iMedPub Journals

2013 ARCHIVES OF CLINICAL MICROBIOLOGY
Vol. 4 No. 5:2 doi: 10.3823/273

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Characterization of extended-spectrum beta-lactamases in some enterobacteriaceae clinical isolates from Egyptian patients

Salwa Afifi1, Rania Abdel Khalek2, Amany Elsharif1, Marwa Yousry3, Hanan El-Mohammady2 and M. Seif Ashour1
1   Microbiology and Immunology Dep., Faculty of Pharmacy, Al-Azhar University. 2   Laboratory Unit, Molecular Epidemiology Dep., Clinical Trials and Military Service, NAMRU. 3  Central public health laboratories, MOH. CairoEgypt.
Correspondencia:  amanyelsharif@gmail.com

Amany El-Sharif, Ph.D., Prof. Microbiology & Immunology. Department of microbiology & immunology, Faculty of pharmacy (girls). Al-Azhar University Yousef Abbas St. Nasr city, Cairo, Egypt. Telephone: 00202- 26716092. Fax: 00202- 26716092. Mail Address: Nasr City, El-Sefarat area, block1 building 10, beside ministry of higher education. Cairo-Egypt.

Abstract
Objectives: to investigate and characterize ESBLs enzymes among Enterobacteriaceae clinical strains isolated from patients in Egypt.

Methods and findings: ESBLs and AmpC producers were identified phenotypically. Beta-lactamases genotypic identification was performed for Escherichia, Klebsiella and Enterobacter spp. TEM, CTX-M-I CTX-M-IV, OXA-IIIand SHV genes were detected. This study reported Gram negative bacilli as the predominant pathogens as 343 (89.5%) isolates were recovered from 419 clinical samples isolated from public hospitals, Enterobacteriaceae represent 84.2% of the identified isolates. Escherichia spp. were the most frequent isolates, other isolates were identified as Klebsiella, Enterobacter and Proteusspecies in frequency of 49.48%, 37.02 %, 5.88 % and 3.46% respectively. TEM was found as the most predominant gene producing ESBLs among Escherichia spp. (81.9%) and less frequent among Klebsiella and Enterobacter spp., 40.5% & 41%respectively. CTX-M-gp I genes were detected among 72.2%, of Escherichia and56.1% of Klebsiella spp., while CTX-M-IV genes were detected among 52.9% of Enterobacter spp. Regarding OXA-III genes, these were detected in 44.4%, 28.1% & 11.7% of examined Escherichia, Klebsiella and Enterobacter species respectively. While SHV genes were the least frequent among Escherichia spp., SHV was the predominant gene among Klebsiella spp. and moderate in Enterobacter spp. by 6.9%, 72% & 29.4% respectively. TEM-type allele is the most common ESBLs.

Conclusion: this is the first report demonstrate different types of ESBLs genes
among ESBL and AmpC positive Enterobacteriaceae clinical isolates in Egypt. Our finding reported that Enterobacteriaceae isolates are more predominant among hospital clinical isolates. ESBLs and AmpC producing Enterobacteriaceae are becoming increasingly emerged and involved in infection.

This article is available from: www.acmicrob.com
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Key words: Enterobacteriaceae, ESBL, AmpC, Escherichia, Klebsiella and Enterobacter.

1

ceftazidime. they are also found in other species of Gram-negative bacteria with increasing frequency such as Enterobacteraerogenes. especially against the oxyimino-cephalosporins. Most ESBLs are derivatives of TEM or SHV enzymes. aztreonam. ESBL was detected by an increase in the diameter of inhibition zone to ≥ 5-mm for either ceftazidime or cefotaxime in combination with clavulanic acid versus its zone when tested alone. The majority of SHV-type ESBLs are found in strains of K. CTX-M and OXA III betalactamases by PCR using the primers listed in Table 1. Over the last few years. The antibiotic discs used throughout this study were the product of Oxoid Laboratories. TEM is the most commonly reported beta-lactamase in Gram-negative bacteria [27]. Molecular charecterization of ESBLs Enterobacteriaceaeby polymerase chain reaction (PCR)The DNA template was prepared by boiling method. new beta-lactamases have been emerged and cause resistance to that class of antibiotics [6]. There are more than 90 TEM-type beta-lactamases and more than 25 SHV-type enzymes. AmpC phenotypic detectionScreening with cephamycin (cefoxitin) disc resistance for the presence of AmpC type enzyme was used. 9]. cefotaxime. However. 9]. PCRs were performed using 6. The selective pressure and overuse of new antibiotics in the treatment of patients has led to new variants of beta-lactamases. Until recently. sputum. these enzymes have also been found in Citrobacter diversus.25 μL of Dream Taq green PCR Master Mix (Fermentas) in a full automated Applied Biosystem/ Gene Amp PCR system 9700. However. coli and K. Recently OXA-type ESBLs are detected in Enterobacteriaceae [7] and they are characterized by their poor inhibition by clavulanic acid [18]. these enzymes were called extended. Plasmid-mediated ESBLs called CTX-M hydrolyze cefotaxime and they have mainly been found in strains of Salmonellatyphimurium. and P.iMedPub Journals 2013 ARCHIVES OF CLINICAL MICROBIOLOGY Vol. over 150 different ESBLs have been described. Morganella morganii and Proteus species [22]. many new beta-lactam antibiotics have been developed. cefpodoxime and cefotaxime (30 µg/each) [12]. their antimicrobial-resistance profiles and detection of predominant resistance genes among Enterobacteriaceae clinical strains. blood.com/ Introduction Gram-negative bacteria are important etiological agents of nosocomial and community acquired infections.imedpub. pneumonia [27]. attending Abou-Elreesh Hospital (AEH) and Central Public Health Laboratories (CPHL) in Cairo. with each new class of antibiotics that has been used to treat patients. It has been suggested that the naturally occurring TEM-type ESBLs are the result of fluctuating selective pressure from several beta-lactams within a given institution rather than selection with a single agent. 5].3823/273 Our Site: http://www. Bacterial isolates were tested for susceptibility to antibiotics by the disc diffusion method recommended by the Clinical Laboratory Standards Institute [31]. These beta-lactamases have been found worldwide in many different genera of Enterobacteriaceae [5]. we investigated the prevalence of ESBL senzymes. or ceftriaxonediscs (30µg per each). ESBL phenotypic detectionDisc diffusion method by the following antimicrobial discs was used: ceftazidime. Today. and wound swabs) were collected from inpatients. E. no data were available regarding molecular characterization and frequency of ESBLs in clinical samples isolated from Egyptian patients. Because of their increased spectrum of activity. body fluids. Double-disc synergy test (DDST) was also used.spectrum beta-lactamases (ESBLs). aeruginosa [6]. coli. before administration of antibiotics. Clinical samples were submitted for bacterial cultures and identification for both Gram negative and Gram Positive bacteria using standard microbiological techniques. Material and Methods Study design In the present study 419 clinical samples (urine. UK. 2 © Copyright iMedPub . Egypt. resistance to expandedspectrum beta-lactam antibiotics due to beta-lactamases has emerged rapidly. In this study. ESBL-positive isolates were tested for the genes encoding TEM. SHV. Discs were used include aztreonam. 5:2 doi: 10. pneumonia [6. 4 No. Unlike the TEM typebeta-lactamases. there are relatively few derivatives of SHV-1. Some studies have shown the prevalence of multidrug resistant and ESBLs Enterobacteriaceae in hospitals in Middle Eastcountries including Egypt [2. Confirmation was done using CLSI combined method test [31]. Ethical approval to perform the study was obtained from the management board. Over the past few decades the treatment of Gram-negative bacteria infection has become a challenge due to their ability to acquire antimicrobial resistance [2. Although TEM-typebeta-lactamases are most often found in E. Cefoxitin/cefotaxime or ceftazidime disc antagonism tests was also used to detect inducible AmpC which can be recognized because of blunting of the CAZ or CTX zone adjacent to the FOX disc [11]. Unfortunately.

GTA AGC TGA CGC AAC GTC TG OXA-1-S: 5’. (1. and Yersinia spp. Enterobacter spp.7% and 43.33% 0. table 2. a total of 419 clinical samples included urine..com/ Table 1. was 0.08% 0. cefotaxime and ceftazidime) and fourth generation (cefepime) cephalosporins were 35. Escherichia spp. Primers used for detection of ESBLs encoding gene.9% 4. the incidence of sensitivity was 31. Gene Ruler.46%) and Salmonella spp. (%) of isolates 107 26% 0.gp-IV [23] bla OXAIII-gp [15] Primer sequence TEM/F: 5’. From which 289 (84. Proteus spp.16% 0.   Proteus mirabilis Proteus vulgaris Salmonella spp. Out of the 375 recovered isolates.45% 0.AGC CGC CGA CGC TAA TAC A -3.imedpub. Detection of antimicrobial resistance to examined isolates revealed that highlevel of resistance to beta-lactam antimicrobial agents was reported.29% No.02 %). Klebsiella pneumoniae Klebsiella oxytoca Klebsiella terrigena Klebsiella ozaenae Escherichia spp.48%).87% 0.29% Results Identification of isolates In this study. CTX-M914F: 5’.CTT GAT TGA AGG GTT GGG CG -3’ Product size (bp) 1074 1016 499 474 908 The amplified PCR product were analyzed by gel electrophoresis (BioRad Power PAC 300) with 2% agarose stained with Gel red (Phenix research) and visualized by UV transillumination (BioRad). and © Copyright iMedPub 3 .58% 113 29 1 17 2. Enterobacter cloacae   Enterobacter aerogenes Enterobacter agglomerans Enterobacter asburie Proteus spp.AGC CGT TAA AAT TAA GCC C -3’ OXA-1-AS: 5’.6%. (3. a number of 343 isolates (91. were represented by 1.gp-I [23] BlaCTX-M.69%. Other frequently isolates were Klebsiella spp. Isolated organisms Klebsiella spp.negative bacilli. blood. The incidence of sensitivity of the third generation (ceftriaxone.GCT GGA GAA AAG CAG CGG AG -3’ CTX-M914R: 5’.GAA GAC GAA AGG GCC TCG TG-3’ TEM/R: 5’.38%).16% 89 3 14 1 143 32.9% 8. Target gene bla TEM [30] bla SHV [30] Bla CTX-M. 35. For monobactams (aztreonam).29% 0. (5. was the most frequently isolated organisms among Enterobacteriaceae isolates (49.GAC GAT GTC ACT GGC TGA GC -3’ CTXM1-R2: 5.6%. Antimicrobial susceptibility testing The antibiotic susceptibility pattern among the Enterobacteriaceae isolates is illustrated in table 3.58% 1.88 %). Cairo-Egypt. sputum.iMedPub Journals 2013 ARCHIVES OF CLINICAL MICROBIOLOGY Vol.100 bp plus DNA ladder from (Fermentas) was used as a marker according to the product size.  Enterobacteriaceae species isolated from different clinicalspecimens in Egypt. body fluids and wound swabs were collected according to physicians’ request before administration of any antibiotics to perform bacterial culture and sensitivity test in Central public health laboratories. Escherichia coli Escherichia coli (inactive) Escherichia hermanii Enterobacter spp.2%) were Enterobacteriaceae species. Citrobacter freundii Yersinia enterocolitica Morganella morganii 8 2 4 3 3 2 9 1 3 4 10 2. 37.GGT CTG ACA GTT ACC AAT GC -3’ SHV/F: 5’.TCT TTC CGA TGC CGC CGC CAG TCA -3’ CTXM1-F3: 5’.87% 1. 5:2 doi: 10.87% 0.9% respectively.CGC CGG GTT ATT CTT ATT TGT CGC -3’ SHV/R: 5’. 4 No. For carbapenems. (37.14 %.3823/273 Our Site: http://www. Each of Citrobacter spp.4 %) were found to be Gram.03% and Morganella spp. Table 2.6% 0.

0 0 Enterobacter spp. No.1%) isolates out of Klebsiellaspp.4%) 72 (50. Discs: ceftiaxone30 μg. 0 0 2(66.7%) Trimethoprim/ 37 (25.iMedPub Journals 2013 ARCHIVES OF CLINICAL MICROBIOLOGY Vol. quinolones used.8%) 74 (51. and 100% of Enterobacter spp.3%) Yersinia spp.07%) 103(35. amoxicillin/clavulanic acid.6%) 103(35.7%) 75(25.7%) 127(43. 4 © Copyright iMedPub .8%) 71 (48. 0 0 1 (25%) 1 (25%) 1 (25%) 1 (25%) 1 (25%) 4 (100%) 2 (12. spp.3%) 3(100%) 1(33. cefotaxime 30 μg.2%) 89 (62. 4 No. Moreover folate inhibitors showed less activity against Enterobacteriaceae isolates. ceftazidime 30 μg.3%) 150(51. were supposed to carry ESBLs.9%) 72(24. (%) susceptible Antibiotics Ampicillin Amoxicillin/ Clavulanic acid Ceftriaxone Cefotaxime Ceftazidime Cefepime Aztreonam Imipenem Gentamicin Amikacin Ciprofloxacin Escherichia spp. Strains 0 0 1(50%) 1(50%) 1(50%) 1(50%) 0 2 (100%) 1 (50%) 1 (50%) 2 (100%) 1 (50%) 6 (2.8%) 3 (17.3823/273 Our Site: http://www.9%) 90(31.9%) 17(15.8%) sulphamethoxazole.3%) 1 (33.6%) 2(66. 5:2 doi: 10.73%) 72 (50.6%) 2(66.6%) 109(37.5%) 5 (29. Figure 1.3%) 1 (33. 0 0 3 (17. 0 0 Klebsiella spp.9%) 70 (48.95%) 102(35.3%) isolates of Escherichiaspp.3%) % of Morganella Susceptible spp.com/ Table 3.CLSI phenotypic confirmatory tests for ESBLs production were used in this study for all Enterobacteriaceae.4%) 10 (58.6%) 3(100%) 2(66.2%) 31(28. Detection of ESBL producing enterbacteriaceae isolates It was found that 72 (50..3%) 11(10.3%) 1 (33.9% were sensitive to ciprofloxacin.4%) 13 (76.6%) 3 (17.3%) 142 (99. aztreonam 30 μg.3%) 0 3 (100% ) 1 (33. Antibiotic susceptibility pattern of Enterobacteriaceae species isolated from different clinical specimens in Egypt.6%) 3 (17.6%) Proteus spp.1%) 5 (29. For aminoglycosides about 25.5%) 1 (25%) 4 (100%) 2 (50%) 0 0 0 0 0 1 (33.3 % were susceptible to gentamicin and amikacin respectively.7%) 18(16. it was observed that 92. 0 6(60%) 9(90%) 8(80%) 10(100%) 10(100%) 10(12%) 10(100%) 8(80%) 10(100%) 10(100%) 8(80%) Salmonella Citrobacter spp.  Detection of ESBL production by Double-disc synergy test. the organism Enterobacter cloacae where there is an extension of edge of inhibition zone of cefepime only towards amoxicillin/clavulanic acid disc.7%) 0 91(85%) 4 (3. Double-disc synergy test (Figure 3) was done to all Enterobacteriaceae isolates and results of the two methods are tabulated collectively in table 4.3%) 1(33.6%) 8 (47.8%) 80 (55.4%) 4 (23.6%) 3(100% ) 1(33.9%) 23(21. 89 (83.9%) 54 (37.9%) 19(17.imedpub. cefepime 30 μg.9% and 35.. It shows that more than one disc is recommended for double disc method for detection of ESBLs in Enterobacteriaceae isolates.9%) 17(15.14%) 268(92.7% of all Enterobacteriaceae isolate were sensitive to imipenem and 51. centre.

(72) Klebsiella spp.8% 5 (29. Salmonella spp. Klebsiellaspp.25%) 16 Total no of positive screening for AmpC isolates Escherichia spp.2%) 42 (47.5%) 4 (25%) 24 20 © Copyright iMedPub 5 . Enterobacteriaceae isolates TEM N (%) 11 (84..6%) 0 2 (50%) 0 0 1 (50%) Double disc test [13] CTX 61 (42.(89) Enterobacter spp.9%) 8 (24.6%) 9 (56.8%) 63 (58.(16) Total No.25%) 36 OXA-III N (%) 7 (6.7%) 59 Table 6.1%) 9 (52.(17) Total No.28%) 4 (23.5%) 0 3 (75%) 0 0 0 CRO 57 (39. No of positive screening for ESBLs isolates Escherichia spp.9%) 36 (40.2%) 1 (6.6%) SHV N (%) 0 CTX-M-I N (%) (69.45% 4 (23.2%) 12 (36.1%) 2 (11. 4 No.5%) 0 2 (50%) 0 0 1 (50%) FEP 61 (42. of isolates (178) TEM No (%) 59 (81.5%) 63 (58.8%) 3 (17.(13) Klebsiella spp.1%) 70 (65.3823/273 Our Site: http://www.2%) 6 (29.8%) 4 (23.46%) 72 (67.15%) 21 (63.5%) 0 3 (75%) 0 0 1 (50%) CAZ/CA vs CAZ 55 (38.25%) 22 1 9 CTX-M-IV N (%) 6 (46. and Enterobacter spp.4%) 74 CTX-M-I No (%) 52 (72.1%) 102 SHV No (%) 5 (6.1%) 2 (11.6%) 72 (67.(33) Enterobacter spp. 5:2 doi: 10.9%) 64 (72%) 5 (29.4%) 16 (48.7%) 96 CTX-M-IV No (%) 23 (31.6%) 63 (58.68%) 4 (23.5%) 7 (41. Enterobacter spp. Citrobacter spp.iMedPub Journals 2013 ARCHIVES OF CLINICAL MICROBIOLOGY Vol.3% 6 (35.3%) (6. Morganella spp.  Detection of ESBLs by different phenotypic confirmatory tests among Enterobacteriaceae species isolated from different clinical specimens in Egypt. Phenotypic confirmatory tests Enterobacteriaceae isolates Escherichia spp. Yersinia spp. Combined disc method [8] CTX/CA vs CTX 62 (43.imedpub. Klebsiella spp.4%) 25 (28.2%) 1 (10%) 3 (75%) 0 0 1 (50%) Table 5.4%) 0 3 (75%) 0 0 1 (50%) ATM 56 (39.  Distribution of ESBLs genes by PCR among positive ESBL for Escherichia spp.com/ Table 4. of isolates (62) 7 (21.  Distribution of ESBLs genes by PCR among positive AmpC for examined Enterobacteriaceaeisolated from different clinical specimens in Egypt.9%) 82 OXA-III No (%) 32 (44.5%) 0 3 (75%) 0 0 1 (50%) CAZ 58 (40.35%) 66 (61. isolated from different clinical specimens in Egypt. Proteus spp.9%) 50 (56.

Klebsiella spp.9%) followed by TEM (41%) while SHV represents only (29.1%) while TEM was (40. respectively.9%) followed by CTX-M-gp I (72..5%) of ESBLs.3823/273 Our Site: http://www. (44.2%) while SHV represents only 6. Figure 4.4%).. showing lanes of positive bands of PCR products for each enzymes group and ladders lanes in between each group of samples.  Detection of bla CTX-M-IV gene by conventional PCR where positive isolates show bands at 474 bp product size.& Citrobacter spp. isolates and only in 11.   Detection of bla CTX-M-I gene by conventional PCR where positive isolates show bands at 499 bp product size.7% of Enterobacter spp.  Detection of bla SHV gene by conventional PCR where positive isolates show bands at 1016 bp product size.. (81. while they were in considerable percentage in Escherichia spp..com/ Detection of AmpC inducible Enterobacteriaceae isolates Co-existence of both AmpC beta-lactamases and ESBL in some Enterobacteriaceae strainshas been detected in this study which led to false negative results.16 and 3 isolates of Escherichiaspp.imedpub.  Detection of bla TEM gene by conventional PCR where positive isolates show bands at 1074 bp product size Figure 5. (52.AmpC inducible strains were detected in 13. PCR for genotypic detection of ESBLs: (TEM/ SHV/ CTX-M-I CTX-M-IV/ OXA-III) PCR test was done to positive ESBLs tests for Escherichia spp. 6 © Copyright iMedPub . 4 No. On the other hand SHV was the predominant gene among Klebsiella spp.1% of Klebsiella spp. and Enterobacter spp.9%. Figure 2. 5:2 doi: 10. Results are tabulated in table 5.iMedPub Journals 2013 ARCHIVES OF CLINICAL MICROBIOLOGY Vol. (72%) followed by CTX-M-gp IV genes (56. Klebsiella spp. Figures 2-6 show the pictures shot to the gel after electrophoresis. Enterobacter spp. Figure 3.33. TEM represents the most predominant gene producing ESBLs among Escherichia spp.4%). OXA-III genes were found in 28. CTX-M-IV genes was relatively the most predominant among Enterobacter spp.

ESBL producing strains are not only showed highlevel of resistance to beta lactam antimicrobial agents but also exhibited resistance to other groups of antimicrobials like gentamicin (26%).9%) followed by TEM (41%) while SHV represents only (29. CTX-M was reported as the predominance in Morocco [3. Figure 6. this finding was reported previously [9].6% respectively.2%) while SHV represents only 6. Prevalence of ESBLs among clinical strains of these Enterobacteriaceae spp. 5:2 doi: 10. © Copyright iMedPub 7 . Enterobacteriaceae spp. On genus level.25% of the examined isolates. representing 49. sulpha-methoxazole (24. were 65.9%). 43. were formerly reported [3. 20. For Enterobacter spp.3823/273 Our Site: http://www.42% and 17. 10. 29] and it was reported among Egyptian clinical Enterobacteriaceae [24]. CTX-M-I. Different enzymes are reported as a common ESBL in other settings.3% were ESBL producers. [9] and Klebsiella spp.iMedPub Journals 2013 ARCHIVES OF CLINICAL MICROBIOLOGY Vol. were previously reported as the most commonly isolated pathogens in clinical settings [2. they were also detected in other species of Gram-negative bacteria with increasing frequency as Enterobacteraerogenes [17]. It was observed in our study that TEM represents the most predominant gene producing ESBLs among Escherichia spp.02%) and Enterobacter spp. there was a variation in distribution of different resistant genes. It was reported that up to 90% of ampicillin resistance in E. 4]. This means that resistance to two different kinds of antibiotics could be a selective pressure for spreading such resistant strains [17. (5. Upon observing susceptibility pattern in present study it was found that. Escherichia spp. This was attributed to the high mobility of genes encoding ESBLs which are usually located on plasmids and hence can harbor resistance genes to several other unrelated classes of antimicrobials. 32].9%..48%.1%). (72%) followed by CTX-M-gp IV genes (56. 27]. In the present study. we detected a variety of beta-lactamases encoding genes among the examined Enterobacteriaceae strains. This demonstrates the importance of studying the geographical distribution and mobilization of resistance genes among clinical bacterial isolates. represented 84.88 %). 26].8% were non-fermenters. such as the plasmid-mediated quinolone-resistance genes and aminoglycoside-resistance genes [25.2% while 15. These are plasmidencoded beta-lactamases which were reported as less sensitive than TEM to clavulanic acid inhibition. The prevalence of ESBL among Klebsiella spp. CTX-M-IV genes was relatively the most predominant (52. Regarding CTX-M-type ESBL enzyme.imedpub. TEM-type was the most predominant ESBL in the present study (52. in the present study.5%) followed by equal frequency for both of CTXM-I&IV (49 % for each).4%). coli is due to the production of TEM-1[27] and it was the first TEM-type beta-lactamase that displayed the ESBL phenotype [21]. These results are close to those reported by an Indian study in 2010 [27].25%) were the least but in considerable frequent detected among examined Enterobacteriaceae. ciprofloxacin (52 %). This indicates that TEM-type allele is the most common ESBL in Egypt. (81. Among isolated Escherichia spp. while TEM represents about 40. Other less frequent isolates were identified as Klebsiella spp.5% of ESBLs encoding genes. Other studies reported similar finding where ESBL producing isolates showed a high degree resistance to different groups of antimicrobial agents [20. Enterobacteriaceae spp. 4 No. amikacin (35%). They have become the most prevalent type of ESBLs described during the last few years [1. 16. 29]. CTX-M-IV.  Detection of bla OXA-III gene by conventional PCR where positive isolates show bands at 908 bp product size. On the other hand SHV was the predominant gene among Klebsiella spp.com/ Regarding molecular characterization. SHV and OXA-III. The detected genes include TEM. while SHV (39%)and OXA-III (31. 14]. 29]. (37. Although TEM-type beta-lactamases were reported mostlyin Escherichia spp. and Enterobacter spp. OXA-III enzymes encoding genes were found in 31. it was detected in 49% of examined isolates and it constitute a novel and rapidly growing family of plasmid-mediated ESBLs that are currently replacing mutant TEM or SHV ESBLs. 4] and Portugal [17].4%).9%) followed by CTX-M-gp I (72. Discussion The current study showed that Gram-negative bacilli were the predominant isolates (91. The types of the enzyme CTX-M-1 to 15are varied with geographical distribution [4. were the most frequent isolates. OXA-type ESBLs are increasingly reported recently [27.[21].

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