THE INTERNATIONAL ARABIC JOURNAL

OF ANTIMICROBIAL AGENTS
Under License of Creative Commons Attribution 3.0 License 1
2014
Vol. 4 No. 1:2
doi: 10.3823/744
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Antimicrobial resistance patterns
of diarrheagenic and non-
diarrheagenic Escherichia coli
isolates from Libyan children
1 Benghazi Children Hospital, Libya and
2 Department of Pathology-Microbiology
Faculty of medicine, The Jordan
University, Amman, Jordan.
Corresponding author:
Prof. Asem A. Shehabi
ashehabi@ju.edu.jo
ashehabi@go.com.jo
Entisar Alnagi Omran
1,2
,
Azmi M. Mahafzah
2
,
Asem A. Shehabi
2
Abstract
Background: Diarrhea continues to be one of the most common cause
of morbidity and mortality among infants and children in developing
countries. This study was carried out among Libyan children hospital-
ized in Benghazi children hospital, to be investigated for the incidence
of diarrheagenic E.coli types and antimicrobial susceptibility proles of
all E.coli isolates in their stool samples.
Methods and patients: A total of 200 children with diarrhea and 90
without diarrhea were their stools investigated using culture on Mac-
Conkey agar, and the E.coli isolates were examined for detection of
diarrheagenic E. coli types, antimicrobial susceptibility pattern, pres-
ence of integrons, ESBL-CTX-M and uroquinolone resistance genes
using PCR.
Results: The study has indicated that diarrheagenic E.coliisolates were
found only in stools of children with diarrhea. The detected diarrhea-
genic E. coli types were the following: 4 (2%) enteroaggregative E.
coli (EAEC), 3 (1.5%) enteroinvasive E. coli (EIEC), and 1(0.5%) entero-
hemorrhagic E. coli (EHEC), and both enterotoxigenic E.coli(ETEC) and
enteropathogenic E.coli(EPEC) were not present. It has also found that
multidrug resistant E.coli (> 3 drugs) was higher prevalent in com-
mensal intestinal E.coli than in diarrheagenic E.coli isolates, and both
carried high rates of Class 1 integrons, bla(CTX-M) and uroquinolone
resistance genes.
Conclusion: This study revealed the low incidence of diarrheagenic
E. coli isolates and high prevalent of antimicrobial resistance among
normal intestinal E.coli of hospitalized children in Benghazi/Libya.
Key words: Diarrheagenic E.coli, antimicrobial-resistance genes, Libya.
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Introduction
Infectious diarrhea continues to be one of the most
common cause of morbidity and mortality affect-
ing children in many developing countries. It is the
second leading cause of death in children under
ve years old, and both Rotavirus and diarrheagen-
ic E.coli are the leading cause of diarrheal disease
[1]. Among the bacterial pathogens, diarrheagenic
Escherichia coli (E.coli) is an important agent of en-
demic and epidemic diarrhea worldwide and espe-
cially in developing countries [1,2].
Among the E. coli causing diarrhea, there were ve
commonly recognized types : enterotoxigenic E. coli
(ETEC), enteropathogenic E. coli (EPEC), and en-
teroinvasive E. coli (EIEC), enteroaggregative E. coli
(EAEC), enterohemorhagic E. coli (EHEC). Each type
has specic virulence factors that are used for their
identication and classication. With the exception
of EHEC , especially E. coli 0157:H7 , diarrheagenic
E. coli strains are not routinely detected in most
clinical laboratories [2].
Diarrheal disease caused by E.coli are usually trans-
mitted through food or water contaminated with
human or animal feces [3,4]. Person-to-person
transmission might also take place, but it is probably
less common. There are few studies from the Arab
countries including Libya which have investigated
the occurrence of diarrheagenic E.coli genotypes
and their antimicrobial susceptibility proles during
the last 10-year [5-11].
Accurate detection and identication of diarrhea-
genic E.coli cant be done only by culture, biochemi-
cal and serotyping tests, since they are indistinguish-
able from the non- pathogenic E.coli commonly
found in human feces. Therefore, only DNA based
method such as polymerase chain reaction (PCR)
assay can be used for rapid and reliable diagnosis,
and which has a high sensitivity and specicity for
their detection [12,13].
The present study carried out with the aim to de-
termine the incidence of diarrhoeagenic E. coli in
hospitalized children in Benghazi Children Hospital,
Libya, using multiplex PCR , and to investigate the
antimicrobial resistance proles of commensal intes-
tinal E.coli isolates in these children.
Patients & Methods
Patients
A total of 290 stool samples were collected from
hospitalized children in the Children Hospital of
Benghazi, Libya, over a period of 3 months (March
to June 2012). Of these, 200 stool samples were
obtained from patient with diarrhea and 90 samples
from healthy controls without diarrhea. The study
was approved by the administration of Benghazi
Children Hospital, Libya. An informed consent was
obtained from parents. Data collection included the
following: age, gender, presence or absence of wa-
tery or bloody diarrhea, fever, antibiotic treatment,
and presence of specic associated disease.
Collection of stool samples
Stool samples were collected from children using
a cotton swabs and these were directly inoculated
into transport uid medium. All samples were trans-
ferred to the microbiology laboratory for culture in
the laboratory of Benghazi Children Hospital.
Isolation and Conrmation the identity of
E.coli isolates
Each fresh stool sample was cultured directly on
MacConkey agar plate (Oxoid, Basingstoke, Eng-
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doi: 10.3823/744
Under License of Creative Commons Attribution 3.0 License 3
land) and incubated aerobically at 37c for 18-24h.
A total of 10 red colonies that morphologically sus-
pected to be E.coli were picked up and incubated
in 1 ml brain-heart infusion broth tubes which con-
tained 25% glycerol, and the tubes were stored at
-70C for further investigation. All other investiga-
tions were carried out at the Research Microbiology
Laboratories, Faculty of Medicine, The Jordan Uni-
versity, Amman, Jordan. All collected E.coli isolates
were identied rst on basis of lactose fermentation
on MacConkey, biochemical tests including fermen-
tation of Triple sugar iron agar test(TSI), positive in-
dole and citrate utilization test, and negative urease
production.
Multiplex PCR reaction for detection
Diarrheagenic E. coli
DNA extraction was performed using G-spin To-
tal DNA Extraction Kit ( INTRON Biotechnology /
Gyeonggi-do 462-807 Korea). The DNA extracts of
investigated E.coli isolates were used after spectro-
photometric quantitation for detection of the fol-
lowing markers: eaeA (structural gene for intimin of
EHEC and EPEC), bfpA (structural gene for EPEC),
vt1 and/or vt2 (Shiga toxins 1 and 2 of EHEC), eltB
and/or estA (enterotoxins of ETEC), ial (EIEC), and
pCVD (EAEC) as described by Shehabi et al. [11].
The primers selected for use in the amplication
are matched the sequences of the corresponding
genes of EAEC, EHEC, EIEC, EPEC, and ETEC in the
GenBank and EMBL database libraries as shown in
Table 1.
Table 1. Primers used for detection of diarrheagenic E.coli and antimicrobial resistant genes.
Primer Target gene Primer sequence (5-3) Amplicon size (bp)
LT eltB
5-TCTCTATGTGCATACGGAGC-3
322
5-CCATACTGATTGCCGCAAT-3
ST estA
5-GCTAAACCAGTAG AGGTCTTCAAAA-3
147
5-CCCGGTACAG AGCAGGATTACAACA-3
VT1 vt1
5-GAAGAGTCCGTGGGATTACG-3
130
5-GAAGAGTCCGTGGGATTACG-3
VT2 vt2
5-ACCGTTTTTCAGATTTTGACACATA-3
298
5-TACACAGGAGCAGTTTCAGACAGT-3
Eae eaeA
5-CACACGAATAAACTGACTAAAATG-3
376
5-AAAAACGCTGACCCGCACCTAAAT-3
SHIG Ial
5-CTGGTAGGTATGGTGAGG-3
320
5-CCAGGCCAACAATTATTTCC-3
bfpA bfpA
5-TTCTTGGTGCTTGCGTGTCTTTT-3
367
5-TTTTGTTTGTTGTATCTTTGTAA-3
EA PCVD
5-CTGGCGAAAGACTGTATCAT-3
630
5-CAATGTATAGAAATCCGCTGTT-3
THE INTERNATIONAL ARABIC JOURNAL
OF ANTIMICROBIAL AGENTS
2014
Vol. 4 No. 1:2
doi: 10.3823/744
This article is available from: www.iajaa.org 4 Received 10 June 2014; accepted 6 July 2014
Antimicrobial Susceptibility testing
Antimicrobial susceptibility testing of E.coli isolates
was performed by the Kirby-Bauer disk diffusion
method on Mueller-Hinton agar medium (Oxoid,
Basingstoke, England), MICs of 4 antimicrobials were
determined using Etest (BioMerieux Inc., France).
The results were interpreted according to the rec-
ommendation guidelines of the Clinical Laboratory
and Standards Institute (CLSI,2012) (14 ). In addition,
the isolates were investigated for presence of inte-
grons (classes I, II, and III) and antibiotic-resistance
genes of bla(CTX-M) as reported by AbSalah et al.
2013 [15]. The antimicrobial drugs tested are shown
in Table 3. E. coli ATCC 25922 strain was included
as a control in all laboratory assays.
Results
This prospective study investigated a total of 290
hospitalized children with and without diarrhea
(control group) aged between one month and ap-
proximately 48 months. The 200 patients with di-
arrhea included 115 (57.5%) males and 85 (42.5%)
females divided according their age in 7 groups as
shown in Table 2. A total of 62% of children with
watery / bloody diarrhea and have fever were aged
one year. The control group included 90 children
without diarrhea, of these 50 (55.6%) were females
and 40 (44.4%) were males (Table 2).
Table 2. Distribution of age among the two groups of examined children.
Total
No. (%) Age/months
Children group
37-48 31- 36 25 -30 19 -24 13- 18 7-12 1-6
200
14
(7)
8
(4)
7
(3.5)
15
(7.5)
32
(16)
77
(38.5)
47
(23.5)
Diarrhea
90
4
(4.4)
7
(7.8)
12
(13.3)
16
(17.8)
19
(21.1)
16
(17.8)
16
(17.8)
Control
290 18 15 19 31 51 93 63 Total
Table 3. Distribution of diarrheagenic E.coli types in stools of 290 children.
No. (%) Children
Diarrheagenic E. coli
Without diarrhea** With diarrhea*
0 3 (1.5) EIEC
0 1 (0.5) EHEC
0 4 (2) EAEC
0 0 EPEC
0 8 (4) Total
* 102 (51%) and ** 41(45.6% ) were on antibiotic treatment during collection of stools
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The following diarheagenic E.coli isolates were re-
covered from all examined 290 stool samples of
children; 4 (2%) enteroaggregative E. coli (EAEC, 3
(1.5%) enteroinvasive E. coli (EIEC), and one 1(0.5%)
enterohemorrhagic E. coli (EHEC) (Table 3).
The antibiotic susceptibility results of the 8 diarrhea-
genic E. coli isolates are shown in Table 4. The re-
sults has shown that most of 8 diarrheagenic E.coli
isolates were susceptible to ciprooxacin (100%),
cefotixin (100%), gentamycin (100%), nalidixic acid
(100%), amikacin (87.5%), nitrofurantoin (87.5%),
ceftazidime (75%), ceftriaxone (75%), cefotixim
(75%), augmentin (50%) and cotrimoxazole (37.5%)
(Table 3). The susceptibility results of the 15 non-
diarrheagenic E. coli isolates which were resistant to
3 drugs (Multidrug Resistant; MDR) were the fol-
lowing: cefotixin (73.3%), amikacin (53.3%), genta-
mycin (40%), nitrofurantoin (40%), ceftazidime
(33.3%), ciprooxacin (33.3%), ceftriaxone (26.7%),
cefotixime (26.7%), cotrimoxazole (26.7%) nalidixic
acid (26.7%) and augmentin (6.7 %). High MICs
90

(mg/L) (10. 12 to >128 ) were observed for the fol-
lowing examined drugs; ciprooxacin, gentamycin,
ceftriaxone and cefotaxime, respectively (Table 4).
The distribution results of bla CTX-M genes among
15 MDR non-diarrheagenic E.coli isolates were the
following: CTX-M group I was found in 8(53.3%),
CTX-M group II in 3(20%), CTX-M 15 in 9 (60%),
CTX-M 8 and CTX-M 9 were not detected in any of
the isolates, respectively (Table 5). While diarrhea-
genic E.coli results showed that CTX-M 8 and CTX-
M 9 were detected in 100%, CTX-M group II in 7
(87.5%), CTX-M group I in 3 (37.5%), and CTX-M
15 in 1 (12.5%) of the isolates, respectively ( Table
5). Both diarrheagenic and commensal E,coli carried
only 47% and 50% of Class I integrons, respectively
(Table 5). The distribution of potential quinolone
resistance genes (Gyr A, Parc) and integrons among
Table 4. Antimicrobial susceptibility of 15 representative MDR of commensal E.coli and 8 diarrheagenic
E. coli isolates from stool of children*
Antibiotics
Diarrheagenic E.coli Non-diarrheagenic E.coli Non-diarrheagenic E.coli
(%) Susceptible (%) Susceptible MICs90 (mg/L)
Ciprooxacin 100 33.3 10.12
Cefotixin 100 73.3 -
Gentamycin 100 40 >64
Nalidixic acid 100 26.7 -
Amikacin 87.5 53.3 -
Nitrofurantoin 87.5 40 -
Ceftazidime 75 33.3 -
Ceftriaxone 75 26.7 >32
cefotaxime 75 26.7 >128
Augmentin 50 6.7 -
Cotrimoxazole 37.5 26.7 -
*MDR accounted for 64 % of all 290 E.coli isolates
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Vol. 4 No. 1:2
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MDR commensal E.coli isolates were the following:
11/15 (73.3%) carried both Gyr A, Parc genes and
7/15 (47% ) harbored Class 1 integrons, whereas
8/8 (100%), 7/8 (87.5%) and 4/8(50%) of diarrhea-
genic E.coli isolates carried Gyr A, Parc genes and
integrons, respectively.
Discussion
This study demonstrates that the majority of chil-
dren with watery or bloody diarrhea (62%) were
aged less than1-year and presented with fever.
These features are similar to many other studies
described from the developing countries [1, 6-8-11].
The present study showed that diarrheagenic E.coli
isolates were found only in 4 % of children with di-
arrhea and no single diarrheagenic E.coli isolate was
detected in the control children group. The study
also indicated the presence of (EAEC), (EIEC) and
(EHEC), whereas the two types (EPEC and ETEC)
were not detected in any child (Table 3). The pres-
ence rate of EAEC among diarrheal cases in this
study is much similar to studies recently reported
from Libya, Egypt and Iran [5,6,16-17], but in con-
trast to the other studies carried out in Kuwait and
Jordan which had shown that EAEC was not a cause
of diarrhea in their examined pediatric population
[8,11]. However, the absence or low occurrence rate
of EIEC (1.5%) in diarrhea cases and controls in this
study is similar to the results of other reported stud-
ies from Egypt, Kuwait and Jordan [6,8,11]. In addi-
tion, it is important to note here that about half of
the examined children were on antibiotic treatment
during collection of their stool samples, and this
might has been interfered with rate of recovery of
diarrheagenic E.coli.
The results of this study showed high rates of an-
timicrobial resistance (24-93%) to many antimicro-
bial classes, including 3-generation cephasporines
(Ceftazidim, ceftriaxone, cefotixime ), and MDR
E.coli accounted for 64% of all isolates (Table 4).
All MDR commensal intestinal and diarrheagenic
E.coli isolates carried various resistance rates (12-
100%) bla(CTX-M) genes, and particularly CTXM-
15 found more frequently in commensal intestinal
E.coli than diarrheagenic E.coli isolates (60% versus
12.5%). These results are similar to some extend
Table 5. Distribution of integrons, genes of bla(CTX-M) , and uoroquinolone resistance (Gyr A and Par
C) in diarrheagenic E.coli and multidrug resistant of commensal E.coli isolates
No.(%) of 8 Diarrheagenic
E.coli isolates
No.(%) of 15 Multidrug resistant
commensal E.coli isolates
Genes
3 (37.5) 8 (53.3) CTX-M I
7 (87.5) 3 (20) CTX-M II
8 (100) Null CTX-M 8
8 (100) Null CTX-M 9
1 (12.5) 9 (60) CTX-M 15
4(50) 7 (47) Class 1 integrons
8 (100) 11 (73.3) Gyr A gene
7 (87.5) 11 (73.3) Par c gene
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Under License of Creative Commons Attribution 3.0 License 7
to many recent studies carried out in other Arabic
countries [15,18-21]. Over the past ten years, the
bla(CTX-M) genes have become the most preva-
lent ESBLs among multidrug resistant organisms
worldwide, started rst in certain countries of Eu-
rope and South America, and later spread to India
China, and other countries[ 15, 18,19, 21,23, 24].
In addition, this study showed high rates of Class I
integrons in both MDR intestinal commensal E.coli
and diarrheagenic E.coli isolates (73-100%) which
carried one or both potential uroquinolone resist- both potential uroquinolone resist- uinolone resist-
ance genes (gyrA and parC) (Table 5). It has been
previously established that high prevalence of Class
I integrons contributes to increase the development
of MDR in Enterobacteriaceae and particularly in fe-
cal E.coli [25- 27]. Also, uoroquinolone resistance
inE. colirepresents a substantial threat among com-
munity patients, since these drugs are increasingly
used in empirical therapy of urinary tract and other
infections [28-29].
In conclusion, diarrheagic E.coli types are not widely
detected as cause of diarrhea in Libyan children of
Benghazi , whereas high rates of normal intestinal
E. coli isolates from children were MDR, carried bla-
CTX-M , Class I integrons and potential uroquino- uino-
lone resistance genes. This study conrms the ur- genes. This study conrms the ur-
gent need to monitor antimicrobial resistance trends
of commensal intestinal E. coli in Libya.
Declaration of interest
Nothing to declare.
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