC disk test, the cephamycin Hodge test, the AmpC Etest, and the boronic acid combined-disk test. In addition, carbapenemase production was determined using the modified Hodge test, the EDTA disk synergy test, and the boronic acid combined-disk test. The performances of various phenotypic methods were evaluated by the comparison of their results with polymerase chain reaction (PCR) method as the gold standard. Results
Of the 100 isolates, 19 (19%) were demonstrated to harbor the PMABL-resistance gene by the multiplex PCR method. The PCR result indicated the presence of carbapenemase genes in 12 isolates. The performance of various phenotypic tests carried out for detection of carbapenemase-producing isolates varied widely, ranging in sensitivity from 30% to 100% and in specificity from 90.8% to 100%. Conclusion
This is the first report of MOX-type AmpC β-lactamase and blaGES in K. pneumoniae in Iran. A comparison of the phenotypic methods showed that a combination of cefoxitin plus boronic acid is optimal for detecting plasmid-mediated AmpC enzymes in K. pneumoniae, whereas the implementation of molecular methods is often complex, requires specially trained personnel, and is associated with higher costs.
Citations
Citations to this article as recorded by
The Global and Regional Prevalence of Hospital-Acquired Carbapenem-Resistant Klebsiella pneumoniae Infection: A Systematic Review and Meta-analysis Xing-chen Lin, Chang-li Li, Shao-yang Zhang, Xiao-feng Yang, Meng Jiang Open Forum Infectious Diseases.2024;[Epub] CrossRef
High frequency of NDM-1 and OXA-48 carbapenemase genes among Klebsiella pneumoniae isolates in central Iran Elnaz Abbasi, Ehsanollah Ghaznavi-Rad BMC Microbiology.2023;[Epub] CrossRef
Detection of ESBL and AmpC producing Klebsiella pneumoniae ST11 and ST147 from urinary tract infections in Iran Shaghayegh Shahkolahi, Pegah Shakibnia, Shahla Shahbazi, Samira Sabzi, Farzad Badmasti, Mohammad Reza Asadi Karam, Mehri Habibi Acta Microbiologica et Immunologica Hungarica.2022;[Epub] CrossRef
Plasmid-mediated AmpC β-Lactamase gene analysis in Klebsiella Pneumoniae clinical isolates Nabi Jomehzadeh, Khadijeh Ahmadi, Hasti Shaabaninejad, Gholamali Eslami Biomedical and Biotechnology Research Journal (BBR.2022; 6(4): 582. CrossRef
Characterization of Antimicrobial Resistance Patterns of Klebsiella pneumoniae Isolates Obtained from Wound Infections Roya Ghanavati, Hossein Kazemian, Parisa Asadollahi , Hamid Heidari, Gholamreza Irajian, Fatemeh Navab-Moghadam, Shabnam Razavi Infectious Disorders - Drug Targets .2021; 21(1): 119. CrossRef
An investigation of extended-spectrum β-lactamases (ESBLs) in Klebsiella isolated from foodborne outbreaks in Iran Farnaz Hajikarim, Mohammad Mehdi Soltan Dallal, Mohammad Reza Pourmand, Milad Abdi Gene Reports.2020; 19: 100632. CrossRef
Prevalence and Mechanisms of Carbapenem Resistance in Klebsiella pneumoniae and Escherichia coli: A Systematic Review and Meta-Analysis of Cross-Sectional Studies from Iran Mohammad Javad Nasiri, Mehdi Mirsaeidi, Seyyed Mohammad Javad Mousavi, Mania Arshadi, Fatemeh Fardsanei, Behnaz Deihim, Sara Davoudabadi, Samin Zamani, Bahareh Hajikhani, Hossein Goudarzi, Mehdi Goudarzi, Zahra Sadat Seghatoleslami, Hossein Dabiri, Payam Microbial Drug Resistance.2020; 26(12): 1491. CrossRef
Characterization of β-lactam resistance in K. pneumoniae associated with ready-to-eat processed meat in Egypt Shaymaa H. Abdel-Rhman, Grzegorz Woźniakowski PLOS ONE.2020; 15(9): e0238747. CrossRef
Multiplex PCR to detect pAmpC β-lactamases among enterobacteriaceae at a tertiary care laboratory in Mumbai, India Mubin Kazi, Kanchan Ajbani, Jeffrey A. Tornheim, Anjali Shetty, Camilla Rodrigues Microbiology.2019; 165(2): 246. CrossRef
AmpC β lactamases in Urinary Klebsiella pneumoniae Isolates: First Report of ACC Type AmpC β-lactamase Resistance in Iran Maryam Ghane, Laleh Babaeekhou, Mahdi Jafar Shanjani Journal of Advances in Medical and Biomedical Rese.2019; 27(123): 23. CrossRef
The Molecular and Clinical Epidemiology of Extended-Spectrum Cephalosporin– and Carbapenem-Resistant Enterobacteriaceae at 4 US Pediatric Hospitals Danielle M Zerr, Scott J Weissman, Chuan Zhou, Matthew P Kronman, Amanda L Adler, Jessica E Berry, Jaipreet Rayar, Jeff Myers, Wren L Haaland, Carey-Ann D Burnham, Alexis Elward, Jason Newland, Rangaraj Selvarangan, Kaede V Sullivan, Theoklis Zaoutis, Xua Journal of the Pediatric Infectious Diseases Socie.2017; 6(4): 366. CrossRef
Previous Antibiotic Exposure Increases Risk of Infection with Extended-Spectrum-β-Lactamase- and AmpC-Producing Escherichia coli and Klebsiella pneumoniae in Pediatric Patients Danielle M. Zerr, Arianna Miles-Jay, Matthew P. Kronman, Chuan Zhou, Amanda L. Adler, Wren Haaland, Scott J. Weissman, Alexis Elward, Jason G. Newland, Theoklis Zaoutis, Xuan Qin Antimicrobial Agents and Chemotherapy.2016; 60(7): 4237. CrossRef
Molecular characterization of extended-spectrum β-lactamase, plasmid-mediated AmpC cephalosporinase and carbapenemase genes among Enterobacteriaceae isolates in five medical centres of East and West Azerbaijan, Iran Mohammad Reza Sadeghi, Reza Ghotaslou, Mohammad Taghi Akhi, Mohammad Asgharzadeh, Alka Hasani
Journal of Medical Microbiology
.2016; 65(11): 1322. CrossRef
High Prevalence of AmpC β-Lactamases in Clinical Isolates of Escherichia coli in Ilam, Iran Abbas Maleki, Afra Khosravi, Sobhan Ghafourian, Iraj Pakzad, Shiva Hosseini, Rashid Ramazanzadeh, Nourkhoda Sadeghifard Osong Public Health and Research Perspectives.2015; 6(3): 201. CrossRef
Objectives
Horizontal transfer of integrons is one of the important factors that can contribute to the occurrence of multidrug-resistant (MDR) bacteria. This study aimed to determine the prevalence of integrons among MDR Escherichia coli strains isolated from stool specimens and investigate the associations between the existence of integrons and MDR properties in the southwest of Iran. Methods
There were 164 E. coli strains isolated from January 2012 to June 2012. Fecal specimens identified as E. coli by the conventional methods. Subsequently the antibiotic resistance was assessed using Clinical and Laboratory Standard Institute criteria. The presence of class 1–3 integrons and embedded gene cassettes was verified using specific primers by multiplex polymerase chain reaction assay. Results
Among a total of 164 studied samples, 69 (42.07%) isolates were multidrug resistant. Class 1 and class 2 integrons were present in 78.26% and 76.81% MDR isolates, respectively. For the first time in Iran, class 3 integron was observed in 26.09% MDR isolates. Significant correlations were identified between: class 1 integron and resistance to amikacin, gentamicin, chloramphenicol, ampicillin, tetracycline, nalidixic acid, and co-trimoxazole; class 2 integron and resistance to aminoglycosides, co-trimoxazole, cefalexin, ampicillin, and chloramphenicol; and class 3 integron and resistance to gentamicin, kanamycin, and streptomycin. Conclusion
Our results indicate that integrons are common among MDR isolates and they can be used as a marker for the identification of MDR isolates. Therefore, due to the possibility of a widespread outbreak of MDR isolates, molecular surveillance and sequencing of the integrons in other parts of the country is recommended.
Citations
Citations to this article as recorded by
Municipal wastewater treatment plant showing a potential reservoir for clinically relevant MDR bacterial strains co-occurrence of ESBL genes and integron-integrase genes Kuldeep Soni, David Kothamasi, Ram Chandra Journal of Environmental Management.2024; 351: 119938. CrossRef
Detection of virulence factor genes, antibiotic resistance genes and biofilm formation in clinical Gram-negative bacteria and first report from Türkiye of K.oxytoca carrying both blaOXA-23 and blaOXA-51 genes Azer Özad Düzgün, Gamze Yüksel Biologia.2023; 78(8): 2245. CrossRef
Antimicrobial Resistance in Romania: Updates on Gram-Negative ESCAPE Pathogens in the Clinical, Veterinary, and Aquatic Sectors Ilda Czobor Barbu, Irina Gheorghe-Barbu, Georgiana Alexandra Grigore, Corneliu Ovidiu Vrancianu, Mariana Carmen Chifiriuc International Journal of Molecular Sciences.2023; 24(9): 7892. CrossRef
Extended-Spectrum β-Lactamase-Producing Escherichia coli Isolated from Food-Producing Animals in Tamaulipas, Mexico Antonio Mandujano, Diana Verónica Cortés-Espinosa, José Vásquez-Villanueva, Paulina Guel, Gildardo Rivera, Karina Juárez-Rendón, Wendy Lizeth Cruz-Pulido, Guadalupe Aguilera-Arreola, Abraham Guerrero, Virgilio Bocanegra-García, Ana Verónica Martínez-Vázqu Antibiotics.2023; 12(6): 1010. CrossRef
Antimicrobial susceptibility and integrons detection among extended-spectrum β-lactamase producing Enterobacteriaceae isolates in patients with urinary tract infection Karzan Taha Abubaker, Khanda Abdulateef Anwar PeerJ.2023; 11: e15429. CrossRef
Brucella abortus antigen omp25 vaccines: Development and targeting based on Lactococcus lactis Somaye Tirbakhsh Gouran, Abbas Doosti, Mohammad Saeid Jami Veterinary Medicine and Science.2023; 9(4): 1908. CrossRef
Integrons in the development of antimicrobial resistance: critical review and perspectives Basharat Ahmad Bhat, Rakeeb Ahmad Mir, Hafsa Qadri, Rohan Dhiman, Abdullah Almilaibary, Mustfa Alkhanani, Manzoor Ahmad Mir Frontiers in Microbiology.2023;[Epub] CrossRef
Tracing the Evolutionary Pathways of Serogroup O78 Avian Pathogenic Escherichia coli Eun-Jin Ha, Seung-Min Hong, Seung-Ji Kim, Sun-Min Ahn, Ho-Won Kim, Kang-Seuk Choi, Hyuk-Joon Kwon Antibiotics.2023; 12(12): 1714. CrossRef
Molecular Detection of Integrons, Colistin and β-lactamase Resistant Genes in Salmonella enterica Serovars Enteritidis and Typhimurium Isolated from Chickens and Rats Inhabiting Poultry Farms Tsepo Ramatla, Kealeboga Mileng, Rendani Ndou, Nthabiseng Mphuti, Michelo Syakalima, Kgaugelo E. Lekota, Oriel M.M. Thekisoe Microorganisms.2022; 10(2): 313. CrossRef
Prevalence of the Integrons and ESBL Genes in Multidrug-Resistant Strains of Escherichia coli Isolated from Urinary Tract Infections, Ardabil, Iran Soheyla Barzegar, Mohsen Arzanlou, Amir Teimourpour, Majid Esmaelizad, Mehdi Yousefipour, Jafar MohammadShahi, Roghayeh Teimourpour Iranian Journal of Medical Microbiology.2022; 16(1): 56. CrossRef
Migration of antibiotic resistance genes and evolution of flora structure in the Xenopus tropicalis intestinal tract with combined exposure to roxithromycin and oxytetracycline Xiaojun Lin, Yanbin Xu, Ruiqi Han, Wenshi Luo, Li Zheng Science of The Total Environment.2022; 820: 153176. CrossRef
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 Khorshidi, NadiaMohammad Zadeh, Azad Khaledi, GholamAbbas Moosavi, Ali Shakerimoghaddam, Azade Matinpur International Archives of Health Sciences.2022; 9(1): 47. CrossRef
Prevalence and characterisation of antimicrobial resistance genes and class 1 and 2 integrons in multiresistant Escherichia coli isolated from poultry production Przemysław Racewicz, Michał Majewski, Hanna Biesiada, Sebastian Nowaczewski, Jarosław Wilczyński, Danuta Wystalska, Magdalena Kubiak, Marcin Pszczoła, Zofia E. Madeja Scientific Reports.2022;[Epub] CrossRef
Prevalence of integrons in multidrug-resistant Escherichia coli isolates from waters and vegetables in Nsukka and Enugu, Southeast Nigeria Chinyere B. Chigor, Ini-Abasi I. Ibangha, Nkechinyere O. Nweze, Valentino C. Onuora, Chizoba A. Ozochi, Yinka Titilawo, Matthew C. Enebe, Tatyana N. Chernikova, Peter N. Golyshin, Vincent N. Chigor Environmental Science and Pollution Research.2022; 29(40): 60945. CrossRef
Antimicrobial resistance and genetic diversity of Staphylococcus aureus collected from livestock, poultry and humans Sangeeta Rao, Lyndsey Linke, Roberta Magnuson, Linzy Jauch, Doreene R. Hyatt One Health.2022; 15: 100407. CrossRef
The Emergence of Carbapenem-Resistant Gram-Negative Bacteria in Mizoram, Northeast India Vanlalruati S. C. Ralte, Archana Loganathan, Prasanth Manohar, Christine Vanlalbiakdiki Sailo, Zothan Sanga, Lalremruata Ralte, John Zothanzama, Sebastian Leptihn, Ramesh Nachimuthu, Nachimuthu Senthil Kumar Microbiology Research.2022; 13(3): 342. CrossRef
Common Etiological Agents in Adult Patients with Gastroenteritis from Central Iran Elnaz Abbasi, Alex van Belkum, Ehsanollah Ghaznavi-Rad Microbial Drug Resistance.2022; 28(11): 1043. CrossRef
Antibiotic Resistance in Proteus mirabilis: Mechanism, Status, and Public Health Significance Ebtehal Alqurashi, Khaled Elbanna, Iqbal Ahmad, Hussein H. Abulreesh Journal of Pure and Applied Microbiology.2022; 16(3): 1550. CrossRef
Antibiotic Susceptibility Profiles and Resistance Mechanisms to β-Lactams and Polymyxins of Escherichia coli from Broilers Raised under Intensive and Extensive Production Systems Mariana Ferreira, Célia Leão, Lurdes Clemente, Teresa Albuquerque, Ana Amaro Microorganisms.2022; 10(10): 2044. CrossRef
Antimicrobial Resistance, Integron Carriage, and Fluoroquinolone Resistance Genes in Acinetobacte baumannii Isolates Parastoo Ashouri, Jafar Mohammadshahi, Vajihe Sadat Nikbin, Hadi Peeridogaheh, Behnam Mohammadi-Ghalehbin, Soheila Refahi, Amir Teimourpour, Majid Esmaelizad, Hafez Mirzaneghad, Roghayeh Teimourpour Archives of Clinical Infectious Diseases.2022;[Epub] CrossRef
Multidrug resistance-encoding gene in Citrobacter freundii isolated from healthy laying chicken in Blitar District, Indonesia Adiana Mutamsari Witaningrum, Freshinta Jellia Wibisono, Dian Ayu Permatasari, Mustofa Helmi Effendi, Emmanuel Nnabuike Ugbo International Journal of One Health.2022; : 161. CrossRef
Evaluation of Retail Meat as a Source of ESBL Escherichia coli in Tamaulipas, Mexico Ana Verónica Martínez-Vázquez, Antonio Mandujano, Eduardo Cruz-Gonzalez, Abraham Guerrero, Jose Vazquez, Wendy Lizeth Cruz-Pulido, Gildardo Rivera, Virgilio Bocanegra-García Antibiotics.2022; 11(12): 1795. CrossRef
Characterization of Integrons and Quinolone Resistance in Clinical Escherichia coli Isolates in Mansoura City, Egypt Shaymaa H. Abdel-Rhman, Rehab M. Elbargisy, Dina E. Rizk, Ahmed Majeed Al-Shammari International Journal of Microbiology.2021; 2021: 1. CrossRef
Prevalence and Characterization of ESBL/AmpC Producing Escherichia coli from Fresh Meat in Portugal Lurdes Clemente, Célia Leão, Laura Moura, Teresa Albuquerque, Ana Amaro Antibiotics.2021; 10(11): 1333. CrossRef
Association of phylogenetic distribution and presence of integrons with multidrug resistance in Escherichia coli clinical isolates from children with diarrhoea Yesmi Patricia Ahumada-Santos, María Elena Báez-Flores, Sylvia Páz Díaz-Camacho, Magdalena de Jesús Uribe-Beltrán, Carlos Alberto Eslava-Campos, Jesús Ricardo Parra-Unda, Francisco Delgado-Vargas Journal of Infection and Public Health.2020; 13(5): 767. CrossRef
Class 1 Integrons in Clinical Multi Drug Resistance E. coli, Sana’a Hospitals, Yemen Mukhtar A. Al-Hammadi, Hassan A. Al-Shamahy, Abdulaziz Q. Ali, Mahfoudh A.M. Abdulghani, Hassan Pyar, Ibrahim AL-Suboal Pakistan Journal of Biological Sciences.2020; 23(3): 231. CrossRef
Occurrence, Phenotypic and Molecular Characterization of Extended-Spectrum- and AmpC- β-Lactamase Producing Enterobacteriaceae Isolated From Selected Commercial Spinach Supply Chains in South Africa Loandi Richter, Erika M. du Plessis, Stacey Duvenage, Lise Korsten Frontiers in Microbiology.2020;[Epub] CrossRef
Dissemination of antibiotic resistance genes (ARGs) via integrons in Escherichia coli: A risk to human health Shaqiu Zhang, Muhammad Abbas, Mujeeb Ur Rehman, Yahui Huang, Rui Zhou, Siyue Gong, Hong Yang, Shuling Chen, Mingshu Wang, Anchun Cheng Environmental Pollution.2020; 266: 115260. CrossRef
Multi-Drug-Resistant Diarrheagenic Escherichia coli Pathotypes in Pediatric Patients with Gastroenteritis from Central Iran
Elnaz Abbasi, Mahdieh mondanizadeh, Alex van Belkum, Ehsanollah Ghaznavi-Rad Infection and Drug Resistance.2020; Volume 13: 1387. CrossRef
The Relationship of Class I Integron Gene Cassettes and the Multidrug-Resistance in Extended -Spectrum β-Lactamase Producing Isolates of Escherichia coli Alisha Akya, Roya Chegene Lorestani, Mosayeb Rostamian, Azam Elahi, Shokofe Baakhshii, Minoo Aliabadi, Keyghobad Ghadiri Archives of Pediatric Infectious Diseases.2019;[Epub] CrossRef
Integrons in Enterobacteriaceae : diversity, distribution and epidemiology Megha Kaushik, Sanjay Kumar, Rajeev Kumar Kapoor, Jugsharan Singh Virdi, Pooja Gulati International Journal of Antimicrobial Agents.2018; 51(2): 167. CrossRef
Molecular analysis of Shiga toxin-producing Escherichia coli O157:H7 and non-O157 strains isolated from calves Maryam Kohansal, Ali Ghanbari Asad Onderstepoort Journal of Veterinary Research.2018;[Epub] CrossRef
Prevalence of Integrons and Insertion Sequences in ESBL-Producing E. coli Isolated from Different Sources in Navarra, Spain Lara Pérez-Etayo, Melibea Berzosa, David González, Ana Vitas International Journal of Environmental Research an.2018; 15(10): 2308. CrossRef
Frequency of antimicrobial resistance and integron gene cassettes in Escherichia coli isolated from giant pandas (Ailuropoda melanoleuca) in China Wencheng Zou, Caiwu Li, Xin Yang, Yongxiang Wang, Guangyang Cheng, Jinxin Zeng, Xiuzhong Zhang, Yanpeng Chen, Run Cai, Qianru Huang, Lan Feng, Hongning Wang, Desheng Li, Guiquan Zhang, Yanxi Chen, Zhizhong Zhang, Heming Zhang Microbial Pathogenesis.2018; 116: 173. CrossRef
Colistin-Resistant Klebsiella pneumoniae: Prevalence of Integrons and Synergistic Out Turn for Colistin-Meropenem Prasanth Manohar, Thamaraiselvan Shanthini, Pandey Ekta, Mahesan J B, Kodiveri Muthukaliannan Gothandam, Bulent Bozdogan, Nachimuthu Ramesh Archives of Clinical Infectious Diseases.2018;[Epub] CrossRef
Evaluation of integrons classes 1–3 in extended spectrum beta-lactamases and multi drug resistant Escherichia coli isolates in the North of Iran Shahla Asgharzadeh Kangachar, Ali Mojtahedi Gene Reports.2018; 12: 299. CrossRef
Association of Glycerol Kinase Gene with Class 3 Integrons: A Novel Cassette Array within Escherichia coli Rajkumari Elizabeth, Debadatta Dhar Chanda, Atanu Chakravarty, Deepjyoti Paul, Shiela Chetri, Deepshikha Bhowmik, Jayalaxmi Wangkheimayum, Amitabha Bhattacharjee Indian Journal of Medical Microbiology.2018; 36(1): 104. CrossRef
Emergence of class 1 to 3 integrons among members of Enterobacteriaceae in Egypt Dina E. Rizk, Areej M. El-Mahdy Microbial Pathogenesis.2017; 112: 50. CrossRef
Detection of Class I and II integrons for the assessment of antibiotic and multidrug resistance amongEscherichia coliisolates from agricultural irrigation waters in Bulacan, Philippines Cielo Emar M. Paraoan, Windell L. Rivera, Pierangeli G. Vital Journal of Environmental Science and Health, Part .2017; 52(5): 306. CrossRef
Distribution of Integrons and Phylogenetic Groups among Enteropathogenic Escherichia coli Isolates from Children <5 Years of Age in Delhi, India Taru Singh, Shukla Das, V. G. Ramachandran, Sayim Wani, Dheeraj Shah, Khan A. Maroof, Aditi Sharma Frontiers in Microbiology.2017;[Epub] CrossRef
The distribution of carbapenem- and colistin-resistance in Gram-negative bacteria from the Tamil Nadu region in India Prasanth Manohar, Thamaraiselvan Shanthini, Ramankannan Ayyanar, Bulent Bozdogan, Aruni Wilson, Ashok J. Tamhankar, Ramesh Nachimuthu, Bruno S. Lopes
Journal of Medical Microbiology
.2017; 66(7): 874. CrossRef
Multidrug-Resistant Escherichia coli Strains Isolated from Patients Are Associated with Class 1 and 2 Integrons Hamid Lavakhamseh, Parviz Mohajeri, Samaneh Rouhi, Pegah Shakib, Rashid Ramazanzadeh, Afshin Rasani, Majid Mansouri Chemotherapy.2016; 61(2): 72. CrossRef
Variability in gene cassette patterns of class 1 and 2 integrons associated with multi drug resistance patterns in Staphylococcus aureus clinical isolates in Tehran-Iran Mahdi Mostafa, Seyed Davar Siadat, Fereshteh Shahcheraghi, Farzam Vaziri, Alireza Japoni-Nejad, Jalil Vand Yousefi, Bahareh Rajaei, Elnaz Harifi Mood, Nayyereh Ebrahim zadeh, Arfa Moshiri, Seyed Alireza Seyed Siamdoust, Mohamad Rahbar BMC Microbiology.2015;[Epub] CrossRef