Review

Epidemiology of common resistant bacterial pathogens in

the countries of the Arab League
Rima A Moghnieh, Zeina A Kanafani*, Hussam Z Tabaja*, Sima L Sharara, Lyn S Awad, Souha S Kanj

No uniformly organised collection of data regarding antimicrobial resistance has occurred in the countries of the Arab Lancet Infect Dis 2018
League. 19 countries of the Arab League have published data for antimicrobial susceptibility for the WHO priority Published Online
organisms, and seven of 14 of these organisms are included in this Review (Escherichia coli, Klebsiella spp, Pseudomonas October 3, 2018
http://dx.doi.org/10.1016/
aeruginosa, Acinetobacter baumannii, Salmonella spp, Staphylococcus aureus, and Streptococcus pneumoniae). Although
S1473-3099(18)30414-6
E coli and Klebsiella spp resistance to third-generation cephalosporins is common in all countries, with prevalence
*These authors contributed
reaching more than 50% in Egypt and Syria, carbapenem resistance is emerging, albeit with a prevalence of less than equally
10%. Conversely, a large amount of carbapenem resistance has been reported for P aeruginosa and A baumannii across Division of Infectious Diseases,
the Arab League, reaching 50% and 88% of isolates in some countries. As for Salmonella spp, the prevalence of Department of Internal
fluoroquinolone resistance has exceeded 30% in several areas. With regards to the Gram-positive pathogens, the Medicine, Makassed General
prevalence of meticillin resistance in S aureus is reported to be between 20% and 30% in most countries, but exceeds Hospital, Beirut, Lebanon
(R A Moghnieh MD); and
60% in Egypt and Iraq. The prevalence of penicillin non-susceptibility among pneumococci has reached more than Division of Infectious Diseases,
20% in Algeria, Egypt, Morocco, Saudi Arabia, and Tunisia. These findings highlight the need for structured national Department of Internal
plans in the region to target infection prevention and antimicrobial stewardship. Medicine (Z A Kanafani MD,
H Z Tabaja MD, Prof S S Kanj MD)
and Faculty of Medicine
Introduction standardised approach to the collection, analysis, and (S L Sharara MD), American
Antimicrobial resistance has become a major pandemic sharing of antimicrobial resistance data at a global level.4 University of Beirut, Beirut,
of the 21st century.1,2 In 2013 and 2014, WHO did an GLASS published the first set of data from four countries Lebanon; and Pharmacy
Department, Makassed General
initial analysis of the practices and structures that of the Arab League in January, 2018,5 and is expected to
Hospital, Beirut, Lebanon
addressed antimicrobial resistance, and where gaps generate structured and standardised data from the (L S Awad PharmD)
remained.3 The reports concluded that little was invested countries of the Arab League by 2020.4 Thus, a Correspondence to:
in laboratory surveillance of antimicrobial resistance in comprehensive review of the existing data is crucial to Prof Souha S Kanj, Division of
the eastern Mediterranean and north African regions, assess the current antimicrobial resistance situation in Infectious Diseases, Department
which include most of the member countries of the Arab the region. of Internal Medicine, American
University of Beirut Medical
League (figure 1). In 2017, the WHO antimicrobial resistance study group Centre, Beirut, Lebanon
In 2015, WHO implemented the Global Antimicrobial used a multicriteria decision analysis to prioritise the list of sk11@aub.edu.lb
Resistance Surveillance System (GLASS), to support a antibiotic-resistant bacteria and guide efforts for the

Key messages
• Standardised regional and national antimicrobial resistance
surveillance data are scarce in countries of the Arab League
• Antimicrobial resistance data on the WHO priority
pathogens are only available from some countries of the
Arab League
• The resistance patterns of third-generation
cephalosporin-resistant Enterobacteriaceae,
carbapenem-resistant Enterobacteriaceae,
carbapenem-resistant Pseudomonas aeruginosa, and
carbapenem-resistant Acinetobacter baumannii in the
countries of the Gulf Cooperation Council and Yemen are
similar to those from countries in northern and western
Europe, including France, the Netherlands, and Germany
• Antimicrobial resistance prevalence from the Levant is close
to those from countries in southern Europe, such as Italy
and Greece, or eastern Europe such as Romania
• We recommend the inclusion of antimicrobial resistance
prevention and control as part of national health strategic
plans of the countries of the Arab League, in addition to the
establishment of structured antimicrobial resistance
surveillance systems
• Infection prevention and control policies should be
incorporated into each hospital’s policies and should be
regarded as high priority
• The judicious use of antimicrobials is of paramount
importance through establishing antimicrobial stewardship
programmes
• Improving awareness about antimicrobial resistance and
the inappropriate use of antimicrobials through regional
and national campaigns is highly recommended, targeting
health-care providers, administrators, legislators, and the
public at large
• Controlling the procurement, quality, and dispensing of
antimicrobials in agriculture, veterinary medicine, and
poultry and fishery industries has become essential due to
the spread of resistant microbial strains in the food chain
• We recommend critical evaluation of the quality of generic
antibiotics in the countries of the Arab League
• We encourage adaptation of antimicrobial use behaviours
and infection prevention and control practices to the local
sociodemographic, economic, and even religious
particularities in the different countries of the Arab League

www.thelancet.com/infection Published online October 3, 2018 http://dx.doi.org/10.1016/S1473-3099(18)30414-6 1

 Review

Syria
Lebanon
Tunisia
Morocco Palestinian territories Iraq

Jordan
Kuwait
Algeria Bahrain
Libya
Qatar
Egypt Saudi
Arabia
UAE
Oman

Mauritania

Sudan
Yemen

Djibouti Somalia

African countries of the Arab League

Gulf countries of the Arab League 0 1000 2000 km
Levant countries of the Arab League

Figure 1: Map of the Arab League countries

The Gulf countries of the Arab League are the members of the Gulf Cooperation Council (Bahrain, Kuwait, Oman, Qatar, Saudi Arabia, and United Arab Emirates
[UAE]) and Yemen. The Levant countries of the Arab League are Iraq, Jordan, Lebanon, Palestinian territories, and Syria. The African countries of the Arab League are
Algeria, Comoros, Djibouti, Egypt, Libya, Morocco, Mauritania, Somalia, Sudan, and Tunisia.

25 615 112
18 756
41 51
4113
449 190
712
519 796 629
17 895

150
509

214

Prevalence of resistance
Data not available
<10%
10–30%
31–50%
0 1000 2000 km
>50%

Figure 2: Distribution of third-generation cephalosporin-resistant Enterobacteriaceae (only Escherichia coli and Klebsiella pneumoniae) in the countries of the
Arab League
The numbers in each country represent the tested organisms in the corresponding country.

2 www.thelancet.com/infection Published online October 3, 2018 http://dx.doi.org/10.1016/S1473-3099(18)30414-6

 Review

discovery, research, and development of new antibiotics.6 A wide range of resistance genes have been reported
Seven of these priority organisms have been well described from ESBL-producing Enterobacteriaceae and 3GCRE,
in the published literature from the Arab League,7–16 so we although there seems to be a predominance of ctx-M See Online for appendix
selected them for discussion in this Review: third‑generation
cephalosporin-resistant Enterobacteriaceae, carbapenem- A
resistant Enteroacteriaceae, carbapenem-resistant Pseu-​ 25 448 18 713 111
domonas aeruginosa, carbapenem-resistant Acinetobacter 51
2955 338 41
baumannii, fluoro­quinolone-resistant Salmonella spp,
meticillin-resistant Staphylococcus aureus, and penicillin 668
519 629
non-susceptible Streptococcus pneumoniae. 796
620
150
Third-generation cephalosporin-resistant 503
Enterobacteriaceae
16 countries reported third-generation cephalosporin-
resistant Enterobacteriaceae (3GCRE; by reporting either
the incidence of resistance to third-generation cepha-​
losporins or the incidence of extended spectrum Prevalence of resistance
β-lactamase [ESBL]-producing Enterobacteriaceae) be-​ Data not available
0%
tween 2011 and 2015 (figure 2; appendix). In the countries
0–5%
of the Gulf Cooperation Council (GCC), the prevalence 6–10% 0 1000 2000 km
ranged from 4% to 25% (25% of 190 isolates in Kuwait,17 11–30%
17% of 629 in Qatar18, 7% of 17 895 in Saudi Arabia,19–24 B
and 4% of 150 in Oman25; figure 2). Larger proportions of
resistant isolates were detected in the Levant. In the 186
3920
Palestinian territories and Syria, more than 50% of the 155 3119 97
100
tested isolates were 3GCRE (66% of 41 in Palestinian 450
territories26 and 53·5% of 112 in Syria;27,28 figure 2), as 398
36 586 60
were 30–50% of isolates in Iraq, Jordan, and Lebanon 8049
(47% of 51 in Iraq,29,30 45% of 449 in Jordan,31,32 and 31% of 1512
21
18 756 in Lebanon;33–36 figure 2). In the African countries,
the highest prevalence of resistance was seen in Egypt
(55% of 796),37–43 followed by Sudan (35% of 214),23,44
whereas the lowest was in Tunisia (9% of 25 615),45–53
Morocco (9% of 4113),54–60 and Algeria (14% of 712;
Prevalence of resistance
figure 2).61,62
Data not available
Pertinent subgroups in the published literature <10%
included Escherechia coli and Klebsiella pneumoniae. 10–30%
More isolates of E coli than K pneumoniae were tested 31–50%
>50% 0 1000 2000 km
overall (52 517 vs 16 773). In the GCC countries and the
Levant, where data were available, resistance was C
similar between E coli and K pneumoniae, whereas in
the African countries, the prevalence of resistance was 260
1742 3552
higher among K pneumoniae compared with E coli 41 126
451
(appendix). Another subgroup analysis was based on 64 399
resistance in the community versus hospital settings. 125 454
25 48
Resistance was reported among community isolates in 320 639
170
studies from Kuwait,17 Oman,25 Algeria,62 and Libya,63,64
17
and among hospital isolates for Qatar18 and Egypt.41,43 In
Tunisia and Morocco, data were available from both
community-acquired and hospital-acquired isolates.

Figure 3: Distribution of carbapenem-resistant bacteria in the countries of Prevalence of resistance

the Arab League Data not available
Distribution of carbapenem-resistant Enterobacteriaceae (only Escherichia coli 0%
and Klebsiella pneumoniae; A), carbapenem-resistant Pseudomonas aeruginosa (B), 30–50%
and carbapenem-resistant Acinetobacter baumannii (C). The numbers in each 51–80% 0 1000 2000 km
country represent the tested organisms in the corresponding country. >80%

www.thelancet.com/infection Published online October 3, 2018 http://dx.doi.org/10.1016/S1473-3099(18)30414-6 3

 Review
genes.18,19,22,26,31,32,37,45,48,49,56,57,62,63,65 Concomitant production of
carbapenemases and ESBL enzymes was also noted.66
Carbapenem-resistant Enterobacteriaceae
E coli and K pneumoniae isolates were tested for
carbapenem resistance in 14 countries between 2008 and
2017 (figure 3A; appendix). However, the first available
data about carbapenem-resistant Enteroacteriaceae (CRE)
detection in the area were from specimens collected in
Egypt in 2009.39 Of the GCC countries, only Saudi Arabia
and Qatar described carbapenem resistance among
Enterobacteriaceae isolates, reporting a prevalence of 1%
(of 620 isolates in Saudi Arabia19–22 and 629 in Qatar18),
whereas Oman reported an absence of CRE from
two medical centres (figure 3A).25 In the Levant, prevalence
of CRE was reported at a range of 1–4% in Lebanon
(1% of 18 713),33,36 Syria (3% of 111),27,28 and Iraq (4% of 51),29,30
and at a higher percentage in the Palestinian territories
(22% of 41 E coli isolates)26 and Jordan (22·5% of 338 E coli
isolates; figure 3A).32 In the African countries, reports
from Algeria, Libya, Morocco, Mauritania, and Tunisia
have described a prevalence of CRE of 2% or less,45–59,63,64,66–69
and reports from Egypt revealed the highest prevalence of
resistance in the region (28% of 796 isolates; figure 3A).37–42
Subgroup analysis was similar to that of 3GCRE, with
tested isolates consisting more of E coli than K pneumoniae
(38 481 vs 11 455). Where data were available, carbapenem
resistance was detected at slightly higher frequencies in
K pneumoniae than in E coli in Saudi Arabia (2% for
K pneumoniae vs 0·5% for E coli),19–22 Lebanon (3% vs
1%),33,36 Egypt (40% vs 5%),37–43 Morocco (2% vs 1·5%),54–59
Libya (2·5% vs 0·3%),63,64,66 and Tunisia (2·5% vs 0%),45–53
but not in Mauritania (0% vs 1%).67 As for community
versus hospital settings, resistance was detected among
community isolates in Syria,28 and among hospital
isolates in Saudi Arabia,21 Qatar,18 and Egypt.41,43 In
Morocco, data were available from both community-
acquired and hospital-acquired isolates.55–57,59
Data from the Arab League are abundant enough to
suggest that the prevalence of CRE is rising steadily, with
a predominance of OXA-48 and NDM-1 enzymes in most
countries of the region. Few studies from the GCC
countries reported on the molecular mechanisms of
resistance in CRE. The most commonly produced
carbapenemases were NDM-1 (46·5%), OXA-48-like
(32·5%), or both (8·9%), and no K pneumoniae
carbapenemase (KPC) enzymes were detected.10 Conco-​
mitant production of carbapenemases and ESBL
enzymes was also noted.65 The published literature so far
corroborates NDM-1 and OXA-48 enzymes as the only
carbapenemases expressed in the Eastern Mediterranean
region,70–73 except for one report describing production of
KPC among Enterobacteriaceae isolates from Jordan and
Saudi Arabia.13 One study from Lebanon reported isolates
with multiple concomitant mechanisms of resistance.74
Studies from Africa describe a more varied mole​cular
epidemiology,75,76 particularly in Egypt, where KPC
4 www.thelancet.com/infection Published online October 3, 2018 http://dx.doi.org/10.1016/S1473-3099(18)30414-6
production was notable.77 In the only article describing
colistin-resistant Enterobacteriaceae in the Arab League,
four E coli isolates (one from Saudi Arabia, two from
Bahrain, and one from United Arab Emirates) were
identified carrying the mcr1 gene on conjugative
plasmids.78 Owing to the observed predominance of
OXA‑48 enzyme production in the region, the challenge
inherent to the detection of this family of enzymes
should be highlighted.79 The wide-ranging phenotypic
expression of resistance contributes to this challenge,
with some isolates appearing to be susceptible to broad-
spectrum cephalosporins and carbapenems, others
resistant to broad-spectrum cephalosporins but sus-​
ceptible to carbapenems, and still others resistant to both
broad-spectrum cephalosporins and carbapenems. A
result of this variability could be the under-reporting of
OXA-48 enzymes and hence of CRE, the extent of which
is difficult to determine. Therefore, establishing reliable
methods that can be applied consistently is crucial to
improve detection rates.
Carbapenem-resistant Pseudomonas aeruginosa
14 countries reported carbapenem-resistant Pseudomonas
aeruginosa (CRPA) among isolates between 2002 and 2015
(figure 3B; appendix). In the countries of the GCC, CRPA
prevalence ranged between 3% and 21%, with higher
percentages in Oman (15% of 21),80 United Arab Emirates
(19·5% of 1512),81,82 and Saudi Arabia (21% of 8049),83–89
and a much lower percentage in Kuwait (3% of 450;
figure 3B).90,91 In the Levant, Jordan had the highest
percentage of CRPA (93% of 100; figure 3B).92 In
Lebanon, CRPA was described in 28% of 3920 isolates
(figure 3B).33,34,93,94 In the African countries, data were
available from five countries. The highest prevalence of
resistance was found in Egypt (51% of 586)95–101 and Libya
(56% of 36),102,103 followed by Algeria (50% of 398),104–107 and
the lowest prevalence was found in Tunisia (19% of 3119)108–
110
and Morocco (28% of 155; figure 3B).59,111–114
The source of specimens was not homogeneous. Some
of the reports described P aeruginosa isolates from
general hospital laboratory specimens, while others
described isolates from specific units, such as intensive
care units (ICUs) or burn units.
The production of metallo-β-lactamases (mostly VIM
and IMP) is the most important mechanism of
carbapenem resistance in P aeruginosa throughout the
Arab League countries.83,105,112,115–117 Other rare enzymes
were reported for the first time globally in the Arab
League, including PME-1 from Qatar, produced by an
international clone of P aeruginosa that might have
contributed to the global spread of multiple antibiotic
resistance mechanisms.118 Mutations in gyrA and parC
genes, both inducing quinolone resistance, have
been described in Lebanon.119 Other mechanisms of
resistance, such as mutation of oprD enhancing porin
loss, have also been identified in Lebanon and
Algeria.120,121

Carbapenem-resistant Acinetobacter baumannii
Between 2008 and 2016, carbapenem-resistant Acine-​
tobacter baumannii (CRAB) was reported in 15 countries
(figure 3C; appendix). Of the GCC countries the highest
prevalence of resistance was in Qatar (100% of 48;
figure 3C).76 In the other GCC countries, CRAB
prevalence ranged from 36% to 79% (36% of 639 in
United Arab Emirates,78,82 44% of 399 in Kuwait,122–124
58% of 454 in Bahrain,125 and 79% of 170 in
Saudi Arabia;21,126,127 figure 3C). No carbapenem resistance
was reported in 17 A baumannii isolates from Oman
(figure 3C).80 In the Levant, the highest CRAB prevalence
was reported in Iraq (89% of 126)30,128 and Lebanon
(82% of 3552),33,129,130 followed by Syria (70·5% of 260)131
and Jordan (64% of 64; figure 3C).132 In the African
countries, Egypt (93% of 320)19,133 and Libya (88% of 25)103
reported the highest resistance prevalence, followed by
Algeria (75% of 125),134 Morocco (75% of 451),113,135 and
Tunisia (76% of 1742; figure 3C).136–138 Colistin resistance
was reported in five A baumannii isolates from Lebanon,139
and in one isolate from Tunisia.99
Similar to P aeruginosa, the source of specimens was
variable. Some of the reports described A baumannii
isolates collected from general hospital laboratories,33,128,135,140
whereas others were from specific units.30,122,126,138 In Kuwait
and Egypt, resistance among A baumannii patient isolates
was more pronounced in ICU compared with non-ICU
settings (78% vs 39% in Kuwait,122–124 and 96% vs 70% in
Egypt19,133). A baumannii is also an important pathogen for
257
335
215
19
Prevalence of resistance
Data not available
0%
0–5%
6–10%
11–20%
21–30% 0 1000
>30%
Figure 4: Distribution of fluoroquinolone-resistant Salmonella spp in the countries of the Arab League
The numbers in each country represent the tested organisms in the corresponding country.
www.thelancet.com/infection Published online October 3, 2018 http://dx.doi.org/10.1016/S1473-3099(18)30414-6 5
Review
patients with burns, according to studies from Iraq30 and
Tunisia.136,137 The prevalence of CRAB in these reports
varied between 33% and 89%.30,136,137
One of the few multinational studies on CRAB in the
Arab League comes from the GCC, in which
117 carbapenem-resistant isolates were found to harbour
the blaOXA-51 gene and 91% of them were also positive for
blaOXA-23; NDM, KPC, and VIM enzymes were not
detected.16 Additionally, in one study from a tertiary care
centre in Lebanon, a predominance of OXA-23 was
found.124 These results were confirmed in a report 3 years
later.141 Of note, two studies140,142 have commented on the
effect of the various carbapenemase enzymes on the
amount of carbapenem resistance. High-level resistance
was associated with OXA-23 and OXA-24, whereas GES,
PER, and OXA-51 enzymes mostly predicted low-level
resistance.140,142 Most countries report a polyclonal spread,
with the predominant carbapenemases being OXA-23
and OXA-24, and a rapid emergence of NDM1.8,13
Fluoroquinolone-resistant Salmonella spp
13 countries in the Arab League have published data for
human isolates of fluoroquinolone-resistant Salmonella
spp between 1999 and 2016 (figure 4; appendix). In the
GCC countries, more than 30% of isolates consisted of
fluoroquinolone-resistant Salmonella spp in Saudi Arabia
(32% of 404)143–145 and Kuwait (37·5% of 47),146 a prevalence of
10% of 52 isolates was reported in Qatar (figure 4).147 In
Yemen no resistance was reported (figure 4).148 In the
685
136 33
48 47
52
49
404
73
2000 km
 Review
1848
652
307
408
275
Prevalence of resistance
Data not available
<10%
10–30%
31–50% 0 1000
>50%
Figure 5: Distribution of meticillin-resistant Staphylococcus aureus in the countries of the Arab League
The numbers in each country represent the tested organisms in the corresponding country.
Levant, the highest proportion of resistance came from
Iraq (45·5% of 33; figure 4).149 In the Palestinian territories,
22% of 136 tested isolates were fluoroquinolone
resistant,150,151 compared with only 4% of 685 in Lebanon,33,152
and none in Jordan (figure 4).153 In the African countries,
the prevalence of fluoroquinolone resistance was high in
Morocco (42% of 335)154–156 and Libya (63% of 19),110 and
lower in Egypt (18% of 49),157–159 Tunisia (17% of 257),160–163
and Algeria (2% of 215; figure 4).164,165
In studies from the Saudi Arabia,143,144 Lebanon,33,152 and
the Palestinian territories,150 fluoroquinolone suscep-​
tibility was reported for all Salmonella enterica subspecies
grouped together. In other studies, the results
differentiated between typhoidal146,147,153,164 and non-
typhoidal Salmonella spp.110,145,147–149,151,154–158,160–162,165 More
susceptibility reports were published for non-typhoidal
than typhoidal isolates (891 vs 419). In countries where
both typhoidal and non-typhoidal fluoroquinolone
resistance was reported (Egypt and Algeria), the
prevalence of resistance was higher among non-
typhoidal Salmonella spp (appendix); fluoro-​quinolone
resistance was highest in Libya (63% of 19),110 Iraq
(45·5% of 33),149 Morocco (42% of 335),154–156 Egypt
(33% of 9),157,158 and the Palestinian territories (30% of 71;
figure 4).151 It was lowest in Saudi Arabia (3% of 158)145
and Tunisia (3% of 186; figure 4).160–162 No fluoroquinolone
resistance was reported for non-typhoidal Salmonella
spp in Qatar147 or Yemen.147,148
6 www.thelancet.com/infection Published online October 3, 2018 http://dx.doi.org/10.1016/S1473-3099(18)30414-6
5023
599 937
418
84
53
756
520
38
29
425
2000 km
Similar to other Enterobacteriaceae, the most frequently
identified β-lactam resistance genes among Salmonella
spp belonged to the CTX-M family.165–168 Other reported
genes are from the TEM, OXA, and CMY groups. As for
quinolone resistance genes, few studies have recognised
mutations at position 83 or 87 of the gyrA gene.151,159
Meticillin-resistant Staphylococcus aureus
Meticillin-resistant Staphylococcus aureus (MRSA) was
reported in 16 countries between 1998 and 2015 (figure 5;
appendix). In the GCC, MRSA constituted 12–24% of all
S aureus in Saudi Arabia (24% of 520),169–171 Oman
(14% of 29),80 Qatar (13% of 53),147 and United Arab Emirates
(12% of 38; figure 5).172 In Kuwait, MRSA was detected in
more than 50% of isolates from patients with diabetic foot
infections (71% of 84; figure 5).90 In the Levant, the reported
prevalence of MRSA was lowest in Lebanon (27% of 5023)33,173
and the Palestinian territories (29% of 599),174–177 than in
Jordan (37% of 418),178,179 and the highest resistance
prevalence was noted in Iraq (55% of 937; figure 5).180–182 In
Africa, MRSA was detected in 30–41% of isolates in most
Arab League countries (33% of 307 in Algeria,183,184 32% of
408 in Libya,185,186 41% of 425 in Sudan,187–189 and 30% of 275 in
Mauritania;190 figure 5). It was observed to a lesser extent in
Morocco (24% of 652 isolates)59,191–193 and the highest
percentage was in Egypt (60% of 756 isolates; figure 5).43,169,194
Subgroup analysis addressed the variation in specimen
source, whether from carriers or infected patients, from

1536
231
644
Prevalence of resistance
Data not available
0%
0–2%
3–10%
11–20%
>20% 0 1000
Figure 6: Distribution of penicillin non-susceptible Streptococcus pneumoniae in the countries of the Arab League
The numbers in each country represent the tested organisms in the corresponding country.
health-care workers or non-health-care workers, and
whether it was acquired from the community or the
hospital. Community-acquired MRSA was reported in
countries like Egypt,194 Algeria,183 Tunisia,195 Sudan,187 and
Mauritania.190 The highest prevalence of community-
acquired MRSA among S aureus isolates was reported in
Mauritania (30% of 275)190 and the lowest in Egypt
(11·5% of 183),194 but it was between 20–30% in the other
reporting countries. Hospital-acquired MRSA was reported
in Iraq,182 Egypt,43,194 Algeria,183 and Morocco.59 Excluding
Morocco, which contributed only seven isolates,59 hospital-
acquired MRSA constituted around 70% of S aureus isolates
from the remaining countries.43,182,183,194 Carriage in health-
care workers was noted in the Palestinian territories
(82% of 77),177 Iraq (61% of 41),181 Libya (49% of 45),185
Saudi Arabia (45% of 80),171 and Sudan (33% of 55).189
Various studies from the Arab League have shown a
predominance of SCCmec IV among colonising and
infecting MRSA strains, with less frequent reports of
SSCmec III and V.169,172,175,183,184,196–198 The Panton Valentine
Leukocidin gene appears to be prevalent in colonising
(5–33%) and infecting (20–62%) MRSA strains.169,172,175,183,184,
196–198
Another virulence factor that has been investigated is
tst1, which was found in more than 20% of strai
ns.169,172,175,183,184,196–198 As for the clone types, the
Vienna/Hungarian/Brazilian hospital-acquired MRSA
was most widely identified in the hospital setting,
followed by UK Epidemic MRSA-15 hospital-acquired
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Review
329
211
53 744
100
31 118 48
165
137
18
2000 km
MRSA.196,199,200 In the community setting, the European
community-acquired MRSA was frequently recovered,
along with the so-called Gaza clone, particularly in the
Gaza strip, Lebanon, and Jordan, with a 76% pulsed-field
gel electrophoresis pattern similarity to UK Epidemic
MRSA-15.175
Penicillin non-susceptible Streptococcus
pneumoniae
Penicillin non-susceptible Streptococcus pneumoniae
(PNSSP) were defined as the sum of penicillin-
intermediate and penicillin-resistant S pneumoniae
isolates based on the 2017 Clinical and Laboratory
Standards Institute breakpoints.201
Non-susceptibility data for S pneumoniae isolates were
reported from 14 countries in the Arab League between
2001 and 2016 (figure 6; appendix). Data were also
available from pilgrims from countries all over the world
travelling to Saudi Arabia for the Hajj pilgrimage
(appendix). The GCC countries reported the highest
prevalence of PNSSP isolates, with Saudi Arabia
(70% of 165),202–204 United Arab Emirates (67% of 48),205
and Oman (57% of 137)205,206 reporting the largest
proportions, followed by Bahrain (40% of 100)205 and
Qatar (44% of 118; figure 6).207 The prevalence of PNSSP
was lowest in Kuwait (29% of 744; figure 6).208,209 In the
Levant region, non-susceptibility was identified in
45% of 329 isolates in Lebanon33,166,210 and 67% of
 Review
211 isolates in the Palestinian territories,211 whereas a
study in Jordan showed non-susceptibility to penicillin in
only 9% of 53 isolates (figure 6).212 In the African
countries, the highest prevalence of resistance was
56%, which was reported in Tunisia (1536 isolates;
figure 6).63,163,213–217 Resistance was detected in around
35% of isolates in Algeria (36% of 644)218–220 and Morocco
(35% of 231),167,221,222 in 22·5% of 31 invasive isolates from
three medical centres in Egypt,223 and in none of
18 isolates in Sudan (figure 6).224
Subgroup analysis was based on whether the isolates
were collected from healthy carriers or infected patients,
and whether they were collected from invasive or non-
invasive pneumococcal disease among infected patients.
S pneumoniae in healthy carriers was reported from
Jordan212 and the Palestinian territories,211 as well as from
the Hajj pilgrims.225 In the Palestinian territories, 67% out
of 211 isolates of S pneumoniae in healthy carriers were
PNSSP (figure 6).211 Among the isolates collected from
patients with pneumococcal disease, six countries
(Saudi Arabia, Qatar, Egypt, Algeria, Morocco, and
Sudan) reported non-susceptibility in purely invasive
pneumococcal diseases, and another six (Oman, Bahrain,
United Arab Emirates, Lebanon, Morocco, and Tunisia)
reported non-susceptibility in isolates from non-invasive
pneumococcal disease (appendix). In Morocco, in non-
invasive pneumococcal disease, prevalence of penicillin-
resistant S pneumoniae was 13% (14 of 105 isolates),226
whereas, in invasive pneumococcal diseases, PNSSP was
at 25% (25 of 102 isolates).221
Multidrug-resistant strains of S pneumoniae from the
Arab League belong to different serotypes, the most
predominant of which are 19F, 23F, 6B, and 19A.56,167,202,207,225
Macrolide resistance genes that have been identified in
the available studies include mefA, mefE, and ermB.166,167 A
study from Egypt has also reported the presence of ply,
lytA, and psaA genes.56
Discussion
Potential bias in presented data
Although the compilation of data in this Review is an
important source of information about resistant bacterial
pathogens in the Arab League countries, caution should
be exercised in generalising these data. Most of the
information came from cross-sectional, observational
studies. Potential sources of bias include sample
selection, source of information, measurement error,
and data restricted to subgroups.227
Most studies included a pool of isolates from single or
multiple centres, which might not constitute a representative
epidemiological sample from the country.43 To avoid sample
selection bias, we tried to include the largest possible
numbers of organisms from multiple sources. Furthermore,
for each organism, the source of specimens and the number
of organisms tested were specified.
To prevent bias from information sources, only articles
published in peer-reviewed journals were included,
8 www.thelancet.com/infection Published online October 3, 2018 http://dx.doi.org/10.1016/S1473-3099(18)30414-6
except for one grey literature source (website of the
Tunisian Society for Infectious Diseases). Moreover, the
inclusion criteria specified the year of the publication of
the article and not the year the organisms were collected.
We avoided measurement error by excluding all reports
with microbiological methods that were not clearly
described or were not in concordance with Clinical and
Laboratory Standards Institute or the 2018 European
Committee on Antimicrobial Susceptibility Testing criteria.
To reduce confounding factors, a description of data
from various subgroups was included in this Review.
Comparative epidemiology of priority antimicrobial-
resistant organisms
In January, 2018, WHO released the first GLASS report
in its early implementation phase (2016–17), which
included antimicrobial resistance data from only four
member states of the Arab League.228 By comparison with
this Review, the GLASS report was based on prospective
isolate-based and sample-based surveillance for eight
pathogens: Acinetobacter spp, E coli, K pneumoniae,
Neisseria gonorrhoeae, Salmonella spp, Shigella spp,
S aureus, and S pneumoniae.5 Unlike our Review,
P  aeruginosa was not covered in the GLASS report.
GLASS collected antimicrobial resistance data through a
case-finding surveillance system, based on clinical
specimens sent to laboratories with standardised
surveillance methods on a yearly basis (2015 and 2016 in
the first report),5 whereas in this Review, the antimicrobial
resistance trends were retrospectively retrieved from
previously published articles over the past decade, where
the specimen collection dates were from 2007 to 2016.
The reported number of clinical isolates per country also
differed. For instance, the total number of E coli isolates
tested for third-generation cephalosporin resistance in
Lebanon was 14 979 in this Review versus 84 isolates in
the GLASS report. From Egypt, the total number of
Klebsiella spp isolates tested for third-generation
cephalosporin resistance was 520 herein, by comparison
with only 22 in the GLASS report. Therefore, despite
being a promising and a long-awaited report, GLASS
results are still a premature illustration of the
antimicrobial resistance situation in the region because
of the small sample size. Until GLASS recruits more
laboratories in different Arab countries, this Review
serves to highlight the antimicrobial resistance situation
in the countries of the Arab League.
In a systematic review of antimicrobial resistance in
Africa, Tadesse and colleagues229 reported antimicrobial
resistance trends in seven Arab countries. In their
Review, they reported on a large number of organisms
and on resistance to a wide variety of antibiotics.229 In this
Review, however, we restricted the search to seven bacteria
from the WHO priority list of resistant pathogens.230 The
antimicrobial resistance trends were not similar, because
Tadesse and colleagues229 used data as reported in all the
articles they reviewed, whereas, for this Review, we

included data only from those papers that included
methods compliant with Clinical and Laboratory
Standards Institute or European Committee on
Antimicrobial Susceptibility Testing guidelines. The
difference in resistance trends in the same countries
underscores the importance of initiating a structured
and standardised surveillance system in all countries of
the Arab League.
In comparing the resistance data in this report with
the European data from the EARS-Net (2016),58 we
found that, much like those observed throughout
Europe, epidemiological resistance patterns among the
countries of the Arab League are not homogenous.
These wide-varying differences are not surprising
given the vast geographical spread of the Arab
countries, with distinct population types, climates, and
social and health-care structures. For example, the
resistance patterns of 3GCRE, CRE, CRPA, and CRAB
in the GCC countries were similar to data from
countries in northern and western Europe, including
France, the Netherlands, and Germany (10–25%),
whereas percentages from the Levant were more
similar to those from countries in southern Europe,
such as Italy and Greece, or eastern Europe, such as
Romania (25–50%).
Effect on policies and practice
The heterogeneous prevalence of different antimicrobial
resistance trends in the countries of the Arab League
calls for interventions at the clinical practice and public
health levels. In general, the rational use of antimicrobials
represents an integral part of good clinical practice.231
The appropriateness of antimicrobial therapy is mostly
dependent on the availability of regional epidemiological
data and resistance profiles.231,232 The latter affects
therapeutic efficacy of antimicrobial treatment and
minimises the risks associated with the selection of
resistant strains.232 Accordingly, the development
of national or regional guidelines for the management of
common infectious diseases tailored to the local
antimicrobial resistance patterns has become a necessity.
However, advocating judicious use of antibiotics in such
guidelines is crucial in preventing further emergence
and spread of antimicrobial resistance. In this spirit,
some efforts have been welcomed such as the GCC
guidelines for management of community-acquired
pneumonia233 and the Lebanese Society of Infectious
Diseases guidelines for community-acquired pneumonia,
urinary tract in-​ fections, and febrile neutropenia at a
national level.234–236 The importance of antimicrobial
stewardship programmes (ie, coordinated interventions
designed to improve appropriate use of antimicrobial
drugs, including prevention of inappropriate
antimicrobial use and reduction of antimicrobial
exposure) in reducing antibiotic selection pressure has
been demonstrated in a prospective study from
Saudi Arabia, where the implementation of the
www.thelancet.com/infection Published online October 3, 2018 http://dx.doi.org/10.1016/S1473-3099(18)30414-6 9
Review
programme in a 1000-bed hospital resulted in a
significant reduction in the prevalence of antimicrobial
resistance-related infections, notably A baumannii, along
with a decrease in broad-spectrum antibiotic con-​
sumption.237,238 Moreover, the alarming rise in the
prevalence of resistant organisms in countries of the
Arab League calls attention to the need for improved
infection prevention and control (IPC) practices to
prevent their spread. Many Arab countries have
developed state of the art IPC programmes in accordance
with international standards, including GCC countries
and Lebanon;239–243 however, many hospitals in the region
are still lacking such programmes. It is well established
that antimicrobial stewardship initiatives, local guideline
implementation, and application of strict IPC measures
collectively decrease the incidence of infections caused
by antimicrobial resistant pathogens and reduce broad-
spectrum antibiotic use.244,245 In the hospital setting, the
role of IPC programmes is vital in reducing the number
of hospital-acquired infections.246 Thus, establishing
rigorous IPC programmes should be a priority in the
strategic plans of all health-care institutions. This priority
has been emphasised by the ministries of health in
certain countries, such as Lebanon and GCC countries,
where having an active IPC programme is a requirement
for hospital accreditation.239–241,243
Additionally, the extensive use of over-the-counter
antibiotics is of paramount importance in aggravating
the antimicrobial resistance. In a systematic review
investigating self-medication in the Middle East,
consumption of antibiotics without prescription ranged
from 20% to 85% in some communities.247 Given this
situation, governments in the Arab League need to
establish and implement legislation that forbids the
dispensing of antibiotics over the counter.
Antimicrobial resistance is not only restricted to
organisms isolated from humans. Several reports from
our region have confirmed the presence of resistant
organisms in the environment, including superficial
water, wastewaters, poultry, and farm animals, with
potential spread of these resistant bacterial strains to
humans via the food chain.68,148,248–250 Antibiotic use in
livestock appears to be a major contributing factor, yet
control over the prescription and use of antibiotics are
almost non-existent.251 Consequently, national policies
that oversee the procurement, quality, storage,
dispensing, and use of antimicrobials in the veterinary
field are urgently needed.
Although the presented antimicrobial resistance data in
this Review cover the common resistant pathogens in the
Arab League, they are seldom based on structured
national surveillance studies and are mostly a compilation
of reported literature by independent scientists from
countries of the Arab League. Consequently, data
concerning other priority antimicrobial resistant
organisms like vancomycin-resistant Enterococcus spp,
were not included because available data were scarce.
 Review
Search strategy and selection criteria
We searched PubMed (MEDLINE) and Web of Science for articles published in English,
French, and Arabic between Jan 1, 2008, and Dec 31, 2017, addressing seven of the WHO
priority pathogens: third-generation cephalosporin-resistant Enterobacteriaceae (3GCRE),
carbapenem-resistant Enterobacteriaceae, carbapenem-resistant Pseudomonas aeruginosa,
carbapenem-resistant Acinetobacter baumannii, fluoroquinolone-resistant Salmonella spp,
methicillin-resistant Staphylococcus aureus, and penicillin non-susceptible Streptococcus
pneumoniae. Data for 3GCRE, however, were only included from articles published between
Jan 1, 2013, and Dec 31, 2017. We undertook a comprehensive grey literature search for
relevant antimicrobial resistance data during the same period. We used Google Scholar to
retrieve articles not indexed in the aforementioned databases, mainly for countries without
available antimicrobial resistance data. Search terms were “antimicrobial”, “resistance”, and
“susceptibility”, in addition to the names of the Arab League countries and those of the
priority organisms. We excluded articles with an unclear antibiotic susceptibility method, or
a method non-concordant with that of the 2017 Clinical and Laboratory Standards Institute
guidelines, or that of the 2018 European Committee on Antimicrobial Susceptibility
Testing guidelines. We also excluded articles containing antimicrobial resistance data from
undefined sources and articles with preselected resistant organisms with no denominator
from which the percentage of resistance could be calculated.
Moreover, no or very limited data were available from
some countries, such as Djibouti, Comoros, Somalia, and
Mauritania. While we await a more representative future
GLASS report, this Review provides an initial assessment
of antimicrobial resistance in the region.
The lack of structured data from the Arab League
highlights the need for national surveillance in individual
countries and enrolment of a representative number of
laboratories in each country into the GLASS project. So
far, GLASS is active in a limited number of countries
with few included laboratories.5 Factors that affect
enrolment into GLASS include the quality of the
generated data. Consequently, standardised laboratory
techniques are needed to detect and monitor trends of
antimicrobial resistance in the region. This approach
should be a priority for national health strategic plans as
part of an aim for regional containment of antimicrobial
resistance. The WHO global action plan for antimicrobial
resistance based on the One Health Approach252 includes
all these recommendations and is well defined in the
WHO antimicrobial resistance toolkit.
Conclusion
Data for antimicrobial resistance from the countries of
the Arab League mostly exist for the organisms classified
as critical priority in the WHO antimicrobial resistance
priority pathogen list6 (CRAB, CRPA, 3GCRE, and CRE),
in addition to fluoroquinolone-resistant Salmonella spp,
MRSA from the high priority category, and PNSSP from
the medium priority category. The prevalence of
resistance of the reviewed pathogens varies widely in the
different countries. In general, the resistance patterns of
3GCRE, CRE, CRPA, and CRAB in the countries of the
GCC were similar to data from countries in northern and
western Europe, including France, the Netherlands, and
10 www.thelancet.com/infection Published online October 3, 2018 http://dx.doi.org/10.1016/S1473-3099(18)30414-6
Germany, whereas prevalence in the Levant was closer to
that in countries in southern Europe, such as Italy and
Greece, or eastern Europe, such as Romania.
Although this Review provides an overview of existing
antimicrobial resistance patterns, it highlights the clear
need for standardisation of microbiological methods and
antimicrobial surveillance techniques in the countries of
the Arab League and calls for the urgent need to address
the antimicrobial stewardship and IPC efforts in the
region and the need to adopt the One Health Approach
proposed by WHO.
Contributors
RAM, HZT, and ZAK did the literature search and wrote the first
draft of the paper. HZT and ZAK worked on equal numbers of
pathogens. SLS and LSA critically reviewed and edited the manuscript
and figures. RAM and SSK drafted the manuscript concept and design
and critically revised the manuscript for important intellectual content.
SSK supervised the writing of the Review. All authors approved the final
version of the manuscript.
Declaration of interests
We declare no competing interests.
Acknowledgments
We would like to acknowledge Ribale Haidar for the graphic conception
of the maps.
References
1 Anderson RM. The pandemic of antibiotic resistance.
Nat Med 1999; 5: 147–49.
2 Peterson LR. Bad bugs, no drugs: no ESCAPE revisited.
Clin Infect Dis 2009; 49: 992–93.
3 WHO. Worldwide country situation analysis: response to
antimicrobial resistance. 2015. http://www.who.int/drugresistance/
documents/situationanalysis/en/ (accessed Feb 8, 2018).
4 WHO. Global antimicrobial resistance surveillance system. 2015.
http://www.who.int/antimicrobialresistance/publications/
surveillance-system-manual/en/ (accessed Feb 8, 2018).
5 WHO. Global antimicrobial resistance surveillance system
(GLASS) report. 2018. http://www.who.int/glass/resources/
publications/early-implementation-report/en/
(accessed Feb 8, 2018).
6 WHO. Global priority list of antibiotic-resistant bacteria to guide
research, discovery, and development of new antibiotics. 2017.
http://www.who.int/medicines/publications/global-priority-list-
antibiotic-resistant-bacteria/en/ (accessed Feb 8, 2018).
7 Zigmond J, Pecan L, Hájek P, Raghubir N, Omrani A.
MRSA infection and colonization rates in Africa and Middle East:
a systematic review & meta-analysis. Int J Infect Dis 2014; 21: 391.
8 Djahmi N, Dunyach-Remy C, Pantel A, Dekhil M, Sotto A,
Lavigne JP. Epidemiology of carbapenemase-producing
Enterobacteriaceae and Acinetobacter baumannii in Mediterranean
countries. Biomed Res Int 2014; 2014: 305784.
9 El Moujaber G, Osman M, Rafei R, Dabboussi F, Hamze M.
Molecular mechanisms and epidemiology of resistance in
Streptococcus pneumoniae in the Middle East region. J Med Microbiol
2017; 66: 847–58.
10 Sonnevend A, Ghazawi AA, Hashmey R, et al. Characterization
of carbapenem-resistant Enterobacteriaceae with high rate of
autochthonous transmission in the Arabian Peninsula. PLoS One
2015; 10: e0131372.
11 Tadesse G, Tessema TS, Beyene G, Aseffa A. Molecular
epidemiology of fluoroquinolone resistant salmonella in Africa:
a systematic review and meta-analysis. PLoS One 2018;
13: e0192575.
12 Tokajian S. New epidemiology of Staphylococcus aureus infections in
the Middle East. Clin Microbiol Infect 2014; 20: 624–8.
13 Zahedi Bialvaei A, Samadi Kafil H, Ebrahimzadeh Leylabadlo H,
Asgharzadeh M, Aghazadeh M. Dissemination of carbapenemases
producing Gram negative bacteria in the Middle East.
Iran J Microbiol 2015; 7: 226–46.

14 Zowawi HM, Balkhy HH, Walsh TR, Paterson DL. β-Lactamase
production in key Gram-negative pathogen isolates from the
Arabian Peninsula. Clin Microbiol Rev 2013; 26: 361–80.
15 Zowawi HM, Sartor AL, Balkhy HH, et al.
Molecular characterization of carbapenemase-producing Escherichia
coli and Klebsiella pneumoniae in the countries of the Gulf
cooperation council: dominance of OXA-48 and NDM producers.
Antimicrob Agents Chemother 2014; 58: 3085–90.
16 Zowawi HM, Sartor AL, Sidjabat HE, et al. Molecular epidemiology
of carbapenem-resistant Acinetobacter baumannii isolates in the
Gulf Cooperation Council States: dominance of OXA-23-type
producers. J Clin Microbiol 2015; 53: 896–903.
17 Sewify M, Nair S, Warsame S, et al. Prevalence of urinary tract
infection and antimicrobial susceptibility among diabetic patients
with controlled and uncontrolled glycemia in Kuwait.
J Diabetes Res 2016; 2016: 6573215.
18 Sid Ahmed MA, Bansal D, Acharya A, et al. Antimicrobial
susceptibility and molecular epidemiology of extended-spectrum
β-lactamase-producing Enterobacteriaceae from intensive care units
at Hamad Medical Corporation, Qatar.
Antimicrob Resist Infect Control 2016; 5: 4.
19 Al-Agamy MH, Shibl AM, Hafez MM, Al-Ahdal MN, Memish ZA,
Khubnani H. Molecular characteristics of extended-spectrum
β-lactamase-producing Escherichia coli in Riyadh: emergence of
CTX-M-15-producing E coli ST131.
Ann Clin Microbiol Antimicrob 2014; 13: 4.
20 Al-Otaibi FE, Bukhari EE. Clinical and laboratory profiles of urinary
tract infections caused by extended-spectrum
β-lactamase-producing Escherichia coli in a tertiary care center in
central Saudi Arabia. Saudi Med J 2013; 34: 171–76.
21 Al-Otaibi FE, Bukhari EE, Badr M, Alrabiaa AA. Prevalence and risk
factors of Gram-negative bacilli causing blood stream infection in
patients with malignancy. Saudi Med J 2016; 37: 979–84.
22 Al-Qahtani AA, Al-Agamy MH, Ali MS, Al-Ahdal MN,
Aljohi MA, Shibl AM. Characterization of extended-spectrum
β-lactamase-producing Klebsiella pneumoniae from Riyadh,
Saudi Arabia. J Chemother 2014; 26: 139–45.
23 Ibrahim ME, Bilal NE, Hamid ME. Comparison of phenotypic
characteristics and antimicrobial resistance patterns of clinical
Escherichia coli collected from two unrelated geographical areas.
Glob J Health Sci 2014; 6: 126–35.
24 Somily AM, Habib HA, Absar MM, et al. ESBL-producing
Escherichia coli and Klebsiella pneumoniae at a tertiary care hospital
in Saudi Arabia. J Infect Dev Ctries 2014; 8: 1129–36.
25 Sharef SW, El-Naggari M, Al-Nabhani D, Al Sawai A,
Al Muharrmi Z, Elnour I. Incidence of antibiotics resistance among
uropathogens in Omani children presenting with a single episode of
urinary tract infection. J Infect Public Health 2015; 8: 458–65.
26 Adwan K, Jarrar N, Abu-Hijleh A, Adwan G, Awwad E.
Molecular characterization of Escherichia coli isolates from patients with
urinary tract infections in Palestine. J Med Microbiol 2014; 63: 229–34.
27 Al-Assil B, Mahfoud M, Hamzeh AR. Resistance trends and risk
factors of extended spectrum β-lactamases in Escherichia coli
infections in Aleppo, Syria. Am J Infect Control 2013; 41: 597–600.
28 Teicher CL, Ronat JB, Fakhri RM, et al. Antimicrobial drug-resistant
bacteria isolated from Syrian war-injured patients,
August 2011–March 2013. Emerg Infect Dis 2014; 20: 1949–51.
29 Aljanaby AAJ, Alhasnawi H. Phenotypic and molecular
characterization of multidrug resistant Klebsiella pneumoniae
isolated from different clinical sources in Al-Najaf Province—Iraq.
Pak J Biol Sci 2017; 20: 217–32.
30 Ronat JB, Kakol J, Khoury MN, et al. Highly drug-resistant
pathogens implicated in burn-associated bacteremia in an Iraqi
burn care unit. PLoS One 2014; 9: e101017.
31 Aqel AA, Meunier D, Alzoubi HM, Masalha IM, Woodford N.
Detection of CTX-M-type extended-spectrum β-lactamases among
Jordanian clinical isolates of Enterobacteriaceae.
Scand J Infect Dis 2014; 46: 155–57.
32 Badran EF, Qamer Din RA, Shehabi AA. Low intestinal
colonization of Escherichia coli clone ST131 producing CTX-M-15 in
Jordanian infants. J Med Microbiol 2016; 65: 137–41.
33 Chamoun K, Farah M, Araj G, et al. Surveillance of antimicrobial
resistance in Lebanese hospitals: retrospective nationwide compiled
data. Int J Infect Dis 2016; 46: 64–70.
www.thelancet.com/infection Published online October 3, 2018 http://dx.doi.org/10.1016/S1473-3099(18)30414-6 11
Review
34 Matta R, Hallit S, Hallit R, Bawab W, Rogues A, Salameh P.
Epidemiology and microbiological profile comparison between
community and hospital acquired infections: a multicenter
retrospective study in Lebanon. J Infect Public Health 2018; 11: 405–11.
35 Moghnieh R, Estaitieh N, Mugharbil A, et al. Third generation
cephalosporin resistant Enterobacteriaceae and multidrug resistant
Gram-negative bacteria causing bacteremia in febrile neutropenia
adult cancer patients in Lebanon, broad spectrum antibiotics use as
a major risk factor, and correlation with poor prognosis.
Front Cell Infect Microbiol 2015; 5: 11.
36 Moghnieh RA, Musharrafieh UM, Husni RN, et al. E coli,
K pneumoniae and K oxytoca community-acquired infections
susceptibility to cephalosporins and other antimicrobials in
Lebanon. J Med Liban 2014; 62: 107–12.
37 Abdallah HM, Wintermans BB, Reuland EA, et al.
Extended-spectrum β-lactamase- and carbapenemase-producing
Enterobacteriaceae isolated from Egyptian patients with suspected
blood stream infection. PLoS One 2015; 10: e0128120.
38 Abdel-Aziz Elzayat M, Barnett-Vanes A, Dabour MFE, Cheng F.
Prevalence of undiagnosed asymptomatic bacteriuria and associated
risk factors during pregnancy: a cross-sectional study at two tertiary
centres in Cairo, Egypt. BMJ Open 2017; 7: e013198.
39 Abdelaziz MO, Bonura C, Aleo A, Fasciana T, Cala C, Mammina C.
Cephalosporin resistant Escherichia coli from cancer patients in
Cairo, Egypt. Microbiol Immunol 2013; 57: 391–5.
40 Rizk DE, El-Mahdy AM. Emergence of class 1 to 3 integrons among
members of Enterobacteriaceae in Egypt. Microb Pathog 2017;
112: 50–56.
41 Shehab El-Din EM, El-Sokkary MM, Bassiouny MR, Hassan R.
Epidemiology of neonatal sepsis and implicated pathogens: a study
from Egypt. Biomed Res Int 2015; 2015: 509484.
42 Wassef M, Abdelhaleim M, AbdulRahman E, Ghaith D. The role of
OmpK35, OmpK36 porins, and production of β-lactamases on
imipenem susceptibility in Klebsiella pneumoniae clinical isolates,
Cairo, Egypt. Microb Drug Resist 2015; 21: 577–80.
43 Talaat M, El-Shokry M, El-Kholy J, et al. National surveillance of
health care-associated infections in Egypt: developing a sustainable
program in a resource-limited country. Am J Infect Control 2016;
44: 1296–301.
44 Ibrahim ME, Magzoub MA, Bilal NE, Hamid ME. Distribution of
Class I integrons and their effect on the prevalence of multi-drug
resistant Escherichia coli clinical isolates from Sudan. Saudi Med J
2013; 34: 240–47.
45 Tanfous FB, Achour W, Raddaoui A, Ben Hassen A.
Molecular characterization and epidemiology of extended
spectrum β-lactamase producing Klebsiella pneumoniae isolates from
immunocompromised patients in Tunisia. J Glob Antimicrob Resist
2018; 13: 154–60.
46 Cherif T, Saidani M, Decre D, Boutiba-Ben Boubaker I, Arlet G.
Cooccurrence of multiple AmpC β-lactamases in Escherichia coli,
Klebsiella pneumoniae, and Proteus mirabilis in Tunisia.
Antimicrob Agents Chemother 2015; 60: 44–51.
47 Ferjani S, Saidani M, Amine FS, Boutiba Ben Boubaker I.
A comparative study of antimicrobial resistance rates and
phylogenetic groups of community-acquired versus
hospital-acquired invasive Escherichia coli. Med Mal Infect 2015;
45: 133–38.
48 Ferjani S, Saidani M, Ennigrou S, Hsairi M, Slim AF,
Ben Boubaker IB. Multidrug resistance and high virulence
genotype in uropathogenic Escherichia coli due to diffusion of
ST131 clonal group producing CTX-M-15: an emerging problem in
a Tunisian hospital. Folia Microbiol 2014; 59: 257–62.
49 Hammami S, Saidani M, Ferjeni S, Aissa I, Slim A,
Boutiba-Ben Boubaker I. Characterization of extended spectrum
β-lactamase-producing Escherichia coli in community-acquired urinary
tract infections in Tunisia. Microb Drug Resist 2013; 19: 231–36.
50 Mansour W, Grami R, Ben Haj Khalifa A, et al. Dissemination of
multidrug-resistant blaCTX-M-15/IncFIIk plasmids in Klebsiella
pneumoniae isolates from hospital- and community-acquired
human infections in Tunisia. Diagn Microbiol Infect Dis 2015;
83: 298–304.
51 Smaoui S, Abdelhedi K, Marouane C, Kammoun S,
Messadi-Akrout F. Antibiotic resistance of community-acquired
uropathogenic Enterobacteriaceae isolated in Sfax (Tunisia).
Med Mal Infect 2015; 45: 335–37 (in French).
 Review
52 Société Tunisienne de Pathologie Infectieuse. LART Data. E coli.
2014. https://www.infectiologie.org.tn/pdf_ppt_docs/
lart2012-2013-2014/LART2014Ecoli.pdf (accessed Feb 9, 2018).
53 Société Tunisienne de Pathologie Infectieuse. LART Data. K
pneumoniae. 2014. https://www.infectiologie.org.tn/pdf_ppt_docs/
lart2012-2013-2014/LART2014Kpneumoniae.pdf
(accessed Feb 9, 2018).
54 Alem N, Frikh M, Srifi A, et al. Evaluation of antimicrobial
susceptibility of Escherichia coli strains isolated in Rabat University
Hospital (Morocco). BMC Res Notes 2015; 8: 392.
55 Arhoune B, Oumokhtar B, Hmami F, et al. Rectal carriage of
extended-spectrum β-lactamase- and carbapenemase-producing
Enterobacteriaceae among hospitalised neonates in a neonatal
intensive care unit in Fez, Morocco. J Glob Antimicrob Resist 2017;
8: 90–96.
56 Barguigua A, El Otmani F, Talmi M, et al. Prevalence and genotypic
analysis of plasmid-mediated β-lactamases among urinary Klebsiella
pneumoniae isolates in Moroccan community. J Antibiot 2013;
66: 11–16.
57 Barguigua A, El Otmani F, Talmi M, Zerouali K, Timinouni M.
Prevalence and types of extended spectrum β-lactamases among
urinary Escherichia coli isolates in Moroccan community.
Microb Pathog 2013; 61–62: 16–22.
58 El Bouamri MC, Arsalane L, Kamouni Y, Berraha M, Zouhair S.
Recent evolution of the epidemiological profile of extended-
spectrum β-lactamase producing uropathogenic enterobacteria
in Marrakech, Morocco. Prog Urol 2014; 24: 451–55 (in French).
59 El Kettani A, Zerouali K, Diawara I, et al. Les bactériémies associées
aux soins en réanimation au Centre hospitalier universitaire Ibn
Rochd, Casablanca, Maroc. Santé Publique 2017; 29: 209–13 (in French).
60 Saez-Lopez E, Cossa A, Benmessaoud R, et al. Characterization of
vaginal Escherichia coli isolated from pregnant women in
two different African sites. PLoS One 2016; 11: e0158695.
61 El Fertas-Aissani R, Messai Y, Alouache S, Bakour R.
Virulence profiles and antibiotic susceptibility patterns of
Klebsiella pneumoniae strains isolated from different clinical
specimens. Pathol Biol 2013; 61: 209–16.
62 Yahiaoui M, Robin F, Bakour R, Hamidi M, Bonnet R, Messai Y.
Antibiotic resistance, virulence, and genetic background of
community-acquired uropathogenic Escherichia coli from Algeria.
Microb Drug Resist 2015; 21: 516–26.
63 Ahmed SF, Ali MM, Mohamed ZK, Moussa TA, Klena JD.
Fecal carriage of extended-spectrum β-lactamases and
AmpC-producing Escherichia coli in a Libyan community.
Ann Clin Microbiol Antimicrob 2014; 13: 22.
64 Dau AA, Tloba S, Daw MA. Characterization of wound infections
among injured patients during Libyan conflict.
East Mediterr Health J 2013; 19: 356–61.
65 Abujnah A, Zorgani A, Sabri M, El-Mohammady H, Khalek R,
Ghenghesh K. Multidrug resistance and extended-spectrum
β-lactamases genes among Escherichia coli from patients with urinary
tract infections in northwestern Libya. Libyan J Med 2015; 10: 26412.
66 Jamal W, Rotimi VO, Albert MJ, Khodakhast F, Nordmann P,
Poirel L. High prevalence of VIM-4 and NDM-1 metallo-β-lactamase
among carbapenem-resistant Enterobacteriaceae.
J Med Microbiol 2013; 62: 1239–44.
67 Hailaji NS, Ould Salem ML, Ghaber SM. Sensitivity to antibiotics
uropathogens bacteria in Nouakchott—Mauritania. Prog Urol 2016;
26: 346–52 (in French).
68 Agabou A, Lezzar N, Ouchenane Z, et al. Clonal relationship
between human and avian ciprofloxacin-resistant Escherichia coli
isolates in north-eastern Algeria. Eur J Clin Microbiol Infect Dis 2015;
35: 227–34.
69 Agabou A, Pantel A, Ouchenane Z, et al. First description of
OXA-48-producing Escherichia coli and the pandemic clone ST131
from patients hospitalised at a military hospital in Algeria.
Eur J Clin Microbiol Infect Dis 2014; 33: 1641–46.
70 Gunness P, Aleksa K, Bend J, Koren G. Acyclovir-induced
nephrotoxicity: the role of the acyclovir aldehyde metabolite.
Transl Res 2011; 158: 290–301.
71 Aqel AA, Giakkoupi P, Alzoubi H, Masalha I, Ellington MJ,
Vatopoulos A. Detection of OXA-48-like and NDM carbapenemases
producing Klebsiella pneumoniae in Jordan: a pilot study.
J Infect Public Health 2017; 10: 150–55.
12 www.thelancet.com/infection Published online October 3, 2018 http://dx.doi.org/10.1016/S1473-3099(18)30414-6
72 Lerner A, Solter E, Rachi E, et al. Detection and characterization of
carbapenemase-producing Enterobacteriaceae in wounded Syrian
patients admitted to hospitals in northern Israel.
Eur J Clin Microbiol Infect Dis 2016; 35: 149–54.
73 El-Herte RI, Araj GF, Matar GM, Baroud M, Kanafani ZA, Kanj SS.
Detection of carbapenem-resistant Escherichia coli and Klebsiella
pneumoniae producing NDM-1 in Lebanon. J Infect Dev Ctries 2012;
6: 457–61.
74 Baroud Á, Dandache I, Araj GF, et al. Underlying mechanisms of
carbapenem resistance in extended-spectrum
β-lactamase-producing Klebsiella pneumoniae and Escherichia coli
isolates at a tertiary care centre in Lebanon: role of OXA-48 and
NDM-1 carbapenemases. Int J Antimicrob Agents 2013; 41: 75–79.
75 Lahlaoui H, Bonnin RA, Moussa MB, Khelifa ABH, Naas T.
First report of OXA-232-producing Klebsiella pneumoniae strains in
Tunisia. Diagn Microbiol Infect Dis 2017; 88: 195–97.
76 Rolain JM, Loucif L, Al-Maslamani M, et al. Emergence of
multidrug-resistant Acinetobacter baumannii producing OXA-23
carbapenemase in Qatar. New Microbes New Infect 2016; 11: 47–51.
77 Metwally L, Gomaa N, Attallah M, Kamel N. High prevalence of
Klebsiella pneumoniae carbapenemase-mediated resistance in
K pneumoniae isolates from Egypt. East Mediterr Health J 2013;
19: 947–52.
78 Sonnevend A, Ghazawi A, Alqahtani M, et al. Plasmid-mediated
colistin resistance in Escherichia coli from the Arabian Peninsula.
Int J Infect Dis 2016; 50: 85–90.
79 Poirel L, Potron A, Nordmann P. OXA-48-like carbapenemases:
the phantom menace. J Antimicrob Chemother 2012; 67: 1597–606.
80 Al-Yaqoubi M, Elhag K. Susceptibilities of common bacterial
isolates from Oman to old and new antibiotics. Oman Med J 2008;
23: 173–78.
81 Al-Dhaheri AS, Al-Niyadi MS, Al-Dhaheri AD, Bastaki SM.
Resistance patterns of bacterial isolates to antimicrobials from
3 hospitals in the United Arab Emirates. Saudi Med J 2009;
30: 618–23.
82 Al-Kaabi MR, Tariq WU, Hassanein AA. Rising bacterial resistance
to common antibiotics in Al Ain, United Arab Emirates.
East Mediterr Health J 2011; 17: 479–84.
83 Abdalhamid B, Elhadi N, Alabdulqader N, Alsamman K,
Aljindan R. Rates of gastrointestinal tract colonization of
carbapenem-resistant Enterobacteriaceae and Pseudomonas
aeruginosa in hospitals in Saudi Arabia.
New Microbes New Infect 2016; 10: 77–83.
84 Al Johani SM, Akhter J, Balkhy H, El-Saed A, Younan M,
Memish Z. Prevalence of antimicrobial resistance among
gram-negative isolates in an adult intensive care unit at a tertiary
care center in Saudi Arabia. Ann Saudi Med 2010; 30: 364–69.
85 Al-Agamy MH, Shibl AM, Zaki SA, Tawfik AF. Antimicrobial
resistance pattern and prevalence of metallo-β-lactamases in
Pseudomonas aeruginosa from Saudi Arabia. Afr J Microbiol Res 2011;
5: 5528–33.
86 Asghar AH. Antimicrobial susceptibility and metallo-β-lactamase
production among Pseudomonas aeruginosa isolated from Makkah
hospitals. Pak J Med Sci 2012; 28: 781–86.
87 Khan MA, Faiz A. Antimicrobial resistance patterns of Pseudomonas
aeruginosa in tertiary care hospitals of Makkah and Jeddah.
Ann Saudi Med 2016; 36: 23–28.
88 Memish ZA, Shibl AM, Kambal AM, Ohaly YA, Ishaq A,
Livermore DM. Antimicrobial resistance among non-fermenting
Gram-negative bacteria in Saudi Arabia.
J Antimicrob Chemother 2012; 67: 1701–05.
89 Tawfik AF, Shibl AM, Aljohi MA, Altammami MA, Al-Agamy MH.
Distribution of Ambler class A, B and D β-lactamases among
Pseudomonas aeruginosa isolates. Burns 2012; 38: 855–60.
90 Al Benwan K, Al Mulla A, Rotimi VO. A study of the microbiology
of diabetic foot infections in a teaching hospital in Kuwait.
J Infect Public Health 2012; 5: 1–8.
91 Al Benwan K, Al Sweih N, Rotimi VO. Etiology and antibiotic
susceptibility patterns of community- and hospital-acquired urinary
tract infections in a general hospital in Kuwait.
Med Princ Pract 2010; 19: 440–46.
92 Elnasser ZA, Al Aseel SM. Antibiotic resistance of Pseudomonas
aeruginosa isolates from patients in King Abdullah University
Hospital in Jordan. J Chemother 2009; 21: 356–59.

93 El Kary N, El Rassy E, Azar N, Choucair J. Ciprofloxacin and
imipenem resistance and cross-resistance in Pseudomonas
aeruginosa: a single institution experience. Am J Infect Control 2016;
44: 1736–37.
94 Mouawad R, Afif C, Azar E, et al. Effect of antibiotic consumption
on resistance of Pseudomonas aeruginosa isolated from Lebanese
patients with emphasis on MBL production. Adv Microbiol 2013;
3: 382–88.
95 Abaza AF, El Shazly SA, Selim HSA, Aly GSA.
Metallo-beta-lactamase producing Pseudomonas aeruginosa in a
healthcare setting in Alexandria, Egypt. Pol J Microbiol 2017;
66: 297–308.
96 Aboushleib HM, Omar HM, Abozahra R, Elsheredy A, Baraka K.
Correlation of quorum sensing and virulence factors in
Pseudomonas aeruginosa isolates in Egypt. J Infect Dev Ctries 2015;
9: 1091–99.
97 El-Kholy A, Saied T, Gaber M, et al. Device-associated nosocomial
infection rates in intensive care units at Cairo University hospitals:
first step toward initiating surveillance programs in a
resource-limited country. Am J Infect Control 2012; 40: e216–20.
98 Hashem H, Hanora A, Abdalla S, Shawky A, Saad A. Carbapenem
susceptibility and multidrug-resistance in Pseudomonas aeruginosa
isolates in Egypt. Jundishapur J Microbiol 2016; 9: e30257.
99 Mansour SA, Eldaly O, Jiman-Fatani A, Mohamed ML, Ibrahim EM.
Epidemiological characterization of P aeruginosa isolates of
intensive care units in Egypt and Saudi Arabia.
East Mediterr Health J 2013; 19: 71–80.
100 Saied T, Elkholy A, Hafez SF, et al. Antimicrobial resistance in
pathogens causing nosocomial bloodstream infections in university
hospitals in Egypt. Am J Infect Control 2011; 39: e61–65.
101 Zafer MM, Al-Agamy MH, El-Mahallawy HA, Amin MA,
Ashour MS. Antimicrobial resistance pattern and their
beta-lactamase encoding genes among Pseudomonas aeruginosa
strains isolated from cancer patients. Biomed Res Int 2014;
2014: 101635.
102 Franka EA, Shembesh MK, Zaied AA, et al. Multidrug resistant
bacteria in wounds of combatants of the Libyan uprising.
J Infect 2012; 65: 279–81.
103 Mathlouthi N, Areig Z, Al Bayssari C, et al. Emergence of
carbapenem-resistant Pseudomonas aeruginosa and Acinetobacter
baumannii clinical isolates collected from some Libyan hospitals.
Microb Drug Resist 2015; 21: 335–41.
104 Drissi M, Ahmed ZB, Dehecq B, Bakour R, Plesiat P, Hocquet D.
Antibiotic susceptibility and mechanisms of β-lactam resistance
among clinical strains of Pseudomonas aeruginosa: first report in
Algeria. Med Mal Infect 2008; 38: 187–91.
105 Meradji S, Barguigua A, Bentakouk MC, et al. Epidemiology and
virulence of VIM-4 metallo-β-lactamase-producing Pseudomonas
aeruginosa isolated from burn patients in eastern Algeria.
Burns 2016; 42: 906–18.
106 Meradji S, Barguigua A, Zerouali K, et al. Epidemiology of
carbapenem non-susceptible Pseudomonas aeruginosa isolates in
eastern Algeria. Antimicrob Resist Infect Control 2015; 4: 27.
107 Sefraoui I, Berrazeg M, Drissi M, Rolain JM. Molecular
epidemiology of carbapenem-resistant Pseudomonas aeruginosa
clinical strains isolated from western Algeria between 2009 and
2012. Microb Drug Resist 2014; 20: 156–61.
108 Ben Abdallah H, Noomen S, Ben Elhadj Khélifa A, Sahnoun O,
Elargoubi A, Mastouri M. Profil de sensibilité aux antibiotiques des
souches de Pseudomonas aeruginosa isolées dans la région de
Monastir. Med Mal Infect 2008; 38: 554–56.
109 Zoghlami A, Kanzari L, Boukadida J, Messadi AA, Ghanem A.
Epidemiological profile and antibiotic resistance of Pseudomonas
aeruginosa isolates in burn and traumatology center in Tunisia over
a three-year period. Tunis Med 2012; 90: 803–06 (in French).
110 Rahouma A, Klena JD, Krema Z, et al. Enteric pathogens associated
with childhood diarrhea in Tripoli—Libya. Am J Trop Med Hyg 2011;
84: 886–91.
111 Essayagh T, Zohoun A, Essayagh M, et al. Épidémiologie
bactérienne à l’unité des brûlés de l’Hôpital militaire d’instruction
de Rabat. Ann Biol Clin 2011; 69: 71–76.
112 Maroui I, Barguigua A, Aboulkacem A, et al. First report of VIM-2
metallo-β-lactamases producing Pseudomonas aeruginosa isolates in
Morocco. J Infect Chemother 2016; 22: 127–32.
www.thelancet.com/infection Published online October 3, 2018 http://dx.doi.org/10.1016/S1473-3099(18)30414-6 13
Review
113 Shimi A, Touzani S, Elbakouri N, Bechri B, Derkaoui A, Khatouf M.
Les pneumopathies nosocomiales en réanimation de CHU Hassan
II de Fès. Pan Afr Med J 2015; 22: 285.
114 Zohoun A, Moket D, El Hamzaoui S. Prevalence of Acinetobacter
baumannii and Pseudomonas aeruginosa isolates resistant to
imipenem by production of metallo-β-lactamases in Rabat Military
Teaching Hospital Mohammed V. Ann Biol Clin 2013;
71: 27–30 (in French).
115 Hashem H, Hanora A, Abdalla S, Shaeky A, Saad A. Dissemination
of metallo-β-lactamase in Pseudomonas aeruginosa isolates in Egypt:
mutation in blaVIM-4. APMIS 2017; 125: 499–505.
116 Ktari S, Mnif B, Znazen A, et al. Diversity of β-lactamases in
Pseudomonas aeruginosa isolates producing metallo-β-lactamase in
two Tunisian hospitals. Microb Drug Resist 2011; 17: 25–30.
117 Al-Agamy MH, Jeannot K, El-Mahdy TS, et al. Diversity of
molecular mechanisms conferring carbapenem resistance to
Pseudomonas aeruginosa isolates from Saudi Arabia.
Can J Infect Dis Med Microbiol 2016; 2016: 4379686.
118 Zowawi HM, Ibrahim E, Syrmis MW, Wailan AM, AbdulWahab A,
Paterson DL. PME-1-producing Pseudomonas aeruginosa in Qatar.
Antimicrob Agents Chemother 2015; 59: 3692–93.
119 Salma R, Dabboussi F, Kassaa I, Khudary R, Hamze M. gyrA and
parC mutations in quinolone-resistant clinical isolates of
Pseudomonas aeruginosa from Nini Hospital in north Lebanon.
J Infect Chemother 2013; 19: 77–81.
120 Al Bayssari C, Diene SM, Loucif L, et al. Emergence of-2 and
IMP-15 carbapenemases and inactivation of oprD gene in
carbapenem-resistant Pseudomonas aeruginosa clinical isolates from
Lebanon. Antimicrob Agents Chemother 2014; 58: 4966–70.
121 Sefraoui I, Berrazeg M, Drissi M, Rolain JM. Molecular
epidemiology of carbapenem-resistant Pseudomonas aeruginosa
clinical strains isolated from western Algeria between 2009 and
2012. Microb Drug Resist 2014; 20: 156–61.
122 Al-Mousa HH, Omar AA, Rosenthal VD, et al. Device-associated
infection rates, bacterial resistance, length of stay, and mortality in
Kuwait: International Nosocomial Infection Consortium findings.
Am J Infect Control 2016; 44: 444–49.
123 Al-Sweih NA, Al-Hubail MA, Rotimi VO. Emergence of tigecycline
and colistin resistance in Acinetobacter species isolated from
patients in Kuwait hospitals. J Chemother 2011; 23: 13–16.
124 Vali L, Dashti K, Opazo-Capurro AF, Dashti AA, Al Obaid K,
Evans BA. Diversity of multi-drug resistant Acinetobacter baumannii
population in a major hospital in Kuwait. Front Microbiol 2015;
6: 743.
125 Mugnier PD, Bindayna KM, Poirel L, Nordmann P. Diversity of
plasmid-mediated carbapenem-hydrolysing oxacillinases
among carbapenem-resistant Acinetobacter baumannii isolates from
Kingdom of Bahrain. J Antimicrob Chemother 2009; 63: 1071–73.
126 Alsultan AA, Evans BA, Elsayed EA, et al. High frequency of
carbapenem-resistant Acinetobacter baumannii in patients with
diabetes mellitus in Saudi Arabia. J Med Microbiol 2013;
62: 885–88.
127 Somily AM, Absar MM, Arshad MZ, et al. Antimicrobial
susceptibility patterns of multidrug-resistant Pseudomonas
aeruginosa and Acinetobacter baumannii against carbapenems,
colistin, and tigecycline. Saudi Med J 2012; 33: 750–55.
128 Ganjo AR, Maghdid DM, Mansoor IY, et al. OXA-carbapenemases
present in clinical Acinetobacter baumannii-calcoaceticus complex
isolates from patients in Kurdistan region, Iraq.
Microb Drug Resist 2016; 22: 627–37.
129 Al Atrouni A, Hamze M, Jisr T, et al. Wide spread of
OXA-23-producing carbapenem-resistant Acinetobacter baumannii
belonging to clonal complex II in different hospitals in Lebanon.
Int J Infect Dis 2016; 52: 29–36.
130 Ballouz T, Aridi J, Afif C, et al. Risk factors, clinical presentation,
and outcome of Acinetobacter baumannii bacteremia.
Front Cell Infect Microbiol 2017; 7: 156.
131 Hamzeh AR, Al Najjar M, Mahfoud M. Prevalence of antibiotic
resistance among Acinetobacter baumannii isolates from Aleppo,
Syria. Am J Infect Control 2012; 40: 776–77.
132 Obeidat N, Jawdat F, Al-Bakri AG, Shehabi AA. Major biologic
characteristics of Acinetobacter baumannii isolates from hospital
environmental and patients’ respiratory tract sources.
Am J Infect Control 2014; 42: 401–04.
 Review
133 Alkasaby NM, El Sayed Zaki M. Molecular study of
Acinetobacter baumannii isolates for metallo-β-lactamases and
extended-spectrum-β-lactamases genes in intensive care unit,
Mansoura University Hospital, Egypt. Int J Microbiol 2017;
2017: 3925868.
134 Khorsi K, Messai Y, Hamidi M, Ammari H, Bakour R.
High prevalence of multidrug-resistance in Acinetobacter baumannii
and dissemination of carbapenemase-encoding genes
blaOXA-23-like, blaOXA-24-like and blaNDM-1 in Algiers hospitals.
Asian Pac J Trop Med 2015; 8: 438–46.
135 Uwingabiye J, Frikh M, Lemnouer A, et al. Acinetobacter infections
prevalence and frequency of the antibiotics resistance: comparative
study of intensive care units versus other hospital units.
Pan Afr Med J 2016; 23: 191.
136 Thabet L, Turki A, Ben Redjeb S, Messadi A. Bacteriological profile
and antibiotic resistance of bacteria isolates in a burn department.
Tunis Med 2008; 86: 1051–54 (in French).
137 Thabet L, Zoghlami A, Boukadida J, Ghanem A, Messadi AA.
Comparative study of antibiotic resistance in bacteria isolated from
burned patients during two periods (2005–2008, 2008–2011) and in
two hospitals (Hospital Aziza Othmana, Trauma and Burn Center).
Tunis Med 2013; 91: 134–38 (in French).
138 Fekih Hassen M, Ben Haj Khalifa A, Tilouche N, et al.
Severe community-acquired pneumonia admitted at the intensive
care unit: main clinical and bacteriological features and prognostic
factors: a Tunisian experience. Rev Pneumol Clin 2014;
70: 253–59 (in French).
139 Mahfoud M, Al Najjar M, Hamzeh AR. Multidrug resistance in
Pseudomonas aeruginosa isolated from nosocomial respiratory and
urinary infections in Aleppo, Syria. J Infect Dev Ctries 2015;
9: 210–13.
140 Al-Agamy MH, Khalaf NG, Tawfick MM, Shibl AM, El Kholy A.
Molecular characterization of carbapenem-insensitive Acinetobacter
baumannii in Egypt. Int J Infect Dis 2014; 22: 49–54.
141 Kanj SS, Tayyar R, Shehab M, et al. Increase of blaOXA-23-like in
Acinetobacter baumannii at a tertiary care center in Lebanon between
2007 and 2013. J Infect Dev Ctries 2018; 12 (suppl): 4S.
142 Al-Agamy MH, Shibl AM, Ali MS, Khubnani H, Radwan HH,
Livermore DM. Distribution of β-lactamases in
carbapenem-non-susceptible Acinetobacter baumannii in Riyadh,
Saudi Arabia. J Glob Antimicrob Resist 2014; 2: 17–21.
143 Somily AM, Sayyed SB, Habib HA, et al. Salmonella isolates
serotypes and susceptibility to commonly used drugs at a tertiary
care hospital in Riyadh, Saudi Arabia. J Infect Dev Ctries 2012;
6: 478–82.
144 El-Tayeb MA, Ibrahim ASS, Al-Salamah AA, Almaary KS,
Elbadawi YB. Prevalence, serotyping and antimicrobials resistance
mechanism of Salmonella enterica isolated from clinical and
environmental samples in Saudi Arabia. Braz J Microbiol 2017;
48: 499–508.
145 Elhadi N, Aljindan R, Aljeldah M. Prevalence of nontyphoidal
salmonella serogroups and their antimicrobial resistance patterns
in a university teaching hospital in Eastern Province of
Saudi Arabia. Infect Drug Resist 2013; 6: 199–205.
146 Dashti AA, Jadaon MM, Habeeb F, West PW, Panigrahi D,
Amyes SG. Salmonella enterica serotype Typhi in Kuwait and its
reduced susceptibility to ciprofloxacin. J Chemother 2008;
20: 297–302.
147 Khan FY, Elshafie SS, Almaslamani M, et al. Epidemiology of
bacteraemia in Hamad general hospital, Qatar: a one year
hospital-based study. Travel Med Infect Dis 2010; 8: 377–87.
148 Taha RR, Alghalibi SM, Saeedsaleh MG. Salmonella spp. in patients
suffering from enteric fever and food poisoning in Thamar city,
Yemen. East Mediterr Health J 2013; 19: 88–93.
149 Harb A, O’Dea M, Hanan ZK, Abraham S, Habib I. Prevalence, risk
factors and antimicrobial resistance of salmonella diarrhoeal
infection among children in Thi-Qar Governorate, Iraq.
Epidemiol Infect 2017; 145: 3486–96.
150 Abu-Elamreen FH, Abed AA, Sharif FA. Viral, bacterial and
parasitic etiology of pediatric diarrhea in Gaza, Palestine.
Med Princ Pract 2008; 17: 296–301.
151 Al-Dawodi R, Farraj MA, Essawi T. Antimicrobial resistance in
non-typhi Salmonella enterica isolated from humans and poultry in
Palestine. J Infect Dev Ctries 2012; 6: 132–36.
14 www.thelancet.com/infection Published online October 3, 2018 http://dx.doi.org/10.1016/S1473-3099(18)30414-6
152 Fadlallah SM, Shehab M, Cheaito K, et al. Molecular epidemiology and
antimicrobial resistance of Salmonella species from clinical specimens
and food Items in Lebanon. J Infect Dev Ctries 2017; 11: 19–27.
153 Al-Sanouri TM, Paglietti B, Haddadin A, et al. Emergence of
plasmid-mediated multidrug resistance in epidemic and
non-epidemic strains of Salmonella enterica serotype Typhi from
Jordan. J Infect Dev Ctries 2008; 2: 295–301.
154 Ammari S, Laglaoui A, En-nanei L, et al. Characterization of
Salmonella Enteritidis isolated from foods and patients in
northern Morocco. J Infect Dev Ctries 2009; 3: 695–703.
155 Le Hello S, Harrois D, Bouchrif B, et al. Highly drug-resistant
Salmonella enterica serotype Kentucky ST198-X1: a microbiological
study. Lancet Infect Dis 2013; 13: 672–79.
156 Ohmani F, Khedid K, Britel S, et al. Antimicrobial resistance in
Salmonella enterica serovar Enteritidis in Morocco.
J Infect Dev Ctries 2010; 4: 804–09.
157 Osman KM, Hassan WM, Mohamed RA. The consequences of a
sudden demographic change on the seroprevalence pattern,
virulence genes, identification and characterisation of
integron-mediated antibiotic resistance in the Salmonella enterica
isolated from clinically diarrhoeic humans in Egypt.
Eur J Clin Microbiol Infect Dis 2014; 33: 1323–37.
158 Osman KM, Marouf SH, Alatfeehy N. Antimicrobial resistance and
virulence-associated genes of Salmonella enterica subsp enterica
serotypes Muenster, Florian, Omuna, and Noya strains isolated from
clinically diarrheic humans in Egypt. Microb Drug Resist 2013;
19: 370–77.
159 Saleh FO, Ahmed HA, Khairy RM, Abdelwahab SF. Increased
quinolone resistance among typhoid salmonella isolated from
Egyptian patients. J Infect Dev Ctries 2014; 8: 661–65.
160 Abbassi-Ghozzi I, Jaouani A, Aissa RB, Martinez-Urtaza J,
Boudabous A, Gtari M. Antimicrobial resistance and molecular
analysis of non-typhoidal salmonella isolates from human in
Tunisia. Pathol Biol 2011; 59: 207–12.
161 Guedda I, Taminiau B, Ferjani A, Boukadida J, Bertrand S,
Daube G. Antimicrobial and molecular analysis of Salmonella
serovar Livingstone strains isolated from humans in Tunisia and
Belgium. J Infect Dev Ctries 2014; 8: 973–80.
162 Ktari S, Arlet G, Verdet C, et al. Molecular epidemiology and genetic
environment of acquired bla ACC-1 in Salmonella enterica serotype
Livingstone causing a large nosocomial outbreak in Tunisia.
Microb Drug Resist 2009; 15: 279–86.
163 Belkhouja K, Ben Romdhane K, Ghariani A, et al.
Severe pneumococcal community-acquired pneumonia admitted to
medical Tunisian ICU. J Infect Chemother 2012; 18: 324–31.
164 Bouzenoune F, Kellab Debbih K, Boudersa F, Kouhil S, Nezzar N.
Sensibilité aux antibiotiques des Salmonella enterica sérotype Typhi
isolées des hémocultures à l’hôpital d’Ain M’lila (Algérie), entre
2005 et 2008. Med Mal Infect 2011; 41: 181–85.
165 Djeffal S, Bakour S, Mamache B, et al. Prevalence and clonal
relationship of ESBL-producing salmonella strains from humans
and poultry in northeastern Algeria. BMC Vet Res 2017; 13: 132.
166 Daoud Z, Kourani M, Saab R, Nader MA, Hajjar M. Resistance of
Streptococcus pneumoniae isolated from Lebanese patients between
2005 and 2009. Rev Esp Quimioter 2011; 24: 84–90.
167 El Mdaghri N, Jilali N, Belabbes H, Jouhadi Z, Lahssoune M,
Zaid S. Epidemiological profile of invasive bacterial diseases in
children in Casablanca, Morocco: antimicrobial susceptibilities and
serotype distribution. East Mediterr Health J 2012; 18: 1097–101.
168 Rotimi VO, Jamal W, Pal T, Sovenned A, Albert MJ. Emergence of
CTX-M-15 type extended-spectrum β-lactamase-producing
Salmonella spp in Kuwait and the United Arab Emirates.
J Med Microbiol 2008; 57: 881–86.
169 Abou Shady HM, Bakr AEA, Hashad ME, Alzohairy MA.
Staphylococcus aureus nasal carriage among outpatients
attending primary health care centers: a comparative study of
two cities in Saudi Arabia and Egypt. Braz J Infect Dis 2015; 19: 68–76.
170 Eed EM, Ghonaim MM, Hussein YM, Saber TM, Khalifa AS.
Phenotypic and molecular characterization of HA-MRSA in
Taif hospitals, Saudi Arabia. J Infect Dev Ctries 2015; 9: 298–303.
171 Al-Humaidan OS, El-Kersh TA, Al-Akeel RA. Risk factors of nasal
carriage of Staphylococcus aureus and methicillin-resistant
Staphylococcus aureus among health care staff in a teaching hospital
in central Saudi Arabia. Saudi Med J 2015; 36: 1084–90.

172 Sonnevend Á, Blair I, Alkaabi M, et al. Change in
meticillin-resistant Staphylococcus aureus clones at a tertiary care
hospital in the United Arab Emirates over a 5-year period.
J Clin Pathol 2012; 65: 178–82.
173 Sfeir M, Obeid Y, Eid C, et al. Prevalence of Staphylococcus aureus
methicillin-sensitive and methicillin-resistant nasal and pharyngeal
colonization in outpatients in Lebanon. Am J Infect Control 2014;
42: 160–63.
174 Al Laham N, Mediavilla JR, Chen L, et al. MRSA clonal complex
22 strains harboring toxic shock syndrome toxin (TSST-1) are
endemic in the primary hospital in Gaza, Palestine. PLoS One 2015;
10: e0120008.
175 Biber A, Abuelaish I, Rahav G, et al. A typical hospital-acquired
methicillin-resistant Staphylococcus aureus clone is widespread in
the community in the Gaza strip. PLoS One 2012; 7: e42864.
176 El Aila NA, Al Laham NA, Ayesh BM. Nasal carriage of
methicillin resistant Staphylococcus aureus among health care
workers at Al Shifa hospital in Gaza Strip. BMC Infect Dis 2017;
17: 28.
177 Kaibni MH, Farraj MA, Adwan K, Essawi TA.
Community-acquired meticillin-resistant Staphylococcus aureus in
Palestine. J Med Microbiol 2009; 58: 644–47.
178 Al-Zoubi MS, Al-Tayyar IA, Hussein E, Jabali AA, Khudairat S.
Antimicrobial susceptibility pattern of Staphylococcus aureus
isolated from clinical specimens in Northern area of Jordan.
Iran J Microbiol 2015; 7: 265–72.
179 Bazzoun DA, Harastani HH, Shehabi AA, Tokajian ST.
Molecular typing of Staphylococcus aureus collected from a major
hospital in Amman, Jordan. J Infect Dev Ctries 2014; 8: 441–47.
180 Co EM, Keen EF 3rd, Aldous WK. Prevalence of methicillin-
resistant Staphylococcus aureus in a combat support hospital in
Iraq. Mil Med 2011; 176: 89–93.
181 Hussein NR, Assafi MS, Ijaz T. Methicillin-resistant
Staphylococcus aureus nasal colonisation amongst healthcare
workers in Kurdistan Region, Iraq. J Glob Antimicrob Resist 2017;
9: 78–81.
182 Qader AR, Muhamad JA. Nosocomial infection in Sulaimani Burn
Hospital, Iraq. Ann Burns Fire Disasters 2010; 23: 177–81.
183 Alioua MA, Labid A, Amoura K, Bertine M, Gacemi-Kirane D,
Dekhil M. Emergence of the European ST80 clone of
community-associated methicillin-resistant Staphylococcus aureus
as a cause of healthcare-associated infections in Eastern Algeria.
Med Mal Infect 2014; 44: 180–83.
184 Djoudi F, Benallaoua S, Aleo A, et al. Descriptive epidemiology of
nasal carriage of Staphylococcus aureus and methicillin-resistant
Staphylococcus aureus among patients admitted to two healthcare
facilities in Algeria. Microb Drug Resist 2015; 21: 218–23.
185 Al-haddad OH, Zorgani A, Ghenghesh KS. Nasal carriage of
multi-drug resistant Panton-Valentine leucocidin-positive
methicillin-resistant Staphylococcus aureus in children in
Tripoli-Libya. Am J Trop Med Hyg 2014; 90: 724–27.
186 Buzaid N, Elzouki AN, Taher I, Ghenghesh KS.
Methicillin-resistant Staphylococcus aureus (MRSA) in a tertiary
surgical and trauma hospital in Benghazi, Libya.
J Infect Dev Ctries 2011; 5: 723–26.
187 El Shallaly GH, Hassan AN, Siddig NO, Mohammed RA,
Osman EA, Ibrahim MA. Study of patients with
community-acquired abscesses. Surg Infect 2012; 13: 250–56.
188 Elhassan MM, Ozbak HA, Hemeg HA, Elmekki MA, Ahmed LM.
Absence of the mecA gene in methicillin resistant Staphylococcus
aureus isolated from different clinical specimens in Shendi City,
Sudan. Biomed Res Int 2015; 2015: 895860.
189 Mahmoud AM, Albadawy HS, Bolis SM, Bilal NE, Ahmed AO,
Ibrahim ME. Inducible clindamycin resistance and nasal carriage
rates of Staphylococcus aureus among healthcare workers and
community members. Afr Health Sci 2015; 15: 861–67.
190 Salem ML, Ghaber SM, Baba SE, Maouloud MM.
Antibiotic susceptibility of community-acquired strains of
Staphylococcus aureus in Nouakchott Region (Mauritania).
Pan Afr Med J 2016; 24: 276 (in French).
191 Elhamzaoui S, Benouda A, Allali F, Abouqual R, Elouennass M.
Antibiotic susceptibility of Staphylococcus aureus strains isolated in
two university hospitals in Rabat, Morocco. Med Mal Infect 2009;
39: 891–95 (in French).
www.thelancet.com/infection Published online October 3, 2018 http://dx.doi.org/10.1016/S1473-3099(18)30414-6 15
Review
192 Souly K, Ait el kadi M, Lahmadi K, et al. Epidemiology and prevention
of Staphylococcus aureus nasal carriage in hemodialyzed patients.
Med Mal Infect 2011; 41: 469–74.
193 Zriouil SB, Bekkali M, Zerouali K. Epidemiology of Staphylococcus
aureus infections and nasal carriage at the Ibn Rochd University
Hospital Center, Casablanca, Morocco. Braz J Infect Dis 2012;
16: 279–83.
194 Abdel-Maksoud M, El-Shokry M, Ismail G, et al. Methicillin-resistant
Staphylococcus aureus recovered from healthcare- and
community-associated infections in Egypt. Int J Bacteriol 2016;
2016: 5751785.
195 Kechrid A, Perez-Vazquez M, Smaoui H, et al. Molecular analysis of
community-acquired methicillin-susceptible and resistant
Staphylococcus aureus isolates recovered from bacteraemic and
osteomyelitis infections in children from Tunisia.
Clin Microbiol Infect 2011; 17: 1020–26.
196 Senok A, Ehricht R, Monecke S, Al-Saedan R, Somily A.
Molecular characterization of methicillin-resistant Staphylococcus
aureus in nosocomial infections in a tertiary-care facility:
emergence of new clonal complexes in Saudi Arabia.
New Microbes New Infect 2016; 14: 13–18.
197 Aqel AA, Alzoubi HM, Vickers A, Pichon B, Kearns AM.
Molecular epidemiology of nasal isolates of methicillin-resistant
Staphylococcus aureus from Jordan. J Infect Public Health 2015;
8: 90–97.
198 Tokajian ST, Khalil PA, Jabbour D, et al. Molecular characterization of
Staphylococcus aureus in Lebanon. Epidemiol Infect 2010; 138: 707–12.
199 Monecke S, Skakni L, Hasan R, et al. Characterisation of MRSA
strains isolated from patients in a hospital in Riyadh, Kingdom of
Saudi Arabia. BMC Microbiol 2012; 12: 146.
200 Udo EE, Boswihi SS, Al-Sweih N. High prevalence of toxic shock
syndrome toxin-producing epidemic methicillin-resistant
Staphylococcus aureus 15 (EMRSA-15) strains in Kuwait hospitals.
New Microbes New Infect 2016; 12: 24–30.
201 Clinical and Laboratory Standards Institute. Performance standards
for antimicrobial susceptibility testing, 27th edn. Wayne, PA: Clinical
and Laboratory Standards Institute, 2017.
202 Al Ayed MS, Hawan AA. Retrospective review of invasive pediatric
pneumococcal diseases in a military hospital in the southern region
of Saudi Arabia. Ann Saudi Med 2011; 31: 469–72.
203 Al-Sheikh YA, K Gowda L, Mohammed Ali MM, John J,
Khaled Homoud Mohammed D, Chikkabidare Shashidhar P.
Distribution of serotypes and antibiotic susceptibility patterns among
invasive pneumococcal diseases in Saudi Arabia. Ann Lab Med 2014;
34: 210–15.
204 Almazrou Y, Shibl AM, Alkhlaif R, et al. Epidemiology of invasive
pneumococcal disease in Saudi Arabian children younger than
5 years of age. J Epidemiol Glob Health 2016; 6: 95–104.
205 Jamsheer A, Rafay AM, Daoud Z, Morrissey I, Torumkuney D.
Results from the Survey of Antibiotic Resistance (SOAR) 2011–13 in
the Gulf States. J Antimicrob Chemother 2016; 71: 45–61.
206 Al-Yaqoubi MM, Elhag KM. Serotype prevalence and
penicillin-susceptibility of Streptococcus pneumoniae in Oman.
Oman Med J 2011; 26: 43–47.
207 Elshafie S, Taj-Aldeen SJ. Emerging resistant serotypes of invasive
Streptococcus pneumoniae. Infect Drug Resist 2016; 9: 153–60.
208 Johny M, Babelly M, Al-Obaid I, Al-Benwan K, Udo EE. Antimicrobial
resistance in clinical isolates of Streptococcus pneumoniae in a tertiary
hospital in Kuwait, 1997–2007: implications for empiric therapy.
J Infect Public Health 2010; 3: 60–66.
209 Mokaddas E, Albert MJ. Impact of pneumococcal conjugate vaccines
on burden of invasive pneumococcal disease and serotype
distribution of Streptococcus pneumoniae isolates: an overview from
Kuwait. Vaccine 2012; 30: 37–40.
210 Araj GF, Avedissian AZ, Ayyash NS, et al. A reflection on bacterial
resistance to antimicrobial agents at a major tertiary care center in
Lebanon over a decade. J Med Liban 2012; 60: 125–35.
211 Nasereddin A, Shtayeh I, Ramlawi A, Salman N, Salem I, Abdeen Z.
Streptococcus pneumoniae from Palestinian nasopharyngeal carriers:
serotype distribution and antimicrobial resistance. PLoS One 2013;
8: e82047.
212 Swedan SF, Hayajneh WA, Bshara GN. Genotyping and serotyping of
macrolide and multidrug resistant Streptococcus pneumoniae isolated
from carrier children. Indian J Med Microbiol 2016; 34: 159–65.
 Review
213 Charfi F, Smaoui H, Kechrid A. Non-susceptibility trends and
serotype coverage by conjugate pneumococcal vaccines in a Tunisian
paediatric population: a 10-year study. Vaccine 2012; 30: 18–24.
214 Ktari S, Jmal I, Mroua M, et al. Serotype distribution and antibiotic
susceptibility of Streptococcus pneumoniae strains in the south of
Tunisia: a five-year study (2012–2016) of pediatric and adult
populations. Int J Infect Dis 2017; 65: 110–15.
215 Marzouk M, Ferjani A, Bouafia N, Harb H, Ben Salem Y, Boukadida J.
Serotype distribution and antimicrobial resistance of invasive and
noninvasive pneumococcal isolates in Tunisia.
Microb Drug Resist 2015; 21: 85–89.
216 Raddaoui A, Simoes AS, Baaboura R, et al. Serotype distribution,
antibiotic resistance and clonality of Streptococcus pneumoniae isolated
from immunocompromised patients in Tunisia. PLoS One 2015;
10: e0140390.
217 Smaoui H, Amri J, Hajji N, Kechrid A. Antimicrobial susceptibility
and serotype distribution of Streptococcus pneumoniae isolates in
children in Tunis. Arch Pediatr 2009; 16: 220–26 (in French).
218 Ramdani-Bouguessa N, Ziane H, Bekhoucha S, et al. Evolution of
antimicrobial resistance and serotype distribution of Streptococcus
pneumoniae isolated from children with invasive and noninvasive
pneumococcal diseases in Algeria from 2005 to 2012.
New Microbes New Infect 2015; 6: 42–48.
219 Tali-Maamar H, Laliam R, Bentchouala C, et al. Serotyping and
antibiotic susceptibility of Streptococcus pneumoniae strains isolated in
Algeria from 2001 to 2010. Med Mal Infect 2012; 42: 59–65.
220 Ziane H, Manageiro V, Ferreira E, et al. Serotypes and antibiotic
susceptibility of Streptococcus pneumoniae isolates from invasive
pneumococcal disease and asymptomatic carriage in a pre-vaccination
period, in Algeria. Front Microbiol 2016; 7: 803.
221 Elmdaghri N, Benbachir M, Belabbes H, Zaki B, Benzaid H.
Changing epidemiology of pediatric Streptococcus pneumoniae isolates
before vaccine introduction in Casablanca (Morocco). Vaccine 2012;
30: 46–50.
222 Warda K, Oufdou K, Zahlane K, Bouskraoui M. Antibiotic resistance
and serotype distribution of nasopharyngeal isolates of Streptococcus
pneumoniae from children in Marrakech region (Morocco).
J Infect Public Health 2013; 6: 473–81.
223 Abdelkader MM, Aboshanab KM, El-Ashry MA, Aboulwafa MM.
Prevalence of MDR pathogens of bacterial meningitis in Egypt and
new synergistic antibiotic combinations. PLoS One 2017; 12: e0171349.
224 Afifi S, Karsany MS, Wasfy M, Pimentel G, Marfin A, Hajjeh R.
Laboratory-based surveillance for patients with acute meningitis in
Sudan, 2004–2005. Eur J Clin Microbiol Infect Dis 2009; 28: 429–35.
225 Memish ZA, Al-Tawfiq JA, Almasri M, et al. A cohort study of the
impact and acquisition of naspharyngeal carriage of Streptococcus
pneumoniae during the Hajj. Travel Med Infect Dis 2016; 14: 242–47.
226 Bouskraoui M, Soraa N, Zahlane K, et al. Study of nasopharyngeal
colonization by Streptococcus pneumoniae and its antibiotics resistance
in healthy children less than 2 years of age in the Marrakech region
(Morocco). Arch Pediatr 2011; 18: 1265–70 (in French).
227 Hammer GP, du Prel JB, Blettner M. Avoiding bias in observational
studies: part 8 in a series of articles on evaluation of scientific
publications. Dtsch Arztebl Int 2009; 106: 664–68.
228 WHO. Global antimicrobial resistance surveillance system (GLASS)
report: early implementation 2016–2017. Geneva: World Health
Organization, 2017.
229 Tadesse BT, Ashley EA, Ongarello S, et al. Antimicrobial resistance in
Africa: a systematic review. BMC Infect Dis 2017; 17: 616.
230 Tacconelli E, Carrara E, Savoldi A, et al. Discovery, research, and
development of new antibiotics: the WHO priority list of
antibiotic-resistant bacteria and tuberculosis. Lancet Infect Dis 2018;
18: 318–27.
231 WHO. Antimicrobial resistance: global report on surveillance 2014.
http://www.who.int/drugresistance/documents/surveillancereport/
en/ (accessed May 29, 2018).
232 Barlam TF, Cosgrove SE, Abbo LM, et al. Implementing an antibiotic
stewardship program: guidelines by the infectious Diseases Society of
America and the Society for Healthcare Epidemiology of America.
Clin Infect Dis 2016; 62: e51–77.
233 Memish ZA, Arabi YM, Ahmed QA, Shibl AM, Niederman MS,
Group GCW. Executive summary of the Gulf Cooperation Council
practice guidelines for the management of community-acquired
pneumonia. J Chemother 2007; 19 (suppl 1): 7–11.
16 www.thelancet.com/infection Published online October 3, 2018 http://dx.doi.org/10.1016/S1473-3099(18)30414-6
234 Husni R, Atoui R, Choucair J. The Lebanese Society of Infectious
Diseases and Clinical Microbiology guidelines for the treatment of
urinary tract infections. Lebanese Med J 2017; 65: 208–19.
235 Moghnieg R, Kanafani Z, Abi Hanna P. 2016 Lebanese Society of
Infectious Diseases and Clinical Microbiology guidelines on the
management of febrile neutropenia in adult cancer patients in the era
of growing antimicrobial resistance. Lebanese Med J 2017; 65: 63–82.
236 Moghnieh R, Yared Sakr N, Kanj SS, et al. The Lebanese Society for
Infectious Diseases and Clinical Microbiology (LSIDCM) guidelines
for adult community-acquired pneumonia (Cap) in Lebanon.
J Med Liban 2014; 62: 40–47.
237 Alawi MM, Darwesh BM. A stepwise introduction of a successful
antimicrobial stewardship program. Experience from a tertiary care
university hospital in western, Saudi Arabia. Saudi Med J 2016;
37: 1350–58.
238 Infectious Diseases Society of America. Combating antimicrobial
resistance: policy recommendations to save lives. Clin Infect Dis 2011;
52 (suppl 5): S397–428.
239 Kingdom of Saudi Arabia Ministry of National Guard Health
Affairs—Infection Prevention and Control Department. The GCC
Infection Prevention and Control Manual, 3rd edn. 2018 ngha.med.
sa/English/MedicalCities/AlRiyadh/MedicalServices/Lab/
Documents/InfectionControlManual.pdf (accessed May 23, 2018).
240 Ammar W, Wakim R, Hajj I. Accreditation of hospitals in Lebanon: a
challenging experience. 2007. http://apps.who.int/iris/
handle/10665/117235?locale=zh (accessed May 29, 2018).
241 Balkhy HH, Assiri AM, Al Mousa H, et al. The strategic plan for
combating antimicrobial resistance in Gulf Cooperation Council
States. J Infect Public Health 2016; 9: 375–85.
242 Kanafani ZA, Zahreddine N, Tayyar R, et al. Multi-drug resistant
Acinetobacter species: a seven-year experience from a tertiary care
center in Lebanon. Antimicrob Resist Infect Control 2018; 7: 9.
243 Egyptian Ministry of Health and Population (ICP Egypt). The National
Infection Control Guidelines (Parts 1 and 2), 3rd edn. 2016.
http://www.mohp.gov.eg/Publications.aspx?cat_id=1020 (accessed
May 27, 2018).
244 Liu L, Liu B, Li Y, Zhang W. Successful control of resistance in
Pseudomonas aeruginosa using antibiotic stewardship and infection
control programs at a Chinese university hospital: a 6-year prospective
study. Infect Drug Resist 2018; 11: 637–46.
245 Viale P, Tumietto F, Giannella M, et al. Impact of a hospital-wide
multifaceted programme for reducing carbapenem-resistant
Enterobacteriaceae infections in a large teaching hospital in northern
Italy. Clin Microbiol Infect 2015; 21: 242–47.
246 Viale P, Giannella M, Bartoletti M, Tedeschi S, Lewis R.
Considerations about antimicrobial stewardship in settings with
epidemic extended-spectrum β-lactamase-producing or
carbapenem-resistant Enterobacteriaceae. Infect Dis Ther 2015;
4 (suppl 1): 65–83.
247 Khalifeh MM, Moore ND, Salameh PR. Self-medication misuse in
the Middle East: a systematic literature review.
Pharmacol Res Perspect 2017; 5: e00323.w
248 Dandachi I, Sokhn ES, Dahdouh EA, et al. Prevalence and
characterization of multi-drug-resistant Gram-negative Bacilli isolated
from Lebanese poultry: a nationwide study. Front Microbiol 2018;
9: 550.
249 Al Bayssari C, Dabboussi F, Hamze M, Rolain JM. Emergence of
carbapenemase-producing Pseudomonas aeruginosa and Acinetobacter
baumannii in livestock animals in Lebanon. J Antimicrob Chemother
2014; 70: 950–51.
250 Daoud Z, Farah J, Sokhn ES, et al. Multidrug-resistant
Enterobacteriaceae in Lebanese hospital wastewater: implication in
the one health concept. Microb Drug Resist 2018; 24: 166–74.
251 Assiri AM, Banjar WM. The strategic plan for combating
antimicrobial resistance in Gulf Cooperation Council States,
KSA perspective. J Infect Public Health 2017; 10: 485–86.
252 WHO. WHO Global action plan for antimicrobial resistance based on
the One Health Approach. 2015. http://www.wpro.who.int/entity/
drug_resistance/resources/global_action_plan_eng.pdf (accessed
Feb 8, 2018).
© 2018 Elsevier Ltd. All rights reserved.