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Original research

Detection of genes TEM, OXA, SHV and

CTX-M in 73 clinical isolates of Escherichia
coli producers of extended spectrum Betalactamases and determination of their
susceptibility to antibiotics.
Tabbouche Sana1,5, Khudary Rami1,2, Beyrouthy
Racha1,6, Dabboussi Fouad1,5, Achkar Marcel3,
Mallat Hassan1, Hlais Sani1,4, Hamze Monzer1,5
Abstract
A total of 73 clinical isolates of extended spectrum - lactamase producing
Escherichia coli were sampled in North Lebanon. The ESBL resistance was screened
using disc diffusion method, while the resistance genes were detected by polymerase chain reaction (PCR). The results marked the high prevalence of gene CTX-M
(72 strains), whereas 33 strains carried the gene OXA, 16 strains carried the gene
TEM and 3 carried the SHV gene. The majority of the strains carried two or more
genes. This study points out the high rate of transmission of these genes among
Escherichia coli strains in NorthLebanon and shows a reduced sensitivity to quinolones (pipemidic acid(12.1%); ofloxacin (21.9%) and ciprofloxacin (23.9%), in addition,
all tested strains were highly susceptible to tigecycline (100%), fosfomycin (98.6%)
and imipenem (97.2%).

1Doctoral School of Sciences and Technology,

Azm center for Research in Biotechnology and
its Applications, Lebanese University, Tripoli,
Lebanon
2 American University of Middle East, Kuwait
3 Nini Hospital, Clinical laboratory, Tripoli,
Lebanon
4 Saint-Joseph University, Faculty of Medicine,
Beirut Lebanon
5Lebanese University, Faculty of Health, Tripoli,
Lebanon
6Laboratory of Bacteriology, Faculty of
medicine, Auvergne University, ClermontFerrand, France.
Correspondent: [email protected]
Tel.: +961 (6) 213 252 Mob: +961 (3) 228 881,
Tripoli, Lebanon.

Key words: ESBLs genes, E. coli, antibiotic susceptibility.

Introduction
The Enterobacteriaceae is a source of serious threatening diseases worldwide, with the occurrence of Escherichia coli (E. coli)
secondary to Gram positive cocci (1). Beta-lactam antibiotics
such as long spectrum cephalosporins and carbapenems are
the preferred treatment of enterobacterial infections (1). The
genes of extended spectrum beta-lactamases (ESBLs) are encoded by transferable plasmids (2); thus enabling these bacteria
to acquire ESBL by different resistance mechanisms. In recent
years, the emergence of -lactamases worldwide, increased
the challenge of infections caused by bacteria species carried
these enzymes (2). Moreover, the excessive and unregulated
use of antibiotics are the fundamental cause in the selection of
resistance mechanisms (1). The Enterobacteriaceae producers of
ESBLs have become a serious problem of public health worldwide since 1995, because of the increased emergence of new
variants; especially CTX-M) (3,4). In fact, the majority of the enterobacterial infections caused by ESBL producing organisms
are E. coli and K. pneumoniae strains carrying the CTX-M gene
responsible for community infections, especially the urinary
tract infections (1, 5).
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The aim of this study is to evaluate the susceptibility of the

ESBL producing E. coli strains to commonly used antibiotics
and to detect the presence of the four common ESBL genes:
TEM, OXA, CTX-M and SHV using PCR method.

Material and Methods

Bacterial Strains. A total of 73 clinical strains were isolated between the years 2007 and 2009 in the Microbiology department of the Nini laboratory hospital in Tripoli, North Lebanon.
Of these strains, 58 were isolated from urine, 3 from blood, 4
from bronchial fluid, 6 from deep wounds and 2 from peritoneal fluid. The strains were identified by the API 20E system
(bioMrieux France). A strain of E. coli CMUL 028 sensitive to
all antibiotics (Collection Microbiologie Universit Libanaise)
was used as control.
The other positive controls used in PCR, were E.coli strains obtained from the Collection dInstitut Pasteur: The CIP 103983
strain is TEM-4 positive, the CIP 105836 is SHV-1 positive and the
CIP 103982 strain is CTX-M positive. E.coli strain Imp 15 was
used as positive control for the gene OXA-1 (Table 1).

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TABLE 1. Primers sequences and PCR cycles performed for each tested gene (8).
Primer

Primer sequences

PCR cycles

TEM-1/F
TEM-1/R

ATGAGTATTCAACATTTCCG
CTGACAGTTACCAATGCTTA

1 cycle of 5 minutes (min) at 96 oC; 35 cycles of [1min at 96oC, 1min at 58 oC,

1min at 72 oC]; 1 cycle of 10min at 72 oC.

SHV-1/F
SHV-1/R

GGTTATGCGTTATATTCGCC
TTAGCGTTGCCAGTGCTC

1 cycle of 5min at 96 oC; 35 cycles of [1min at 96 oC, 1min at 60 oC, 1min at

72 oC; 1 cycle of 10min at 72 oC

OXA-1/F
OXA-1/R

ACACAATACATATCAACTTCGC
AGTGTGTTTAGAATGGTGATC

1 cycle 5min at 96 oC; 35 cycles of

[1min at 96 oC, 1min at 60oC, 2min at 72 oC]; 1 cycle of 10 min at 72 oC

CTX-MU1
CTX-MU2

ATGTGCAGYACCAGTAARGT
TGGGTRAARTARGTSACCAGA

1 cycle of 7 min at 94oC; 35 cycles of

[50seconds (sec) at 94 oC, 40sec at 50 oC, 1min at 72 oC]; 1 cycle of 5min at 72 oC

CTX-M1-A2
CTX-M1- B2

CTT CCA GAA TAA GGA ATC

CCG TTT CCG CTA TTA CAA

1 cycle of 10min at 94 oC, 30 cycles of [1min at 94 oC, 1min at 48 oC, 1 min at

72 oC], 1 cycle of 7min at 72 oC.

R and Y are variable nucleotides. R: Purine (adenine or guanine). Y: Pyrimidine (thymine or cytosine) (http://www.chem.qmul.ac.uk/iubmb/misc/naseq.html)

Antibiotics Susceptibility
The susceptibility of strains to antibiotics was performed using the disc diffusion method on Mller-Hinton agar following
the recommendations of the Comit Antibiogramme, Socit
Franaise de Microbiologie (CA-SFM) (www.sfm-microbiologie.
org).
The following antibiotic discs were used:
Ampicillin (AMP) (10g); ticarcillin (TIC) (75 g); piperacillin (PP)
(75g); amoxicillin clavulanic acid (AUG) (20/10g); piperacillin-tazobactam (TZP) (75/10g); cephalexin (CFL) (30g); cefuroxime (CXM) (30g); cefoxitin (FOX) (30g); cefixime (FIX)
(30g); cefotaxime (CTX) (30g); ceftazidime (CAZ) (30g); cefepime (FEP) (30g); imipenem (IMI) (10g); tigecycline (TGC)
(15g) ; aztreonam (AZM) (30g); trimethoprim - sulfamethoxazole (STX) (1,25/23,75g); colistine (Cs) (50g); ticarcillin - clavulanique acid (TCC) (75/10g); gentamicin (GEN) (15g); tobramicin (TM) (10g); amikacin (AMK) (30g); netilmicin (NET)
(30g); nitrofurantoin (FT) (300g); pipemidic acid (PIP) (20g);
pefloxacin (PEF) (5g); ciprofloxacin (CIP) (5g); fosfomycin
(FOS) (50 g) (BioRad, France).
The ESBL presence was screened using the disc diffusion
method on Mller-Hinton agar. The synergy between the clavulanic acid (Beta-lactamases inhibitor) and a third generation
cephalosporin: cefotaxime, ceftazidime, cefepime, and aztreonam, was detected following the recommendations of CASFM (www.sfm-microbiologie.org). The amoxicillin-clavulanic
acid disc was placed in the center of the plate at a distance of
25-30 mm between the cephalosporins and the amoxicillinclavulanic acid. The clavulanic acid inhibits the production of
ESBL by E. coli thus forcing sensitivity to cephalosporins upon
viewing visible expansion of the sensitivity zone by the side
of clavulanic acid disc, forming a mushroom shape confirms
the test.

The ESBL genes detection

The detection of gene sequences coding for the TEM, OXA,
SHV and CTX-M-type enzymes was performed by using a commercial Plasmid Miniprep kit ( GenEluteTM ) (Sigma-Aldrich), following the protocol delivered by the manufacturer. PCR was
applied using the ready Mix Kit (REDTaq ReadyMixTM PCR reaction Mix with MgCl2), Sigma - Aldrich, and the primers used to
amplify the above mentioned genes are listed in table I. Sixteen strains show none of these 4 genes. The Isoelectric focusing of these 16 strains was performed with a polyacrylamide
gel containing ampholines with a pH range of 3.5 to 10.0, using
the Multiphor II flat - bed (Pharmacia Biotech, Uppsala, Sweden); 2 hours of migration at 3000 V, 150 mA, 15W)(6). TEM-1 (pI
5.4), OXA-1 (pI 7.5), CTX-M-14 (PI 7.9) and CTX-M-15 (pI 8.6) were
used as standards. Molecular screening of blaCTX-M was performed using the primer of CTX-M1 as shown in the Table 1.

Results
The results shown in the Table 2 revealed a predominance of
the CTX-M gene among the strains of E. coli isolated in North
Lebanon (32 strains). The majority of the E. coli strains carried
two or more ESBL genes, and only one strain carried all 4 gene
types.
TABLE 2. CTX-M Genes distribution among 73 tested strains.
Gene type

No. of strains

CTX-M

32

OXA-1

CTX-M + TEM-1

CTX-M + OXA-1

22

CTX-M + SHV

CTX-M + OXA + TEM

CTX-M + OXA + TEM-1 + SHV

9
1

The number of strains carrying the CTX-M gene was 72 strains. The number of
strains carrying OXA-1 was 33 strains. The number of strains carrying only the
CTX-M gene (32 strains) and only the OXA-1 gene (1 strain) are shown above.

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The isoelectric focusing experiments pointed that 16 strains

produced -lactamases of pI 8.6 in addition to their natural respective -lactamases. The PCR-based analysis of -lactamaseencoding genes revealed that all these 16 strains harbored the
CTX-M1 gene.
Table 3 shows the results of susceptibility to antibiotics for
the 73 tested E. coli ESBLs producers. The results shows a low
susceptibility of these strains to quinolones (pipemidic acid:
12.5%) and fluoroquinolones (ofloxacin;25% and ciprofloxacin;28%). Two of the isolates were resistant to imipenem; the
first one carried 3 resistance genes (OXA, TEM & CTX-M) and
the second one carried the CTX-M gene alone.
TABLE 3. Antibiotics Susceptibility of the 73 tested strains.
Antibiotic

% Susceptibility

AMP

TIC

PP

AUG

23.3

TZP

82.2

CFL

CXM

FOX

82.2

FIX

CTX

CAZ

FEP

IMI

97.2

TGC

100

ATM

SXT

19.2

CS

100

TCC

23.19

GEN

35.2

TM

23.3

AMK

81.94

NET

60.9

FT

89.7

PIP

12.06

PEF/OF

21.9

CIP

23.9

FOS

98.6

ampicillin (AMP), ticarcillin (TIC), piperacillin (PP), amoxicillin clavulanic acid (AUG), piperacillin - tazobactam (TZP), cephalexin (CFL),
cefuroxime (CXM), cefoxitin (FOX), cefixime (FIX), cefotaxime (CTX),
ceftazidime (CAZ), cefepime (FEP), imipenem (IMI), tigecycline
(TGC), aztreonam (AZM), trimethoprim - sulfamethoxazole (STX),
colistine (Cs), ticarcillin - clavulanic acid (TCC), gentamicin (GEN),
tobramicin (TM), amikacin (AMK), netilmicin (NET), nitrofurantoin
(FT), pipemidic acid (PIP), pefloxacin (PEF), ciprofloxacin (CIP), fosfomycin (FOS).
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The susceptibility rates of these strains to the following antibiotics were: amoxicillin - clavulanic acid: 23.3%; ticarcillin clavulanic acid: 23.19%; imipenem97.2%; tazobactam - piperacillin 82.2%; cefoxitin 82.2%; trimethoprim - sulfamethoxazole
19.2%; amikacin 81.94%; gentamicin 35.2%; tobramycin 23.3%;
netilmicin 60.9%; tigecycline 100%; fosfomycin 98.6%; and nitrofurantoin 89.7%.

Discussion
The results of the study confirm the high prevalence of CTXM gene, while the prevalence of other SHV genes was very
low (Table 2). Recently, the ESBL distribution in Europe showed
a dramatic increase of CTX-M gene instead of TEM and SHV
genes (7). The ESBL production is much less frequent in Europe
than in Latin America and Asia, and they are even less frequent
in the Pacific than in North America (7).
Recent European studies on Enterobacteriaceae have also confirmed the persistence of strains producing TEM and SHV, and
the increasing prevalence of strains producing CTX-M (2). Other types of ESBL such as PER, GES, IBC and some OXA types are
existing. These genes are mostly detected in Pseudomonas aeruginosa and in Acinetobacter spp.(9). The prevalence of ESBL
productions revealed a significant geographical differences,
ranging from 0% (Iceland) to less than 1% (Estonia) to 41% for
E. coli (Romania) and 91% (Romania) for K. pneumonia (7).
In the past several years, the emergence of new variants of ESBL
producers, especially CTX-M has suggested the involvement of
the co-resistance to other drug classes during endemic condition. This co-resistance is due to the transmission of different
types of resistance genes within the same clone. Several studies showed that blaCTX-M genes are commonly found on large
plasmids that often carry other genes conferring resistance to
other antimicrobial agents including aminoglycosides, fluoroquinolones, chloramphenicols, tetracyclins and others (particularly, blaOXA-1, blaTEM-1, tetA, aac(6)-lbcr) (9-11). This may
explain the high rate of transmission of CTX-M gene among the
E. coli strains by acquiring R-plasmid, and often the high prevalence of the CTX-M resistance gene is combined with another
resistance genes in these strains.
The CTX-M gene predominates in Europe, while in other countries, the ESBL genes are more diverse (2,9). In the United Kingdom, a recent dramatic increase of the ESBL producing strains
was observed both in hospitals and in the community, and this
increase is attributed to CTX-M-15 (7). In Norway and Portugal,
the CTX-M is the ESBL enzyme most frequently found in E. coli
(12-13). In Italy, the prevalence of E. coli producers of ESBL has
also increased with a predominance of TEM (45.4%), SHV-12
and the emergence of CTX-M and PER (14). Few of these studies reported the type of ESBL produced by these strains and
some showed the presence of TEM, OXA, SHV and the dramatic
emergence of CTX-M (10,15,16,17).

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The major prevalence of ESBLs was attributed first to K. pneumonia strains which have produced TEM and SHV, and then
followed by the emergence of E. coli strains producers of CTXM which become the prevalent type (10,17).
In Turkey, a study conducted by Ozgumus et al. 2007, showed
that 15% of Enterobacteriaceae isolates are producers of ESBLs.
The 2 commonly TEM and SHV genes were detected. Of these
strains, 5 were carrying the gene TEM, 12 were carrying the
two genes TEM and SHV and 3 were negative for both of the 2
genes (18). Also, Kiratisin et al.2008 in Taland, have studied 235
strains of E. coli producers of ESBLs, and found that 87.3 % of
the strains were carriers of the gene CTX-M, 77% were carrying
TEM gene, and 3.8% were carriers of the gene SHV. In addition,
few strain produced VEB-1 and OXA-10, and non of the isolate
produced of PER and GES (19).
The general susceptibility pattern of ESBL producer strains to
antibiotics has decreased in recent years in many countries
(15,17,20). However, the present study showed high susceptibility patterns to the most effective antibiotics used against
E. coli producers of ESBLs. In addition, E.coli producer of ESBLs have mostly a reduced susceptibility to the trimethoprim
- sulfamethoxazole (19.2%), whereas other studies conducted in Bahrain and in Khartoum have shown different results
(21,22,23). But on the other site, this study revealed an alarming
decrease in the susceptibility of our isolates to the quinolones
and the fluoroquinolones (table 3). Similar results are found in
a study previously conducted in Lebanon (15), whereas other
studies carried out in the Middle East areas have shown higher
susceptibility rates of their isolates to fluoroquinolones (23, 24).
It is important to note that 23.3% of our isolates were susceptible to the clavulanic acid associated with the amoxicillin or
ticarcillin, whereas this percentage increased significantly in
the case of tazobactam associated with the piperacillin (82.2%).
Our results show a similarity with a study conducted by Oliver
et al. 2002 (25). The susceptibility of our isolates to cefoxitin
was 82.2%, which is similar to the results of study performed
in Iran by Mehrgan et al. 2008 (24).
With regards to the aminoglycosides, our results showed that
amikacin remains the most active drug (81.4%). Kader et al.
2005, have shown similar results in their study conducted in
Saudi Arabia (27). The susceptibility of gentamicin and tobramycin was low (35.2%, 23.3%) respectively, in comparison
to study carried out in recently in Sudan which has reported
higher susceptibility to aminoglycosides (23).
Among the 73 strains of E. coli producers of ESBLs, 58 (79.5%)
were isolated from urine; which indicates the highly occurrence
of these strains in urinary tract infections. A previous study
from the Calgary Health Region in Canada, demonstrated that
CTX-M - producing E. coli is emerging as an important cause of
community- onset urinary tract infections (28,29).

2011
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doi: 10:3823/704

It should be noted that the percentage of E. coli resistance to

ampicillin, aminoglycosides, tetracycline, chloramphenicol and
sulphonamides are lower in the industrialized countries than in
the developing countries (11), since the overuse and the uncontrolled use of antibiotics and the low standard of personal and
community hygiene are favoring the spread of resistant strains
between humans in the developing countries.
The results of the study confirm the high prevalence of CTXM gene, while the prevalence of other SHV genes was very
low (Table 2). Recently, the ESBL distribution in Europe showed
a dramatic increase of CTX-M gene instead of TEM and SHV
genes (7). The ESBL production is much less frequent in Europe
than in Latin America and Asia, and they are even less frequent
in the Pacific than in North America (7).
Recent European studies on Enterobacteriaceae have also confirmed the persistence of strains producing TEM and SHV, and
the increasing prevalence of strains producing CTX-M (2). Other
types of ESBL such as PER, GES, IBC and some OXA types are
exist. These genes are mostly detected in Pseudomonas aeruginosa and in Acinetobacter spp.(9). The prevalence of ESBL
productions revealed a significant geographical differences,
ranging from 0% (Iceland) to less than 1% (Estonia) to 41% for
E. coli (Romania) and 91% (Romania) for K. pneumonia (7).
In the past several years, the emergence of new variants of ESBL
producers, especially CTX-M has suggested the involvement of
the co-resistance to other drug classes during endemic condition. This co-resistance is due to the transmission of different
types of resistance genes within the same clone. Several studies showed that blaCTX-M genes are commonly found on large
plasmids that often carry other genes conferring resistance to
other antimicrobial agents including aminoglycosides, fluoroquinolones, chloramphenicols, tetracyclins and others (particularly, blaOXA-1, blaTEM-1, tetA, aac(6)-lbcr) (9-11). This may
explain the high rate of transmission of CTX-M gene among the
E. coli strains by acquiring R-plasmid, and often the high prevalence of the CTX-M resistance gene is combined with another
resistance genes in these strains.
The CTX-M gene predominates in Europe, while in other countries, the ESBL genes are more diverse (2,9). In the United Kingdom, a recent dramatic increase of the ESBL producing strains
was observed both in the hospitals and in the community, and
this increase is attributed to CTX-M-15 (7). In Norway and Portugal, the CTX-M is the ESBL enzyme most frequently found in
E. coli (12-13). In Italy, the prevalence of E. coli producers of ESBL
has also increased with a predominance of TEM (45.4%), SHV-12
and the emergence of CTX-M and PER (14). Few of these studies reported the type of ESBL produced by these strains and
some showed the presence of TEM, OXA, SHV and the dramatic
emergence of CTX-M (10,15,16,17).
The major prevalence of ESBLs was attributed first to K. pneumonia strains which have produced TEM and SHV, and then

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followed by the emergence of E. coli strains producers of CTXM which become the prevalent type (10,17).
In Turkey, a study conducted by Ozgumus et al. 2007, showed
that 15% of Enterobacteriaceae isolates are producers of ESBLs.
The 2 commonly TEM and SHV genes were detected. Of these
strains, 5 were carrying the gene TEM, 12 were carrying the
two genes TEM and SHV and 3 were negative for both of the
2 genes (18).
In Taland, Kiratisin et al.2008, have studied 235 strains of E.
coli producers of ESBLs, and found that 87.3 % of the strains
were carriers of the gene CTX-M, 77% were carrying TEM gene,
and 3.8% were carriers of the gene SHV. In addition, few strain
produced VEB-1 and OXA-10, and non of the isolate produced
of PER and GES (19).
The general susceptibility pattern of ESBL producer strains to
antibiotics has decreased in recent years in many countries
(15,17,20). However, the present study showed high susceptibility patterns to the most effective antibiotics used against
E. coli producers of ESBLs. In addition, E.coli producer of ESBLs have mostly a reduced susceptibility to the trimethoprim
- sulfamethoxazole (19.2%), whereas other studies conducted in Bahrain and in Khartoum have shown different results
(21,22,23). But on the other site, this study revealed an alarming
decrease in the susceptibility of our isolates to the quinolones
and the fluoroquinolones (table 3). Similar results are found in
a study previously conducted in Lebanon (15), whereas other
studies carried out in the Middle East areas have shown higher
susceptibility rates of their isolates to fluoroquinolones (24, 25).
It is important to note that 23.3% of our isolates were susceptible to the clavulanic acid associated with the amoxicillin or
ticarcillin, whereas this percentage increased significantly in
the case of tazobactam associated with the piperacillin (82.2%).
Our results show a similarity with a study conducted by Oliver
et al. 2002 (25). The susceptibility of our isolates to cefoxitin
was 82.2%, which is similar to a study performed in Iran by
Mehrgan et al. 2008 (24).
With regards to the aminoglycosides, our results showed that
amikacin remains the most active drug (81.4%) against tested
E.coli strains. Kader et al. 2005, have shown a similar result in
their study conducted in Saudi Arabia (27).
This study has also demonstrated that 58/73 (79.5%) of E. coli
strains which produced ESBLs, were isolated from urine; which
indicates the highly occurrence of these strains in urinary tract
infections. A previous study from the Calgary Health Region in
Canada, demonstrated that CTX-M-producing E. coli is emerging as an important cause of community-onset urinary tract
infections (27). Pitout, JD et al. 2008, have documented that
extended-spectrum -lactamase producing Enterobacteriaceae are becoming an emerging public-health concern (28).
It should be noted that the percentage of E. coli resistance to
ampicillin, aminoglycosides, tetracycline, chloramphenicol and
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sulphonamides is lower in the industrialized countries than in

the developing countries (11), since the overuse and the uncontrolled use of antibiotics and the low standard of personal and
community hygiene are favoring the spread of resistant strains
between humans in the developing countries.

Conclusion
This study confirms the large dissemination of the gene CTX-M
among E. coli in the North Lebanon, and the results of antibiotic susceptibility revealed a high rates of resistance against
the quinolones and the fluoroquinolones which are widely
used in treatment of the urinary tract infections in Lebanon.
These results should draw the attention of the Lebanese medical authorities to the serious consequences of increasing antimicrobial resistance, therefore, it is import to increase efforts
to monitor and control the spread of antimicrobial resistant
strains in hospitals and community.

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