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High Levels of Extended-Spectrum Beta-Lactamases in a Major Teaching
Hospital in Ghana: The Need for Regular Monitoring and Evaluation of Antibiotic
Resistance
Article in The American journal of tropical medicine and hygiene · September 2013
DOI: 10.4269/ajtmh.12-0642 · Source: PubMed
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OBENG-NKRUMAH AND OTHERS
EXTENDED-SPECTRUM BETA-LACTAMASES IN GHANA
High Levels of Extended-Spectrum Beta-Lactamases in a Major Teaching Hospital
in Ghana: The Need for Regular Monitoring and Evaluation of Antibiotic
Resistance
Noah Obeng-Nkrumah, Kingsley Twum-Danso, Karen A. Krogfelt,* and Mercy J. Newman
Department of Microbiology, University of Ghana Medical School, Korle-Bu, Ghana
* Address correspondence to Karen A. Krogfelt, Statens Serum Institut, Artillerivej, Copenhagen S, Denmark. E-mail:
kak@ssi.dk
Abstract.
Infections with bacteria producing extended-spectrum beta-lactamases (ESBLs) are increasing across Africa. This
study reports on ESBL-producing Enterobacteriaceae as significant causes of infections and antibiotic resistance at
Korle-Bu Teaching Hospital in Accra, Ghana. Of 300 isolates examined, 49.3% produced ESBLs. The prevalence of
ESBLs was significantly high among isolates from neonates (28 of 43, 65.1%; relative risk = 1.62, 95% confidence
interval = 1.33–2.13, P = 0.002) and adult patients > 65 years of age (36 of 51, 70.5%; relative risk = 1.89, 95%
confidence interval = 1.41–2.40, P = 0.001). A marked increase in minimum inhibitory concentrations of ESBL-
positive species was noticed compared with those for the other strains. Using these concentrations, we found that 26
(17%) ESBL producers were resistant to two or more antibiotics (aminoglycosides, fluoroquinolones, sulfonamide,
and carbapenems) whereas 5 (3.2%) non–ESBL producers were multidrug resistant. Regular ESBL detection and
evaluation of antibiotic resistance may help reduce the spread of ESBLs and antibiotic resistance in Ghana.
INTRODUCTION
Favored by their comparatively high effectiveness, low toxicity, and low cost, beta-lactams
1,2
are prescribed more often than any other antibiotic. Heavy use of this antibiotic has resulted in
selection of drug-resistant bacteria caused by the production of beta-lactamases, and is now an
increasing problem, especially in Enterobacteriaceae. Extended-spectrum beta-lactamase
(ESBL)–producing Enterobacteriaceae are resistant to penicillins, narrow-spectrum and
3–5
extended-spectrum cephalosporins, except the cephamycins, and aztreonam.
Most importantly, in a large prospective study of consecutive patients with bacteremia,
treatment failure was observed although the strains were susceptible in vitro to the antibiotics
used. This failure of beta-lactam antibiotics was attributed to inoculum effect, under-dosing, and
4,6
failure to achieve pharmacodynamic targets. Despite these public health concerns, few studies
have reported on the problem of ESBLs in Africa in general and Ghana in particular. In Africa,
7–
outbreaks of infection with ESBL-producing enterobacteria have been reported in South Africa,
9 10,11 12 13 14 15
Egypt, Tunisia, Morocco, Tanzania, and Nigeria. In Ghana, routine ESBL detection
is absent. Moreover, no systematic survey of ESBL-producing bacteria has been conducted, and
the extent of the ESBL problem remains unclear.
To investigate the extent of the ESBL problem, we examined clinical isolates of
Enterobacteriaceae collected at Korle-Bu Teaching Hospital (KBTH) in Accra, Ghana. The aim
of this study was to determine the occurrence of ESBLs in the hospital and report on the
resistance of ESBL-producing and non-producing strains to potentially useful antimicrobial
agents.
Copyright 2013 by the American Society of Tropical Medicine and Hygiene
MATHERIALS AND METHODS
Settings and study design.
Korle-Bu Teaching Hospital has 1,600 beds and intensive care units that are used for
surgical, medical, and trauma emergencies. It serves a pediatric and adult population > 3 million
in the Greater Accra region, and acts as a major referral health facility for an estimated
population of 22 million Ghanaians. The Central Microbiology Laboratory of KBTH processes >
40,000 clinical cultures annually.
Specimens, culture, and identification.
During a three-month period (February–April 2008), 6,105 clinical samples were submitted to
the microbiology laboratory of KBTH for bacteriologic investigations. All enterobacterial isolates
cultured within the study period as causes of clinical infection were prospectively included in the
study. A total of 1,815 samples were culture-positive for various infections. From these samples, 300
non-duplicate isolates of Enterobacteriaceae implicated as causative agents of infections were
prospectively collected. The isolates were cultured from urine (n = 105), blood cultures (n = 57),
wound swabs (n = 40), respiratory specimens (n = 28), high vaginal swabs (n = 59), and aspirates
from various anatomic sites (n = 5). All isolates were speciated by using standard bacteriologic
16
procedures and API-20E rapid test kits (BioMerieux, Marcy l’Etoile, France). Isolates were
stored in trypticase soy broth containing 10% glycerol at –20°C until further workup.
ESBL screening.
All isolates were screened for presumptive presence of ESBLs with cefpodoxime (10 µg),
ceftazidime (30 µg), and cefotaxime (30 µg) antibiotic disks (MAST Group Ltd., Bootle, United
17
Kingdom) according to the guidelines of the Clinical and Laboratory Standard Institute (CLSI).
Antibiotic disk diffusion tests were performed with 0.5 McFarland standard inoculum on Mueller
Hinton agar (bioMerieux). Using CLSI screening guidelines, we reported Escherichia coli,
Klebsiella pneumoniae, Klebsiella oxytoca, and Proteus mirabilis with zone inhibition diameters
22 mm for ceftazidime and 27 mm for cefotaxime as positive for ESBL screening. As
recommended by the CLSI, a cefpodoxime disk was included in the ESBL screening with
breakpoints of 22 mm for P. mirabilis and 17 mm for E. coli, K. pneumoniae, and K. oxytoca
strains. Isolates resistant at these breakpoints were reported as positive for ESBL screening.
ESBL screening for other enterobacteria was performed as for E. coli and Klebsiella spp. All
isolates with a positive result in the ESBL screening test with at least one of three screening
agents were selected for ESBL confirmation.
ESBL confirmation.
Screen-positive enterobacteria isolates were confirmed for ESBL production by the
17
combined-disk method according to CLSI guidelines. Zones of inhibition were determined for
each isolate to antibiotic disks containing 30 g of cefotaxime, 30 g of ceftazidime, and 10 g
of cefpodoxime either alone or in combination with 10 g of clavulanic acid (MAST Group
Ltd.). An isolate was classified as having an ESBL-producer phenotype if the inhibition zone
differed by 5 mm between at least one of the standard antibiotic disks and its corresponding
clavulanate combination disk. All the study isolates including Citrobacter freundii and
Enterobacter cloacae were tested for ESBL expression as determined by CLSI. Escherichia coli
control strain ATCC 25922 was used to monitor the performance of ESBL detection agents.
Antibiogram.
The susceptibilities of isolates to the antibiotics ampicillin (10 g), cefuroxime (30 g),
cefotaxime (30 g), meropenem (10 g), tetracycline (30 g), chloramphenicol (30 g),
cotrimoxazole (25 g), gentamicin (30 g), amikacin (30 g), and ciprofloxacin (5 g) (Oxoid,
Basingstoke, United Kingdom) were determined by using agar disk diffusion according to CLSI
17
reference guidelines and breakpoints. Minimum inhibitory concentrations (MICs) were
18
determined by using the standard microbroth dilution method for meropenem (0.015–32
g/mL), ciprofloxacin (0.06–128 g/mL), amikacin (0.125–256 g/mL), and sulfamethoxazole
(4–8,192 g/mL). Minimum inhibitory concentrations were interpreted according to CLSI
17
guidelines. Reference strains E. coli NCTC 10418 and E. coli ATCC 25922 were included as
quality controls in each susceptibility test.
Statistical analyses.
All statistical analyses were conducted by using SPSS version 16(SPSS Inc., Chicago, IL).
Associations between demographic variables (sex, site of infection, and age) and ESBL
infections were analyzed by using relative risk and a multinomial logistic regression model when
appropriate. Minimum inhibitory concentrations of ESBL-producing isolates were compared
with ESBL-negative study isolates by using the chi-square test. P values < 0.05 were considered
significant.
Ethical considerations.
Isolates recovered from patient specimens were assigned arbitrary numbers. This study was
approved by the Ethical and Protocol Review Committee of University of Ghana Medical School
College of Health Sciences (Protocol identification no. MSEt/M.3P.7/20072008).
RESULTS
A total of 300 Enterobacteriaceae isolates were identified during the study period.
Escherichia coli and Klebsiella species were the most commonly isolated bacteria (n = 231,
77.0%).
Occurrence of ESBL-producing Enterobacteriaceae.
Of the 300 enterobacterial isolates, the combined-disk method showed that 148 (49.3%) were
characterized by synergy between clavulanate and at least one of the standard antibiotic disks
(Table 1). When data were expressed as prevalence within each species, ESBL phenotype was
highest among Enterobacter cloacae (18 of 24, 75.0%), followed by K. pneumoniae (59 of 96,
661.5%), C. freundii (6/12, 50.0%), K. oxytoca (n = 5 of 11, 45.0%) (high beta-lactamase
producers of this species may mimic ESBLs), and E. coli (55 of 126, 43.0%,).
Distribution of ESBL-producing Enterobacteriaceae.
The urinary tract was the most abundant source (70 of 105, 66.70%) of ESBL producers.
When the distribution of ESBL-producing isolates was compared across age groups, ESBL
prevalence was significantly high (P = 0.001) among isolates from patients at extremes of ages,
specifically neonates (28 of 43, 65.1%; relative risk [RR] = 1.62. 95% confidence interval [CI] =
1.33–2.13, P = 0.002) and adult patients > 65 years of age (36 of 51, 70.5%; RR = 1.89, 95% CI
= (1.41–2.40, P = 0.001).
Susceptibility patterns of isolates.
The susceptibility pattern of Enterobacteriaceae to potentially useful antimicrobial agents for
ESBL producers and non–ESBL producers by disk diffusion method of sensitivity testing is
shown in Figure 1. The ESBL producers comprised a large proportion of the isolates resistant to
various antibiotic classes. The ESBL-producing isolates (n = 148) significantly (P < 0.05) had
increased resistance compared with non–ESBL producers (n = 158) to cotrimoxazole (92.6%,
57.2%), gentamicin (91.2%, 50.6%), amikacin (44.8%, 20.5%), and ciprofloxacin (41.1%,
21.1%), respectively. All isolates were susceptible to meropenem.
Results of MICs in evaluating the burden of resistance attributable to ESBLs against
amikacin, ciprofloxacin, meropenem, and sulfonamide are shown in Table 2. The ESBL–non-
producing isolates were used to evaluate the impact of ESBLs on antimicrobial drug resistance.
The particularly high MICs for the isolates in this study were caused mainly by contributions of
ESBL-producing isolates. The ESBL producers had significantly decreased susceptibilities
compared with the non–ESBL producers. The MIC50 and MIC90 values of all antibiotics, except
meropenem, were significantly higher for ESBL-positive isolates compared with those for other
strains. Meropenem was the most active agent, with an MIC90 (mode = 0.5 g/mL) two-fold
lower than that for susceptibility breakpoint.
Some strains expressed resistance (by broth microdilution) to two or more antibiotics
(aminoglycosides, fluoroquinolones, sulfonamide, and carbapenems), and were defined as
multidrug resistant (MDR). Of the ESBL producers, 26 (17%) were MDR strains, whereas only
5 (3.2%) of the non–ESBL producers were MDR strains. The difference was statistically
significant (P < 0.05).
DISCUSSION
In the present study, we report an overall high ESBL prevalence of 49.3% during a three-
month period. Approximately half of all the isolates from urinary or respiratory tract infections
were ESBL producers. The high prevalence may have been caused by the fact that the ESBL
problem has existed in our institution for a long time, and lack of awareness may have increased
the burden. The prevalence of ESBLs differed considerably between isolates from pediatric and
adult patients (Table 3). The ESBL prevalence was significantly higher in isolates from patients
at the extremes of ages: neonates (28 of 43, 65.1%; RR = 1.62, 95% CI = 1.33–2.13, P = 0.002)
and adult patients > 65 years of age (36 of 51, 70.5%; RR = 1.89. 95% CI = 1.41–2.40, P =
0.001). In these groups of patients, empirical antimicrobial use is likely to be higher because of
responsive medical attention and greater antibiotic pressure, especially in the elderly. Our finding
of ESBL producers among Enterobactericeae in hospitals is higher compared with that
9 12
documented in some ESBL-affected institutions in South Africa (36.1%), Tunisia (38.5%)
14 15 19
Tanzania (15%), Nigeria (40%), and in many other reviews for Europe (5.4–25%) and the
20
United States (1–25%).
The general antibiotic susceptibility of the study isolates shows an overall high drug
resistance prevalence to many routinely tested drugs. It has been the experience at KBTH that
resistance to these drugs among clinical isolates of Enterobacteriaceae is high (e.g., tetracycline
19
= 82%, chloramphenicol = 75%, cotrimoxazole = 73%) and the prevalence is increasing. Using
MICs, we found that 26 (17%), of the ESBL producers were resistant to two or more antibiotics
(aminoglycosides, fluoroquinolones, sulfonamide, and carbapenems, whereas 5 (3.2%) of non–
ESBL producers were MDR strains. In this study, the resistance levels in non–ESBL-producing
Enterobacteriacae (cefotaxime = 29.1%, ceftazidime = 21.9%, gentamicin = 57.2%,
cotrimoxazole = 52.6%, and ciprofloxacin = 21.1%) would still be considered high compared
21
with such isolates reported from the European Antibiotic Resistance Surveillance Network.
Meropenem was the only antibiotic active against all the study strains and, perhaps, the best
choice for empiric treatment. Meropenem has been on the Ghanaian market for a relatively short
period of time since 2002. However, systemic meropenem therapy over a period may also favor
the selection of meropenem-resistant strains.
Korle-Bu Teaching Hospital acts as a major referral health facility for an estimated
population of 22 million Ghanaians. Although the high prevalence and drug resistance levels
may be biased by the referral policy of this main hospital in Ghana, the antibiotic resistance
levels in these pathogens are extremely worrisome and indicative of heavy antibiotic selection
pressure in primary care and in Ghanaian hospitals. In recent years, enterobacteria producing
ESBLs have emerged as major pathogens in our institution. In 2007, 39 of 50 blood stream
isolates of Enterobactericeae involved in an outbreak of septicemia in the neonatal intensive care
unit of KBTH were cephalosporin resistant (Codjoe FS, unpublished data). We are unable to
determine if the high ESBL prevalence was part of a nosocomial outbreak because of insufficient
data on inpatient and outpatient status in relation to culture dates.
Regular ESBL detection, rational antibiotic drug monitoring, and evaluation of drug
resistance may help reduce the spread of ESBLs and antibiotic resistance in KBTH. There is a
need to strengthen the clinical microbiologic research and diagnostic capacity of health
professionals for surveillance of antibiotic resistance, antibiotic consumption, and the quality of
antibiotics on the Ghanaian market. The judicious use of antibiotics, especially meropenem, for
improved human health should be urgently promoted in Ghana.
Received October 18, 2012.
Accepted for publication April 14, 2013.
Acknowledgments:
We thank staff members of Central Microbiology Laboratory, KBTH, and Microbiology Department, University of
Ghana Medical School, Korle-Bu, for assistance and Professor Niels Frimodt-Møller for inspiring discussions. The
authors are members of ADMER (http://admerproject.org), a DANIDA (Project code: 09-099SSI) supported
research and development project.
Financial support: This study was supported in part by a grant from the College of Health Sciences, University of
Ghana Medical School, Korle-Bu.
Authors’ addresses: Noah Obeng-Nkrumah, Kingsley Twum-Danso, and Mercy J. Newman, Department of
Microbiology, University of Ghana Medical School, Korle-Bu, Ghana, E-mails:
successfulnoahforchrist@yahoo.com, ktwumdanso@yahoo.com, and newmerci@yahoo.co.uk. Karen A. Krogfelt,
Statens Serum Institut, Artillerivej, Copenhagen S, Denmark, E-mail: kak@ssi.dk.
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*outlegends*f1*Figure 1. Prevalence of antimicrobial resistance among extended-spectrum beta-lactamase (ESBL)–
a,b,c
producing and non-ESBL–producing Enterobacteriaceae at Korle-Bu Teaching Hospital, Accra, Ghana. indicate
significant difference (P < 0.05, by chi-square test) in antibiotic susceptibility between ESBL producers and ESBL
non-producers for all antibiotics, except ampicillin, tetracycline, chloramphenicol, and meropenem.
TABLE 1
Prevalence of ESBL-producing isolates among members of the family Enterobacteriaceae, Ghana*
Species Distribution of ESBL-producing isolates in specimens (%)
Within Total Urine, n Blood, Wound, Sputum, HVS, n = CSF, ASP, n Other,
species = 105 n =577 n = 40 n = 28 59 n = 2 = 5 n = 4
Escherichia 55/126 55/14 37/67 5/17 4/16 (25) 6/10 (60) 3/14 0/1 0/1 0
coli (43.7) 8 (56.1) (29.4) (21.4)
(37.2)
Klebsiella 59/96 59/14 24/27 13/26 6/11 10/23 3/6 (50) 0/1 1/1 0/1
pneumoniae (61.5) 8 (88.9) (50) (54.5) (43.4) (100)
(39.8)
Klebsiella 5/11 5/148 3/3 0/3 0/2 2/2 (100) 0/1 0 0 0
oxytoca (45.5) (3.4) (100)
Enterobacter 18/24 18/14 2/2 7/9 4/8 (50) 3/3 (100) 2/2 (100) 0 0 0
cloacae (75.0) 8 (100) (77.8)
(2.2)
Enterobacter 2/7 2/148 0 1/1 1/4 (25) 0 0/1 0 0/1 0
aerogenes (28.5) (1.4) (100)
Proteus 3/17 3/148 2/3 0 1/10 (10) 0 0/2 0 0/1 0/1
mirabilis (17.0) (2.0) (66.6)
Proteus 0/4 0 0/1 0 0/3 0 0 0 0 0
vulgaris
Citrobacter 6/12 4/148 2/2 0/1 2/4 (50) 1/1 (100) 1/2 (50) 0 0/1 0/1
freundii (50.0) (4.0) (100)
Citrobacter 0/3 0 0 0/1 0/1 0 0 0 0 0/1
koseri
Total (%) 148/300 (100) 70/105 26/57 19/40 22/28 10/59 0 1/5 (20) 0
(49.3) (66.7) (45.6) (22.5) (78.5) (16.9)
* ESBL = extended-spectrum beta-lactamase; Total = overall number of ESBL producers in a particular species expressed
as a percentage (in parentheses) of the total number of ESBL producers (148) in the study; HVS = high vaginal specimen;
CSF = cerebrospinal fluid; Asp = Aspirate; Other = bacteria isolated from specimens not indicated (e.g., ear swab, pus).
TABLE 2
Minimum inhibitory concentrations (MICs) of non-beta-lactams and meropenem for ESBL-producing and ESBL-non-producing enterobacteria strains, Ghana*
Antibiotic/organism Phenotype† No. strains resistant at MIC (µg/mL) MIC50‡ MIC90‡ %
< 0.06 0.125 0.25 0.5 1 2 4 8 16 32 64 128 256 512 > Res§
0.03 1,024
Amikacin
Escherichia. coli ESBL+ 0 0 0 1 2 3 5 3 17 7 2 3 5 3 2 2 8 256 27.2
ESBL 2 3 2 8 13 19 4 5 4 5 4 2 0 0 0 0 1 16 8.5
Klebsiella spp. ESBL+ 0 0 1 3 5 5 5 12 12 5 2 5 2 5 2 0 8 256 25.0
ESBL 0 2 3 3 11 5 3 3 5 2 1 2 1 0 0 0 1 16 9.7
Other ESBL+ 0 1 1 2 2 1 1 4 2 4 2 1 2 3 2 1 16 512 37.9
ESBL 0 1 2 4 9 4 3 5 1 2 2 2 1 2 0 0 1 64 18.4
Ciprofloxacin
E. coli ESBL+ 0 1 13 6 6 16 0 4 1 2 3 2 1 0 0 0 1 32 23.6
ESBL 0 11 22 12 9 5 6 5 1 0 0 0 0 0 0 0 0.25 2 16.9
Klebsiella spp. ESBL+ 1 4 11 8 13 10 1 6 2 2 4 2 0 0 0 0 0.5 16 26.5
ESBL 1 3 13 10 5 3 3 1 1 1 0 0 0 0 0 0 0.25 2 14.6
Other ESBL+ 1 1 3 2 6 8 3 2 3 0 0 0 0 0 0 0 1 8 27.5
ESBL 1 3 10 9 5 4 4 2 0 0 0 0 0 0 0 0 0.25 2 15.3
Sulfonamide
E. coli ESBL+ 0 0 0 0 0 0 0 0 0 0 0 0 4 8 22 21 512 > 78.2
1,024
ESBL 0 0 0 0 0 0 0 0 0 2 8 12 28 10 5 8 128 1,024 18.3
Klebsiella spp. ESBL+ 0 0 0 0 0 0 0 0 0 0 0 0 6 6 31 21 256 > 81.2
1,024
ESBL 0 0 0 0 0 0 0 0 0 0 3 3 12 7 10 6 256 1,024 39.0
Other ESBL+ 0 0 0 0 0 0 0 0 0 0 0 1 3 6 12 7 512 1,024 65.5
ESBL 0 0 0 0 0 0 0 0 0 1 3 4 16 4 5 5 64 1,024 26.3
Meropenem
E. coli ESBL+ 1 4 15 20 10 4 0 0 0 0 0 0 0 0 0 0 0.25 0.5 0
ESBL 0 4 20 27 14 5 0 0 0 0 0 0 0 0 0 0 0.25 0.5 0
Klebsiella spp. ESBL+ 2 6 7 23 19 7 0 0 0 0 0 0 0 0 0 0 0.25 1 0
ESBL 3 2 21 10 7 0 0 0 0 0 0 0 0 0 0 0 0.125 0.25 0
Other ESBL+ 1 3 8 14 3 0 0 0 0 0 0 0 0 0 0 0 0.25 0.5 0
ESBL 0 6 12 18 2 0 0 0 0 0 0 0 0 0 0 0 0.25 0.5 0
* ESBL = extended-spectrum beta-lactamase; Klebsiella spp. = K. pneumoniae, K. oxytoca; Other = Enterobacter aerogenes, Enterobacter cloacae, Proteus mirabilis, P.
vulgaris, Citrobacter freundii, C. koseri.
† ESBL+ = strains producing ESBL; ESBL = non–ESBL-producing strains.
‡ MIC50/90 = minimum inhibitory concentrations for 50% and 90% of the organisms, respectively, in µg/mL.
§ % Res = percentage resistance.
TABLE 3
Demographic factors associated with ESBL infections in Korle-Bu Teaching Hospital, Ghana*
Variable ESBL (n = 148) Non-ESBL (n = 152) Relative risk (95% CI) P
No. % No. %
Sex
M (n = 162) 78 48.1 84 51.8 0.93 (0.75–1.17)
F (n = 138) 70 50.7 68 49.2 0.93 (0.75–1.17) 0.569
Source of infection
Urinary tract (n = 105) 70 66.7 35 33.3 1.69 (1.36–2.100) 0.001
Blood (n = 57) 26 45.6 31 54.4 0.89 (0.57–1.42) 0.643
Respiratory specimen (n = 40) 22 55.0 18 45.0 1.23 (0.93–1.62) 0.177
HVS (n = 28) 9 32.1 19 67.9 0.643 (0.38–1.07) 0.53
Wound (n = 59) 20 32.2 39 67.8 0.67 (0.47–0.82) 0.616
Aspirate (n = 5) 1 20.0 4 80.0 0.50 (0.15–1.70) 0.163
CSF (n = 2) 0 0 2 100.0 – –
Other (n = 4) 0 0 4 100.0 – –
Age
28 days (n = 43) 28 65.1 15 34.9 1.62 (1.33–2.13 0.002
> 28 days – 1 year (n = 41) 7 17.1 15 34.9 0.33 (0.17–0.67) 0.001
> 1–5 years (n = 37) 14 37.8 34 82.9 0.83 (0.54–1.29) 0.348
> 5–15 years (n = 35) 10 28.6 25 71.4 0.62 (0.36–1.06) 0.051
> 15–65 years (n = 63) 24 38.1 39 698.2 0.83 (0.58–1.57) 0.275
> 65 years (n = 51) 36 70.5 15 29.5 1.89 (1.41–2.40) 0.001
* ESBL = extended-spectrum beta-lactamase; CI = confidence interval; HVS = high vaginal swab; CSF = cerebrospinal fluid; Other = bacteria isolated from specimens not
indicated (e.g., ear swab, pus).
Figure 1 Prevalence of antimicrobial resistance among ESBL-producing and non-ESBL-
pFrigoduureci n1g Enterobacteriaceae in Korle-Bu Teaching Hospital, Accra, Ghana
Perecentage resistance
a
b
c
Overall ESBL producers Non ESBL producers
a,b,c Significant difference (P < 0.05, Chi-square test) in antibiotic susceptibility between ESBL-
producers and ESBL-non-producers were noticed for all antibiotics, except for ampicillin,
tetracycline, chloramphenicol and meropenem.
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Antimicrobial agents