IF: 0.957
Cite Score:
1.46
THOMSON REUTERS - SCOPUS

Prevalence of Extended-Spectrum β-Lactamases and Antibiotic Resistance Patterns in Acinetobacter baumannii Isolated from Clinical Samples in Kermanshah, Iran

AUTHORS

Mohsen Azizi 1 , Seyed Hamidreza Mortazavi 2 , Misagh Etemadimajed 3 , Simin Gheini 4 , Siavash Vaziri 5 , Amirhooshang Alvandi 6 , Mahsa Kashef 1 , Kamal Ahmadi ORCID 1 , *

AUTHORS INFORMATION

1 Research Assistant, MSc in Medical Microbiology, Kermanshah University of Medical Sciences, Kermanshah, Iran

2 Pediatric Immunologist and Allergist, Assistant Professor of Kermanshah University of Medical Sciences, Kermanshah, Iran

3 Students Research Committee, Kermanshah University of Medical Sciences, Kermanshah, Iran

4 Pediatrician, Assistant Professor of Kermanshah University of Medical Sciences, Kermanshah, Iran

5 Associate Professor of Infection Disease, Kermanshah University of Medical Sciences, Kermanshah, Iran

6 Associate Professor, Department of Medical Microbiology, Kermanshah University of Medical Sciences, Kermanshah, Iran

ARTICLE INFORMATION

Jundishapur Journal of Microbiology: 10 (12); e61522
Published Online: November 21, 2017
Article Type: Research Article
Received: April 8, 2017
Revised: September 10, 2017
Accepted: September 26, 2017
Crossmark

Crossmark

CHEKING

READ FULL TEXT
Abstract

Background: Acinetobacter is an opportunistic bacterial pathogen with intrinsic and acquired resistance to many antibiotics.

Objectives: This study aimed to determine the prevalence of extended-spectrum β-lactamases (ESBLs) and antibiotic resistance patterns in A. baumannii isolated from clinical samples at Imam Reza hospital in Kermanshah, Iran, using phenotypic and genotypic methods.

Methods: In this descriptive-analytical study, 80 Acinetobacter isolates obtained from clinical samples were confirmed using standard biochemical tests. After antibiotic susceptibility testing using disk diffusion method, the presence of ESBLs was detected using the combined disk test (CDT). The Polymerase chain reaction (PCR) method was employed to identify the frequency of blaTEM, blaCTX-M, and blaSHV genes using their specific primers.

Results: Among the A. baumannii isolates, 62.5% showed multidrug resistance (MDR). The highest rate of antibiotic resistance was to ceftriaxone (100%), followed by amikacin (96.2%), and the lowest was to polymyxin B (13.8%) and ampicillin/sulbactam (52.8%). Forty-three (53.8%) ESBL-producing isolates expressing SHV (n = 18, 41.9%), TEM (n = 11, 25.6%), and CTX-M (n = 3, 7%) genes were identified.

Conclusions: This study revealed an increased prevalence of ESBL-encoding genes in A. baumannii isolates. The increased frequency of these genes may be due to overuse or inappropriate use of antibiotics in this region. To combat overuse and prevent further development of drug resistance in Kermanshah, Iran, more attention should be paid to prescribing practices for various antibiotics, including cephalosporins.

Keywords

Extended-Spectrum Beta-Lactamase (ESBL) Antibiotic Resistance Multidrug Resistance Acinetobacter baumannii

Copyright © 2017, Jundishapur Journal of Microbiology. This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International License (http://creativecommons.org/licenses/by-nc/4.0/) which permits copy and redistribute the material just in noncommercial usages, provided the original work is properly cited.
1. Background

Acinetobacter is a Gram-negative, polymorphic, nonmotile, strictly aerobic bacterium, which can be easily grown in a conventional laboratory environment (1). Different species of Acinetobacter cause urinary tract infections, wound infections, meningitis, endocarditis, peritonitis, and dermal and soft tissue infections (2). This opportunistic bacterium can survive on various surfaces, including patient’s skin and used medical equipment. Thus, prolonged hospitalization in the intensive care unit, severe disease, immune system deficiency, burn injuries, long-term use of antimicrobial agents, and catheter use are risk factors for Acinetobacter infection (3).

Acinetobacter baumannii is more prevalent than other strains of Acinetobacter, and it is the most common cause of bacterium-induced infections. To treat infections caused by Acinetobacter, various antibiotics, including β-lactams, fluoroquinolones, and aminoglycosides, are used; however, inappropriate and indiscriminate use of these antibiotics in recent years has led to the emergence of strains that are highly resistant to antimicrobial agents (4). Such resistance can be innate or caused by genetic resistance factors (5). Multidrug resistance (MDR) of Acinetobacter has been reported (6). The production of β-lactamase enzymes is a major mechanism of antimicrobial resistance and a major problem in the treatment of various infectious diseases. These enzymes can disable β-lactam antibiotics by hydrolysis of the central core of the antibiotics. Of various β-lactamases, ESBLs have greater functions (7). The vast majority of ESBLs are the result of mutations in CTX-M, SHV (sulphydryl variable), and TEM (Temoneira) genes (8).

With the increase in drug resistance, ESBLs limit the choice of common antibiotics that can be used. Drug resistance can be caused by the transfer of resistant genes carried on plasmids and simultaneous transfer of other antibiotic-resistance genes (9). In some cases, due to high resistance to common antibiotics, ESBL-producing bacteria can lead to mortality by disrupting the treatment of infectious diseases (10). Given the high prevalence of hospital infections, studies on the causative microorganisms, including their antibiotic resistance patterns, are of paramount importance.

2. Objectives

There are no recent comprehensive studies in Kermanshah on the prevalence of CTX-M, TEM, and SHV genes in A. baumannii. Thus, the aim of the present study was to determine the prevalence of extended-spectrum β-lactamases (ESBLs) and antibiotic resistance patterns in A. baumannii isolated from clinical samples at Imam Reza hospital in Kermanshah, Iran, using phenotypic and genotypic methods.

3. Methods
3.1. Ethics Statement

The ethics committee of Kermanshah University of Medical Sciences approved the study protocol (No.: 1394.250).

3.2. Bacterial Isolates and Identification

In this descriptive cross-sectional study, 385 clinical samples were collected from different sources (endotracheal tubes, blood, sputum, urine, catheters, wounds, and various liquids) at Imam Reza hospital in Kermanshah from January 2016 to November 2016. Following collection, the samples were transported to the laboratory, cultured on blood agar and Mac Conkey agar (Merck, Germany), and then incubated for 24 hours at 37°C. In total, 80 isolates of A. baumannii were identified and confirmed using standard biochemical tests, including growth on citrate media and nonfermentable lactose, oxidase and catalase activity, immobility on SIM medium, ALK/ALK patterns on TSI medium (Himedia CO, India), and lack of pigment production. The PCR method using OXA-51 gene was used for final confirmation of the Acinetobacter isolates (11).

3.3. Antibiotic Susceptibility Testing

The antibiotic resistance of the isolates was determined using Kirby–Bauer disk diffusion method, according to the guidelines of the clinical and laboratory standards institute (CLSI) (12). To this end, 14 antibiotic discs (MAST, U.K.) were used: gentamicin (10 µg), amikacin (30 µg), tobramycin (10 µg), imipenem (10 µg), meropenem (10 µg), ceftazidime (30 µg), cefotaxime (30 µg), ceftriaxone (30 µg), ciprofloxacin (5 µg), levofloxacin (5 µg), piperacillin/tazobactam (10/100 µg), ticarcillin/clavulanic acid (10/75 µg), ampicillin/sulbactam (20 µg), and polymyxine B (300 µg). The A. baumannii suspension was spread on Mueller-Hinton agar medium (Himedia CO, India) after incubation at 37°C and compared with a 0.5 McFarland standard using the lawn culture method. The disks were then placed on them. After incubation in an incubator for 24 hours, the growth inhibition diameter was measured and compared with that listed in CLSI tables. Escherichia coli ATCC 25922 was used for quality control of the reaction. Acinetobacter isolates showing resistance to three or more antibiotic strains were regarded as MDR strains.

3.4. Amplification of blaTEM, blaSHV, and blaCTX-M Genes by the PCR Method

To identify ESBL-producing isolates, the combined disk method was used. First, a standard concentration of A. baumannii was lawn cultured on Mueller-Hinton medium. Then, discs containing ceftazidime, ceftazidime/clavulanic acid, cefotaxime, and cefotaxime/clavulanic acid were placed 15 mm away from each other on the plates. After incubation for 24 hours at 37°C, the zone of inhibition around the disk containing clavulanic acid only was compared to that of the same ESBL disk as the enzyme inhibitor was measured. If the zone of inhibition around the disk containing clavulanic acid was greater than or equal to 5 mm as compared to that of the same disk without clavulanic acid, the strain was considered an ESBL-producing strain in accordance with CLSI guidelines. A standard Escherichia coli strain, ATCC 25922, was used as positive control. For PCR, DNA was extracted from the isolates using boiling method, and the frequencies of SHV, TEM, and CTX-M genes were investigated using specific primers (Takapou Zist Co., Iran), as shown in Table 1 (13, 14).

Table 1. The Nucleotide Sequence of Primers Used in the Detection of ESBL-Producing A. Baumannii
GeneNucleotide Sequence (5’ - 3’)Annealing, °CProduct Size, bp
blaSHV5’-CTTTACTCGCTTTATCG-3’53868
5’-TCCCGCAGATAAATCAC-3’
blaTEM5’-GAGTATTCAACATTTCCGTGTC-3’45800
5’-TAATCAGTGAGGCACCTATCTC-3’
blaCTX-M5’-ATGTGCAGTACCAGTAAGGT-3’53594
5’-TGGGTAAAGTAGGTCACCAGA -3’
3.5. PCR Assay

The PCR assay was conducted using 12.5 mL Master Mix (SinaClon Company, Iran), 1 µg of each primer, 3 µg bacterial DNA, and distilled water to obtain a final volume of 25 mL. Except for the annealing temperature, the PCR reaction temperature was the same for all the three β-lactamase genes. It consisted of initial denaturation for 4 minutes at 94°C, followed by 35 cycles of denaturation for 1 minute at 94°C, amplification at 72°C for 40 seconds, and final amplification at 72°C for 5 minutes (Table 1). Finally, the PCR products were examined using electrophoresis and staining with ethidium bromide.

3.6. Statistical Analysis

Chi-square and Fisher’s tests were conducted. All statistical analyses were performed using statistical package for the social sciences (SPSS), version 20.

4. Results

In the 385 clinical samples examined in this study, 80 (20.8%) isolates of A. baumannii were detected. In the study, 43 (53.8%) samples were obtained from males, and 37 (46.2%) from females, with a mean age of 48.38 ± 14.7, ranging from 19 to 82 years. Majority of the isolates were detected in respiratory samples (n = 40, 50%). The lowest detection frequency was in cerebrospinal fluid and pleural fluid (n = 4, 5%) (Figure 1).

The Frequency of ESBL-Producing Isolates of A. Baumannii Isolated from Clinical Specimens Examined
Figure 1. The Frequency of ESBL-Producing Isolates of A. Baumannii Isolated from Clinical Specimens Examined

As shown by the antibiotic resistance patterns of A. baumannii given in Table 2, the highest resistance was observed against ceftriaxone (100%) and amikacin (96.2%), whereas the lowest resistance was against polymyxin B (13.8%) and ampicillin/sulbactam (52.8%). Among the isolates, 50 (62.5%) showed MDR against the antibiotics tested. Based on the results of the confirmatory combined-disk test, 43 (53.8%) of the 80 A. baumannii isolates showed ESBL production. The frequency of ESBL genes in the clinical samples is shown in Figure 1. ESBL genes were not significantly correlated with the age and gender of the patients (P > 0.05).

Table 2. Results of Antibiotic Resistance of A. Baumannii Strains Isolated from Clinical Specimensa
AntibioticA. Baumannii Isolated
ResistantIntermediateSusceptible
Ceftazidime76 (95)04 (5)
Ceftriaxone80 (100)00
Cefotaxime73 (91.2)1 (1.2)6 (7.5)
Ciprofloxacin64 (80)4 (5)12 (15)
Levofloxacin57 (71.2)10 (12.5)13 (16.2)
Gentamicin63 (78.8)2 (2.5)15 (18.8)
Amikacin77 (96.2)03 (3.8)
Tobramycin54 (67.5)4 (5)22 (27.5)
Imipenem68 (85)2 (2.5)10 (12.5)
Meropenem64 (80)2 (2.5)14 (17.5)
Ampicillin/sulbactam42 (52.5)13 (16.2)25 (31.2)
Piperacillin/tazobactam58 (72.5)3 (3.8)19 (23.8)
Ticarcillin/clavulanic acid55 (68.8)5 (6.2)20 (25)
Polymyxin B11 (13.8)6 (7.5)63 (78.8)

aValues are expressed as No. (%).

18 (41.9%), 11 (25.6%), and 3 (7%) ESBL-producing isolates expressed SHV, TEM, and CTX-M β-lactamase genes, respectively. The frequency of ESBL genes in the MDR Acinetobacter isolates according to the type of clinical sample is shown in Table 3. There was a statistically significant association between ESBL genes and resistance to some antibiotics. For example, there was a significant relationship between the expression of SHV gene and resistance to cefotaxime (P = 0.038) and tobramycin (P = 0.002). In addition, the expression of TEM gene was associated with resistance to piperacillin/tazobactam (P = 0.021), and the expression of CTX-M gene was associated with resistance to levofloxacin (P = 0.05). The results of PCR assay are given in Figure 2.

Table 3. The Frequency of ESBL Genes in the MDR Isolates of A. Baumannii
VariablesTrachealUrineBloodSputumCatheterWoundCSFPleural FluidTotal
MDR19966541050
SHV8140110015
TEM6120100010
CTX-M000010001
Figure 2. Gel Electrophoresis of PCR Products of ESBL
Gel Electrophoresis of PCR Products of ESBL

TEM, 1- Lader (100 bp), 2- Negative control, 3- Positive control (800 bp), 4, 5- Positive sample (800 bp); SHV, 1- Lader (100 bp), 2-Positive control (867 bp), 3- Negative control, 4 - 6- Positive sample (867 bp); CTX-M, 1- Lader (100 bp), 2- Negative control, 3- Positive control (594 bp), 4- Positive sample (594 bp).

5. Discussion

In this study, similar to studies by Farajnia in Tabriz, Iran, and Sinha in India, the majority of isolates of A. baumannii were detected in respiratory samples (15, 16). In contrast, in a study by Vazirzadeh et al., isolates were more commonly obtained from catheter samples (17). Various factors, including consumption of antibiotics, clonal spread of resistant microorganisms, and drug resistance mechanisms of different species, result in the dissemination of highly resistant pathogens to commonly used antibiotics. Previous research reported increased resistance of A. baumannii to various antibiotics and MDR strains hampered the recovery of patients by lowering the efficacy of many common antibiotics (18). The frequency of A. baumannii isolates detected in the present study (62.5%) was in line with that reported by Mirnejad et al., who found that the prevalence of MDR A. baumannii isolates ranged from 32.7% to 93% (19).

In the current study, the highest rate of antibiotic resistance was observed against ceftriaxone (100%), amikacin (96.2%), ceftazidime (95%), and cefotaxime (91.2%), and the highest rate of antibiotic susceptibility was observed against polymyxin B (13.8%). Furthermore, 95.4% of the A. baumannii isolates were resistant to various cephalosporins. This finding is consistent with the results of other studies, which reported that 60% - 100% of A. baumannii isolates were resistant to this class of drugs (19-22). In a study by Kheltabadi et al., only 20% of isolates were resistant to ampicillin/sulbactam (20). In contrast, in the present study, 52.5% of the isolates showed resistance to ampicillin/sulbactam. Due to its ability to inhibit β-lactamases, ampicillin/sulbactam is generally used to treat respiratory and urinary infections. The discord in the findings may be due to differences in the pattern of consumption of antibiotics in this area, as well as increased Acinetobacter resistance to ampicillin/sulbactam.

Carbapenems are one of the most commonly used antibiotics to treat bacterial infections. Hujer et al. reported that only 25% and 20% of A. baumannii isolates were resistant to the carbapenems meropenem and imipenem, respectively (23). However, recent reports pointed to the increased A. baumannii resistance to carbapenems (17, 21, 22), in common with the observations in the present study.

Among various drug resistance-inducing mechanisms, ESBLs play an important role in resistance to commonly used antibiotics, such as penicillin and cephalosporins. Due to the widespread dissemination among nosocomial pathogens via plasmids and integrons, ESBL genes can cause further expansion of drug resistance, including MDR isolates (14, 24). Various studies have reported frequencies of ESBL genes in A. baumannii ranging from 25% to 93.45% (25-28). In the present study, among the 80 examined isolates of A. baumannii, 53.8% were ESBL producers, which is consistent with the results of previous studies. Among the study genes, SHV (41.9%) was the most frequent, followed by TEM (25.6%). Similarly, Safari et al. reported that SHV (58%) and TEM (20%) were the most frequent ESBL genes detected in their study (14). In a study conducted in Iraq, Azhar et al. reported that SHV (25%) was the most frequently detected ESBL gene (29).

In line with the findings of the present research, another study also found that the prevalence of SHV gene was higher in A. baumannii isolates (30). Khalilzadegan et al. reported that CTX-M (19.4%) and TEM (3.2%) were the most frequently detected ESBL genes (21). On the contrary, in the present study, the most frequent gene was SHV. SHV gene is originated from Klebsiella pneumoniae (31). A high frequency of K. pneumoniae bearing SHV gene could likely explain the increased spread and diffusion of SHV gene in bacterial isolates, especially A. baumannii in hospital settings in Kermanshah (32). Various factors can explain the discord in reports on the frequencies of ESBL-producing isolates. These include differences in patterns, especially overuse and misuse, of the consumption of antibiotics; differences in the types of antibiotics used; prolonged hospital stays; use of invasive techniques in diagnoses; and differences in diagnostic methods used to identify genes (33).

6. Conclusion

In this study, A. baumannii isolates exhibited high levels of resistance against the study antibiotics, and a high percentage of the isolates showed MDR. At present, polymyxine B appears to be the only effective antibiotic in the treatment of infections induced by A. baumannii. The frequency of ESBL-encoding genes in A. baumannii isolates may be due to overuse and inappropriate use of antibiotics in the region. To combat overuse and prevent further development of drug resistance in Kermanshah, Iran, more attention should be paid to prescribing practices for various antibiotics, including cephalosporins.

Acknowledgements
Footnotes
References
1 Dent LL, Marshall DR, Pratap S, Hulette RB. Multidrug resistant Acinetobacter baumannii: a descriptive study in a city hospital. BMC Infect Dis. 2010; 10: 196[DOI][ PubMed ]
2 Jeon BC, Jeong SH, Bae IK, Kwon SB, Lee K, Young D, et al. Investigation of a nosocomial outbreak of imipenem-resistant Acinetobacter baumannii producing the OXA-23 beta-lactamase in korea. J Clin Microbiol. 2005; 43(5): 2241-5[DOI][ PubMed ]
3 Ellis D, Cohen B, Liu J, Larson E. Risk factors for hospital-acquired antimicrobial-resistant infection caused by Acinetobacter baumannii. Antimicrob Resist Infect Control. 2015; 4: 40[DOI][ PubMed ]
4 Michalopoulos A, Falagas ME. Treatment of Acinetobacter infections. Expert Opin Pharmacother. 2010; 11(5): 779-88[DOI][ PubMed ]
5 Fournier PE, Richet H. The epidemiology and control of Acinetobacter baumannii in health care facilities. Clin Infect Dis. 2006; 42(5): 692-9[DOI][ PubMed ]
6 Izadpour F, Ranjbari N, Aramesh MR, Moosavian M, ShahAli S, Larki F, et al. An Investigation of Antibacterial Resistance Patterns Among Acinetobacter baumannii and Pseudomonas aeruginosa Isolates Collected from Intensive Care Units of a University-Affiliated Hospital in Ahvaz, Iran. Jundishapur J Microbiol. 2016; 9(8)[DOI][ PubMed ]
7 Zamani K, Emami A, Bazargani A, Moattari A. Phenotypic and molecular characterization of CTX-M extended-spectrum beta-lactamase-producing Escherichia coli isolates in Shiraz, Iran. Rev Soc Bras Med Trop. 2015; 48(4): 479-82[DOI][ PubMed ]
8 Oteo J, Perez-Vazquez M, Campos J. Extended-spectrum [beta]-lactamase producing Escherichia coli: changing epidemiology and clinical impact. Curr Opin Infect Dis. 2010; 23(4): 320-6[DOI][ PubMed ]
9 Paterson DL. Recommendation for treatment of severe infections caused by Enterobacteriaceae producing extended-spectrum beta-lactamases (ESBLs). Clin Microbiol Infect. 2000; 6(9): 460-3[ PubMed ]
10 Rawat D, Nair D. Extended-spectrum beta-lactamases in Gram Negative Bacteria. J Glob Infect Dis. 2010; 2(3): 263-74[DOI][ PubMed ]
11 Turton JF, Woodford N, Glover J, Yarde S, Kaufmann ME, Pitt TL. Identification of Acinetobacter baumannii by detection of the blaOXA-51-like carbapenemase gene intrinsic to this species. J Clin Microbiol. 2006; 44(8): 2974-6[DOI][ PubMed ]
12 Clinical and Laboratory Standards Institute . Performance standards for antimicrobial susceptibility testing; Twenty-fourth informational supplement (M100 S24). 2014;
13 Ahanjan M, Kholdi S, Rafiei A. Antibiotic-resistance patterns and frequency of TEM and CTX type extended-spectrum β-lactamases in acinetobacter clinical isolates [In Persian]. J Mazandaran Univ Med Sci. 2014; 24(116): 32-40
14 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][ PubMed ]
15 Farajnia S, Azhari F, Alikhani MY, Hosseini MK, Peymani A, Sohrabi N. Prevalence of PER and VEB Type Extended Spectrum Betalactamases among Multidrug Resistant Acinetobacter baumannii Isolates in North-West of Iran. Iran J Basic Med Sci. 2013; 16(6): 751-5[ PubMed ]
16 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 ]
17 Vazirzadeh J, Ghajavand H, Heidari L, Behshood P. Prevalence of extended spectrum beta lactamases (ESBLs) and antibiotic resistance pattern acinetobacter baumannii strains isolated from clinical specimens in Isfahan City, Iran [In Persian]. Med Lab J. 2015; 9(3): 32-9
18 Agodi A, Barchitta M, Quattrocchi A, Maugeri A, Aldisio E, Marchese AE, et al. Antibiotic trends of Klebsiella pneumoniae and Acinetobacter baumannii resistance indicators in an intensive care unit of Southern Italy, 2008-2013. Antimicrob Resist Infect Control. 2015; 4: 43[DOI][ PubMed ]
19 Mirnejad R, Vafaei S. Antibiotic resistance patterns and the prevalence of ESBLs among strains of Acinetobacter baumannii isolated from clinical specimens. J Gen Microbes Immunity. 2013; 2013: 1-8[DOI]
20 Kheltabadi RF, Moniri R, Shajari GR, Nazem Shirazi MH, Musavi SGA, Ghasemi A, et al. Antimicrobial susceptibility patterns and the distribution of resistance genes among acinetobacter species isolated from patients in shahid Beheshti hospital, Kashan. Feyz J Kashan Univ Med Sci. 2009; 12(4)
21 Khalilzadegan S, Sade M, Godarzi H, Eslami G, Hallajzade M, Fallah F, et al. Beta-Lactamase Encoded Genes blaTEM and blaCTX Among Acinetobacter baumannii Species Isolated From Medical Devices of Intensive Care Units in Tehran Hospitals. Jundishapur J Microbiol. 2016; 9(5)[DOI][ PubMed ]
22 Shakibaie MR, Adeli S, Salehi MH. Antibiotic resistance patterns and extended-spectrum beta-lactamase production among Acinetobacter spp. isolated from an intensive care Unit of a hospital in Kerman, Iran. Antimicrob Resist Infect Control. 2012; 1(1): 1[DOI][ PubMed ]
23 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][ PubMed ]
24 Ribera A, Vila J, Fernandez-Cuenca F, Martinez-Martinez L, Pascual A, Beceiro A, et al. Type 1 integrons in epidemiologically unrelated Acinetobacter baumannii isolates collected at Spanish hospitals. Antimicrob Agents Chemother. 2004; 48(1): 364-5[DOI][ PubMed ]
25 Gupta V, Garg R, Garg S, Chander J, Attri AK. Coexistence of Extended Spectrum Beta-Lactamases, AmpC Beta-Lactamases and Metallo-Beta-Lactamases in Acinetobacter baumannii from burns patients: a report from a tertiary care centre of India. Ann Burns Fire Disasters. 2013; 26(4): 189-92[ PubMed ]
26 Shrivastava G, Bajpai T, Bhatambare GS, Patel KB. Sensitivity profile of multidrug resistant Acinetobacter Spp. isolated at ICUs of tertiary care hospital. Int J Health Sys Disaster Manag. 2013; 1(4): 200[DOI]
27 Banerjee M, Chaudhary B, Shukla S. Prevalence of ESBL and MBL in acinetobacter species isolated from clinical samples in tertiary care hospital. Int J Sci Res. 2015; 4(6): 1183-6
28 Alyamani EJ, Khiyami MA, Booq RY, Alnafjan BM, Altammami MA, Bahwerth FS. Molecular characterization of extended-spectrum beta-lactamases (ESBLs) produced by clinical isolates of Acinetobacter baumannii in Saudi Arabia. Ann Clin Microbiol Antimicrob. 2015; 14: 38[DOI][ PubMed ]
29 AL-Thahab AA. Molecular detection of extended-spectrum beta-lactamases in clinical isolates of Acinetobacter baumannii. J Biol Agric Healthc. 2013; 3(7): 32-9
30 Huang ZM, Mao PH, Chen Y, Wu L, Wu J. [Study on the molecular epidemiology of SHV type beta-lactamase-encoding genes of multiple-drug-resistant acinetobacter baumannii]. Zhonghua Liu Xing Bing Xue Za Zhi. 2004; 25(5): 425-7[ PubMed ]
31 Jain A, Mondal R. TEM & SHV genes in extended spectrum beta-lactamase producing Klebsiella species beta their antimicrobial resistance pattern. Indian J Med Res. 2008; 128(6): 759-64[ PubMed ]
32 Feiz Sardhar MH, Akya A. The frequency of extended spectrum β-lactamase genes of SHV-2a, SHV-5 and SHV-12 in clinical isolates of klebsiella pneumoniae isolated from Kermanshah medical centers in 2014. J Arak Univ Med Sci. 2016; 19(107): 59-67
33 Sedighi I, Arabestani MR, Rahimbakhsh A, Karimitabar Z, Alikhani MY. Dissemination of Extended-Spectrum beta-Lactamases and Quinolone Resistance Genes Among Clinical Isolates of Uropathogenic Escherichia coli in Children. Jundishapur J Microbiol. 2015; 8(7)[DOI][ PubMed ]
COMMENTS

LEAVE A COMMENT HERE: