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Abstract
Background: Emergence of antimicrobial resistance by Staphylococcus aureus has limited treatment options against
its infections. The purpose of this study was to determine the pooled prevalence of resistance to different antimicrobial
agents by S. aureus in Ethiopia.
Methods: Web-based search was conducted in the databases of PubMed, Google Scholar, Hinari, Scopus and the Directory
of Open Access Journals (DOAJ) to identify potentially eligible published studies. Required data were extracted and entered
into Excel spread sheet. Statistical analyses were performed using Stata version 13.0. The metaprop Stata command was used
to pool prevalence values. Twenty-one separate meta-analysis were done to estimate the pooled prevalence of the resistance
of S. aureus to twenty-one different antimicrobial agents. Heterogeneity among the studies was assessed using the I2 statistic
and chi-square test. Publication bias was assessed using Egger’s test. Because of significant heterogeneity amongst the studies,
the random effects model was used to pool prevalence values.
Results: The electronic database search yielded 1317 studies among which 45 studies met our inclusion criteria. Our analyses
demonstrated very high level of resistance to amoxicillin (77% [95% confidence interval (CI): 68%, 0.85%]), penicillin (76%
[95% CI: 67%, 84%]), ampicillin (75% [95% CI: 65%, 85%]), tetracycline (62% [95% CI: 55%, 68%]), methicillin (47%
[95% CI: 33%, 61%]), cotrimoxaziole (47% [95% CI: 40%, 55%]), doxycycline (43% [95% CI: 26%, 60%]), and erythromycin
(41% [95% CI: 29%, 54%]). Relatively low prevalence of resistance was observed with kanamycin (14% [95% CI: 5%,
25%]) and ciprofloxacin (19% [95% CI: 13%, 26%]). The resistance level to vancomycin is 11% 995% CI: (4%,
20%). High heterogeneity was observed for each of the meta-analysis performed (I2 ranging from 79.36% to
95.93%; all p-values ≤0.01). Eggers’ test did not show a significant publication bias for all antimicrobial agents
except for erythromycin and ampicillin.
Conclusions: S. aureus in Ethiopia has gotten notoriously resistant to almost to all of antimicrobial agents in
use including, penicillin, cephalosporins, tetracyclines, chloramphenicol, methicillin, vancomycin and sulphonamides.
The resistance level to vancomycin is bothersome and requires a due attention. Continued and multidimensional efforts
of antimicrobial stewardship program promoting rational use of antibiotics, infection prevention and containment of AMR
are urgently needed.
Keywords: Antimicrobial resistance, Staphylococcus aureus, Meta-analysis, Ethiopia
* Correspondence: dserawit@gmail.com
1
Department of Pharmacology, School of Medicine, College of Medicine and
Health Sciences, Hawassa University, P. O. Box 1560, Hawassa, Ethiopia
Full list of author information is available at the end of the article
© The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver
(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Deyno et al. Antimicrobial Resistance and Infection Control (2017) 6:85 Page 2 of 15
of drug sensitive isolates (q) was reported, the number for all bacterial pathogen isolated [25–28], eleven did not
of resistant isolates was calculated by multiplying the address our study question [29–36], six studies were based
number of isolates (n) by one minus the proportion of on samples taken from of healthy carriers [37–42], one
drug sensitive isolates (1-q) and if the proportion of drug study [43] was part of another study [44], and one study
resistant isolates was given the number of resistant iso- [45] suffered from environmental contamination of the
lates was found by multiplying the proportion (p) with samples during processing. Thus, 45 studies met our
total number of isolates (n). inclusion criteria (Fig. 1). Forty-one of the studies were
journal articles, three were unpublished works [46–48]
Statistical analysis and reporting and one was an official government document from the
Statistical analyses were performed using Stata version Drug Administration and Control Authority (DACA) of
13.0 (Statacorp, LP, college station, TX). The prevalence Ethiopia [49].
values from the different studies were pooled using the S. aureus isolates from a total of 4570 patients were
metaprop command in Stata [8]. We did twenty-one tested for their antimicrobial resistance. The isolates were
separate meta-analyses to estimate the pooled prevalence from ear discharge [50–57], eye discharge [47, 58–60],
of the resistance of S. aureus to twenty one different blood [61–68], wound infection [69–74], surgical site
antimicrobial agents. The number of studies included in infection [30, 73, 75–78], mixed samples [6, 46, 48, 49,
each of the meta-analyses ranged from 4 to 39. Hetero- 79–83], leprosy ulcer [84, 85], and urine sample [86, 87].
geneity amongst the studies was assessed using the I2 Twenty nine studies used primary data while nineteen
statistic. Because of significant heterogeneity amongst studies used records from hospitals or regional laborator-
the studies the random-effects model (REM) was used ies (the characteristics of each included study is summa-
to estimate the pooled prevalence and 95% CIs using the rized Table 1).
DerSimonian and Laird method [9]. The Freeman-Tukey
double arcsine transformation was used so that studies Publication bias and heterogeneity
reporting proportions near or at 0 and 1 would not be Evidence of high heterogeneity was observed for each of
excluded from the meta-analysis. The possible presence the meta-analyses performed (I2 ranging from 79.36% to
of publication bias was checked using Egger’s test [10]. 95.93%; all p-values ≤ 0.01). Eggers’ test did not suggest
For studies that appeared to report unusually higher any significant publication bias except for erythromycin
prevalence of resistance compared to others, we did sen- and ampicillin (see Additional file 2: S2).
sitivity analysis after dropping the study which we sus-
pected of reporting a higher-than-usual result. If the Prevalence of S. aureus resistance to different
point estimate of pooled prevalence after dropping a antimicrobial agents
study lies within the 95% CI of the overall pooled esti- Summary of the pooled prevalence of S. aureus AMR
mate for all studies combined, we considered the given prevalence for twenty-one different antimicrobial agents
study as having non-significant influence on the overall and the number of studies included in the meta-analysis
pooled estimate. Otherwise, the study was considered as for each agent are presented in Table 2. Prevalence of S.
having significantly influencing the overall estimate. aureus resistance for each antimicrobial agent based on
Results of the current meta-analysis are reported as pharmacological classification of the agents is given below.
per the Preferred Reporting Items for Systematic As new anti-MRSA agents such as linezolid, daptomycin,
Reviews and Meta-Analysis (PRISMA) guideline. The tigecycline, telavancin and ceftaroline are rarely available
PRISMA checklist was used to ensure inclusion of in Ethiopia and no published studies available on resist-
relevant information (the filled checklist is included ance to this agents, our results do not cover such agents.
as Additional file 1: S1) [11].
Prevalence of resistance to glycopeptides (vancomycin)
Results Nineteen studies were included for meta-analysis of
Included studies and characteristics vancomycin resistance prevalence. The pooled preva-
The electronic database search yielded 1317 from lence for S. aureus resistance to vancomycin in Ethiopia
PubMed and 17,400 from Google scholar, Hinari, and is 11% (95% confidence interval [CI]: 4%, 20%). The for-
Google search of which 16,083 articles remained after est plot for vancomycin resistance is presented in Fig. 2.
removing duplicate articles. Title and abstract screening The results of sensitivity analysis after exclusion of the
reduced eligible articles to 76 for full text evaluation. two studies that appeared to report outlier prevalence
After reading the full texts, 31 studies were excluded for values separately and both together showed non-
various reasons. Thirteen studies were excluded as their significant influence of the two studies on the overall esti-
report is based on small number of isolates (less than or mate. The pooled prevalence of vancomycin resistance
equal to10) [12–24], four studies reported crude resistance when Guta et al. and Desalegn et al. were removed
Deyno et al. Antimicrobial Resistance and Infection Control (2017) 6:85 Page 4 of 15
Fig. 1 Flow diagram of retrieval of studies: Number of studies screened, assessed for eligibility, and included in the meta-analysis with reasons
separately was 0.09, (95% CI: 0.03, 0.17). When, both Guta carbencilin (β-lactam-sensitive antibiotic) was relatively
et al. and Desalegn et al. were excluded, vancomycin re- lower than other β-lactam-antibiotics (34% [95% CI:
sistance was 0.07 (95% CI: 0.02, 0.14). All the three pooled 17%, 54%]).
values lie within the overall pooled estimate. Relatively lower resistance rate was observed to β-
lactamase-resistant penicillin’s: methicillin (47% [95% CI:
Prevalence of resistance to penicillin’s 33%, 61%]) and amoxicillin-clavulanic acid (30% [95% CI:
Here, the pooled prevalence of S. aureus resistance to 19%, 43%]). The forest plots for methicillin and amoxacilin
penicillin G, amoxicillin, ampicillin, and amoxacilin- resistance are presented in Figs. 3 and 4, respectively while
caluvanic acid was estimated. Resistance to penicillin G the forest plots for penicillin G, ampicillin, amoxicillin-
was estimated based on 33 studies, to amoxicillin based clavulanic acid, and carbencillin resistance are presented in
on 18 studies, to ampicillin based on 27 studies and to Additional file 3: S3, Additional file 4: S4, Additional file 5:
amoxacilin-caluvanic acid based on 12 studies. Pooled S5 and Additional file 6: S6.
resistance rates were highest for β-lactamase-sensitive
penicillin’s. Resistance to amoxicillin was 77% (95% CI: Prevalence of resistance to cephalosporins
68%, 85%), to penicillin G 75% (95% CI: 65%, 85%) and Prevalence of the resistance of S. aureus to cephalospo-
to ampicillin 76% (95% CI: 67%, 84%). Resistance to rins is similar to the prevalence of resistance to
Deyno et al. Antimicrobial Resistance and Infection Control (2017) 6:85 Page 5 of 15
Comparison of the prevalence of S. aures resistance to antimicrobial agents in Ethiopia was alarmingly high ran-
different antimicrobial agents ging from 11% to vancomycin to 77% to amoxicillin.
Comparison of the prevalence of S. aures resistance to The pooled estimate of the prevalence of S. aureus re-
different antimicrobial agents addressed by this meta- sistance particularly to methicillin (MRSA) in Ethiopia is
analysis is given in Fig. 9. It is found that the magnitude similar to 2014 global surveillance reports of the World
of S.aureus resistance to the different antimicrobial Health Organization (WHO) 2014 [88], which showed
agents ranges from 11% to vancomycin to 77% to amoxicil- MRSA prevalence between 33% to 95% in Africa. The
lin. Accordingly, invitro antimicrobial effectiveness in de- pooled prevalence of MRSA in Ethiopia 47% (95% CI:
creasing order believed to be vancomycin, kanamycin, 33%–61%) is within the range of the global WHO report
ciprofloxacilin, amikacin, clindamycin, amoxacilin-clavulanic for Africa.
acid, cephalothin, carbencilin, ceftriaxone, cefoxitine, chlor- The pooled estimate in study for MRSA is in agree-
amphenicol, erythromycin, doxycycline, methicillin, cotri- ment with the pooled estimate of community acquired-
moxazole, tetracycline, ampicillin, pencilin, and amoxacilin. MRSA prevalence in Asia, Europe, and North America
which ranges from 23.1% to 47.4% [89]. However, the
Discussion pooled estimate 47% (95% CI: 33%–61%) MRSA preva-
In this meta-analysis, we estimated the pooled preva- lence in Ethiopia is higher than pooled estimate of com-
lence of S. aureus resistance to 21 different antimicrobial munity acquired MRSA prevalence 30.2% based on 27
agents commonly used in Ethiopia. Generally 45 studies retrospective studies and 37.3% based on 5 prospective
were included for the meta-analysis, however the num- studies [90]. The higher prevalence in our study may be
ber of studies included in each meta-analyses ranged due to the inclusion of both community acquired and
from 4 to 39. Overall, the 45 studies provided evidence nosocomial infection in the original studies. Nosocomial
regarding the level of S. aureus resistance to different infection are believed to have higher rate of resistance
antimicrobial agents based on 4530 isolates. It was due to larger exposure rate to antimicrobial agents. In-
found that S. aureus resistance to commonly available creasing resistance to antimicrobial agents in hospitals is
Deyno et al. Antimicrobial Resistance and Infection Control (2017) 6:85 Page 10 of 15
caused by transmission of resistant strains within hospi- antibiotics, increased efflux to tetracycline [95, 96], presence
tals by cross colonization of patients via hands of health- of acetyltransferase to chloramphenicol, decrease in accu-
care staff and direct patient to patient contact and mulation to macrolide antibiotics [97], aminoglycoside-
subsequent spread [91]. modifying enzymes production to aminoglycosides, altered
Global pattern of AMR shows variation among differ- topoisomerase IV and DNA gyrase expression for fluoroqui-
ent geographic, socioeconomic strata and among studies nolones, and expression of mec gene altering penicillin
[49, 88, 92]. Variation may be to differences in time, binding protein to β-lactam antibiotics [98]. Since the AMR
place, design, and population involved in the study. This for β-lactam sensitive β-lactam antibiotics is very high, it
may be due to healthcare facilities conditions like imple- can be speculated that most strains of S. aureus
mentation and monitoring of infection prevention found in Ethiopia produce the β-lactamase enzyme.
policies and rational antibiotic usage which varies in dif- However, there is no molecular study conducted to
ferent facilities. The most important reason is due to identify the type of resistant strains and mechanism
character of the study. Studies are conducted within a responsible for resistance in Ethiopia.
specified time and locality. It is reasonable to assume Lower rate of resistance was seen with β-lactamase-
population under study might be infected by the same resistant antibiotics (amoxicillin-clavulanic acid, methi-
strains of agent at specified period of time and location. cillin, ceftriaxone, cefoxtine, and cephalothin) compared
This could be a good reason why heterogeneity tests to β-lactamase-sensitive penicillins. Unlike β-lactamase
showed significant variability (p-value ≤0.01) among sensitive penicillin’s, resistance to carbeniciln is signifi-
studies included in this meta-analysis for 2 l anti- cantly lower. The lower rate of resistance observed with
microbial agents. carbencilin and clindamycin may be due to their infre-
S. aureus acquires resistance by various mechanisms: quent use in Ethiopia [99].
formation of alternative pathways for sulphonamides Resistance to methicillin confers resistance to all β-
[93, 94], production of β-lactamase to β-lactam-sensitive lactamase-resistant penicillins and cephalosporins. This
Deyno et al. Antimicrobial Resistance and Infection Control (2017) 6:85 Page 11 of 15
high level of resistance requires the presence of the mec estimate. The prevalence estimates from Guta et al. and
gene that encodes penicillin-binding protein [98]. The Desalegn et al. were unusually high, however sensitivity
implication of high prevalence of MRSA for suspected analysis showed non-significant influence on the overall
or verified S. aureus infections such as common skin pooled prevalence estimate. Larger exposure probability
and wound infections and surgical prophylaxis is that to resistant strains due to larger use of vancomycin in
there is a need for better alternatives drugs. Alternative hospital settings might have resulted in a relatively
drugs needed to treat or prevent S. aureus infections are higher prevalence of vancomycin resistance in the two
more expensive and, because of their adverse effects, studies [73, 77].
monitoring during treatment is advisable which in- In four of the twenty studies (published in 2014 and
creases the costs even further. after) [48, 51, 73, 77], the prevalence of S. aureus resist-
The prevalence of resistance S. aureus to vancomycin ance to vancomycin is higher than 40%. In contrast, in
11% 995% CI: (4%, 20%) in this study is bothersome and studies published before 2014 the prevalence of S. aur-
higher compared to global prevalence estimate [100]. eus resistance to vancomycin in Ethiopia is much lower
The prevalence of VISA was 2.05% before, 2.63% in (0% to 16%). This may indicate a rapid rise and spread
2006–2009, and 7.93% in 2010–2014. Vancomycin resist- of vancomycin resistant S. aureus strains in Ethiopia as
ance is erasing all possible treatment options in Ethiopia the rate of vancomycin use and exposure in Ethiopia
for MRSA. The higher prevalence of vancomycin in increases. This calls for inclusion for effective new
Ethiopia compared to global estimate may be due to larger anti-MRSA antimicrobial agents for treatment of
and irrational use of antimicrobial agents in Ethiopia, staphylococcal infections in the national medicine list
The prevalence estimates of glycopeptides/vancomycin and effective antimicrobial stewardship programs for
resistance from Guta et al., and Desalegn et al., were prevention and containment of antimicrobial resistance.
unusually high, however sensitivity analysis showed non- Staphylococcal infection in Ethiopia can be better treated
significant influence on the overall pooled prevalence by vancomycin, floroquinolones, and aminoglycosides
Deyno et al. Antimicrobial Resistance and Infection Control (2017) 6:85 Page 12 of 15
Fig. 9 Comparison of the prevalence of S. aureus resistance to different antimicrobial agents in Ethiopia
based on the finding of our invitro finding. However, clin- However, interpretation of the findings of this meta-
ical effectiveness study had not yet proved it. Resistance to analysis requires considering the limitations thereof. The
vancomycin, the only choice for MRSA in Ethiopia, is of a limitations arise from the inherent characteristics of the
great concern. It is bothersome due to lack of alternative included individual studies. First, this is invitro anti-
agents in Ethiopia for the treatment of S. aureus infections. microbial resistance testing and its direct translation to
Making things worse, alternative new anti-MRSA agents clinical effectiveness requires caution. Second, many
(like linezolid, daptomycin, tigecycline, telavancin, and cef- studies involved very limited localities and were done
taroline are rarely available in Ethiopia for treatment of mainly in teaching hospitals in bigger cities where pa-
vancomycin resistant S. aureus. tients with advanced, severe stages, recurrent infec-
Many factors contribute to AMR. First, lack of infec- tions are treated. Hence, the resistance level could
tion prevention contributes to recurrent infection then have overestimated.
to spread of resistant strains. Second, misuse of antimi-
crobials from prescription–dispensing-to patient use Conclusions
[101]. In Ethiopia, it is a common practice that antibi- This meta-analysis demonstrates that S. aureus has got-
otics can be purchased without prescription, which leads ten alarmingly resistant to many of common antimicro-
to misuse of antibiotics by the public [102]. Third factor bials used in Ethiopia. It is highly resistant to penicillin,
could be misuse of antibiotics by health professionals cephalosporin, tetracyclines, chloramphenicol, methicil-
and non-standardized practice [101]. The fourth factor lin, sulphonamides, and vancomycin. Resistance to
could be poor hospital hygienic conditions [103]. A last vancomycin is of a great concern and bothersome due to
contributing factor could be lack of routine antimicro- unavailability of treatment options for S. aureus infec-
bial susceptibility testing which diverts to empiric tions in Ethiopia.
therapy [49]. In line to strategies for prevention and con- Continued and multidimensional efforts of antimicro-
tainment of S. aureus there is a need for innovative way bial stewardship programme promoting rational use of
of halting AMR. Combination therapy and availability of antimicrobials, infection prevention and containment of
new anti-MRSA agents will play vital role in fighting AMR are urgently needed. It is deemed necessary to in-
against AMR to S. aureus. clude new anti-MRSA agents in national medicine list to
Deyno et al. Antimicrobial Resistance and Infection Control (2017) 6:85 Page 13 of 15
treat resistant strains. Combination therapy, effective in Ethics approval and consent to participate
battling AMR in many infectious diseases model, Not applicable.
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