Antibiotic Resistance Pattern and Prevalence of blaOXA-51, blaNDM, blaVIM, blaPER, blaVEB, blaCTX, tetA and tetB Genes in Acinetobacter baumannii Isolated from Clinical Specimens of Hospitals in Tabriz city, Iran


avatar Abolfazl Jafari Sales ORCID 1 , * , avatar Sara Naebi ORCID 2 , avatar Hossein Bannazadeh-Baghi ORCID 3 , avatar Morteza Saki ORCID 4

Department of Microbiology, School of Basic Sciences, Kazerun Branch, Islamic Azad University, Kazerun, Iran
Department of Microbiology, Ahar Branch, Islamic Azad University, Ahar, Iran
Infectious and Tropical Diseases Research Center, Tabriz University of Medical Sciences, Tabriz, Iran
Department of Microbiology, Faculty of Medicine, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran

how to cite: Jafari Sales A, Naebi S , Bannazadeh-Baghi H , Saki M . Antibiotic Resistance Pattern and Prevalence of blaOXA-51, blaNDM, blaVIM, blaPER, blaVEB, blaCTX, tetA and tetB Genes in Acinetobacter baumannii Isolated from Clinical Specimens of Hospitals in Tabriz city, Iran. J Clin Res Paramed Sci. 2021;10(2):e118521. doi: 10.5812/jcrps.118521.



Nowadays, the resistance of pathogenic bacteria to antibiotics has become a global problem. Acinetobacter baumannii is an important opportunistic nosocomial pathogen. Acinetobacter baumannii plays a significant role in antibiotic resistance.


The purpose of this study was to investigate the prevalence of the blaOXA-51, blaNDM, blaVIM, blaPER, blaVEB, blaCTX-M, tetA and tetB genes and antibiotic resistance pattern of A. baumannii isolated from hospitals in Tabriz city, Iran.


This study was descriptive cross-sectional research, performed on 129 isolates of Acinetobacter from different clinical specimens. The Isolates were identified using standard laboratory methods and culture in selective mediums. The antibiotic resistance pattern of isolates was also determined by the Kirby-Bauer disk diffusion susceptibility test. Phenotypic and genotypic detection of blaOXA-51, blaNDM, blaVIM, blaPER, blaVEB, blaCTX-M, tetA and tetB genes in the isolates was carried out by a combined disk test (CDT) and polymerase chain reaction (PCR), respectively.


The highest resistance of isolates was determined to cefotaxime (100%) and ceftazidime (100%). The results of CDT showed that 14 (12.96%) isolates could produce extended-spectrum Beta-lactamases (ESBLs). However, the PCR results blaOXA-51, blaNDM, blaVIM, blaPER, blaVEB, blaCTX-M, tetA and tetB genes showed that these genes were in 100%, 18.51%, 16.66%, 32.40%, 16.66%, 31.48%, 32.40% and 21.29% of isolates, respectively.


Due to the high prevalence of antimicrobial resistance in strains, rapid and timely detection of antibiotic-resistant A. baumannii strains is necessary for the selection of an appropriate therapeutic approach and prevention of their prevalence.

1. Background

Acinetobacter spp. are obligate aerobic, oxidase-negative, non-motile, Gram-negative coccobacilli and opportunistic pathogens that can be easily isolated from soil and water, and sometimes from the hospital environments (1, 2). They don’t require a specific nutrient medium to survive. Acinetobacter spp. grow easily in conventional laboratory mediums without any pigment (3, 4). Due to its low nutritional requirements for growth, this bacterium can survive for long periods in adverse conditions, dry surfaces as well as in aquatic environments (5). Acinetobacter baumannii is one of the most common pathogenic bacteria causing nosocomial infections in patients hospitalized in intensive care units. People with neutropenia, cystic fibrosis, and immune deficiency are exposed to the risk of infection with A. baumannii (6). The catheter and other medical equipment may lead to the outbreak of this bacterium in the hospital (7). Owing to the high levels of antibiotic resistance in comparison with other nosocomial isolates and its high prevalence in hospital environments, A. baumannii is known as an important cause of disease, mortality and economic loss in different countries (8, 9). Besides respiratory tract infections, A. baumannii may also responsible for urinary tract and wound infections in hospitals (10). The resistance of A. baumannii strains to antibiotics can be intrinsic or through the obtaining of genetic factors. Most of them are resistant to ampicillin, amoxicillin/clavulanic acid, antistaphylococcal penicillin, extended-spectrum cephalosporins (except ceftazidime and cefepime), tetracycline, macrolides, rifampicin and chloramphenicol (11, 12). As reported in most hospitals worldwide, multidrug-resistant (MDR) A. baumannii has recently become a major concern in hospitals (13). The prevalence of MDR A. baumannii to other sites indicates the role of this organism in the rapid spread of resistance genes (14-16). Beta-lactamases are inactivating enzymes for the beta-lactam antibiotics. The first identified beta-lactamase is penicillinase (17-21). CTX-M type beta-lactamases, firstly identified in Germany in 1989, consist of a group of Extended-spectrum β-lactamases (ESBLs) encoded by the plasmid (22). Based on the amino acid sequences, CTX-M beta-lactamases are classified into five major groups: CTX-M1, CTX-M2, CTX-M8, CTX-M9, and CTX-M25 (23). The CTX-M enzyme mainly hydrolyzes cefotaxime and often has poor activity against ceftazidime. However, CTX-M15 has a strong activity against ceftazidime (24). The prevalence of ESBLs, especially CTX-M, has increased in recent years (25). These enzymes result in the resistance of bacteria to penicillin and a wide range of third-generation cephalosporins. However, ESBLs are sensitive to several antibiotics such as cephamycin and carbapenem. Also, some of the antibiotics such as clavulanic acid, tazobactam and sulbactam completely inhibit these enzymes (26). Acinetobacter baumannii is inherently capable of producing class D oxacillins (belonging to the OXA-51 group of enzymes) and non-induced AmpC cephaloporinases (27). The blaPER-1 gene was first found in Pseudomonas aeruginosa. It has since been widely observed in Acinetobacter (28). The blaVEB-1 gene was first observed during the outbreak of clonal strains of A. baumannii in the ICU of a French hospital (29). Pumping of the drug out of the bacteria by efflux mechanisms is also related to the specificity of MDR. The tetA is involved in resistance to tetracycline and tetB is involved in the minocycline pump in addition to tetracycline (27, 30). VIM-type beta-lactamase in Acinetobacter species was first observed in Europe and then reported worldwide (31, 32). NDM beta-lactamase is a transmissible class B molecular β-lactamase recently identified in New Delhi, India (33). Beta-lactam resistance genes in A. baumannii are usually located on mobile genetic elements and therefore can easily transmit between different strains. Thus, identification of the ESBLs-producing strains can be an essential step in the treatment of their infections.

2. Objectives

Due to the high prevalence of antibiotic resistance genes and nosocomial infections, the aim of the present study was to isolate A. baumannii from clinical specimens and determine the prevalence rate of blaOXA-51, blaNDM, blaVIM, blaPER, blaVEB, blaCTX-M, tetA and tetB genes in the isolates.

3. Methods

This study was descriptive cross-sectional research performed on 129 clinical isolates of Acinetobacter isolated from blood, urine, wound exudates and respiratory secretions in the hospitals in Tabriz city from March to December 2019. All of the isolates were detected using standard laboratory tests, microbiological experiments and differential biochemical tests including oxidase, catalase, urease, oxidation-fermentation (OF), Triple Sugar Iron (TSI) tests, culture in Simmons citrate agar, sulfur indole motility media (SIM), Methyl red-Voges-Proskauer (MR-VP) broth as well as, the growth in 37°C and 42°C. Antibiotic resistance patterns of A. baumannii isolates were determined by agar disc diffusion method based on the guidelines of the clinical & laboratory standards institute (CLSI) (34). The used antibiotic disks are included: ceftazidime (30 μg), ciprofloxacin (5 μg), levofloxacin (10 μg), cefotaxime (30 μg), Aztreonam (30 μg), cefepime (30 μg), gentamicin (10 μg), amikacin (30 μg), imipenem (10 μg), meropenem (10 μg), piperacillin/tazobactam (10/100 μg), tetracycline (30 μg) ) and polymyxin B (300 μg) (Mast Diagnostics Mast group Ltd., Merseyside, UK). The standard strain of A. baumannii ATCC 19606 and Escherichia coli ATCC 25922 was used as positive and negative controls, respectively. The ESBL-producing isolates were identified by combined disk test using ceftazidime (30 μg), cefotaxime (30 μg), ceftazidime/clavulanic acid (30 μg/10 μg) and cefotaxime/clavulanic acid (30µg/10µg). After incubation at 37°C for 24 hours, ESBL-producing isolates had a zone of inhibition with a diameter ≥ of 5 mm around ceftazidime/clavulanic acid discs in comparison with ceftazidime or cefotaxime discs (35). The DNA samples were extracted from the isolates using a commercial kit (Invitek, STRATEC Molecular-Germany). To identify the blaOXA-51, blaNDM, blaVIM, blaPER, blaVEB, blaCTX-M, tetA and tetB genes in the isolates, the polymerase chain reaction (PCR) technique was performed using the specific primers (Table 1). The reaction was performed in a total volume of 20 µL, including 10 µL of Master Mix (Amplicon Denmark), 2 µL of template DNA, 10 pM of primer and distilled water. The heating program in thermocycler was as follows: one cycle of initial denaturation at 94°C for 3 min, 35 cycles of denaturation in 35°C for 30 sec, annealing at 45°C for 1 minute, and extension at 72°C for 1 min. The final extension was carried out at 72°C for 4 minutes. The PCR products were run on 1% agarose gel in TBE buffer for 60 min at 100°C. The gel was then placed in a tank containing ethidium bromide for 15 minutes. The results were visualized using a gel documentation system under the UV light. Standard strains of A. baumannii ATCC 19606, P. aeruginosa ATCC 27853 and E. coli ATCC 25922 were used as quality control according to the CLSI.

Table 1. Sequence of Primers Used
GenesSequencesAmplicon SizeReferences
blaOXA-515′-TAA TGC TTT GAT CGG CCT TG-3′353bp(36)

4. Results

Out of 129 isolates, 108 (83.72%) isolates were identified as A. baumannii. The mean age of patients with A. baumannii infections was 52 ± 24.4 years. The organism was isolated from 58 (53.7%) of urine cultures, 10 (9.26%) of wound discharges, 34 (31.48%) of blood cultures and 6 (5.56%) of respiratory tract secretions. The isolates showed the least resistance to polymyxin B (47.22%). The highest resistance of them was detected to cefotaxime (100%) and ceftazidime (100%) (Figure 1). Out of 108 isolates, 103 isolates (95.37%) were identified as MDR (resistant to more than three classes of antibiotics). The results of the combined disk test showed that 14 (12.96%) isolates were ESBL-positive. PCR results for target genes showed that 43 (39.81%) isolates contained tetA gene, 35 (32.40%) isolates contained blaPER-1 gene, 34 (31.48%) isolates contained blaCTX-M gene, 23 (21.29%) isolates contained tetB gene, 20 (18.51%) isolates contained blaNDM gene,18 (16.66%) isolates contained blaVEB-1 gene and 18 (16.66%) isolates contained blaVIM gene. The blaOXA-51 gene was positive as a genetic marker for the diagnosis of A. baumannii in all isolates. The ESBL-producing isolates showed the highest resistance to the used antibiotic discs among others.

Resistance percentage of Acinetobacter baumannii isolates to different antibiotics

5. Discussion

Production of beta-lactamases by gram-negative bacteria is one of the main mechanisms responsible for their resistance to beta-lactam antibiotics. Since the beta-lactams have wide clinical applications, beta-lactamases have evolved concurrently and played a major role in the failure of antibiotic therapy (43). In the last fifteen years, epidemics of infection caused by beta-lactamase-producing organisms have occurred around the world. So, these enzymes are known as a major threat to the use of cephalosporins. It has also been well established that the treatment of such cephalosporin-resistant infections will not be satisfactory, and the mortality caused by ESBL-producing bacteria is significantly high (44). The emergence and prevalence of ESBL-producing bacteria appear to be due to the widespread use of extended-spectrum beta-lactams. The prevalence of these bacteria in different parts of the hospital has been increased in recent years. In the present study, out of the 129 Acinetobacter isolates, 108 (83.72%) were identified as A. baumannii. This result is almost similar to the findings of Nazari Monazam et al. (45) (76.9%), Constantiniu et al. (46) (71%) and Rit et al. (47) (74.02%). However, Ahmadikia et al. (48) reported higher rates (93.1%) than of the present study. In this study, the antimicrobial resistance analysis indicated that all isolates were resistant to ceftazidime and cefotaxime. Ayan et al. (49) found that all 52 isolates were resistant to piperacillin/tazobactam, cefepime, cefotaxime, ceftazidime, gentamicin, and aztreonam. The resistance to aminofloxacin and tetracycline were reported in 8% and 74% of strains, respectively. Biendo et al., in a study about the antibiotyping of A. baumannii isolates, found that 15 of 18 isolates were resistant to ticarcillin, ticarasilamine/clavulanic acid, piperacillin/tazobactam, ceftazidime and aztreonam (50). Their findings are quite consistent with the results of the present study. In the study of Smolyakov et al., (51) and Wang et al., (52), all strains were resistant to imipenem. Also, Saadatian (2005) reported that 95.5% of A. baumannii isolates were resistant to amikacin. These results were is consistent with the findings of the present study (53). In the present study, the resistance level of A. baumannii isolates to polymyxin B was high, so that 47.22% of isolates were resistant to this antibiotic. Polymyxins are the last-line treatment for MDR isolates of A. baumannii. Therefore, treatment of A. baumannii infections, which is resistant to these antibiotics, is very difficult (54). In the present study, 103 isolates (95.37%) had MDR that was higher than the findings of Joshi (55) (75%) and Bahador (56) (45%) and less than Ahmadikiya (98.9%) (48). In this study, the prevalence of ESBL-producing A. baumannii in clinical specimens was 12.96%, which is higher than the results of Ahmadikiya (48) and lower than the findings of Sinha (57) in India and Maleki (58) in Shiraz. Ranjbar and Farahani in their study of 163 strains of A. baumannii showed that 52.2% of the samples were ESBL positive. Which is more than the findings of the present study (59). In the study of Ahmadikiya et al. (48), 31.6% of isolates were positive for the blaCTX-M gene, which is similar to the findings of present study. Also, in the study of Shahcheraghi et al. (60) and Celenza et al. (61), these rates were 1.2% and 30.4%, respectively, which are lower than the findings of the present study. In the present study, the presence of the blaOXA-51, blaNDM, blaVIM, blaPER, blaVEB, blaCTX-M, tetA and tetB genes are 100%, 18.51%, 16.66%, 32.40%, 16.66%, 31.48%, 32.40% and 21.29%, respectively. Safari et al reported that 58% and 20% of ESBL-positive A. baumannii isolates contained SHV and CTX-M genes, respectively (62). Goudarzi et al. In 2016, the resistance of isolated strains to tested antibiotics was 95.4% to ceftazidime, 100% to cefotaxime, 95.7% to cefepime, 91.7%to imipenem, 91.7% to meropenem, 80.6% to amikacin, 97.2%to piperacillin, 92.6%to ciprofloxacin, 95.4% to piperacillin/tazobactam, 40.7% to gentamicin, 98.1% to ampicillin/sulbactam and 98.1% to co-trimoxazole respectively. PCR results showed that 44.17% of the isolates had blaVIM gene and blaNDM gene was not seen in the strains (63). Mohammadi et al. Showed in a study that antibiotic resistance in 100 isolates of A. baumannii was related to antibiotics: Cefimoimide (97%), Ceftriaxone (95%), Amikacin (95%), Imipenem (76%), Piperacillin-tazobactam (70%), Meropenem (69%), Gentamicin (63%), Tobramycin (56%), Tetracycline (51%), and Ampicillin-Sulbactam (49%) and lowest resistance was related to polymyxin B. PCR results showed that 17% and 20% of the strains carried blaVIM and blaNDM genes, respectively (64). Azizi and Shahcheraghi during a study in 2017 in Tehran hospitals, showed that all samples were resistant to gentamicin, ciprofloxacin, piperacillin, cefotaxime, ceftazidime and tetracycline. Also, all isolates were identified as resistant to several antibiotics. The tetA, tetB, blaVEB, blaCTX-M and blaPER genes were identified as 75.3%, 43%, 35.3%, 76.9% and 61.5% of the isolates, respectively (65). In a 2012 study by Asadollahi et al., The prevalence of tetA and tetB genes was reported to be 95.5% and 65%, respectively (66). The blaOXA-51 gene is located on the chromosome in A. baumannii. The enzyme OXA-51 has poor carbapenemase activity, but the addition of the ISAba 1 complement sequence at the 5 'end of the blaOXA-51 gene leads to its high expression, and this increase in expression causes resistance to carbapenem (67). In 2015, Badmasti et al reported a 44% presence of the blaPER gene in A. baumannii isolates. Which is more than the findings of the present study (68). Ranjbar and Farahani during a study in 2019, the prevalence of blaOXA−23, blaVIM, blaPER−1 and tetB genes was reported to be 85.1%, 60.5%, 42.3% and 67.8%, respectively (59). The differences between the findings of the present study and other researchers may be due to differences in the place of sample collection, the number of samples studied and even the decrease or increase in antibiotic use in the patients studied

5.1. Conclusions

According to the results of this study, the resistance of A. baumannii isolates to various antibiotics especially beta-lactams is an important therapeutic problem. Also, the production of ESBLs is a major threat for use of extended-spectrum cephalosporins. Therefore, in order to treat infections that are suspected for ESBL production, the appropriate antibiotic should be selected based on the results of the antibiogram test. The findings of the present study indicate the need for making the right decision about the reasonable administration of drugs as well as using novel diagnostic methods in microbiology laboratories.



  • 1.

    Kempf M, Rolain JM. Emergence of resistance to carbapenems in Acinetobacter baumannii in Europe: clinical impact and therapeutic options. Int J Antimicrob Agents. 2012;39(2):105-14. doi: 10.1016/j.ijantimicag.2011.10.004. [PubMed: 22113193].

  • 2.

    Peleg AY, Jara S, Monga D, Eliopoulos GM, Moellering RJ, Mylonakis E. Galleria mellonella as a model system to study Acinetobacter baumannii pathogenesis and therapeutics. Antimicrob Agents Chemother. 2009;53(6):2605-9. doi: 10.1128/AAC.01533-08. [PubMed: 19332683]. [PubMed Central: PMC2687231].

  • 3.

    Manuel J, Panaligan M, Coronel R. Acinetobacter baumanni: an emerging nosocomial infection pathogen. J Philipp Microb Infec Dis. 2010;39(1):66-72.

  • 4.

    Bergogne-Berezin E, Towner KJ. Acinetobacter spp. as nosocomial pathogens: microbiological, clinical, and epidemiological features. Clin Microbiol Rev. 1996;9(2):148-65. doi: 10.1128/CMR.9.2.148. [PubMed: 8964033]. [PubMed Central: PMC172888].

  • 5.

    Murray PR, Baron EJ, Pfaller MA. Manual of Clinical Microbiology. 7th ed. Washington, D.C: ASM Press; 1999. p. 539-60.

  • 6.

    Fagon JY, Chastre J, Domart Y, Trouillet JL, Gibert C. Mortality due to ventilator-associated pneumonia or colonization with Pseudomonas or Acinetobacter species: assessment by quantitative culture of samples obtained by a protected specimen brush. Clin Infect Dis. 1996;23(3):538-42. doi: 10.1093/clinids/23.3.538. [PubMed: 8879777].

  • 7.

    Vahdani P, Yaghoubi T, Aminzadeh Z. Hospital acquired antibiotic-resistant acinetobacter baumannii infections in a 400-bed hospital in Tehran, Iran. Int J Prev Med. 2011;2(3):127-30. [PubMed: 21811653]. [PubMed Central: PMC3143524].

  • 8.

    Dijkshoorn L, Nemec A, Seifert H. An increasing threat in hospitals: multidrug-resistant Acinetobacter baumannii. Nat Rev Microbiol. 2007;5(12):939-51. doi: 10.1038/nrmicro1789. [PubMed: 18007677].

  • 9.

    Peleg AY, Seifert H, Paterson DL. Acinetobacter baumannii: emergence of a successful pathogen. Clin Microbiol Rev. 2008;21(3):538-82. doi: 10.1128/CMR.00058-07. [PubMed: 18625687]. [PubMed Central: PMC2493088].

  • 10.

    Bou G, Oliver A, Martinez-Beltran J. OXA-24, a novel class D beta-lactamase with carbapenemase activity in an Acinetobacter baumannii clinical strain. Antimicrob Agents Chemother. 2000;44(6):1556-61. doi: 10.1128/AAC.44.6.1556-1561.2000. [PubMed: 10817708]. [PubMed Central: PMC89912].

  • 11.

    Landman D, Quale JM, Mayorga D, Adedeji A, Vangala K, Ravishankar J, et al. Citywide clonal outbreak of multiresistant Acinetobacter baumannii and Pseudomonas aeruginosa in Brooklyn, NY: the preantibiotic era has returned. Arch Intern Med. 2002;162(13):1515-20. doi: 10.1001/archinte.162.13.1515. [PubMed: 12090889].

  • 12.

    Carmeli Y, Troillet N, Eliopoulos GM, Samore MH. Emergence of antibiotic-resistant Pseudomonas aeruginosa: comparison of risks associated with different antipseudomonal agents. Antimicrob Agents Chemother. 1999;43(6):1379-82. doi: 10.1128/AAC.43.6.1379. [PubMed: 10348756]. [PubMed Central: PMC89282].

  • 13.

    Hidron AI, Edwards JR, Patel J, Horan TC, Sievert DM, Pollock DA, et al. NHSN annual update: antimicrobial-resistant pathogens associated with healthcare-associated infections: annual summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2006-2007. Infect Control Hosp Epidemiol. 2008;29(11):996-1011. doi: 10.1086/591861. [PubMed: 18947320].

  • 14.

    Hospenthal DR, Crouch HK, English JF, Leach F, Pool J, Conger NG, et al. Multidrug-resistant bacterial colonization of combat-injured personnel at admission to medical centers after evacuation from Afghanistan and Iraq. J Trauma. 2011;71(1 Suppl):S52-7. doi: 10.1097/TA.0b013e31822118fb. [PubMed: 21795879].

  • 15.

    Keen E3, Murray CK, Robinson BJ, Hospenthal DR, Co EM, Aldous WK. Changes in the incidences of multidrug-resistant and extensively drug-resistant organisms isolated in a military medical center. Infect Control Hosp Epidemiol. 2010;31(7):728-32. doi: 10.1086/653617. [PubMed: 20500036].

  • 16.

    Jafari Sales A, Naebi S, Nasiri R, Bannazadeh-Baghi H. The Antibiotic Resistance Pattern and Prevalence of blaTEM, blaSHV, blaCTX-M, blaPSE-1, sipB/C, and cmlA/tetR Genes in Salmonella typhimurium Isolated from Children with Diarrhea in Tabriz, Iran. IJHLS. 2021;7(4). e118523. doi: 10.5812/ijhls.118523.

  • 17.

    Jafari Sales A, Mobaiyen H. [Frequency and resistance patterns in clinical isolates of Escherichia coli Extended Spectrum Beta Lactamase producing treatment Centers in Marand city, Iran]. New Cell Mol Biotechnol J. 2017;7(26):19-26. Persian.

  • 18.

    Dizaji AS, Fathi R, Sales AJ. Molecular study of extended-spectrum beta-lactamase (TEM-1) gene in Escherichia Coli isolates collected from Ostad Alinasab Hospital in Tabriz Iran. Marmara Med J. 2016;29(1). doi: 10.5472/MMJoa.2901.06.

  • 19.

    Jafari-Sales A. Study of Antibiotic Resistance and Prevalence of bla-TEM gene in Klebsiella pneumoniae Strains isolated from Children with UTI in Tabriz Hospitals. Focus Med Sci J. 2018;4(1).

  • 20.

    Sales A, Fathi R, Mobaiyen H, Bonab FR, Kondlaji KB. Molecular Study of the Prevalence of CTX-M1, CTX-M2, CTXM3 in Pseudomonas aeruginosa Isolated from Clinical Samples in Tabriz Town, Iran. Electronic J Biol. 2017;13(3):253-9.

  • 21.

    Jafari-Sales A, Bagherizadeh Y, Khalifehpour M, Abdoli-senejan M, Helali-Pargali R. [Antibiotic resistance pattern and bla-TEM gene expression in Acinetobacter baumannii isolated from clinical specimens of Tabriz hospitals]. Zanco J Med Sci. 2019;20(65):20-9. Persian.

  • 22.

    Falagas ME, Karageorgopoulos DE. Extended-spectrum beta-lactamase-producing organisms. J Hosp Infect. 2009;73(4):345-54. doi: 10.1016/j.jhin.2009.02.021. [PubMed: 19596491].

  • 23.

    Bonnet R. Growing group of extended-spectrum beta-lactamases: the CTX-M enzymes. Antimicrob Agents Chemother. 2004;48(1):1-14. doi: 10.1128/AAC.48.1.1-14.2004. [PubMed: 14693512]. [PubMed Central: PMC310187].

  • 24.

    Poirel L, Gniadkowski M, Nordmann P. Biochemical analysis of the ceftazidime-hydrolysing extended-spectrum beta-lactamase CTX-M-15 and of its structurally related beta-lactamase CTX-M-3. J Antimicrob Chemother. 2002;50(6):1031-4. doi: 10.1093/jac/dkf240. [PubMed: 12461028].

  • 25.

    Mirzaee M, Pourmand MR, Chitsaz MOHSEN, Mansouri S. Antibiotic resistance to third generation cephalosporins due to CTX-M-Type Extended-Spectrum β-Lactamases in clinical isolates of Escherichia coli. Iran J Public Health. 2009;38(1):10-7.

  • 26.

    Rupp ME, Fey PD. Extended spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae: considerations for diagnosis, prevention and drug treatment. Drugs. 2003;63(4):353-65. doi: 10.2165/00003495-200363040-00002. [PubMed: 12558458].

  • 27.

    Gordon NC, Wareham DW. Multidrug-resistant Acinetobacter baumannii: mechanisms of virulence and resistance. Int J Antimicrob Agents. 2010;35(3):219-26. doi: 10.1016/j.ijantimicag.2009.10.024. [PubMed: 20047818].

  • 28.

    Tada T, Shrestha S, Shimada K, Ohara H, Sherchand JB, Pokhrel BM, et al. PER-8, a Novel Extended-Spectrum beta-Lactamase PER Variant, from an Acinetobacter baumannii Clinical Isolate in Nepal. Antimicrob Agents Chemother. 2017;61(3). e02300. doi: 10.1128/AAC.02300-16. [PubMed: 28031203]. [PubMed Central: PMC5328513].

  • 29.

    Poirel L, Menuteau O, Agoli N, Cattoen C, Nordmann P. Outbreak of extended-spectrum beta-lactamase VEB-1-producing isolates of Acinetobacter baumannii in a French hospital. J Clin Microbiol. 2003;41(8):3542-7. doi: 10.1128/JCM.41.8.3542-3547.2003. [PubMed: 12904353]. [PubMed Central: PMC179787].

  • 30.

    Vila J, Marti S, Sanchez-Cespedes J. Porins, efflux pumps and multidrug resistance in Acinetobacter baumannii. J Antimicrob Chemother. 2007;59(6):1210-5. doi: 10.1093/jac/dkl509. [PubMed: 17324960].

  • 31.

    Lauretti L, Riccio ML, Mazzariol A, Cornaglia G, Amicosante G, Fontana R, et al. Cloning and characterization of blaVIM, a new integron-borne metallo-beta-lactamase gene from a Pseudomonas aeruginosa clinical isolate. Antimicrob Agents Chemother. 1999;43(7):1584-90. doi: 10.1128/AAC.43.7.1584. [PubMed: 10390207]. [PubMed Central: PMC89328].

  • 32.

    Tsakris A, Pournaras S, Woodford N, Palepou MF, Babini GS, Douboyas J, et al. Outbreak of infections caused by Pseudomonas aeruginosa producing VIM-1 carbapenemase in Greece. J Clin Microbiol. 2000;38(3):1290-2. doi: 10.1128/JCM.38.3.1290-1292.2000. [PubMed: 10699045]. [PubMed Central: PMC88610].

  • 33.

    Yong D, Toleman MA, Giske CG, Cho HS, Sundman K, Lee K, et al. Characterization of a new metallo-beta-lactamase gene, bla(NDM-1), and a novel erythromycin esterase gene carried on a unique genetic structure in Klebsiella pneumoniae sequence type 14 from India. Antimicrob Agents Chemother. 2009;53(12):5046-54. doi: 10.1128/AAC.00774-09. [PubMed: 19770275]. [PubMed Central: PMC2786356].

  • 34.

    Wayne PA. Clinical and Laboratory Standards Institute: Performance standards for antimicrobial susceptibility testing: 27th informational supplement. CLSI document M100-S20. 2017.

  • 35.

    Litake GM, Ghole VS, Niphadkar KB, Joshi SG. Phenotypic ESBL Detection in Acinetobacter baumannii: A Real Challenge. Am J Infect Dis. 2015;11(3):48-53. doi: 10.3844/ajidsp.2015.48.53.

  • 36.

    Woodford N, Ellington MJ, Coelho JM, Turton JF, Ward ME, Brown S, et al. Multiplex PCR for genes encoding prevalent OXA carbapenemases in Acinetobacter spp. Int J Antimicrob Agents. 2006;27(4):351-3. doi: 10.1016/j.ijantimicag.2006.01.004. [PubMed: 16564159].

  • 37.

    Aruhomukama D, Najjuka CF, Kajumbula H, Okee M, Mboowa G, Sserwadda I, et al. blaVIM- and blaOXA-mediated carbapenem resistance among Acinetobacter baumannii and Pseudomonas aeruginosa isolates from the Mulago hospital intensive care unit in Kampala, Uganda. BMC Infect Dis. 2019;19(1):853. doi: 10.1186/s12879-019-4510-5. [PubMed: 31619192]. [PubMed Central: PMC6794873].

  • 38.

    Huang ZY, Li J, Shui J, Wang HC, Hu YM, Zou MX. Co-existence of blaOXA-23 and blaVIM in carbapenem-resistant Acinetobacter baumannii isolates belonging to global complex 2 in a Chinese teaching hospital. Chin Med J (Engl). 2019;132(10):1166-72. doi: 10.1097/CM9.0000000000000193. [PubMed: 30882466]. [PubMed Central: PMC6511418].

  • 39.

    Song W, Lee H, Lee K, Jeong SH, Bae IK, Kim JS, et al. CTX-M-14 and CTX-M-15 enzymes are the dominant type of extended-spectrum beta-lactamase in clinical isolates of Escherichia coli from Korea. J Med Microbiol. 2009;58(Pt 2):261-6. doi: 10.1099/jmm.0.004507-0. [PubMed: 19141747]. [PubMed Central: PMC2884940].

  • 40.

    Mirsalehian A, Feizabadi M, Nakhjavani FA, Jabalameli F, Goli H, Kalantari N. Detection of VEB-1, OXA-10 and PER-1 genotypes in extended-spectrum beta-lactamase-producing Pseudomonas aeruginosa strains isolated from burn patients. Burns. 2010;36(1):70-4. doi: 10.1016/j.burns.2009.01.015. [PubMed: 19524369].

  • 41.

    Edelstein M, Pimkin M, Palagin I, Edelstein I, Stratchounski L. Prevalence and molecular epidemiology of CTX-M extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae in Russian hospitals. Antimicrob Agents Chemother. 2003;47(12):3724-32. doi: 10.1128/AAC.47.12.3724-3732.2003. [PubMed: 14638473]. [PubMed Central: PMC296190].

  • 42.

    Hujer KM, Hujer AM, Hulten EA, Bajaksouzian S, Adams JM, Donskey CJ, et al. Analysis of antibiotic resistance genes in multidrug-resistant Acinetobacter sp. isolates from military and civilian patients treated at the Walter Reed Army Medical Center. Antimicrob Agents Chemother. 2006;50(12):4114-23. doi: 10.1128/AAC.00778-06. [PubMed: 17000742]. [PubMed Central: PMC1694013].

  • 43.

    Sanders CC. Chromosomal cephalosporinases responsible for multiple resistance to newer beta-lactam antibiotics. Annu Rev Microbiol. 1987;41:573-93. doi: 10.1146/annurev.mi.41.100187.003041. [PubMed: 3318679].

  • 44.

    Paterson DL, Ko WC, Von Gottberg A, Casellas JM, Mulazimoglu L, Klugman KP, et al. Outcome of cephalosporin treatment for serious infections due to apparently susceptible organisms producing extended-spectrum beta-lactamases: implications for the clinical microbiology laboratory. J Clin Microbiol. 2001;39(6):2206-12. doi: 10.1128/JCM.39.6.2206-2212.2001. [PubMed: 11376058]. [PubMed Central: PMC88112].

  • 45.

    Nazari Monazam A, Hosseini Doust SR, Mirnejad R. [Prevalence PER and VEB beta-lactamase Genes among Acinetobacter baumannii Isolated from Patients in Tehran by PCR]. Iran J Med Microbiol. 2015;8(4):28-35. Persian.

  • 46.

    Constantiniu S, Romaniuc A, Chiriac R, Berea C, Kalis O, Rezus E, et al. Antibacterial antibodies for some enterobacteria in sera of patients with reactive arthritis and other rheumatoid diseases. Roum Arch Microbiol Immunol. 2008;67(1-2):30-5.

  • 47.

    Rit K, Saha R. Multidrug-resistant acinetobacter infection and their susceptibility patterns in a tertiary care hospital. Niger Med J. 2012;53(3):126-8. doi: 10.4103/0300-1652.104379. [PubMed: 23293410]. [PubMed Central: PMC3531029].

  • 48.

    Ahmadikiya F, Mosadegh A, Moradi M, Hossieni-Nave H. [Antimicrobial ResistancePatterns and Frequency of Extended-SpectrumBeta-Lactamase Genes among Acinetobacter Baumannii]. J Babol Univ Med Sci. 2017;19(7):28-34. Persian.

  • 49.

    Ayan M, Durmaz R, Aktas E, Durmaz B. Bacteriological, clinical and epidemiological characteristics of hospital-acquired Acinetobacter baumannii infection in a teaching hospital. J Hosp Infect. 2003;54(1):39-45. doi: 10.1016/s0195-6701(03)00076-8. [PubMed: 12767845].

  • 50.

    Biendo M, Laurans G, Lefebvre JF, Daoudi F, Eb F. Epidemiological study of an Acinetobacter baumannii outbreak by using a combination of antibiotyping and ribotyping. J Clin Microbiol. 1999;37(7):2170-5. doi: 10.1128/JCM.37.7.2170-2175.1999. [PubMed: 10364581]. [PubMed Central: PMC85111].

  • 51.

    Smolyakov R, Borer A, Riesenberg K, Schlaeffer F, Alkan M, Porath A, et al. Nosocomial multi-drug resistant Acinetobacter baumannii bloodstream infection: risk factors and outcome with ampicillin-sulbactam treatment. J Hosp Infect. 2003;54(1):32-8. doi: 10.1016/s0195-6701(03)00046-x. [PubMed: 12767844].

  • 52.

    Wang SH, Sheng WH, Chang YY, Wang LH, Lin HC, Chen ML, et al. Healthcare-associated outbreak due to pan-drug resistant Acinetobacter baumannii in a surgical intensive care unit. J Hosp Infect. 2003;53(2):97-102. doi: 10.1053/jhin.2002.1348. [PubMed: 12586567].

  • 53.

    Saadatian Farivar A, Nowroozi J, Emami M. The Prevalence of Acinetobacter in Sergical ICU in Rasoul Akram Hospital in 2004-2005. J Rafsanjan Univ Med Sci. 2005;4(4):342-7.

  • 54.

    Sepahvand V, Davarpanah MA, Hejazi SH. Epidemiology of colistin-resistant Acinetobacter baumannii in Shiraz, Iran. J Appl Environ Biol Sci. 2015;5(5):45-8.

  • 55.

    Joshi SG, Litake GM, Ghole VS, Niphadkar KB. Plasmid-borne extended-spectrum beta-lactamase in a clinical isolate of Acinetobacter baumannii. J Med Microbiol. 2003;52(Pt 12):1125-7. doi: 10.1099/0022-1317-52-12-1125. [PubMed: 14614072].

  • 56.

    Bahador A, Taheri M, Pourakbari B, Hashemizadeh Z, Rostami H, Mansoori N, et al. Emergence of rifampicin, tigecycline, and colistin-resistant Acinetobacter baumannii in Iran; spreading of MDR strains of novel International Clone variants. Microb Drug Resist. 2013;19(5):397-406. doi: 10.1089/mdr.2012.0233. [PubMed: 23768166].

  • 57.

    Sinha M, Srinivasa H, Macaden R. Antibiotic resistance profile & extended spectrum beta-lactamase (ESBL) production in Acinetobacter species. Indian J Med Res. 2007;126(1):63-7. [PubMed: 17890826].

  • 58.

    Maleki MH, Sekawi Z, Soroush S, Azizi-Jalilian F, Asadollahi K, Mohammadi S, et al. Phenotypic and genotypic characteristics of tetracycline resistant Acinetobacter baumannii isolates from nosocomial infections at Tehran hospitals. Iran J Basic Med Sci. 2014;17(1):21-6. [PubMed: 24592303]. [PubMed Central: PMC3938882].

  • 59.

    Ranjbar R, Farahani A. Study of genetic diversity, biofilm formation, and detection of Carbapenemase, MBL, ESBL, and tetracycline resistance genes in multidrug-resistant Acinetobacter baumannii isolated from burn wound infections in Iran. Antimicrob Resist Infect Control. 2019;8:172. doi: 10.1186/s13756-019-0612-5. [PubMed: 31719975]. [PubMed Central: PMC6836547].

  • 60.

    Shahcheraghi F, Akbari Shahmirzadi N, Jabbari H, Amirmozafari N. [Detection of blaCTX, blaTEMbeta-lactamase genes in clinical isolates of Acinetobacterspp. from selected Tehran hospitals]. Iran J Med Microbiol. 2009;3(1):1-9. Persian.

  • 61.

    Celenza G, Pellegrini C, Caccamo M, Segatore B, Amicosante G, Perilli M. Spread of bla(CTX-M-type) and bla(PER-2) beta-lactamase genes in clinical isolates from Bolivian hospitals. J Antimicrob Chemother. 2006;57(5):975-8. doi: 10.1093/jac/dkl055. [PubMed: 16510850].

  • 62.

    Safari M, Mozaffari Nejad AS, Bahador A, Jafari R, Alikhani MY. Prevalence of ESBL and MBL encoding genes in Acinetobacter baumannii strains isolated from patients of intensive care units (ICU). Saudi J Biol Sci. 2015;22(4):424-9. doi: 10.1016/j.sjbs.2015.01.004. [PubMed: 26150748]. [PubMed Central: PMC4486466].

  • 63.

    Goudarzi H, Hashemi A, Fatemeh F, Noori M, Erfanimanesh S, Yosefi N, et al. [Detection of blaDIM, blaAIM, blaGIM, blaNDM and blaVIM Genes among Acinetobacter baumannii strains isolated from hospitalized patients in Tehran hospitals, Iran]. Iran J Med Microbiol. 2016;9(4):32-9. Persian.

  • 64.

    Mohammadi M, Bahrami N, Faghri J. [The evaluation of antibiotic resistance pattern and frequency of blaVIM and blaNDM genes in isolated Acinetobacter baumannii from hospitalized patients in Isfahan and Shahrekord]. Razi J Med Sci. 2020;27(4):143-56. Persian.

  • 65.

    Azizi O, Shahcheraghi F. [The Frequency of blaPER, blaVEB, blaCTX-M, tetA and tetB genes among Acinetobacter baumannii strains isolated from hospitalizes patients in Tehran]. J Torbat Heydariyeh Univ Med Sci. 2017;5(3):17-25. Persian.

  • 66.

    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(8):1198-203. doi: 10.1016/j.burns.2012.04.008. [PubMed: 22579564].

  • 67.

    Turton JF, Ward ME, Woodford N, Kaufmann ME, Pike R, Livermore DM, et al. The role of ISAba1 in expression of OXA carbapenemase genes in Acinetobacter baumannii. FEMS Microbiol Lett. 2006;258(1):72-7. doi: 10.1111/j.1574-6968.2006.00195.x. [PubMed: 16630258].

  • 68.

    Badmasti F, Siadat SD, Bouzari S, Ajdary S, Shahcheraghi F. Molecular detection of genes related to biofilm formation in multidrug-resistant Acinetobacter baumannii isolated from clinical settings. J Med Microbiol. 2015;64(Pt 5):559-64. doi: 10.1099/jmm.0.000058. [PubMed: 25813817].

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