Relevance of class 1 integrons and extended‑spectrum β‑lactamases in drug‑resistant Escherichia coli

  • Authors:
    • Li‑Tao Liu
    • Li‑Hong Wan
    • Xiao‑Hong Song
    • Yao Xiong
    • Shao‑Ju Jin
    • Li‑Ming Zhou
  • View Affiliations

  • Published online on: August 12, 2013     https://doi.org/10.3892/mmr.2013.1626
  • Pages: 1251-1255
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Abstract

Escherichia coli is a common cause of community‑ and hospital‑acquired urinary tract infections, and class 1 integrons are the prior elements of gene transference in the capture and distribution of gene cassettes among clinical gram-negative bacillus. In the present study, the resistance of Escherichia coli to antimicrobial agents was investigated. A total of 97 isolates were found to be susceptible to 16 antimicrobial agents and were detected in the production of extended β‑lactamases (ESBLs), distribution of CTX‑M‑type β‑lactamases, presence and characterization of class 1 integrons and a variable region of integron‑positive isolates. Escherichia coli isolates possessing CTX‑M (31; 32%) were detected in 19 isolates (61.5%). The presence of ESBLs was associated with resistance to penicillins, third-generation cephalosporins, ciprofloxacin, aminoglycosides and monocyclic β‑lactam antibiotics. Escherichia coli isolates (69; 71.1%) possessed class 1 integrons associated with resistance to ciprofloxacin and numerous third-generation cephalosporins, penicillins, tobramycin and trimethoprim‑sulfamethoxazole. The four gene cassette arrangements were as follows: dfrA17‑aadA5, aadA1, aacC4‑cmlA1 and dfr2d, and 8 carried two disparate class 1 integrons. Five isolates presented class 1 integrons containing no gene cassettes. The distribution of ESBLs and class 1 integrons in Escherichia coli were prevalent with drug resistance in Chengdu. In addition, the resistance range of Escherichia coli isolates that harboured ESBLs and carried class 1 integrons were similar. The current study demonstrated the presence of class 1 integrons and ESBLs, which jointly mediate the resistance of Escherichia coli isolates to a number of antibacterial agents.

Introduction

Escherichia coli, a commensal bacteria of the gastrointestinal tract in humans and animals, is a common cause of community and hospital-acquired urinary tract infections and varies in its susceptibility to antimicrobials (13). At present, misuse of fluoroquinolones and third-generation cephalosporins has led to an increasing number of drug-resistant strains of Escherichia coli in China (4).

Previous studies have shown that 65% of clinical isolates of Escherichia coli produce extended-spectrum β-lactamases (ESBLs) in China (5,6). ESBL-producing strains are resistant to β-lactams, fluoroquinolones and aminoglycosides (7). Cefotaxime (CTX)-M-type enzymes are the most common types of ESBLs (8) and are the predominant ESBLs in Enterobacteriaceae in China, causing hospital- and community-acquired infections (4).

In addition, a number of studies have indicated that integrons have developed a highly efficient mechanism for spreading antibiotic resistance determinants (9,10). Class 1 integrons play a crucial role in the dissemination of antibiotic resistance in Gram-negative bacteria and occur frequently in Escherichia coli by carrying and capturing genes via site-specific recombination catalyzed by specific integrase genes (1114). Class 1 integrons aid in gene transference in the capture and distribution of gene cassettes among clinical Gram-negative bacillus (15).

To date, the correlation between class 1 integrons and ESBLs of Escherichia coli has not been evaluated. Therefore, the current study focused on analyzing the prevalence of class 1 integrons and CTX-M-type enzymes in clinical isolates of Escherichia coli in Chengdu, China between 2009 and 2011 to determine the correlation between class 1 integrons and ESBLs.

Materials and methods

Samples

A total of 97 non-duplicated clinical Escherichia coli isolates were collected from the sputum of patients from the Chengdu No. 7 People’s Hospital (Sichuan, China) between 2009 and 2011 and were identified using the Microscan WalkAWay-40 (Siemens, Erlangen, Germany). Written informed consent was obtained from the patients.

Isolate susceptibility

Isolate susceptibility was determined by the disc diffusion technique on Mueller-Hinton agar plates (Oxoid Ltd., Basingtoke, Hampshire, UK) in accordance with CLSI guidelines (16). The following reagents were used: 10 μg ampicillin (AMP), 100 μg piperacillin (PIP), 30 μg ceftazidime (CAZ), 30 μg cefepime (FEP), 30 μg ceftriaxone (CRO), 35 μg aztreonam (ATM), 5 μg ciprofloxacin (CIP), 30 μg tetracycline (TCY), 10/10 μg ampicillin-sulbactam (SAM), 100/10 μg piperacillin-tazobactam (TZP), 30 μg cefotaxime (CTX), 75 μg cefoperazone (CFP), 10 μg imipenem (IPM), 10 μg tobramycin (TOB), 10 μg gentamicin (GEN) and 23.75/1.25 μg trimethoprim-sulfamethoxazole (SXT; all Oxoid Ltd.). Escherichia coli ATCC25922 and Staphylococcus aureus ATCC25923 were used as reference strains for susceptibility testing.

A phenotypic confirmatory test was performed with 30 μg CTX, 30/10 μg cefotaxime-clavulanic acid, 30 μg CAZ and 30/10 μg ceftazidime-clavulanic acid (all Becton-Dickinson, Franklin Lakes, NJ, USA) disks on Mueller-Hinton agar. The results were analyzed as previously described (16). Escherichia coli ATCC 25922, Klebsiella pneumoniae ATCC 700603 and Pseudomonas aeruginosa ATCC 27853 were used as controls.

Primers used to amplify CTX-M genes, intI1 and conserved segments are presented in Table I with their corresponding cycling conditions.

Table I

Primer sequences and PCR.

Table I

Primer sequences and PCR.

PrimersPrimer sequence (5′-3′)PCR conditionsReferenceExpected size, bp
CTX-M-F
CTX-M-R
TGTTGTTAGGAAGTGTGCCGC
TCGTTGGTGGTGCCATAGTC
1 cycle of 3 min at 94°C, 35 cycles of 1 min at 94°C, 1 min at 55°C and 2 min at 72°C and 1 cycle of 7 min at 72°C.17687
IntI1-F
IntI1-R
GGGTCAAGGATCTGGATTTCG
ACATGGGTGTAAATCATCGTC
1 cycle of 5 min at 94°C, 30 cycles of 30 sec at 94°C, 1 min at 63°C and 40 sec at 72°C and 1 cycle of 5 min at 72°C.18484
5′CS
3′CS
GGCATCCAAGCAGCAAGC
AAGCAGACTTGACCTGAT
1 cycle of 3 min at 94°C, 35 cycles of 30 sec at 94°C, 30 sec at 55°C and 1 min at 72°C and 1 cycle of 5 min at 72°C.19-

[i] CTX, cefotaxime; CS, conserved segments; PCR, polymerase chain reaction.

Polymerase chain reaction (PCR)

Each PCR was carried out in a 25-μl volume using 1.5 units Taq DNA polymerase (Promega Corporation, Madison, WI, USA) in the reaction buffer provided, which contained 2.5 mM MgCl2, 50 μM each deoxynucleoside triphosphate, 0.4 μM selected primer and 2 μl DNA template. Each PCR product (10 μl) was subjected to electrophoresis on 1.2% agarose gel.

Amplification was performed by a Tpersonal Thermocycler (Biometra, Göttingen, Germany). PCR products were sequenced using an ABI3730 Sequencer (Applied Biosystems, Foster City, CA, USA) and the sequences were compared with the reported sequences from GenBank.

Results

Antibiotic resistance rates

Antibiotic resistance rates were as follows: TCY, 82.5%; PIP, 79.4%; GEN, 73.2%; AMP and CIP, 64.9% each; SXT, 62.9%; CTX, 47.4%; CRO, 43.3%; TOB, 40.2%; CFP, 39.2%; CAZ, FEP and ATM 34.0% each; SAM, 9.3%; TZP, 7.2%; and IPM, 2.1%.

All isolates, with the exception of 3, were sensitive to FEP. Among them, AMP, TCY, aminoglycoside, fluoroquinolones and folic acid metabolic pathway inhibitor resistance was >60% and cephalosporin resistance was ~30%. Notably, 2% of isolates exhibited resistance to IPM.

CTX-M type β-lactamase production

Based on the phenotypic confirmatory test, 31 isolates (32%) were found to be producers of ESBLs. All isolates that tested positive for ESBLs were also multidrug resistant, with a statistically significant difference in resistance against 14 antibacterial drugs between positive and negative isolates (P<0.05; Table II). CTX-M-type β-lactamase was tested in Escherichia coli isolates (Fig. 1) and detected in 19 isolates (61.5%).

Table II

Comparison of resistance for positive and negative strains of extended spectrum β-lactamases.

Table II

Comparison of resistance for positive and negative strains of extended spectrum β-lactamases.

ESBLs positive (n=31)ESBLs negative (n=66)


Paper disk of antimicrobial agentResistance, %Isolates, nResistance, %Isolates, nP-value
CTX74.22334.8230.000a
GEN87.12766.7440.027a
TOB54.81733.3220.037a
CFP58.11830.3200.009a
SXT90.32850.0330.000a
CAZ58.11822.7150.001a
AMP96.83050.0330.000a
FEP61.31921.2140.000a
TCY90.32878.8520.133
CIP90.32853.0350.000a
IPM6.520.000.100
PIP93.52972.7480.014a
SAM29.090.000.000a
TZP19.463.210.004a
CRO67.72131.8210.001a
ATM51.61625.8170.012a

a P<0.05 vs. negative.

{ label (or @symbol) needed for fn[@id='tfn3-mmr-08-04-1251'] } ESBLs, extended spectrum β-lactamases; CTX, cefotaxime; GEN, gentamicin; TOB, tobramycin; CFP, cefoperazone; SXT, trimethoprim-sulfamethoxazole; CAZ, ceftazidine; AMP, ampicillin; FEP, cefepime; TCY, tetracycline, CIP, ciprofloxacin; IPM, imipenem; PIP, piperacillin; SAM, ampicillin-sulbactam; TZP, piperacillin-tazobactam; CRO, ceftriaxone; ATM, aztreonam.

Gene cassettes in class 1 integrons

Of the 97 isolates tested, the intI1 gene was detected in 69 isolates (71.1%; Fig. 2) with a statistically significant resistance to 9 antibacterial drugs identified between positive and negative isolates (P<0.05; Table III). Among these class 1 integron gene-positive strains, conserved segments were amplified in 65 isolates (94.2%). The amplification products sequenced were 100% identical to the reported sequence from GenBank. Six conserved segments were detected in the 65 isolates (Fig. 3). Sequence analysis was identical to the following known sequences: dfr2d (549 bp; accession no, HQ902143), aadA1 (934 bp; accession no, HQ874618), aacC4-cmlA1 (2,327 bp; accession no, HM175867), dfrA17-aadA5 (1,593 bp; accession no, JN108894) and no gene cassette arrays (155 bp; accession no, FM998811), as presented in Table IV. Four gene cassette arrangements were found in 65/69 intI1-positive isolates (Table IV). The gene cassette arrangements were as follows: aacC4-cmlA1 (1.5%), dfr2d (18.45%), dfrA17-aadA5 (73.8%), aadA1 (10.8%) and negative control (7.7%). The variable region of the following integrons is presented in Fig. 3: dfr2d (549 bp), aadA1 (934 bp), aacC4+cmlA1 (2,327 bp), dfrA17+aadA5 (1,593 bp) and no gene cassette arrays (155 bp). Among them, 8 (12.3%) of the Escherichia coli isolates carried two integrons and 57 (87.7%) carried one integron.

Table III

Comparison of resistance for positive and negative strains of class 1 integrons.

Table III

Comparison of resistance for positive and negative strains of class 1 integrons.

Integron-positive (n=69)Integron-negative (n=28)


Antimicrobial agentResistance, %Isolates, nResistance, %Isolates, nP-value
CTX55.13828.680.015a
GEN76.85364.3181.156
TOB50.73514.340.001a
CFP50.73510.730.000a
SXT75.45232.190.000a
CAZ37.72625.070.169
AMP73.95142.9120.004a
FEP39.12721.460.074
TCY85.55975.0210.173
CIP73.95142.9120.004a
IPM14.5114.510.496
PIP88.46157.1160.001a
SAM13.090.000.040a
TZP7.257.120.676
CRO53.63717.950.001a
ATM36.22528.680.317

a P<0.05 vs. negative.

{ label (or @symbol) needed for fn[@id='tfn5-mmr-08-04-1251'] } ESBLs, extended spectrum β-lactamases; CTX, cefotaxime; GEN, gentamicin; TOB, tobramycin; CFP, cefoperazone; SXT, trimethoprim-sulfamethoxazole; CAZ, ceftazidine; AMP, ampicillin; FEP, cefepime; TCY, tetracycline, CIP, ciprofloxacin; IPM, imipenem; PIP, piperacillin; SAM, ampicillin-sulbactam; TZP, piperacillin-tazobactam; CRO, ceftriaxone; ATM, aztreonam.

Table IV

Type and arrangement of gene cassette contained in class 1 integrons.

Table IV

Type and arrangement of gene cassette contained in class 1 integrons.

Sample

Items123456
Integron numbers1D3D5D7D9D3D+5D
Strains of the total amount1440758
Variable length of integrons, bp23275491593934155549+1593
Total ratio, %1.56.1561.510.87.712.3
Containing resistance genesaacC4-cmlA1dfr2ddfrA17-aadA5aadA1-dfr2d -dfrA17-aadA5

Discussion

As shown in Table II, resistance (%) was detected in all Escherichia coli isolates of study. Higher resistance to 14 antimicrobial agents was detected in ESBL-positive isolates compared with ESBL-negative isolates (P<0.05). Resistance to AMP and PIP decreased depending on the inhibition of ESBLs by enzyme inhibitors.

In the current study, a total of 31 isolates (32.0%) producing ESBLs were identified among the 97 Escherichia coli isolates with the higher prevalence of CTX-M (Fig. 1; 61.3%, 19/31), consistent with a previous study (20). These observations indicate that the CTX-M group is dominant in Chengdu.

The aacC4, aadA1 and aadA5 genes encode resistance to aminoglycosides, cmlA1 encodes resistance to chloramphenicols and dfr2d and dfrA17 encode resistance to trimethoprim. The gene cassette array dfrA17+aadA5 is commonly used to detect class 1 integrons (21,22). The prevalence in the present study was lower than that observed previously by Ozgumus et al(23), which showed that all class 1 integron-bearing Escherichia coli contained the aadA5 gene cassette, conferring resistance to streptomycin and spectinomycin. The gene cassette with the lowest detection rate in the present study, aacC4+cmlA1, is infrequent in other studies.

Antimicrobial resistance phenotypes were studied in all isolates and the percentages of resistance detected were as follows (Table III; % integron-positive/% integron-negative isolates): CTX (55.1/28.6), GEN (76.8/64.3), TOB (50.7/14.3), CFP (50.7/10.7), SXT (75.4/32.1), CAZ (37.7/25.0), AMP (73.9/42.9), FEP (39.1/21.4), TCY (39.1/21.4), CIP (73.9/42.9), IPM (14.5/14.5), PIP (88.4/57.1), SAM (13.0/0), TZP (7.2/7.1), CRO (53.6/17.9) and ATM (36.2/28.6).

In addition, two isolates were resistant to IPM, and a higher percentage of resistance to 9 antimicrobial agents (Table III) was detected among integron-positive isolates compared with integron-negative isolates (P<0.05). The percentage of multi-resistant strains detected was 62.3% (43/69) among integron-positive isolates and 25.0% (7/28) among integron-negative isolates (P<0.05). These observations are in agreement with the hypothesis that class 1 integrons are important in the resistance of Escherichia coli to penicillins, third-generation cephalosporins, ciprofloxacin, aminoglycosides and monocyclic β-lactam antibiotic.

Elevated percentages of resistance were observed in a number of β-lactam drugs among ESBL-positive isolates compared with ESBLs-negative isolates. The percentages of resistance were as follows (% ESBL-positive/% ESBL-negative isolates): CTX (74.2/34.8), GEN (87.1/66.7), TOB (54.8/33.3), CFP (58.1/30.3), SXT (90.3/50.0), CAZ (58.1/22.7), AMP (96.8/50.0), FEP (61.3/21.2), TCY (90.3/78.8), CIP (90.3/53.0), IPM (6.5/0.0), PIP (93.5/72.7), SAM (29.0/0.0), TZP (19.4/3.2), CRO (51.6/25.8) and ATM (51.6/25.8). The percentage of multi-resistant strains detected was 80.6% (25/31) among ESBL-positive isolates and 37.9% (25/66) among ESBL-negative isolates (P<0.05). The resistance to third-generation cephalosporins observed was consistent with the existence of ESBLs, as reported by Birgy et al(24).

The resistance profiles of isolates with ESBLs and class 1 integrons are equal. We hypothesize that the presence of the genes resistant to SXT, GEN and TOB in the variable region and ESBLs cause resistance in Escherichia coli isolates to the aforementioned antibacterial drugs. In the current study, 26/31 (83.9%) producers of ESBLs were identified to contain class 1 integrons.

The present study indicates that class 1 integrons contributed to the multidrug resistance of Escherichia coli. Class 1 integrons are important for the transfer of resistance genes (25), as the integrons carry antimicrobial-resistant gene cassettes and specific resistance genes correspond to gene cassettes that are detected in clinical isolates of Gram-negative bacteria (26).

The distribution of ESBLs and class 1 integrons in Escherichia coli is prevalent with drug resistance in Chengdu. According to the results of the present study, the presence of class 1 integrons and ESBLs together mediates the resistance of Escherichia coli isolates to the majority of antibacterial agents. Based on our results, we hypothesize that the combined treatment of ESBLs and class 1 integron may offer a new perspective for treating resistant Escherichia coli.

Acknowledgements

The authors thank the Department of Pharmacology of Preclinical and Forensic Medical College of Sichuan University.

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October 2013
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Liu LT, Wan LH, Song XH, Xiong Y, Jin SJ and Zhou LM: Relevance of class 1 integrons and extended‑spectrum β‑lactamases in drug‑resistant Escherichia coli. Mol Med Rep 8: 1251-1255, 2013
APA
Liu, L., Wan, L., Song, X., Xiong, Y., Jin, S., & Zhou, L. (2013). Relevance of class 1 integrons and extended‑spectrum β‑lactamases in drug‑resistant Escherichia coli. Molecular Medicine Reports, 8, 1251-1255. https://doi.org/10.3892/mmr.2013.1626
MLA
Liu, L., Wan, L., Song, X., Xiong, Y., Jin, S., Zhou, L."Relevance of class 1 integrons and extended‑spectrum β‑lactamases in drug‑resistant Escherichia coli". Molecular Medicine Reports 8.4 (2013): 1251-1255.
Chicago
Liu, L., Wan, L., Song, X., Xiong, Y., Jin, S., Zhou, L."Relevance of class 1 integrons and extended‑spectrum β‑lactamases in drug‑resistant Escherichia coli". Molecular Medicine Reports 8, no. 4 (2013): 1251-1255. https://doi.org/10.3892/mmr.2013.1626