ARTICLE ORIGINAL / ORIGINAL ARTICLE

IN VITRO ACTIVITY OF FOSFOMYCIN AND OTHER ANTIMICROBIALS AGAINST

UROPATHOGENIC ESCHERICHIA COLI AND KLEBSIELLA PNEUMONIAE
AT A TERTIARY CARE CENTER IN LEBANON
http://www.lebanesemedicaljournal.org/articles/60-3/original3.pdf

George F. ARAJ, Fadel A. JABER*

Araj GF, Jaber FA. In vitro activity of fosfomycin and other

antimicrobials against uropathogenic Escherichia coli and
Klebsiella pneumoniae at a tertiary care center in Lebanon.
J Med Liban 2012 ; 60 (3) : 142-147.

ABSTRACT BACKGROUND : The incidence of urinary

tract infections (UTIs) caused by extended-spectrum-lactamase (ESBL) producing Escherichia coli (ESBLEC) and Klebsiella pneumoniae (ESBL-KP) has been
on the rise limiting oral treatment options. Fosfomycin
was reported to be highly efficacious against these
organisms, however, data is lacking in Lebanon and the
Middle East.
OBJECTIVE : To determine the in vitro activity of
fosfomycin against ESBL and non-ESBL-producing
E. coli and K. pneumoniae uropathogens in Lebanon.
METHODS : A total of 542 consecutive non-duplicate
isolates of ESBL-producing E. coli (n = 374) and
K. pneumoniae (n = 168), and 291 isolates of non-ESBLproducing E. coli (n = 236) and K. pneumoniae (n = 55)
were recovered from urine specimens of patients tested
at the American University of Beirut Medical Center
(AUBMC) during 2010. Each isolate was tested against
a battery of 13 antimicrobials by disk diffusion according to the guidelines of CLSI testing and result interpretation criteria.
RESULTS : The fosfomycin susceptibility for ESBLproducing vs. non-ESBL-producing isolates was 86%
vs. 97% for E. coli and 62% vs. 78% for K. pneumoniae. This activity of fosfomycin among ESBL-EC and
ESBL-KP was generally higher than cefepime (26% &
30%), ciprofloxacin (24% & 41%), Trimeth/sulfa (26%
& 19%), Pip/taz (75% and 45%), gentamicin (45% &
42%), and tobramycin (32% & 26%). On the other
hand, higher activity against both species of ESBLproducing bacteria was shown by amikacin (96% &
79%) and imipenem (99.7% & 98.8%). Nitroflurantoin
was highly active against ESBL-EC (95%) but not
against ESBL-KP (29%).
CONCLUSION : Fosfomycin shows good activity, being
higher against ESBL-producing E. coli than K. pneumoniae uropathogens in Lebanon.
* From Department of Pathology and Laboratory Medicine,
American University of Beirut Medical Center, Beirut, Lebanon.
Correspondence: George F. Araj, PhD. Dept Pathology &
Laboratory Medicine. American University of Beirut Medical
Center. P.O. Box: 11-0236. Beirut. Lebanon 1107-2020.
e-mail: garaj@aub.edu.lb
Tel.: +961 1 350 000 ext 5215/8989
Fax: +961 1 370 845
142 Lebanese Medical Journal 2012 Volume 60 (3)

Araj GF, Jaber FA. Activit in vitro de la fosfomycine et

dautres antibiotiques contre les uropathognes Escherichia
coli et Klebsiella pneumoniae dans un centre tertiaire au Liban.
J Med Liban 2012 ; 60 (3) : 142-147.

RSUM CONTEXTE : Lincidence accrue des infections urinaires causes par Escherichia coli et Klebsiella
pneumoniae produisant des -lactamases spectre tendu (BLSE) a limit les options thrapeutiques par voie
orale. La fosfomycine sest avre trs efficace contre
ces organismes, mais les donnes manquent concernant
son utilisation au Liban et au Moyen-Orient.
OBJECTIF : Dterminer lactivit in vitro de la fosfomycine contre les uropathognes E. coli et K. pneumoniae BLSE et non BLSE au Liban.
MTHODES : Un total de 542 colonies non dupliques
de E. coli (n = 374) et K. Pneumoniae BLSE (n = 236),
ainsi que 291 colonies E. coli (n = 236) et K. pneumoniae non BLSE (n = 55) ont t isoles partir dchantillons durine des patients tests lAUBMC durant
lanne 2010. Chaque colonie a t teste contre une
batterie de 13 antibiotiques par la mthode de diffusion
sur disque selon les critres dexamens et dinterprtation des rsultats du CLSI.
RSULTATS : La sensibilit la fosfomycine des colonies produisant BLSE contre celles nen produisant pas
est de 86% contre 97% pour E. coli, et 62% contre 78%
pour K. pneumoniae. Lactivit de la fosfomycine contre
les germes E. coli et K. pneumoniae produisant BLSE est
plus leve que celle de : cfpime (26% contre 30%),
ciprofloxacine (24% contre 41%), Trimeth/sulfa (26%
contre 19%), Pip/taz (75% contre 45%), gentamicine
(45% contre 42%) et tobramycine (32% contre 26%).
Dautre part, lamikacine a dmontr une activit plus
leve contre E. coli et K. pneumoniae produisant BLSE
(96% et 79% respectivement), ainsi que limipenem
(99,7% et 98,8% respectivement). La nitrofurantone
sest avre trs efficace contre E. coli BLSE (95%) mais
non pas contre K. pneumoniae BLSE (29%).
CONCLUSION : La fosfomycine montre une bonne
activit sur les uropathognes au Liban, bien plus prononce sur E. coli BLSE que sur K. pneumoniae BLSE.
INTRODUCTION

Acute uncomplicated cystitis (AUC) and other urinary

tract infections (UTIs) are among the most prevalent bacterial infections seen in general practice, in both nosocomial and outpatient settings. According to the American

College of Obstetricians and Gynecologists (ACOG), an

estimated 11% of women in the U.S. are diagnosed with a
UTI annually, and the lifetime probability for a woman to
develop a UTI is around 60% [1].
Escherichia coli and Klebsiella pneumoniae are major
causative agents of UTIs estimated to be identified in 8085% and 5% of the cases, respectively [2-4]. In Lebanon,
E. coli and K. pneumoniae had an incidence of 72% and
4%, respectively [5].
The increasing prevalence of antimicrobial resistance
especially in those isolates with extended-spectrum-lactamase (ESBL) producing E. coli (ESBL-EC) and K.
pneumoniae (ESBL-KP) is an ever rising challenge for
the eradication of these uropathogens [6]. These ESBL
producing enterobacteriaceae incur resistance to a wide
range of antimicrobial agents including cephalosporins
and penicillins, and even trimethoprim-sulfamethoxazole,
fluoroquinolones and aminoglycosides [7-11]. In Lebanon, an ever increasing prevalence of such multi-drug
resistance (MDR) isolates has been reported [12-17], thus,
warranting the search for alternative and more potent antimicrobials such as fosfomycin. The latter is a phosphonic
acid derivative antimicrobial agent entailing a broad-spectrum activity that has been approved as an efficacious single-dose treatment for uncomplicated UTIs [18]. Recent
studies revealed good activity of fosfomycin against nonESBL as well as ESBL in both outpatient and nosocomial
settings [18-21]. Such data are lacking in Lebanon and the
Middle East, thus, prompting the rationale of this study.
The aim of this study is to determine the in vitro activity of fosfomycin against ESBL versus non-ESBLproducing E. coli and K. pneumoniae uropathogens, as
compared to other commonly used antimicrobials.

submitted for testing at the American University of Beirut

Medical Center (AUBMC) during 2010. The isolates
were identified based on standard biochemical methods.

Antimicrobial susceptibility testing

Antimicrobial susceptibility testing was performed and
interpreted using the disk-diffusion method according to
CLSI 2010 guidelines [22]. Each isolate was tested
against disks of 12 antimicrobials (BD-BBL Sensi-disc,
Becton, Dickinson and Company, Sparks, MD, USA) including amikacin (30 g), aztreonam (30 g), cefepime
(30 g), cefotaxime (30 g), ceftazidime (30 g), ciprofloxacin (10 g), gentamicin (10 g), imipenem (10 g),
nitroflurantoin (300 g), piperacillin-tazobactam ([Pip/
taz] 100/10 g), tobramycin (10 g), trimethoprim-sulfamethoxazole ([Trimeth/sulfa] 1.25/23.75 g), and fosfomycin trometamal (200 g). ESBL production was suspected based on susceptibility to cefoxitin and imipenem
and intermediate susceptibility or resistance to aztreonam, cefotaxime, and/or ceftazidime. The confirmation of
ESBL presence was conducted by testing the following
antibiotic disks (BD-BBL): cefotaxime (30 g), cefotaxime/clavulanate (30/10 g), ceftazidime (30 g), and
ceftazidime/clavulanate (30/10 g) on Mueller-Hinton
agar (BD-BBL) according to the CLSI [22]. An organism
was interpreted as containing an ESBL if there was an
increase of 5 mm in the inhibition zone of the combination disk when compared with that of the cephalosporin
alone.
Quality control
The American type culture collection (ATCC) quality
control strain E. coli (ATCC 25922) was used to ensure
proper performance of the disk diffusion test.

METHODS

Statistical analysis
The differences in susceptibility or resistance between the
groups were compared with 2 test. A p-value < 0.05 was
considered statistically significant. Our data was analyzed
with Statistical Package for the Social Sciences software
for Windows Version 17.0 (SPSS, Inc., Chicago, IL, USA).

Bacterial isolates
A total of 542 non-duplicate consecutive isolates of
ESBL-EC (n = 374) and ESBL-KP (n = 168), and 291 isolates of non-ESBL-EC (n = 236) and non-ESBL-KP
(n = 55) were recovered from urine specimens of patients
TABLE I

Number of isolates
Gender [% female]
Mean age [years (SD)]
Age groups [%]
15
16-60
> 60
Service [%]
Inpatient
Outpatient

PATIENTS DEMOGRAPHICS *

ESBL

ESCHERICHIA COLI
Non-ESBL
236
81
55 ( 24)

17
29
54
42
58

374
75
54 ( 27)

610
78
54 ( 26)

ESBL

168
58
52 (29)

KLEBSIELLA PNEUMONIAE
Non-ESBL
55
86
47 ( 24)

223
67
50 ( 28)

833
74
54 ( 27)

8
41
52

13
34
53

22
24
54

13
52
35

19
33
48

14
34
52

22
88

34
66

52
48

20
80

45
55

37
63

Total

* Decimals were rounded to the nearest figure.

G.F. ARAJ, F.A. JABER Fosfomycin in vitro activity

Total

TOTAL

Lebanese Medical Journal 2012 Volume 60 (3) 143

RESULTS

Patients demographics
The patients demographic characteristics are summarized
in Table I. A total of 833 isolates of uropathogenic E. coli
(n = 610) and K. pneumoniae (n = 223) were collected, of
which, 374 isolates of ESBL-EC and 168 isolates of
ESBL-KP. Overall, 74% of the isolates were from female
patients (75% of ESBL-EC isolates, 58% of the ESBLKP isolates). The overall mean patient age was 54 ( 27)
years; and respectively 54 ( 27) and 52 ( 29) years for
patients with ESBL-EC and ESBL-KP. More than half
of the isolates in both ESBL groups came from patients
> 60 years of age (54% for both ESBL-EC and ESBLKP). The inpatient recovery rates of ESBL-EC and ESBLKP isolates were 42% and 52%, respectively.
Antimicrobial susceptibility
Table II shows the susceptibility rates of ESBL-EC
and ESBL-KP isolates vs. non-ESBL isolates. Imipenem
showed the best activity against ESBL and non-ESBL isolates, 99.7% vs. 100% for E. coli, and 98.8% vs. 100% for
K. pneumoniae. Amikacin showed comparable susceptibility rates to imipenem for E. coli (96% for ESBL-EC
and 100% for non-ESBL-EC) and non-ESBL-KP (100%)
but not in ESBL-KP (79%). Nitroflurantoin was highly
effective against ESBL-EC and non-ESBL-EC (95% and
97%), but it was not as effective against ESBL-KP and
non-ESBL-KP isolates (29% and 44%). Susceptibility
rates to all other antimicrobials simultaneously tested,
including fosfomycin, were significantly higher for nonESBL-producing isolates. Susceptibility to fosfomycin
was 86% vs. 97% for ESBL-EC and non-ESBL-EC isolates, and 62% vs. 78% for ESBL-KP and non-ESBL-KP
isolates. Fosfomycin and nitroflurantoin were significantly
more effective against ESBL-EC than ESBL-KP. CiproTABLE II

floxacin was significantly more effective against ESBLKP than ESBL-EC, whereas tazocin and Trimeth/sulfa
were more effective against ESBL-EC.
Table III compares the susceptibility rates of ESBL-producing isolates to different antimicrobials for inpatients
versus outpatients. Susceptibility rates for fosfomycin and
other antibiotics were not significantly different between
inpatients and outpatients for the ESBL-EC group. Among
the ESBL-KP group, only isolates from outpatients were
significantly more susceptible to gentamicin and tobramycin than isolates from inpatients. For both inpatient-ESBLEC and ESBL-KP isolates, the most effective agents were
imipenem (99.4% and 97.7%, respectively) followed by
amikacin (95% and 72%, respectively). For other antimicrobials, different inpatient susceptibilities were observed
between ESBL-EC and ESBL-KP being higher for the former against nitroflurantoin (93% and 35%), fosfomycin
(87% and 58%) and tazocin (72% and 41%).
Table IV shows the distribution of fosfomycin-resistant
ESBL isolates among different age groups. For ESBL-EC,
resistance was spread with close incidence almost along
all age brackets. For ESBL-KP, the prevalence of resistance was relatively high among all age groups except for
the age group 6-35 years where the number of cases was
too small to evaluate.
DISCUSSION

Fosfomycin is a naturally occurring antibiotic that was

isolated in 1969 from cultures of Streptomyces species. It
is a phosphonic acid derivative that is currently available
in two formulations: fosfomycin tromethamine for oral
use, and fosfomycin disodium for intravenous use. Furthermore, fosfomycin is well tolerated and cause minimal
nephrotoxicity [23]. In March 2011, the IDSA and the
European Society of Clinical Microbiology and Infectious

SUSCEPTIBILITY RATES OF ESBL ESCHERICHIA COLI & KLEBSIELLA PNEUMONIAE ISOLATES

TO FOSFOMYCIN & OTHER ANTIMICROBIALS AS COMPARED TO NON-ESBL ISOLATES
ANTIMICROBIAL SUSCEPTIBILITY

ANTIMICROBIAL AGENTS*
Amikacin
Aztreonam
Cefepime
Cefotaxime
Ceftazidime
Ciprofloxacin
Gentamicin
Imipenem
Nitroflurantoin
Piperacillin-tazobactam (Pip/taz)t
Tobramycin
Trimethoprim-sulfamethoxazole
Fosfomycin

Escherichia coli
ESBL
Non-ESBL
(n = 374)
(n = 236)
360
10
97
7
60
91
168
373
354
281
118
98
321

(96)
(3)
(26)
(2)
(16)
(24)
(45)
(99.7)
(95)
(75)
(32)
(26)
(86)

236
236
236
232
236
166
210
236
229
227
203
134
229

* Decimals were rounded to the nearest figure except for imipenem.

s

(100)
(100)
(100)
(98)
(100)
(70)
(89)
(100)
(97)
(96)
(86)
(59)
(97)

p**

0.003
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
0.427
0.163
< 0.001
< 0.001
< 0.001
< 0.001

[n (%)] AMONG ISOLATES

Klebsiella pneumoniae
ESBL
Non-ESBL
(n = 168)
(n = 55)
133
4
51
7
31
69
71
166
49
75
44
31
104

(79)s
(2)
(30)
(4)
(19)
(41)s
(42)
(98.8)
(29)s
(45)s
(26)
(19)s
(62)s

** p < 0.05 implies a significant difference.

Indicates significant difference for the specified antimicrobial between corresponding K. pneumoniae and E. coli findings.

55
53
56
52
54
39
50
56
24
52
50
40
43

(100)
(96)s
(100)
(95)
(98)s
(71)
(91)
(100)
(44)s
(95)
(91)
(73)
(78)s
t

0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
0.457
0.079
< 0.001
< 0.001
< 0.001
0.022

Pip/taz = Tazocin

SUSCEPTIBILITY RATES OF ESBL ESCHERICHIA COLI & KLEBSIELLA PNEUMONIAE ISOLATES

TO FOSFOMYCIN & OTHER ANTIMICROBIALS IN INPATIENTS VS. OUTPATIENTS

TABLEAU III

ANTIMICROBIAL SUSCEPTIBILITY

ANTIMICROBIAL AGENTS*
Amikacin
Aztreonam
Cefepime
Cefotaxime
Ceftazidime
Ciprofloxacin
Gentamicin
Imipenem
Nitroflurantoin
Piperacillin-tazobactam
Tobramycin
Trimethoprim-sulfamethoxazole
Fosfomycin

ESBL Escherichia coli

Inpatient
Outpatient
(n = 156)
(n = 218)
148
5
39
3
20
36
71
155
145
113
49
40
135

(95)
(3)
(25)
(2)
(13)
(23)
(46)
(99.4)
(93)
(72)
(31)
(26)
(87)

212
5
58
4
41
57
97
218
211
169
70
59
186

(97)
(2)
(27)
(2)
(19)
(26)
(45)
(100)
(97)
(78)
(32)
(27)
(85)

* Decimals were rounded to the nearest figure except for imipenem.

Disease (ESCMID) published new treatment guidelines

for UTIs considering a single dose fosfomycin as an appropriate choice [6]. A systematic review by Falagas et al. [24]
demonstrated that ESBL-EC has more than 90% susceptibility rate to fosfomycin, where as susceptibility rate for
ESBL-KP ranged from 76.7% to 100%. However, more
recent studies show an increased resistance rates to fosfomycin. A multicenter study from Spain on a large number
of isolates showed an increase in rate of uropathogenic
ESBL-EC resistance to fosfomycin form 4.4% in 2005 to
11.4% in 2009 [25]. Another study from Taiwan showed
fosfomycin susceptibility rates of 95.5% and 57.6% for
ESBL-EC and ESBL-KP respectively [26]. These global
increasing rates of resistance to fosfomycin can be explained by the parallel increase in community use [25]. In our
TABLEAU IV

DISTRIBUTION OF FOSFOMYCIN-RESISTANT
ESBL ISOLATES AMONG AGE GROUPS*

Age Group-Years/ No. (%) resistant

(No. of isolates)
E. coli
5
6-15
16-25
26-35
36-45
46-55
56-65
66

(n = 40)
(n = 25)
(n = 14)
(n = 18)
(n = 22)
(n = 29)
(n = 57)
(n = 169)

Total (n = 374)

4
3
3
3
3
5
5
27

(10)
(12)
(21)
(16)
(13)
(17)
(9)
(16)

53 (14)

Age Group-Years/ No. (%) resistant

(No. of isolates) K. pneumoniae
5
6-15
16-25
26-35
36-45
46-55
56-65
66

(n = 31)
(n = 6)
(n = 2)
(n = 4)
(n = 12)
(n = 17)
(n = 25)
(n = 71)

Total (n = 168)

* Decimals were rounded to the nearest figure.

** Numbers are too small to calculate percentages.

G.F. ARAJ, F.A. JABER Fosfomycin in vitro activity

16 (51)
2**
1**
0
5 (42)
7 (41)
4 (16)
29 (40)

64 (38)

p**
0.240
0.590
0.727
0.951
0.122
0.498
0.845
0.237
0.087
0.260
0.886
0.758
0.739

[n (%)] AMONG ISOLATES

ESBL Klebsiella pneumoniae
Inpatient
Outpatient
p
(n = 88)
(n = 80)
63
2
23
2
14
35
23
86
31
36
16
17
51

(72)
(2)
(26)
(2)
(16)
(40)
(26)
(97.7)
(35)
(41)
(18)
(19)
(58)

70
2
28
5
17
33
46
80
19
38
27
14
52

(88)
(3)
(35)
(6)
(21)
(41)
(58)
(100)
(24)
(48)
(34)
(18)
(65)

** p < 0.05 implies a significant difference.

0.056
0.923
0.212
0.198
0.373
0.846
< 0.001
0.175
0.104
0.390
0.021
0.762
0.349

study, susceptibility rates of ESBL-EC and ESBL-KP to

fosfomycin were 86% and 62%, respectively, whereas
higher susceptibility rates were observed for non-ESBLEC and non-ESBL-KP, 97% and 78%, respectively. Such
rates fall lower than ranges reported by Falagas [24] but
are comparable to more recent studies [25, 27]. Although
fosfomycin is significantly more effective against ESBLEC compared to ESBL-KP, it remains an effective therapeutic option for UTIs caused by ESBL and non-ESBLproducing E. coli and K. pneumoniae.
These results of fosfomycin are quite important in our
environment compared to the resistant pathogens rates encountered by other antimicrobial agents as noted below.
Locally and globally, uropathogenic isolates of E. coli
and K. pneumoniae have been showing an increasing
resistance rates to common antimicrobial agents used for
the treatment of UTIs, namely trimethoprim-sulfamethoxazole and fluoroquinolones [26-27]. In our study, only
24% and 41% of ESBL-EC and ESBL-KP isolates were
respectively susceptible to ciprofloxacin, findings which
are comparable to other studies [26-27]. For non-ESBLEC and non-ESBL-KP isolates, the susceptibility rates
of ciprofloxacin were comparable, 70% and 71%, respectively, indicating that fluoroquinolones are not the
best option to treat ESBL-producing enterobacteriaceae.
Trimethoprim-sulfamethoxazole showed low susceptibility rates for ESBL-producing isolates, 26% for ESBL-EC
and 19% for ESBL-KP making it the least effective
antimicrobial option against ESBL-producing enterobacteriaceae.
Imipenem was the most effective antimicrobial agent
against ESBL-producing isolates with susceptibility rates
of 99.7% and 98.8% for ESBL-EC and ESBL-KP, respectively. Imipenem is the drug of choice for treating severe
Lebanese Medical Journal 2012 Volume 60 (3) 145

infections. Nevertheless, its frequent use lead to the emergence of carbapenem resistant enterobacteriaceae isolates
[13, 15-16]
Aminoglycosides are considered as an alternative therapy to ESBL-producing enterobacteriaceae. In our study,
both gentamicin and tobramycin exhibited low susceptibility (26% to 45%) against both ESBL-EC and ESBLKP where amikacin was more effective (79% to 96%)
against both ESBL-producing groups. However, these
agents should be used with caution especially in complicated cases because of its ototoxicity and nephrotoxicity.
Thus, fosfomycin can be an appropriate alternative to
aminoglycosides.
Nitroflurantoin was effective against ESBL-EC (95%)
but not against ESBL-KP (29%). This suggests that nitroflurantoin can be a good choice for treatment of UTIs
caused by ESBL-EC. However, its use is limited because
of its nephrotoxicity.
In treating hospital acquired infections, choosing the
appropriate initial antibiotic has a significant impact on
mortality [28]. In our study, the results show that effective
antimicrobial choices for treating inpatients with ESBLEC uropathogens include imipenem, amikacin, nitroflurantoin, and fosfomycin, while those against ESBL-KP
include imipenem, amikacin and fosfomycin.
The age relation to overall antimicrobial agents in our
study showed increasing resistance with increasing age.
This finding is consistent with what was previously reported on the impact of age on resistance in UTIs [29-31].
Concerning fosfomycin, resistance versus age showed
almost comparable incidence among all age brackets indicating no preference for any age group. The high incidence
of resistance in patients 5 years of age is most likely due
to being mostly hospitalized inpatient cases (Table IV).
The valuable information revealed in this study is not
infallible since a couple of limitations can be cited. For
example, the method used for susceptibility testing in our
study is the disk diffusion method. Although this method
has been well standardized for most antimicrobials tested,
de Cueto et al. [32] described a discrepancy between different methods used for testing the susceptibility to fosfomycin. For example, compared to agar dilution method,
the disk diffusion method reported greater resistance to
fosfomycin in ESBL-KP isolates, but not in ESBL-EC
isolates [32]. Moreover, the classification of inpatient versus outpatient presented in our study may not satisfy the
criteria for classification as hospital-acquired versus community-acquired infections. This is so because some outpatients in this study may have been recently discharged
from a hospital in which they acquired the infection. This
may decrease the susceptibility rates in our outpatient
group.
To conclude, this study shows a high in-vitro activity of
fosfomycin against ESBL-EC and less so against ESBLKP uropathogens in Lebanon in both inpatient and outpatient settings. Such a finding makes fosfomycin a plausible agent to treat these resistant uropathogens. Nitroflurantoin was effective against ESBL-EC only.
146 Lebanese Medical Journal 2012 Volume 60 (3)

ACKNOWLEDGMENT

The excellent technical assistance and support is acknowledged for the Bacteriology staff: Lina Itani, Hassan Beyh,
Sohair Sabi, Rania Hammoud, Aline Avedissian, Rima
Asmar, Maguy Malak, and Nadia Ayyash.
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