World Research Journal of Biology and Biological Sciences

Vol. 3(3), pp. 24-30, October, 2020. © www.premierpublishers.org. ISSN: 2326-3997

Research Article

A study of antibiotic resistance of Extended-Spectrum

Beta-Lactamases producing Enterobacteriaceae and some
their associated factors in the laboratory of the University
Hospital of Befelatanana Antananarivo Madagascar
Zafindrasoa Domoina Rakotovao-Ravahatra*1, Fidiniana Mamy Randriatsarafara2,
Andriamiadana Luc Rakotovao3, Andry Rasamindrakotroka4.
1*Laboratory of Joseph Raseta Befelatanana University Hospital Antananarivo, Madagascar.
2NationalInstitute of Public and Community Health Befelatanana, Antananarivo, Madagascar.
3Laboratory of Joseph Raseta Befelatanana University Hospital Antananarivo, Madagascar.
4Faravohitra Medical Biology Laboratory, Antananarivo, Madagascar.

ABSTRACT

Background: Extended-Spectrum Beta-Lactamases - producing Enterobacteriaceae are common in

hospitals. This study aims to describe the antibiotic resistance of these bacteria and their associated
demographic and clinical factors. Methods: It was a prospective study of 73 isolates of Extended-
Spectrum Beta-Lactamases - producing Enterobacteriaceae for a period of six months from July to
December 2019 in the laboratory of Befelatanana. Results: This study showed 73 (6.3%) isolates of
Extended-Spectrum Beta-Lactamases- producing Enterobacteriaceae, represented by 25 (34.2%)
isolates of Klebsiella spp, 24 (32.9%) isolates of Escherichia coli, 22 (30.1%) isolates of Enterobacter
spp and 2 (2.7%) isolates of Proteus spp. The antibiotic resistance of these bacteria varied from 0% to
100% for all of the antibiotics tested. Resistance to aminoglycosides ranged from 0% (amikacin) to
69.9% (gentamycin). Resistance to quinolones ranged from 43.8% (levofloxacin) to 76.7% (nalidixic
acid). Similarly, 60 (82.2%) isolates were resistant to cotrimoxazole and 25 (34.2%) isolates to
chloramphenicol. Patients under 20 years (57.1%) (p=0.03), men (52.2%)(p=0.11; NS), patients with
respiratory samples (83.3%)(p=0.004), with pus (61.9%)(p=0.02) and hospitalized in surgery and
intensive care units (68.4%)(p=0.0009) were the most affected by these enterobacteria. Conclusion:
Extended-Spectrum Beta-Lactamases - producing Enterobacteriaceae are responsible for severe
infections and the majorities are multi-resistant bacteria.

Keywords: Beta-lactamase, Enterobacteriaceae, antibiotic resistance, amikacin, imipenem.

INTRODUCTION

Bacterial resistance to antibiotics is increasing worldwide management of nosocomial infections, resulting in

in healthcare settings and in the community. The
dissemination of multi-drug *Corresponding Author: Zafindrasoa Domoina
resistant Enterobacteriaceae, i.e. Extended-Spectrum Rakotovao-Ravahatra, Laboratory of Joseph Raseta
Beta-Lactamases (ESBLs)- producing Enterobacteriaceae Befelatanana University Hospital Antananarivo,
and carbapenemase Madagascar, Tel: 61340930120; E-mail:
producing Enterobacteriaceae (CPE), is alarming ravahatradomoina@yahoo.fr
2
(Sangare et al., 2017). ESBLs- producing Co-Author E-mail: fidyrfm@yahoo.fr
3
Enterobacteriaceae represent a major problem in the Co-Author E-mail: lucdina007@yahoo.fr
4
Co-Author E-mail: andryrasamindrakotroka@gmail.com
A study of antibiotic resistance of Extended-Spectrum Beta-Lactamases producing Enterobacteriaceae and some their associated factors in the laboratory of the University Hospital of
Befelatanana Antananarivo Madagascar
Zafindrasoa et al. 25
prolonged hospital stays, increased hospital charges, and
higher mortality and morbidity rates (Mahamat et al.,
2019). Reliable identification of ESBLs-producing
organisms in clinical laboratories can be challenging, so
their prevalence is likely underestimated. ESBLs are
enzymes that have the particularity to hydrolyze all beta-
lactams including third-generation cephalosporins except
cephamycins and carbapenems (Kpodaet al., 2018).
ESBLs are encoded by different genes inserted in genetic
mobile elements, such as plasmids, that facilitate their
spread between bacterial species. The most common
ESBLs belong to the CTX-M, SHV and TEM families
(Mahamat et al., 2019). Infections with ESBLs-producing
organisms have been associated with poor outcomes.
Antimicrobial therapy for infection caused by ESBLs-
producing organisms presents an additional challenge,
because these organisms are also often resistant to other
antimicrobials, such as trimethoprim-sulfamethoxazole,
aminoglycosides, and fluoroquinolones. Production of
ESBLs is one of the most important resistance
mechanisms that hamper the antimicrobial treatment of
infections caused by Enterobacteriaceae (Abhilash et
al.,2010).Therefore, it is imperative to quantify the
problem, and reinforce guidelines promoting appropriate
antibiotic use. Antibiotic resistance studies of these
ESBLs-producing Enterobacteriaceae should be carried
out to improve patient management. This study aims to
describe the antibiotic resistance of ESBL-producing
Enterobacteriaceae and to describe their associated
demographic and clinical factors.
MATERIALS AND METHODS
Type of study
It was a prospective study of 73 isolates of ESBLs-
producing Enterobacteriaceae for a period of six months
from July 2019 to December 2019 in the laboratory of the
University Hospital of Befelatanana.
Inclusion and exclusion criteria
This study includes all patients who have applied for a
bacteriological examination during the study period. This
study excluded non-compliant samples during the study
period.
Study variables
The dependent variable was constituted by the positivity of
the microbiological culture identifying ESBLs- producing
Enterobacteriaceae in an antibiogram. The independent
variables were constituted by the species of
Enterobacteriaceae found in culture and the results of the
antibiogram.
Sample collection
A study of antibiotic resistance of Extended-Spectrum Beta-Lactamases producing Enterobacteriaceae and some their associated factors in the laboratory of the University Hospital of
Befelatanana Antananarivo Madagascar
Samples were collected in sterile vials (stool, urine and
respiratory samples), swabs (pus, vaginal or urethral
swab), sterile tube (pleural fluid, ascites fluid,
cerebrospinal fluid and other fluids) or blood culture
bottles. The samples were transported quickly to the
laboratory (less than 2 hours of transport) at room
temperature.
Bacterial culture
Specific culture media were used according to each type
of sample (for examples: blood agar, chocolate agar, brain
heart broth….), associated with a chromogenic culture
medium (Uriselect® supplied by Bio-Rad company) to
specifically identify the enterobacteria.
Bacterial identification
When bacterial colonies grew in uriselect® agar, bacteria
were identified by colony color, microscopic appearances
after gram staining, and identification test results.The
specific identification tests for Enterobacteriaceae were
the oxidase test (negative for Enterobacteriaceae) and the
Api 20E® strips (manufactured by bioMérieux company).
These strips were identified the species of
Enterobacteriaceae (Escherichia coli, Klebsiella
pneumoniae, Enterobacter cloacae…..).
Antibiotic resistance test
For the antibiogram, discs of antibiotics (brand OXOID®
supplied by Termo Fisher Scientific company) were used.
These antibiotics were represented by amoxicillin 25µg,
amoxicillin-clavulanic acid 20-30µg (AMC), 3rd generation
cephalosporins (3CG)(cefotaxime 5µg, ceftriaxone 30µg,
cefixime 5µg, ceftazidime 10µg), imipenem 10µg,
aminoglycosides (gentamycin 10µg, tobramycin 10µg,
amikacin 30µg), quinolones (nalidixic acid 30µg,
ciprofloxacin 5µg, levofloxacin 5µg), cotrimoxazole
1,25/23,75 µg and chloramphenicol 30µg. Resistance to
antibiotics was determined by the Mueller / Hinton agar
diffusion method, according to the recommendations of the
“comité de l'antibiogramme de la société française de
Microbiologie”(Société Française de Microbiologie, 2019).
Mueller / Hinton agar were provided by Rapid Labs
Company. The detection of ESBLs was carried out by a
method of synergy between the clavulanic acid of the AMC
and ceftriaxone or else cefotaxime, characterized by a
“champagne cork” image and signs the presence of an
ESBLs (Sbitiet al., 2017).
Study parameters
Study parameters were the gender, the age, the clinical
information, the departments, the types of sampling, the
bacteriological results and the results of the antibiogram.
 World Res. J. Biol. Biol. Sci. 26

Ethical considerations RESULTS

This study was authorized by the Director of Establishment Microbiological results

and Department Head of laboratory of the University
Hospital of Befelatanana before its implementation. Notion
of anonymity and confidentiality were respected.
Statistical analysis
The data entry and processing was performed on the
software Epi-info 3.5.2. The comparison of percentages
used the Chi-square tests. The statistical significance
threshold used was p = 0.05.
Among 1150 bacteriological culture, this study showed 73
(6.3%) isolates of ESBLs- producing Enterobacteriaceae,
324 (28.1%) isolates of other bacteria and 753 (65.5%)
negative results (Figure 1). The other bacteria are
represented by non ESBLs-producing
Enterobacteriaceae, non fermentinggram negative bacilli
(Acinetobacter spp, Pseudomonas spp…), other gram
negative bacilli, gram positive bacilli, gram negative cocci
(Neisseria gonorrhoeae…) and gram positive cocci
(staphylococci, streptococci…).

Figure 1: Microbiological results of bacteriological cultures

6.3%

ESBLs-producing
28.1% Enterobacteriaceae
Other bacteria

Negative results
65.5%

These ESBLs- producing Enterobacteriaceaeare represented by 25 (34.2%) isolates of Klebsiella spp, 24 (32.9%) isolates
of Escherichia coli, 22 (30.1%) isolates of Enterobacter spp and 2 (2.7%) isolates of Proteus spp (Figure 2).

A study of antibiotic resistance of Extended-Spectrum Beta-Lactamases producing Enterobacteriaceae and some their associated factors in the laboratory of the University Hospital of
Befelatanana Antananarivo Madagascar
Zafindrasoa et al. 27

Figure 2: ESBLs-producing Enterobacteriaceae species

2.7%

34.2% 32.9% Escherichia coli

Enterobacter spp
Klebsiella spp
Proteus spp

30.1%

Antibiotic resistance of ESBLs-producing Enterobacteriaceae isolates

Regarding antibiotic resistance of these ESBLs- producing
Enterobacteriaceae, it varies from 0% to 100% for all of the
antibiotics tested. All isolates (100%) were resistant to
amoxicillin, AMC and 3CG. Resistance to aminoglycosides
ranges from 0% (amikacin) to 69.9% (gentamycin).
Resistance to quinolones ranges from 43.8%
(levofloxacin) to 76.7% (nalidixic acid). For other
antibiotics, 60 (82.2%) isolates were resistant to
cotrimoxazole and 25 (34.2%) isolates to chloramphenicol
(Figure 3).

Figure 3: Antibiotic resistance of ESBLs-producing Enterobacteriaceae isolates

Amoxicillin 100%
AMC 100%
3CG 100%
Cotrimoxazole 82.2%
Nalidixic acid 76.7%
Ciprofloxacin 75.3%
Gentamycin 69.9%
Tobramycin 52.1%
Levofloxacin 43.8%
Chloramphenicol 34.2%
Amikacin 0%
Imipenem 0%
0% 20% 40% 60% 80% 100% 120%

A study of antibiotic resistance of Extended-Spectrum Beta-Lactamases producing Enterobacteriaceae and some their associated factors in the laboratory of the University Hospital of
Befelatanana Antananarivo Madagascar
 World Res. J. Biol. Biol. Sci. 28

Demographic and clinical associated factors with patients with respiratory samples (83.3%)(p=0.004), pus
ESBLs-producing Enterobacteriaceae (61.9%)(p=0.02) and hospitalized in surgery and intensive
Concerning the associated factors, patients under 20 care units (68.4%)(p=0.0009) are the most affected by
years (57.1%)(p=0.03), men (52.2%)(p=0.11; NS), ESBLs-producing Enterobacteriaceae (table 1).

Table 1. Associated factors with ESBLs-producing Enterobacteriaceae

ESBLs-producing Other Enterobacteriaceae Total p-value
Enterobacteriaceae (n= (n=89) (N=162)
73)
n % n %
Age (years)
≥ 20 37 37.4 60 60.6 99 0.03
< 20 36 57.1 29 46.0 63
Gender
Women 37 39.8 56 60.2 93 0.11
Men 36 52.2 33 47.8 69
Types of sampling
Respiratorysamples 5 83.3 1 16.7 6 0.004
Blood culture 25 62.5 15 37.5 40
Pus 13 48.1 14 51.9 27
Others 30 33.7 59 66.3 89
Departments
Surgery and Intensive Care Units 26 68.4 12 31.6 38 0.0009
Others 47 37.9 77 62.1 124
Clinical information
Pus 13 61.9 8 38.1 21 0.02
Fever 32 53.3 28 46.7 60
Others 28 34.6 53 65.4 81

DISCUSSION

Prevalence of ESBLs-producing Enterobacteriaceae

Emerging β-lactamase-producing-bacteria (ESBLs, AmpC Enterobacteriaceae, particularly the species Escherichia

and carbapenemases) have become a serious problem in
our community due to their startling spread worldwide and
their ability to cause infections which are difficult to treat.
The diagnosis of these β-lactamases is of clinical and
epidemiological interest. Over the past 10 years, several
methods have been developed aiming to rapidly detect
these emerging enzymes, thus preventing their rapid
spread (Al-Bayssari et al., 2015).This study showed
73/1150 (6.3%) isolates of ESBLs-producing
Enterobacteriaceae. This rate is similar to the rate finding
by a study in Amsterdam which identified 145/1695 (8.6%)
isolates of ESBLs-producing Enterobacteriaceae
(Reuland et al., 2016). Excessive uses of third-generation
cephalosporins, which are commonly used as an empiric
and defnitive therapy in hospitals, are expected to trigger
the emergence and spread of ESBL producers (Hariri et
al., 2017).ESBLs are frequently found in Klebsiella
species, Escherichia coli, and other
enterobacteria(Paterson and Bonomo, 2005). This study
also found the high frequency of ESBLs-producing
A study of antibiotic resistance of Extended-Spectrum Beta-Lactamases producing Enterobacteriaceae and some their associated factors in the laboratory of the University Hospital of
Befelatanana Antananarivo Madagascar
coli, Enterobacter sppand Klebsiella spp.
Antibiotic resistance of ESBLs-producing
Enterobacteriaceae
This study shows a very high ESBLs production and
resistance to multiple classes of antibiotics among patients
with bacterial infections.This antibiotic resistance is due to
frequent use of certain antibiotics. Cefotaxime was the
most commonly used oxyimino-b-lactam, a fact that may
have favored the selection of CTX-M–producing isolates,
because such types of ESBLs are mainly cefotaximases
(Paterson and Bonomo, 2005; Bonnet, 2004).
Fluoroquinolone (nalidixic acid, ciprofloxacin, levofloxacin)
use, which was also frequent, has been identified as a risk
factor for other infections caused by ESBLs-producing
Escherichia coli,probably through the action of co-
selection (Pitoutet al., 2005). The empiric use of 3rd and
4th generation cephalosporins should be curtailed, as
cephalosporin use was associated with an increased risk
of ESBLs production. Furthermore, this study showed high
Zafindrasoa et al. 29
resistance of ESBLs-producing Enterobacteriaceae to
cotrimoxazole (82.2%). Indeed, this antibiotic is used
frequently by the Malagasy population. Cotrimoxazole is
sold in small grocery stores. Misuse of these antibiotics
increases antibiotic resistance. Similarly, self-medication
reinforces this high resistance.In view of their excellent in-
vitro activity, carbapenems should be the initial empiric
choice for serious life threatening infections caused by
ESBLs producing Enterobacteriaceae, with prompt de-
escalation when culture and susceptibility results become
available (Ben-Ami et al., 2009). Indeed, no strain of
ESBLs was resistant to carbapenems in this study, in
particular, to imipenem.Similarly, all enterobacteria
isolates tested in this study were susceptible to
amikacin.Another study in Douala also found that
imipenem (1.3% of resistance) and amikacin (12.9% of
resistance) are the most effective antibiotics against
enterobacteria (Ebongueet al., 2015). These data suggest
that penems (imipenem, meropenem) and
aminoglycosides especially amikacin could be an effective
choice in ESBLs producing Enterobacteriaceae. The other
aminoglycosides like gentamicin and tobramycin are less
effective because they are used frequently in the hospital
resulting in the antibiotic resistance of enterobacteria.
Associated factors with ESBLs-producing
Enterobacteriaceae
Subjects under 20 years (57.1%)(p=0.03) are the most
affected by ESBLs-producing Enterobacteriaceae with a
significant difference. Indeed, children are more fragile and
more likely to be infected by these bacteria. Another study
also found the same result. According to this study, both
the very youngest children, aged 0–3 months, and those
aged 4–6 months, were nine and five times more likely to
be colonized with ESBLs positive bacteria than the oldest
children, respectively. This may reflect health-care
associated transmission or resistant strains being
transmitted from mothers to their babies, possibly during
delivery (Telleviket al., 2016). However, according to
another study, age did not have an effect on ESBLs
infection among different age groups (p>0.05) (Saleh et
al., 2018). Otherwise,patients with respiratory tract
infections,with pus and hospitalized in surgery
departments and intensive care units are the most affected
by ESBLs-producing Enterobacteriaceae with significant
differences. In fact, respiratory tract infections and post-
operative wound infections are frequent in surgical
departments and intensive care units. Klebsiella
pneumoniae is one of the most important hospital
pathogens, particularly concerning the multidrug-resistant
strain ESBL+ (Starzyk-Łuszczet al.,2017).Similarly,
invasive procedures such as mechanical ventilation,
tracheostomy or the use of catheters favor nosocomial
infectionsin surgery departments and intensive care units
(Merzouguiet al., 2018).For example, deaths due to
Klebsiella pneumoniae ESBL+ infection were significantly
related to the use of urinary bladder catheters (Starzyk-
A study of antibiotic resistance of Extended-Spectrum Beta-Lactamases producing Enterobacteriaceae and some their associated factors in the laboratory of the University Hospital of
Befelatanana Antananarivo Madagascar
Łuszczet al.,2017). Hospital acquired infections are a
major cause of mortality and morbidity and provide
challenge to clinicians. Measures of infection control
include identifying patients at risk of nosocomial infections,
observing hand hygiene, following standard precautions to
reduce transmission and strategies to reduce VAP, CR-
BSI, CAUTI. Environmental factors and architectural lay
out also need to be emphasized upon. Infection prevention
in special subsets of patients - burns patients, include
identifying sources of organism, identification of
organisms, isolation if required, antibiotic prophylaxis to be
used selectively, early removal of necrotic tissue,
prevention of tetanus, early nutrition and surveillance.
Room ventilation, cleaning and decontamination,
protective clothing with care regarding food requires
special consideration. Monitoring and Surveillance are
prioritized depending upon the needs. Designated
infection control teams should supervise the process and
help in collection and compilation of data. Antibiotic
Stewardship Recommendations include constituting a
team, close coordination between teams, audit, formulary
restriction, de-escalation, optimizing dosing, active use of
information technology among other measure (Mehtaet al.,
2014).
CONCLUSIONS
ESBLs-producing Enterobacteriaceae are frequently
responsible for nosocomial infections. These bacteria are
resistant to many classes of antibiotics. Imipenem and
amikacin are the antibiotics of choice against these
bacteria. Hygiene measures must be reinforced in
intensive care units to limit the spread of these bacteria.
ACKNOWLEDGEMENTS
We would like to thank all the staff of the laboratory of
University Hospital of Befelatanana and all the laboratory
technicians. Similarly, we would like to express our
gratitude to the director of establishment for authorizing us
to carry out this study. We declare no conflict of interest for
this article. As researchers, we did not benefit from any
source of funding but we carried out this study within the
laboratory with the agreement of the Faculty of Medicine
of Antananarivo.
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Accepted 8 October 2020
Citation: Zafindrasoa D R-R, Fidiniana MR,
Andriamiadana LR, Andry R. (2020). A study of antibiotic
resistance of Extended-Spectrum Beta-Lactamases
producing Enterobacteriaceae and some their associated
factors in the laboratory of the University Hospital of
Befelatanana Antananarivo Madagascar. World Research
Journal of Biology and Biological Sciences, 3(3): 24-30.
Copyright: © 2020 Zafindrasoa et al. This is an open-
access article distributed under the terms of the Creative
Commons Attribution License, which permits unrestricted
use, distribution, and reproduction in any medium,
provided the original author and source are cited.