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 Table of Contents  
Year : 2015  |  Volume : 3  |  Issue : 2  |  Page : 74-78

Phenotypic study of Extended-spectrum beta-lactamase, AmpC and Carbapenemase among E.coli clinical isolates in affiliated hospitals of Babol University of Medical Sciences

Department of Laboratory Medicine, School of Medicine, Paramedical Faculty, Infectious and Tropical Disease Research Center, Babol University of Medical Sciences, Mazandaran, Iran

Date of Web Publication12-Feb-2015

Correspondence Address:
Farahnaz Sadighian
Department of Laboratory Medicine, School of Medicine, Paramedical Faculty, Infectious and Tropical Disease Research Center, Babol University of Medical Sciences, Mazandaran
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Source of Support: This study was financially supported by the Babol University of Medical Sciences, Conflict of Interest: None

DOI: 10.4103/2347-9019.151306

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Context: Escherichia coli as a member of Enterobacteriaceae have an important role in infections. Betalactams as a group of antibiotics are used in treatment, widely. Bacteria resist to these antibiotics by producing beta-lactamases. Aims: This study aimed to investigate the phenotypic methods for detecting Extended-spectrum beta-lactamase (ESBL), AmpC and Carbapenemase (Metallobetalactamase (MBL)) in E.coli. Settings and Design: This is a cross-sectional study for detection of beta-lactamases producing E.coli. Subject and Methods: E.coli were isolated from clinical specimens to perform Antimicrobial Susceptibility Test (AST) by disc diffusion method. These bacteria were evaluated for the production of ESBL, AmpC and Metallo-beta-lactamase (MBL) (Imipenem (IMP)-1) enzymes, by using  clinical and laboratory standards institue (CLSI) method and their inhibition by 3-amino-phenyl boronic acid and 2-mercaptopropionic acid, respectively. Also, mask-ESBL production was identified using the different concentration of 3-amino-phenyl boronic acid compound. Statistical Analysis Used: Data were analyzed by the Statistical Package of Social Sciences (SPSS) 18 software. Results: Out of 259 isolated E.coli, 147 (56.8%) isolates were positive for producing at least one type of beta-lactamase. The frequency of ESBL, AmpC and IMP-1 producers were 137 (52.9%), 20 (7.7%) and 80 (31%) isolates, respectively. In addition, 88 (34%) isolates produced two or three types of enzymes simultaneously. Of the 88 isolates, 68 (77.3%) E.coli produced ESBL + IMP-1. Conclusions: This study revealed the high prevalence of beta-lactamase producing E.coli, and there are two or three different types of enzymes in a bacterium.

Keywords: AmpC, E.coli, ESBL, IMP-1

How to cite this article:
Shahandeh Z, Sadighian F, Rekabpou KB. Phenotypic study of Extended-spectrum beta-lactamase, AmpC and Carbapenemase among E.coli clinical isolates in affiliated hospitals of Babol University of Medical Sciences . Int J Health Syst Disaster Manage 2015;3:74-8

How to cite this URL:
Shahandeh Z, Sadighian F, Rekabpou KB. Phenotypic study of Extended-spectrum beta-lactamase, AmpC and Carbapenemase among E.coli clinical isolates in affiliated hospitals of Babol University of Medical Sciences . Int J Health Syst Disaster Manage [serial online] 2015 [cited 2022 May 20];3:74-8. Available from: https://www.ijhsdm.org/text.asp?2015/3/2/74/151306

  Introduction Top

The members of the Enterobacteriaceae are gram-negative, fermentative bacilli and have an important role in nosocomial and acquired infections. [1]  E.coli Scientific Name Search  is the most dominant species of this group in normal flora of the gastrointestinal tract. [2],[3]

Betalactams are a group of antibiotics that act with inhibition of bacterial cell wall synthesis and are divided into different classes. The most important classes which are widely used in treatment include penems (penicillin), cefems (cephalosporins), carbapenems and monobactam (aztreonam). The mechanisms of bacterial antibiotic resistance are intrinsic (chromosomal) or acquired. [4]

One of the most common mechanisms of resistance to these antibiotics is the production of beta-lactamase enzyme with chromosomal or plasmid origin. [5] Betalactamases are divided into A, B, C and D molecular classes in Ambler.


ESBLs belong to A and D classes, AmpC is class C enzyme and carbapenemase categorizes in A, B and D classes. The high prevalence of A and C classes beta-lactamase is observed in Enterobacteriaceae family, especially in E.coli[6],[7] , but some of them such as oxacillin-beta-lactamase (OXA) of class D have less prevalence. [8] The emergence and enlargement of bacteria that produce class B (metallobetalactamases (MBLs)) has been observed in this family in recent years. [9],[10]

ESBL beta-lactamase causes resistance to penicillins, cephalosporins, especially the third generation, and aztereonam [11],[12] AmpC-producing bacteria show resistance against cephamycins in addition to the above-mentioned antibiotics. [3],[11],[13] Carbapenemase enzymes lead to carbapenems resistance, too [14] , and have been categorized to Klebsiella pneumoniae Scientific Name Search  carbapenemase (KPC) enzymes (class A) and mbls like IMP (class B), based on Ambler scheme.

It is necessary to identify all beta-lactamases enzymes for effective treatment. Although CLSI provides a protocol to detect ESBLs in some Enterobacteriaceae species, but appropriate phenotypic method has not been provided for detecting AmpC.

Modified Hodge test method was proposed by CLSI to recognize KPC enzymes, but susceptibility and specificity rate of this test for identifying insignificant mbls was not confirmed. Therefore, it seems that it is essential to find the appropriate phenotypic methods for the diagnosis of beta-lactamase types, except ESBL.

Diagnostic methods for detecting plasmid AmpC are divided into two categories

  • The methods which identify it in bacterial enzyme extract
  • The methods based on inhibiting enzyme activity by compounds such as boronic acids, cloxacillin and syn 2190.

According to our best knowledge, boronic acid-based method was significantly better than the other methods such as cephamycin Hodge test and TE disk methods. Moreover, preparing this compound solution is easier. [15]

Arakawa et al. Revealed among the inhibitor compounds of IMP1 Metallobetalactamas, 2 mercaptopropionic acid is better detector compound than cucl2, fecl2, EDTA and thiol-bearing compounds. [16]

Antibiotic resistance against beta-lactams particularly broad spectrum cephalosporins in E.coli is increasing in Babol (north of Iran). [17],[18] Also, there are no standard diagnostic methods to identity all kinds of beta-lactamase enzymes; so, this study was performed to investigate the phenotypic methods for detecting beta-lactamases enzymes including ESBL, AmpC and MBL (IMP1) in E.coli.

  Subjects and Methods Top

This cross-sectional study was conducted from October 23, 2011 to June 17, 2012, on 259 E.coli which were isolated from various clinical samples including urine, blood, faeces, wound, secretions, sputum, pus, Shaldon-catheter and abscess. These samples were collected from the patients presented to affiliate hospitals. Sreening and Antimicrobial Susceptibility Test (AST). Initially, the isolates were confirmed using analytical profile index (API) 20E (biomerieux SA, France) and differential tests including kligler iron agar (KIA), solfide indole motility (SIM), methyl red (MR) (Himedeae).

According to the CLSI 2010 protocol [6] , the antibiotics, including cefotaxime (CTX), ceftazidime (CAZ), cefpodoxim (CPD) (cephalosporin, generation III), cefepime (CPM) (cephalosporin, generation IV), ertapenem (ETP) (carbapenems) and aztreonam (ATM) (monobactam) (mastdiscs, UK) were used by disk diffusion method on meuller hinton agar (MHA) culture medium. [6]

Phenotypic methods


0The isolates which were resistant to at least two antibiotics obtained in screening step (CAZ ≤ 22 mm, CTX ≤ 27 mm were examined by confirmatory test. In this step, CAZ and CTX disks with and without (CA) Clavulanic acid were used. [7]


This method was used for the bacteria that the confirmatory test of ESBL was negative or the growth inhibitory zone was positive around only one type of combination disk (CAZ + CA or CTX + CA). In addition, this method was used for isolates with positive plasmid AmpC (pAmpC) and negative ESBL confirmatory tests, simultaneously. [19],[20]

  Method Top

Aminophenylboronic acid disk preparation

At first, 120 mg of 3 aminophenylboronic acid (3APBA) (Sigma-Aldrich: MKBH1495V) was dissolved in 3 cc of dimethyl sulfoxide (Sigma-aldrich: D8418 (DMSO)), then, 3 CC of sterile distilled water was added. Twenty microlitre of stock solution was added to the CAZ + CA disc (final concentration of 3 APBA 400 μg).

Combination disks including CAZ + CA and CAZ + CA + 3 APBA were used for detection of mask ESBL producers. [19]


Aminophenylboronic acid disk preparation: In the beginning, 90 mg of 3APBA was dissolved in 3 ml of DMSO, and then 3 cc of sterile distilled water was added to the solution. Twenty microlitre of the solution was dispensed onto ceftazidime disk (final concentration of 3APBA 300 μg). Then, ceftazidime disk with and without 3APBA (300 μg) were used for detection of plasmid AmpC (pAmpC) enzyme producers. [21],[22]

Metallobetalactamase (IMP-1)

The isolates which were resistant to at least two antibiotics in the first stage (screening) (CAZ ≤ 22 mm, CTX ≤ 27 mm), were suspected to produce of enzyme and examined for confirmatory test.

At this stage, two ceftazidime disks and antibiotic test paper (Albert: A22 060) containing 2-3 μl of 2-mercaptopropionic acid (2-MPA) (Meck: S5487787015) were used (16). The results were analyzed by Statistical Package of Social Sciences (SPSS) 18 software. K 2 and descriptive statistics were used.

Ethical consideration

This study was ethically approved by the Ethics Committee of Babol University of Medical Sciences.

  Results Top

Two hundred and fifty-nine E.coli were isolated from clinical specimens, including urine (n = 221), faeces (n = 21), secretions (n = 8), blood (n = 3), sputum (n = 1), wound (n = 1), shaldon-catheter (n = 1), pus (n = 2) and abscess (n = 1).

The interpretation of AST results showed that 105 (40.5%) and 10 (3.9%) isolates were susceptible and resistant against all mentioned betalactam antibiotics, respectively. Also, resistance to ETP, CPM, CAZ, ATM, CTX and CPD was respectively 4.2%, 41.3%, 50.2%, 53.3%, 58.3% and 59.5%.

Distribution of beta-lactamase enzymes production was shown in [Table 1].
Table 1: The frequency of beta-lactamase enzymes in E. coli of clinical samples

Click here to view

ESBL was most commonly found in 137 (52.9%) isolates and the lowest one was related to pAmpC enzyme in 20 (7.7%) isolates.

All of 259 E.coli, 147(56.7%) isolates produced at least one kind of beta-lactamase enzymes. Also, 55 (21.2%) isolates produced only one type of these enzymes-ESBL and IMP-1, 47 (18.1%) and 8 (3.1%), respectively. Also, 88 (34%) isolates produced two or three enzymes simultaneously. The prevalence of co-carriage enzyme-producing E.coli isolates were M.ESBL + pAmpC 16 (6.2%), IMP-1+ ESBL 68 (26.2%), IMP-1 + pAmpC 1 (0.4%) and M.ESBL + IMP-1 + pAmpC 3 (1.2%) isolates. All pAmpC + M.ESBL-producing isolates were sensitive to ertapenem (ETP).

Of 10 (3.9%) isolates resistance to all antibiotics, 8 (1.9%) isolates were ESBL producers and 3 (1.2%) of them were positive in terms of producing IMP1, concurently. Also, 2 (0.8%) isolates did not produce any type of enzyme.

  Discussion Top

The previous study [23] and the present study showed the high prevalence of beta-lactamase-producing E.coli isolates in Babol (north of Iran).

The results of this study were confirmed by different studies. As, in Yulia et al.'s (2013) study, the prevalence of ESBL, MBL and AmpC-producing Entrobacteriacea isolated from intensive care unit (ICU) patients were respectively 58.42%, 27.59% and 1.98% [14] . Also, Shilan et al.'s study (2014) revealed that rate of the ESBL, MBL and AmpC-producing E.coli isolated from female genital were 71/4%, 45/2% and 0%, respectively. [24]

However, in some studies, the prevalence rate of enzymes, producers was not identical with the present study. For example, Nagdeo et al. In India reported that the prevalence of ESBL, MBL and AmpC producing E.coli isolates were 78.2%, 9.9% and 48.5%, respectively. [25]

Numerous studies represented different percentages of diverse beta-lactamase producers. [12],[19],[26],[27]

According to the mentioned studies, it seems that the prevalence of beta-lactamases-producing Enterobacteriacea in different parts of the world can be varied from 0% to over 70%. This difference could be due to the factors such as differences in the type and mode of antibiotic consumption that cause genetic mutations in bacteria and producing the mentioned enzymes. [25] In addition, cultural, nutritional and ethnic differences in various populations caused variations in the normal flora. [28] Different phenotypic methods in various studies could also be another reason.

This survey showed two isolates of E.coli were resistance to all of mentioned antibiotics and produces no beta-lactamases. It seems other mechanisms such as activity of efflux pump or lack of Outer Membrane Proteins (OMPs) involved. [9]

In this study, a total of bacteria produced two or three types of beta-lactamase enzymes at the same time. Among them, co-carriage rate of ESBL and IMP-1 enzymes was highest (26.2%).

Tsakris (2009) reported that 118 (76.1%) isolates of the Enterobacteriaceae carried genes of carbapenemase (KPC) and ESBL, concurrently. [29] Also, Biendo (2008) noted that 26 (42%) Enterobacter aerogense were positive in terms of simultaneous production of MBL and ESBL. [30]

However, Wadekar (India, 2013) claimed that none of the isolates of Enterobacteriaceae family contained simultaneously two types of ESBL and MBL. [31]

The simultaneous presence of ESBL and carbapenemase in a bacterium could be due to the genetic cooperation of them. [32] Also, it seems that mutations and genetic alterations in bacteria can lead to the diversity of beta-lactamases and increasing antibiotic resistance [25] So, it is suggested to perform more research on common genes. On the other hand, if ESBL and carbapenemase enzymes are produced by a bacterium simultaneously and only one type of enzyme like ESBL is detected, an antibiotic of carbapenem group can be selected wrongly. [9] This option is ineffective and causes the persistence of infection, increases the prevalence of resistant bacteria and endangers the public health.

The existence of E.coli produced simultaneously ESBL and pAmpC (7.3%) in the present study confirmed earlier findings that Tenover in USA (2008) and Nagdeo in India (2012) observed. [25],[33] However, Mohanty in India (2010) found 66 (58/4%) isolates of the Enterobacteriaceae family were carriers of both enzymes. [34]

It is noteworthy that 20 (7.7%) isolates were negative in terms of ESBL production by using CLSI method, while they were positive by changing method. In addition, 95% of them were simultaneously positive in terms of pAmpC producing.

Mohanty (2010) reported that 5 (10%) E.coli isolates were ESBL negative by using CLSI method, but they were positive by using PM-CLA method. Moreover, all of them (100%) were positive in terms of producing pAmpC, concurrently. [34]

Simultaneous production of ESBL and pAmpC enzymes in a bacterium causes negative confirmatory test for diagnosis of ESBL-producing isolates in spite of detecting suspected bacteria in screening step. It seems that existence of pAmpC enzyme can mask the presence of ESBL. Since the combination of clavulanic acid is used in confirmatory test cannot inhibit the pAmpC enzyme [34],[35] , therefore the increase of zone diameter is prevented and ESBL producing seems falsely negative. [12],[36],[37] Furthermore, in cases of inhibition zone, diameter around ceftazidime and cefotaxime disks are at the initial range of susceptible (respectively ≥21 and ≥26) may overlap with the standard range for detecting of ESBL producers (respectively ≤22 and ≤27). Lack of diagnosis M-ESBL can lead to choosing incorrect antibiotic and threatening the patient's life.

The rates of E.coli produced concurrently metabetalactamase and pAmpC in the present study and Nagdeo, s investigation were one (0.4%) and 7 (2.31%) isolates [25] While, the percentage of E.coli produced simultaneously three types of enzymes were 3 (1/2%) and 2 (0/66%) isolates, respectively. [25]

The diagnosis of E.coli which produces concurrently variety of beta-lactamases is important, because the genes of these enzymes can be spread by the plasmid and expanded into other bacteria. [25],[38] Therefore, the identification of different enzymes separately seems to be necessary.

Several studies indicate that the use of boronic acid as an inhibitor is a better method than other phenotypic methods to identify the producers of pAmpC. [9],[27],[38],[39] Although, the specific confirmatory phenotypic tests have not been announced for detection of pAmpC and MBL enzymes by CLSI, so far.

  Conclusion Top

The findings confirm lack of CLSI protocol efficiency for detecting ESBL and pAmpC co-producers. Therefore, it is recommended using carbapenems for treatment in cases of negative confirmatory test for the diagnosis of ESBL-producing isolates. In addition, the prevalence of isolates which produce concurrently the variety of beta-lactamases is high. It is suggested to continue the genotypic and phenotypic studies at the same time to identify AmpC and MBL (IMP-1) enzymes and achieving the standard and applicable phenotypic method in clinical laboratories.

  Acknowledgement Top

The authors would like to thank the personnel of the microbiology laboratory of the affiliated hospitals of Babol University of Medical Sciences for their help in this study. Also, our special thanks go to Dr. Narges Kalantary for excellent comments on this article

  References Top

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