Journal of Infection and Public Health (2012) 5, 102108

Three distinct clones of carbapenem-resistant

Acinetobacter baumannii with high diversity of
carbapenemases isolated from patients in two
hospitals in Kuwait
N.A. Al-Sweih , M. Al-Hubail, V.O. Rotimi
Department of Microbiology, Faculty of Medicine, Kuwait University, Kuwait
Received 14 December 2010 ; received in revised form 4 November 2011; accepted 9 November 2011

KEYWORDS
MDR A. baumannii;
Genotypes;
bla genes;
Kuwait hospitals

Summary
Objectives: This study was undertaken to investigate the clonal relatedness of
multidrug-resistant (MDR) Acinetobacter baumannii isolates collected from patients
in two teaching hospitals in Kuwait.
Materials and methods: Clinically signicant consecutive isolates of A. baumannii
obtained from patients in the Mubarak (36) and Adan (58) hospitals over a period
of 6 months were studied. These isolates were identied using molecular methods,
and their antimicrobial susceptibility was determined by the Etest method. The
mechanism of resistance to carbapenem was investigated by PCR, and pulsed-eld
gel electrophoresis (PFGE) was used to determine the clonal relatedness of MDR
isolates.
Results: Of the 94 isolates investigated, 80 (85.1%) were multidrug resistant (MDR).
The A. baumannii PFGE clone A and subclone A1 were the most prevalent in patients
infected with MDR isolates. Fifty-ve (94.8%) and 15 (41.7%) of the MDR isolates
from the Adan and Mubarak hospitals, respectively, belonged to PFGE clone A; isolates in this group showed higher resistance rates to antibiotics than isolates form
other groups. Of the 94 isolates, 40 (42.6%) were resistant to either imipenem or
meropenem or to both (CRAB). Most CRAB isolates (29/40 or 72.5%) carried bla genes,
which code for MBL (VIM-2 and IMP-1) enzymes. Two isolates harbored blaOXA-23 .
Conclusion: Three distinct clones of CRAB were isolated, providing evidence of a
high diversity of carbapenemases among our geographically related isolates.
2011 King Saud Bin Abdulaziz University for Health Sciences. Published by Elsevier
Ltd. All rights reserved.

Corresponding author at: Department of Microbiology, Faculty of Medicine, Kuwait University, P.O. Box 24923, Safat 13110,
Kuwait. Tel.: +965 2498 6062.
E-mail address: nalsweih@hsc.edu.kw (N.A. Al-Sweih).

1876-0341/$ see front matter 2011 King Saud Bin Abdulaziz University for Health Sciences. Published by Elsevier Ltd. All rights reserved.

doi:10.1016/j.jiph.2011.11.004

Three distinct clones of carbapenem-resistant Acinetobacter baumannii

Introduction
Interest in Acinetobacter baumannii has grown
rapidly over the last two decades, primarily as a
result of the emergence and outbreak of multidrugresistant (MDR) strains [1]. A. baumannii represents
an important cause of nosocomial infections including septicemia, ventilator-associated pneumonia
and urinary tract infections [2]. The bacterium is
usually intrinsically resistant to multiple antimicrobial agents, and resistance to -lactam is most
commonly associated with the production of high
levels of naturally produced cephalosporinases
[3]. However, acquired metallo--lactamase (MBL)
enzymes, which confer resistance to the carbapenems, have been reported [4]. Recent reports have
shown that MBLs, such as PER-1, VIM-2 and IMP-1,
are prevalent in Turkey and Korea and are a growing
source of resistance in these countries [5,6]. The
dissemination of the OXA-23 and OXA-58 carbapenemases among A. baumannii isolates has also been
reported in hospitals in Argentina [7,8]. In addition,
hospitals in the UK have experienced outbreaks
with three widespread clones: the South East
clone, OXA-23 clone 1 and OXA-23 clone 2; the latter two are consistently resistant to imipenem and
meropenem [9,10].
Recently, infections due to MDR A. baumannii
strains have become a serious problem in some hospitals in Kuwait, particularly the Mubarak Al-Kabeer
and Al-Adan hospitals, where these isolates are the
second most frequently isolated pathogens, particularly in the ICUs [11]. The Mubarak Al-Kabeer
hospital is the primary teaching hospital and serves
as both a referral and secondary medical center,
whereas Al-Adan hospital, also a teaching hospital, is a secondary medical center, located 16 km
away, in the southern part of the country. This
study was designed to investigate the clonal relatedness of the carbapenem-resistant A. baumannii
strains isolated from infected patients in these
hospitals.

Materials and methods

Bacterial isolates
All consecutive clinically signicant A. baumannii isolates collected from patients with proven
infections requiring antimicrobial therapy were
collected from the Mubarak Al-Kabeer hospital (MKH, Kuwait) and the Al-Adan hospital
(ADH, Kuwait) between May and October 2007.
Only one isolate per patient was tested, and

103

all duplicate strains were excluded. Primary

identication was performed using the API 20
NE system (BioMerieux, ltoile, France) and
conrmed by PCR using the following primers:
5 -CTAATAATTGATCTACTCAAG-3 (blaOXA-69A f ) and
5 -CCAGTGGATGGATGGATAGATTATC-3 (blaOXA-69 r )
for the blaOXA-69 gene, a naturally occurring oxacillinase in A. baumannii. Isolates were serially
labeled with abbreviations reecting the hospital
at which they were collected (158 ADH and 5994
MKH).

Susceptibility test
Susceptibility testing of the isolates was carried out
by determining the minimum inhibitory concentrations (MICs) of 11 antibiotics commonly used in our
hospitals to treat gram-negative infections using
the Etest (AB Biodisk, Solana, Sweden). Briey, a
bacterial suspension with a turbidity of 1.0 McFarland was prepared by inoculating a single colony
of an overnight (1618 h) pure culture of the bacterium into sterile PBS. Using a sterile disposable
cotton swab soaked in the inoculum, a 150 mm
Mueller-Hinton agar (Becton Dickinson, Sparks, MD,
USA) plate was inoculated in three directions and
spread to completely cover the entire surface.
Six Etest strips of the antibiotics were placed on
each plate. The inoculated plates were then incubated at 37 C for 24 h. An inoculated plate without
antibiotics was also included in each run to check
for the purity of the suspension. The MIC values
were estimated based on the concentration of the
antibiotics at which the elliptical zone of inhibition
intersected the Etest strip. The results were interpreted according to criteria suggested by the CLSI
[12]. Escherichia coli ATCC 25922 and Pseudomonas
aeruginosa ATCC 27853 were included in each run
as controls.

Detection of metallo--lactamase (MBL) and

oxacillinase (OXA)
Strains showing non-susceptibility to the carbapenems were screened for production of MBLs
using the disk approximation test as described by
Lee et al. [13] and the MBL Etest (AB Biodisk,
Sweden). Detection of the blaIMP-1 , blaVIM-1 ,
blaVIM-2 , blaSPM-1 , blaOXA-23 , blaOXA-24 and blaOXA-58
genes in carbapenem-resistant isolates was performed under standard PCR conditions using
previously reported primers [1416].

104

N.A. Al-Sweih et al.

Typing by pulsed-eld gel electrophoresis

(PFGE)
Carbapenem-resistant isolates were typed by PFGE
using Apa1 enzyme according to a method previously published by Tenover et al. [17]. Restriction
fragments were separated by electrophoresis on a
CHEF DR II (Bio-Rad, California, USA). The gel was
stained with 1 mg/ml ethidium bromide and visualized under ultraviolet illumination. Gel images
were analyzed using the Gene Genius Imaging system (Syngene Corp., Maryland, USA).

Results
A total of 94 consecutive isolates, 36 from MKH
and 58 from ADH, were studied. The isolates were
obtained from patients with various types of infections: 35 (37.2%) had respiratory tract infections,
21 (22.3%) had bloodstream infections, 14 (14.9%)
had wound infections, 9 (9.6%) had urinary tract
infections and 15 (16%) had miscellaneous infections. Comparative susceptibility data between the
2 hospitals are shown in Table 1. All 94 isolates
were multidrug resistant (MDR), which is dened
as resistance to 3 or more classes of antibiotics;
40 (42.6%) of these isolates were resistant to
the carbapenems (imipenem and/or meropenem).
The MICs of imipenem and meropenem ranged
between 0.125 g/ml and >32 g/ml, with MIC90
values of 12 g/ml and 24 g/ml and overall
resistance rates of 19.2% and 43.6%, respectively. Among the 40 carbapenem-nonsusceptible

Table 1

Antimicrobial susceptibility pattern of A. baumannii isolates.

Antimicrobial agents

Mubarak-Al-Kabeer
hospital
MICs (g/ml)
MIC50

Amikacin
a
Amox-clav
Cefepime
Ceftazidime
Ciprooxacin
Colistin
Gentamicin
Imipenem
Meropenem
b
Pip-tazo
Tigecycline
a
b

(MIC 8 g/ml) A. baumannii isolates, only 18

(45%) were imipenem-nonsusceptible, but all
were meropenem-nonsusceptible. MKH isolates displayed higher resistance rates to imipenem and
meropenem (27.8 and 50%, respectively) than
those from ADH (13.8 and 39.7%, respectively)
(Table 2). Among the total isolates, 7 (7.5%)
were resistant to colistin and 9 (9.6%) to tigecycline. The 9 tigecycline-resistant isolates were
also resistant to all other antibiotics, including
imipenem and meropenem. All isolates displayed
resistance rates to amikacin, amoxicillin-clavulanic
acid, cefepime, ciprooxacin, gentamicin and
piperacillin-tazobactam that were above 84%. The
resistance rates and MICs of these antibiotics were
signicantly higher in isolates from the Adan hospital than the Mubarak hospital.
Investigation of the presence of several genes
related to carbapenem resistance in all the 40 A.
baumannii (CRAB) isolates revealed that, although
no isolates harbored the blaSPM-1 , blaOXA-24 and
blaOXA-58 genes, blaIMP-1 , blaVIM-2 , blaVIM-1 and
blaOXA-23 were detected in 29 (72.5%) isolates. Of
the 29 isolates carrying bla genes, 8 (34.7%) harbored blaIMP-1 (all from ADH), 18 (58.8%) harbored
the blaVIM-2 gene, one strain from each hospital harbored blaOXA-23 , and one strain from MKH carried
the blaVIM-1 gene.
Molecular typing of the 29 bla-gene-positive isolates revealed three distinct PFGE patterns (clones
A, B and C). Using PCR, 8 isolates were found
to be positive for the production of VIM-2-like
carbapenemases among the ADH isolates; these 8
isolates belonged to subclone A1, as shown in the

>256
96
>256
>256
>32
0.75
24
3
4
>256
0.25

Amoxicillin-clavulanic acid.
Piperacillin-tazobactam.

MIC90
>256
>256
>256
>256
>32
4
256
12
24
>256
2

Al-Adan
hospital
MICs (g/ml)
% resistance
(n = 36)

MIC50

86
97
77.8
77.8
83
16.7
77.8
27.8
50
77.8
5.6

>256
>256
>256
>256
>32
1
48
2
4
>256
1.5

MIC90
>256
>256
>256
>256
>32
1.5
>1024
16
32
>256
4

% resistance
(n = 58)
94.8
100
91
93
94.8
1.7
91
13.8
39.7
94.8
13.8

Three distinct clones of carbapenem-resistant Acinetobacter baumannii

Table 2
Isolate

Carbapenem resistance in relation to PFGE clones and presence of carbapenemase enzymes.

PFGE clone

MIC (g/ml)
Imipenem

ADH1
ADH6
ADH7
ADH9
ADH13
ADH17
ADH18
ADH20
ADH21
ADH23
ADH31
ADH35
ADH37
ADH43
ADH47
ADH51
ADH56
MKH4
MKH5
MKH8
MKH12
MKH15
MKH19
MKH20
MKH23
MKH27
MKH29
MKH30
MKH36

105

A
A
A1
A
A1
A
A
A1
A
A
B
A
A1
A1
A1
A1
A1
C
A1
A1
C
A1
A1
C
A1
C
B
C
C

16
32
2
16
16
32
32
4
32
32
>32
16
1
0.5
0.25
1
2
4
16
4
16
4
16
4
8
8
>32
16
16

MBL gene group

OXA gene group

IMP-1
IMP-1
VIM-2
IMP-1
VIM-2
IMP-1
IMP-1
VIM-2
IMP-1
IMP-1

IMP-1
VIM-2
VIM-2
VIM-2
VIM-2
VIM-2
VIM-1
VIM-2
VIM-2
VIM-2
VIM-2
VIM-2
VIM-2
VIM-2
VIM-2

VIM-2
VIM-2

69
69
69
69
69
69
69
69
69
69
23, 69a
69
69
69
69
69
69
69
69
69
69
69
69
69
69
69
23, 69a
69
69

Meropenem
>32
32
32
32
32
>32
>32
32
>32
>32
>32
32
8
8
8
8
16
16
>32
32
>32
>32
32
16
8
32
>32
32
32

ADH, Adan hospital; MKH, Mubarak Al Kabir hospital; MBL, metallo--lactamase; OXA, oxacillinase; PFGE, pulsed-eld gel electrophoresis.
a Oxacillinase-producing carbapenem-resistant A. baumannii (CRAB) isolate from a bloodstream infection in a patient in Adan
hospital and respiratory tract infection in a patient in Mubarak hospital assigned into PFGE clone B.

dendrogram (Fig. 1). The MICs of imipenem

(0.254 g/ml) for 7 of these 8 isolates were in the
susceptible range, but all isolates had meropenem
MIC values 8 g/ml. Isolates harboring blaVIM-2
were predominant among the MKH strains and
belonged to either subclone A1 (5 isolates) or clone
C (5 isolates). Only 3 (30%) of these displayed an
imipenem MIC of 4 g/ml, but all were consistently
resistant to meropenem (MICs 16 to >32 g/ml).
All 8 isolates harboring blaIMP-1 were from ADH
and belonged to clone A; no clone A isolate was
observed at MKH. One isolate in each hospital was
positive for blaOXA-23 and belonged to clone B.
These two isolates, together with those of clone A
harboring blaIMP-1 , were unequivocally resistant to
imipenem and meropenem (MICs 16 to >32 g/ml).
A single isolate positive for blaVIM-1 was from a
patient in MKH and belonged to clone C.

Discussion
Although similar to world trends, the results of
this study demonstrate an unacceptably high rate
of resistance to carbapenems in A. baumannii
isolates collected from hospitalized patients in
Kuwait. There is worldwide variation in the carbapenem resistance rate from one geographical
area to another, but a recent report by Perez et al.
[1] conrmed an increasing worldwide incidence
of carbapenem-resistant A. baumannii (CRAB). For
instance, the global incidence of meropenem resistance in A. baumannii was approximately 6% in
1998 but jumped to approximately 29% in 2005. This
development also applies to our hospitals, where
resistance rates to imipenem and meropenem were
as high as 28% and 50%, respectively, in one hospital and 14% and 40%, respectively, in the other.

106

N.A. Al-Sweih et al.

Figure 1 Genetic relationships of 29 carbapenem-resistant Acinetobacter baumannii isolates harboring MBL and Oxa
bla genes constructed from cluster analysis of PFGE patterns obtained after restriction treatment with Apa I. Hospital
strains (MKH, Mubarak Al Kabir Hospital; ADH, Adan Hospital), clones (A, A1, B, C), bla genes (VIM-1, VIM-2, IMP-1;
OXA-23, OXA-69).

Thus, the choice of antimicrobial agents available

for treating A. baumannii infections is limited.
The high carbapenem resistance rates in strains
from our hospitals are concordant with a recent
report from nearby Turkey, where 50% of their isolates displayed resistance to carbapenems [18].
In this study, CRAB isolates also demonstrated
high rates of co-resistance to all other classes of
antimicrobial agents tested, except tigecycline and
colistin. Isolates from both hospitals showed an
unpredictable susceptibility pattern to the latter
drugs. In MKH, all carbapenem-susceptible isolates
were susceptible to tigecycline but less susceptible
to colistin, whereas approximately 12% of the CRAB
isolates that were resistant to tigecycline were
relatively susceptible to colistin. As the testing
media for both sets of isolates were the same, the
explanation for this observation remains unclear.

A. baumannii isolates with high-level resistance

rates against tigecycline have recently emerged
as a potential problem of clinical signicance in
different parts of the world [19,20]. Relative to previously reported rates of 1.1% and 0% from Kuwait
[21], the prevalence of tigecycline resistance has
increased phenomenally (in just over two years)
observed in this study cannot be explained. The
methods of testing, including media, used in both
the previous study and our study were precisely the
same. We report that 17% of the MKH isolates were
resistant to colistin. This nding is of great concern
because the spread of these resistant strains will
compromise the treatment of MDR Acinetobacter
infections, especially as colistin is one of the last
alternatives to carbapenems. One possible explanation may be the presence of a pmrA mutation that
has been shown to be related to elevated colistin

Three distinct clones of carbapenem-resistant Acinetobacter baumannii

resistance in A. baumannii [22]. However, the colistin resistance mechanisms should be investigated
in greater detail.
The acquisition of carbapenem resistance in
A. baumannii is mainly due to the production of
two types of -lactamases: OXA-type -lactamases
(OBLs) and metallo--lactamases (MBLs). The OBLs
appear to be more prevalent and important to
carbapenem resistance in this bacterium in some
countries [24,23], including Middle Eastern countries such as Bahrain [24] and the UAE [25].
However, the blaVIM-2 and blaIMP-1 genes were
responsible for the majority of carbapenem resistance in our isolates. Only two strains (one from
each hospital) harboring the blaOXA-23 gene were
isolated. The blaIMP-1 and blaVIM-2 genes have been
reported with increased frequency as mediators of
carbapenem resistance in Acinetobacter isolates
from Asia and Europe [26,27] and, more recently,
from Canada and South America [28,29]. No previous data are available about these genes in isolates
obtained from the GCC or Middle East. Thus, our
study constitutes the rst report from this part
of the world on CRAB isolates whose carbapenemresistance is mediated mainly by MBLs. A sizable
percentage of CRAB isolates (27.5%) were negative for all of the MBL and OXA genes investigated.
Hence, we can speculate that the resistance in
these isolates may be due to non-enzymatic mechanisms such as efux pump and porin defects.
Alternatively, resistance could be due to the
production of the NDM-1 -lactamase or its variant, NDM-2, which has been found in a clinical
isolate in Egypt [30]. The Egyptian diaspora is
the largest expatriate population in Kuwait, and
strains showing the latter mechanism of resistance
may have been introduced into the population
by returning workers and should be meticulously
investigated.
The analysis of the clonal patterns obtained by
PFGE for the 29 carbapenem-resistant Acinetobacter isolates, which were positive for at least one
of the tested MBL and oxacillinase genes, showed
that the CRAB isolates belonged to 3 major clones.
The most common clones in MKH were C and A. All
isolates from ADH belonged to clone A, except for a
single isolate that belonged to clone B. These ndings reect the spread and dissemination of clone
A and subclone A1 between the hospitals, but no
evidence of inter-hospital dissemination of clones B
and C was observed. These results indicate that limited clones of A. baumannii may have the capacity
to acquire carbapenem resistance. It is conceivable
that the acquisition of carbapenem resistance may
contribute to the survival of A. baumannii in the
hospital environment.

107

Conclusion
The identication of resistance genes conrms the
high diversity of different carbapenemases in geographically related A. baumannii isolates. Thus, the
high prevalence of MDR and carbapenem-resistant
isolates in these hospitals may be due to more
than one clone of A. baumannii. This nding is
unusual, deserves more attention, and warrants
further investigation of the population-genetics
background of the isolates.

Conict of interest
Funding: Supported by Kuwait University Research
Administration Grant No. YM 01/08.
Competing interests: None declared.
Ethical approval: Not required.

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