Journal of Current Biomedical Reports jcbior.com
Volume 2, Number 3, 2021 eISSN: 2717-1906
1
Original research
Detection of extended-spectrum beta-lactamase genes among
Escherichia coli isolates from urinary tract infection in Mashhad
Maryam Hafiz1, Gholamreza Hashemi Tabar1,*, Mehrnaz Rad1
1Department of Pathobiology, School of Veterinary Medicine, Ferdowsi University of Mashhad, Mashhad, Iran
Abstract
Urinary tract infections (UTIs) are known as one of the most important infections around the world,
and Escherichia coli is the most important cause of UTI. Also, the empiric treatment and misusing of
antimicrobial agents has led to increasing multi-drug resistance around the world which is a worldwide
concern. Extended-spectrum beta-lactamase (ESBLs) is an enzyme group that is produced by the
Enterobacteriaceae family. The three main ESBLs enzyme are as follow: blaCTX-M, blaTEM, and blaSHV,
additionally, there are several types of each of them by the same mechanism. This study was conducted
to evaluate the prevalence of ESBL genes among E. coli isolated from UTI patients. A total of 105 isolates
were collected from UTI patients at two hospitals in Mashhad from 2017 to 2019. Bacterial
identification was performed by standard microbiologic methods. The assessment of antimicrobial
susceptibility was accomplished by the disk diffusion method. The presence of ESBL genes was
investigated by multiplex-PCR. The prevalence of UTI, among females, was identified more than males.
Furthermore, the blaTEM and blaCTX-M genes were detected in all isolates, but only six isolates (5.7%)
were harboring blaSHV. The considerable role of E. coli in UTI infection, as well as the presence of ESBL
genes in E. coli strains, emphasize the need for surveillance of antimicrobial therapy to prevent the
extension of resistance among clinical strains.
Keywords: Escherichia coli, ESBL, Urinary tract infection, Multiplex-PCR
1. Introduction
Urinary tract infections (UTIs) happen through
community-acquired or nosocomial-acquired, which
are one of the most prevalent types of human infection
[1, 2]. Escherichia coli is known as the most important
pathogen in UTIs, among both outpatient and
inpatient [3, 4]. On the other hand, the empiric of
treatment and misusing of antimicrobial agents such
as, beta-lactams, beta-lactamase inhibitor,
fluoroquinolones, and carbapenems, has led to
increasing multi-drug resistance around the world
which is a worldwide concern [5, 6]. Extended-
spectrum beta-lactamase (ESBLs) is an enzyme group
*Corresponding author:
Gholamreza Hashemi Tabar, Ph.D
Azadi Square, Mashhad, Razavi Khorasan Province, Iran,
P.O. Box: 9177948974
Tel/Fax: +98 51 38836056
Email: hashemit@um.ac.ir
https://orcid.org/0000-0001-9760-1096
Received: June, 14, 2021
Accepted: July, 12, 2021
that is produced by the Enterobacteriaceae family,
which are mostly isolated from inpatient cases [7]. The
ESBL positive bacteria are able to inactivate several
antimicrobial agents including an oxyimino-group
such as cephalosporins (e.g. ceftazidime, and
ceftriaxone), monobactam (e.g. aztreonam), but not
able to inactivate cephamycin, and carbapenems [7,
8]. The three main ESBL enzymes are blaCTX-M, blaTEM,
and blaSHV [9, 10]. These enzymes are encoded
generally by genes located on plasmids. Actually, the
mutation in these genes (particularly blaTEM and
blaSHV) led to the change in the form of the enzyme
near its active site to increment the affinity and
© The Author(s) 2021
https://jcbior.com/
Hafiz et al.
2
hydrolytic capability of beta-lactamase for oxyimino
compounds [11]. Also, some of them are encoding on
transposons which could transmit between organisms
[8]. The growing up of ESBL producing strains brings
up some problems including the transmission of
resistance to other organisms, refusing treatment, and
increase in mortality rate. So, more surveillance is
needed to identify the rate of the problem and help to
select appropriate antimicrobial agents to treat the
infection. This study was conducted to evaluate the
prevalence of blaTEM, blaCTX-M, and blaSHV genes by
multiplex polymerase chain reaction (M-PCR) among
E. coli isolated from UTI patients.
2. Materials and Methods
2.1 Sample’s collection
A total of 105 E. coli isolates were collected from
UTI patients at Ghaem and Emamreza hospitals in
Mashhad from 2017 to 2019. Also, the basic
information of patients was gathered, including age
and gender, UTI history, hospital visit reports, and
reports of taken antimicrobial agents from patients.
Isolates cultured on selective-differential media,
MacConkey agar (MAC), and Eosin Methylene Blue
agar (EMB), were incubated overnight at 37°C. Then,
microscopically examination was done by Gram
staining from lactose-positive colonies. Likewise,
biochemical profiling, such as Oxidase/Catalase
activity, Motility, Indole, Urease, Triple Sugar Iron
agar (TSI), and Methyl Red-Voges Proskauer test
(MR-VP) has been studied.
2.2 Antimicrobial susceptibility test
The assessment of antimicrobial susceptibility was
accomplished by the disk diffusion method
recommended by the Clinical and Laboratory
Standards Institute (CLSI, 2020) (13)[12], against 15
antibiotic disks (Padtanteb, Iran) as follow:
ceftazidime (30 μg), imipenem (10 μg), amikacin (30
μg), nalidixic acid (30 μg), ampicillin (10 μg),
ciprofloxacin (5 μg), cefixime (5 μg), cefazoline (30 μg),
ceftriaxone (30 μg), meropenem (10 μg), gentamicin
(10 μg), nitrofurantoin (300 μg), cefepime (30 μg),
cefotaxime (30 μg) and co-trimoxazole (1.25/23.75
μg). E. coli ATCC 25922 was used as a positive control
for antimicrobial susceptibility tests.
2.3 PCR amplification
DNA extraction was done by the boiling method
as described earlier by Nazari et al. [13]. The prepared
DNA samples were assessed for prevalence of blaTEM,
blaSHV, and blaCTX-M genes by M-PCR by using the MJ
mini thermal cycler (Bio-Rad, Hercules, CA, USA)
[14]. The PCR reaction was conducted in 25 volumes
including 12.5 μl of PCR 2X MasterMix (Parstous
company, Iran) containing Taq DNA Polymerase,
reaction buffer, dNTPs mixture, a protein stabilizer,
and the convenience for use was optimized by adding
Table 1. The information of oligonucleotides used as primer in multiplex-PCR
Primer name Primer sequence (5’-3’) Amplicon size (bp) Reference
blaTEM164.SE TCG CCG CAT ACA CTA TTC TCA GAA TGA
445
14
blaTEM164.AS ACG CTC ACC GGC TCC AGA TTT AT
blaSHV.SE ATG CGT TAT ATT CGC CTG TG
724
blaSHV.AS TGC TTT GTT ATT CGG GCC AA
blaCTX-M. U1 ATG TGC AGC ACC AGT AAA GTG ATG GC
593
blaCTX-M. U2 TGG GTA AAG TAA GTG ACC AGA ATC AGC GG
Table 2. The frequency of UTI in different age groups
Age groups <10 11-20 21-30 31-40 41-50 51-60 >60
Female 8 3 9 5 5 10 16
Male 5 0 2 3 6 5 28
Total a 13 3 11 8 11 15 44
a Results presented as number of cases
Hafiz et al.
3
sediment for electrophoresis and 2x solution of
loading dye, 1 μl of each primer (10 pM), 2 μl of DNA
template (100 ng/reaction) and 4.5 μl of Nuclease-free
water. PCR conditions were as follow: initial
denaturation at 95°C for 15 seconds; followed by 35
cycles of denaturation at 94°C for 30 seconds,
annealing at 61°C for 40 seconds, and extension at
72°C for 2 minutes with a final extension at 72°C for 10
minutes [15]. Electrophoresis of amplicons was
performed using 1.5% agarose gels. The primers'
information is listed in Table 1. Also, E. coli ATCC
35218 and distilled water were used as the positive and
negative control, respectively.
3. Results
3.1 Prevalence of UTI in different ages and
genders
Based on the results, it was determined that the
prevalence of UTI among females with 56 (53.3%)
cases was more than males with 49 (46.7%) cases.
Most isolates were recovered from patients with >60
ages, and the lowest rate was observed in 11-20 age
groups. The information of patients’ age groups was
listed in Table 2.
3.2 Antimicrobial susceptibility test
According to the results, amikacin (98%),
meropenem (93%), nitrofurantoin (89%), and
imipenem (88%) revealed the highest activity against
isolates, respectively. All results are listed in Table 3.
3.3 PCR results
The analysis of PCR products on gel
electrophoresis revealed that the most prevalent
ESBLs among studied isolates were blaTEM, and blaCTX-
M genes (100%). While only six (5.71%) isolates were
carried the blaSHV gene.
4. Discussion
UTI is known as one of the most highlighted
healthcare infections. Our finding notes that women
have a higher rate of UTI than men. This fact confirms
earlier findings of the stress UTI in females [16-19].
Also, the most prevalent was observed in the >60 age
group, which was similar to previous surveys [20, 21].
However, this result was in contrast with other
observations, which reported the highest prevalence in
2-10 and 20-29 age groups, respectively [17, 22]. Our
results revealed the highest resistance rate for
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Hafiz et al.
4
ampicillin (82.8%) and cotrimoxazole (70.4%) which
was consistent whit previous surveys [17, 23-25].
However, another study was recorded a lower
resistance rate for ampicillin and cotrimoxazole, 67%
and 45%, respectively [26]. On the other hand, the
highest susceptibility was observed against amikacin,
meropenem, nitrofurantoin, and imipenem. While the
lower susceptibility for amikacin (61%) and
nitrofurantoin (72%) has been reported in an earlier
survey [27]. However, our finding for nitrofurantoin
susceptibility was close to other studies [17, 28]. Also,
the susceptibility rate of isolates to imipenem and
amikacin in the current study was in line with previous
surveys [17, 23, 29].
According to earlier reports, the high rate of ESBL-
E. coli was noted from UTI among both inpatient and
outpatient, whereas it was more significant among
inpatient [24, 30].
Generally, the highest presence of ESBLs was
recorded for blaTEM and blaCTX-M, which was in line
with earlier results [9, 31-34]. Although, some studies
reported a lower rate of blaCTX-M, 28%, and 32%,
respectively [35, 36]. This discrepancy can be
explained by different geography and the increase of
genes transferring during the time. On the other hand,
blaSHV was detected in only six isolates. Our
experiment about the prevalence of the blaSHV gene
was close to previous survey [33]. According to these
results, the blaSHV gene is not predominant as the two
other genes. However, new studies revealed a high
frequency of blaSHV that might increase in the future
[11, 37]. Certainly, further tests such as confirmatory
ESBL test and statistical analysis are required to
determine the relationship between these genes and
resistant phenotype.
The considerable role of E. coli in UTI infection, as
well as the presence of ESBL genes in E. coli strains,
emphasize the need for surveillance of antimicrobial
therapy to prevent the extension of resistance among
clinical strains.
Acknowledgments
The authors would like to thank all Ghaem and
Imam Reza hospitals staff, which collaborating in
collecting isolates.
Author contributions
All authors contributed equally to each part of the
manuscript and approved the final version.
Conflict of interests
The authors claim that there is no conflict of
interest.
Ethical declarations
This study was in accordance with the declaration
of Helsinki and ethical permission was sought from
the institutional Ethics Committee of Ferdowsi
University of Mashhad, Mashhad, Iran. However,
because we only used leftovers from clinical
specimens, the local ethics committee waived the need
for informed consent.
Financial Support
This study was funded by Ferdowsi University of
Mashhad, Mashhad, Iran (Grant number 109).
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