burns 35 (2009) 10201025

available at www.sciencedirect.com

journal homepage: www.elsevier.com/locate/burns

Antimicrobial susceptibility and ESBL prevalence in

Pseudomonas aeruginosa isolated from burn patients in the
North West of Pakistan

Farhat Ullah a,b,*, Salman Akbar Malik a, Jawad Ahmed b

a
Department of Biochemistry/Molecular Biology, Quaid-i-Azam University, Islamabad, Pakistan
b
Khyber Medical College, Peshawar, Pakistan

article info abstract

Article history: Pseudomonas aeruginosa is one of the most prevalent pathogen in burn infections. Infections
Accepted 15 January 2009 with P. aeruginosa are associated with higher mortality rate and antibiotic costs in hospi-
talized patients. These bacteria also produce enzymes called Expanded Spectrum Beta-
Keywords: Lactamases (ESBL) which render penicillins and cephalosporins inactive. The aim of this
Antimicrobial susceptibility study was to assess the antimicrobial susceptibility pattern and prevalence of ESBL in P.
Pseudomonas infections aeruginosa in Peshawar, North West of Pakistan. During 20052006, one hundred and six P.
Burns aeruginosa isolates were collected from burn patients at a tertiary care hospital. Antibiotic
Extended Spectrum susceptibility testing and ESBL detection were carried out according to Clinical Laboratory
Beta-Lactamases and Standards Institute (CLSI) criteria. Eighteen antibiotics were tested in this study. A total
of 38 (35.85%) isolates were found to be ESBL producers. Thirty one (29.24%) isolates were
resistant to 3 or more antibiotics (multidrug resistance). Meropenem and imipenem showed
high potency with 99% and 96% isolates being susceptible respectively. Susceptibility to
amikacin was 70%; gentamicin 25%; ciprofloxacin 49%; enoxacin 47%; gatifloxacin 42%;
doxycycline 21% and to co-trimoxazole only 16%. This study reveals that P. aeruginosa
isolated from burns in this region are multidrug resistant and produce ESBL in large
proportions.
Crown Copyright # 2009 Published by Elsevier Ltd and ISBI. All rights reserved.

1. Introduction onmental source [3]. About 45% of mortality in burns patients

Burns remove the protective skin layer and expose the body to
numerous potential pathogens. Microbial infection after
burns, where a large portion of the skin is damaged, is a very
serious complication that often results in death of the patients
[1]. Pseudomonas aeruginosa is a known opportunistic pathogen
frequently causing infections in burned patients [2]. This
pathogen mostly causes burn wound infections from the
patients endogenous gastrointestinal flora and/or an envir-
is due to infections [4]. Different studies have reported 2273%
Pseudomonas from infections of burn patients [57]. It is an
important cause of septic mortality in burn patients [8]. The
nosocomially acquired resistant P. aeruginosa in burn patients
results in higher mortality rate, antibiotic costs, hospital stay
and surgical procedures [9,10]. In P. aeruginosa resistance to
antimicobials may be due to outer membrane impermeability,
target site modification, enzymatic degradation or multidrug
efflux pumps [11,12]. Resistance to beta-lactams (b-lactams)

* Corresponding author at: Department of Biochemistry/Molecular Biology, Quaid-i-Azam University, Islamabad, Pakistan.
Tel.: +92 3339361513.
E-mail address: farhataziz80@hotmail.com (F. Ullah).
0305-4179/$36.00 . Crown Copyright # 2009 Published by Elsevier Ltd and ISBI. All rights reserved.
doi:10.1016/j.burns.2009.01.005
 burns 35 (2009) 10201025
has been reported to be associated with ESBL [13], which
hydrolyze oxyimino beta-lactams like cefotaxime, ceftriax-
one, ceftazidime and monobactams but have no effect on
cephamycins, carbapenems and related compounds [14].
Detection of ESBL production is important. One major concern
is the spread of ESBL positive bacteria within hospitals, which
may lead to outbreaks or to endemic occurrence [1518].
Another concern is failure to treat infections caused by ESBL
positive organisms, as therapeutic choices are limited [13]. It is
necessary to investigate the prevalence of ESBL positive
strains in hospitals so as to formulate a policy of empirical
therapy in high risk units where infections due to resistant
organisms are much higher [19]. ESBL producing Pseudomonas
in this part of the world has been observed by several workers;
its reported prevalence range from 22 to 36% [20,21]. Anti-
pseudomonal penicillins alone and in combination with beta-
lactamase inhibitor, aminoglycosides, and carbapenems are
effective for treating pseudomonal infections [22,23]. But
resistance is increasing to antimicrobials in P. aeruginosa
especially to ciprofloxacin [24]. Various studies have recorded
high resistance rates to penicillins, cephalosporins and
aminoglycoside in Pseudomonas [25,26]. Multidrug resistance
(MDR) is frequently reported in P. aeruginosa from burn
patients as well as from other pathological conditions
[26,27]. Combination of beta-lactams and aminoglycosides is
useful against such MDR strains [28]. There are few reports on
the susceptibility pattern of Pseudomonas from burns and ESBL
prevalence in Pakistan.
The aim of this study was to determine the antibiotic
susceptibility pattern and detection of ESBL production in P.
aeruginosa from burn patients for effective management of
such infections.
2. Materials and methods
2.1. Bacterial isolates
Between April 2005 and May 2006, a total of 392 wound swab
samples were received from burn unit in the microbiology
section of the Pathology Department at Khyber Teaching
Hospital, Peshawar, in the North West of Pakistan. Only one
isolate per patient was included in the study. The samples
received were inoculated onto Blood agar and MacConkey
agar. After 24 h aerobic incubation at 37 8C, isolates were
identified to the species level using biochemical tests.
2.2. Antimicrobial agents susceptibility testing
Susceptibility to antimicrobial agents was determined both by
Disc Diffusion method of Kirby Bauer and Minimum Inhibitory
Concentration (MIC) method on MullerHinton agar (Oxoid,
England) as described by the Clinical and Laboratory Stan-
dards Institute (CLSI) [29]. The antibiotic discs were obtained
from Oxoid, England.
The antibiotics used for antibiogram determination of the
collected strains were: ampicillin (AMP), amoxicillin/calvulo-
nic acid (AMC), cephradine (CE), cefaclor (CEC), ceftriaxone
(CRO), ceftazidime (CAZ), cefpirome (CPO), doxycycline (DOX),
ciprofloxacin (CIP), gatifloxacin (GTX), enoxacin (ENX), sul-
1021
phamethoxazole/trimethoprim (SXT), meropenem (MEM),
imipenem (IPM), gentamicin (CN) and amikacin (K). Escherichia
coli NCTC 10418 was used as control for susceptibility testing.
2.3. Detection of Extended Spectrum Beta-Lactamases
(ESBL)
The initial screening and phenotypic confirmatory tests
recommended by the CLSI for ESBL detection were carried to
assess the prevalence of ESBL [29]. In the initial screening test a
disc of amoxycillin + clavulonic acid (20 + 10 mg) was placed in
centre of the Petri plate already inoculated with the test
organism while aztreonam (30 mg) cefotaxime (30 mg) ceftazi-
dime (30 mg) cefpodoxime (30 mg) and ceftriaxone (30 mg) discs
were placed at a distance of 2025 mm (centre to centre) from
the amoxycillin + clavulonic acid disc on the same plate. Zones
of inhibition around the third generation cephalosporin discs
and aztreonam were observed after 18 h incubation at 37 8C. If
the zone of inhibition around one or more cephalosporin discs
and aztreonam was extended on the side nearest to the
amoxycillin + clavulonic acid, the organism showing this
synergy was labeled as ESBL positive. In the phenotypic
confirmatory test, the test organisms were grown on Muller
Hinton agar and discs of cefotaxime (30 mg) and ceftazidime
(30 mg) separately and each of these in combination with
clavulanic acid (10 mg) were placed on the surface of the lawn of
bacteria. A difference of 5 mm between the zone of inhibition
of a single disc and in combination with clavulonic acid was
considered as ESBL positive isolate. E. coli NCTC 10418 was used
as ESBL negative control and Klebsiella pneumoniae ATCC 700603
was used as ESBL positive control strain.
3. Results
A total of 392 wound swab samples from burn ward received
for culture and sensitivity were processed. P. aeruginosa was
grown from 106 (27%) specimens. Age range of patients was
between 1 and 60 years with a mean of 22.66 years. More
isolates were recovered from women (57) as compared to men
(49), with a ratio of 1:1.16. More than 70% isolates were
obtained from patients aged up to 30 years. Age-wise
distribution of patients is given in Fig. 1.
Among the beta-lactams tested, the most effective agents
were meropenem and imipenem with 93% and 90% isolates
being susceptible. These were followed by ceftazidime with 54%
activity, cefpirome 50%, ceftriaxone 42%, cefaclor 25%, cephra-
dine 20% and ampicillin had 11% activity (Table 1). Susceptibility
results of combination of beta-lactams and beta-lactamase
inhibitors tested were: 66% isolates susceptible to cefoperazo-
ne + sulbactam, 53% susceptible to piperacillin + tazobactam
and 20% susceptible to amoxicillin + clavulanic acid. Among
aminoglycosides amikacin showed good activity, 70% isolates
were susceptible to it and 23% isolates were susceptible to
gentamicin. Ciprofloxacin had maximum activity among
fluoroquinolones against the isolated P. aeruginosa, followed
by enoxacin and gatifloxacin with 49%, 47% and 42% activity
respectively (Table 2).
Only 21% isolates were susceptible to doxycycline and 16%
to co-trimoxazole. About 60% (n = 46) gentamicin resistant
1022 burns 35 (2009) 10201025

much lower being 12.24% and 10.20% respectively. A total of 31

(29.24%) isolates were multidrug resistant (MDR) (resistant to 3
or more drug classes). The most prevalent MDR pattern was
resistance to beta-lactams, doxycycline, fluoroquinolones and
co-trimoxazole.
In this study 38 (35.85%) P. aeruginosa were found to be ESBL
producers, 20 (52.63%) isolated from men and 18 (47.37%)
isolated from women. Resistance was high in the ESBL positive
strains as compared to the ESBL negative strains. A statisti-
cally significant difference was found in the susceptibilities of
flouroquinolones (CIP, ENX, GTX), amikacin, cefoperazone/
sulbactam, piperacillin/tazobactam, and carbapenems (MEM,
IPM) for ESBL positive and ESBL negative isolates ( p
value < 0.05). Resistance to doxycycline, gentamicin and
sulphamethoxazole + trimethoprim was slightly high in ESBL
positive isolates as compared to ESBL negative ones but it was
not statistically significant ( p value > 0.05).

Fig. 1 Age-wise distribution of patients.

4. Discussion

strains were sensitive to amikacin. Among the 9 strains
resistant to imipenem, 6 (66.67%) were sensitive to amikacin, 5
(55.56%) to meropenem and 4 (44.44%) to enoxacin. There were
a total of 41 isolates resistant to both the third generation
agents (ceftazidime and ceftriaxone) and 32 (78.05%) of these
were sensitive to the carbapenems. Of the 27 amikacin
resistant isolates, 25 (92.60%) were sensitive to imipenem,
24 (89.89%) to meropenem and 7 (25.93%) to ciprofloxacin.
No isolate was found resistant to all the antibiotics and two
isolates were found susceptible to all the antimicrobial agents
tested. Fluoroquinolone resistant isolates were generally co-
resistant to co-trimoxazole (89.80%), gentamicin (83.67%),
doxycycline (81.63%), fourth generation cephalosporin (cefpir-
ome) (75.51%), third generation cephalosporins (ceftazidime
and ceftriaxone) (59.18%), second generation cephalosporin
(cefaclor) (89.80%), first generation cephalosporin (cephradine)
(97.95%) and penicillin (ampicillin) (93.88%), however, resis-
tance among such strains to imipenem and meropenem was
In the present study, P. aeruginosa was obtained from 27%
samples processed. This is lower than reported by other
studies [30,31] but comparable to results from studies [21].
These results reveal that resistance in P. aeruginosa is
increasing to the commonly used antibiotics, i.e., penicillins,
cephalosporins, gentamicin, doxycycline and co-trimoxazole.
Worldwide, resistance to antibiotics has increased in P.
aeruginosa [22,25]. P. aeruginosa may be intrinsically resistant
or have acquired resistance to antibiotics due to permeability
barrier of the cell surface [32], the production of an AmpC b-
lactamase, multidrug efflux pumps [33], b-lactamases,
extended spectrum b-lactamases, metallo-b-lactamases [33].
Carbapenems are the drugs of choice for many infections
caused by gram positive and gram negative bacteria [34,35]. In
this study, the most effective antibiotics were carbapenems. In
total, 99 (93%) isolates were susceptible to meropenem and 96
(90%) isolates were susceptible to imipenem. These results are
in close agreement with other studies [36,37].

Table 1 Antibiotic susceptibility of the isolated P. aeruginosa (n = 106).

Antibiotic Resistant number (%) Intermediate number (%) Susceptible number (%)

AMP 100 (94.34%) 05 (04.72%) 01 (00.94%)

AMC 68 (64.15%) 14 (13.21%) 20 (18.87%)
CE 81 (76.42%) 05 (04.72%) 20 (18.87%)
CEC 76 (71.70%) 05 (04.72%) 25 (23.58%)
CRO 47 (44.34%) 17 (16.04%) 42 (39.62%)
CAZ 45 (42.45%) 07 (06.60%) 54 (50.94%)
CPO 50 (47.17%) 06 (05.66%) 50 (47.17%)
SCF 07 (06.60%) 33 (31.13%) 66 (62.26%)
TZP 25 (23.58%) 28 (26.42%) 53 (50.00%)
MEM 06 (05.66%) 01 (00.94%) 99 (93.40%)
IPM 09 (08.50%) 01 (00.94%) 96 (90.56%)
GTX 49 (46.23%) 12 (11.32%) 45 (42.45%)
ENX 48 (45.28%) 08 (07.55%) 50 (47.17%)
CIP 51 (48.11%) 03 (02.83%) 52 (49.06%)
CN 76 (71.70%) 05 (04.72%) 25 (23.58%)
AK 27 (25.47%) 04 (03.77%) 75 (70.75%)
DO 79 (74.52%) 04 (03.77%) 23 (21.79%)
SXT 84 (79.24%) 05 (04.72%) 17 (16.04%)
 burns 35 (2009) 10201025 1023

Table 2 Comparison of susceptibility to antimicrobial agents tested between ESBL positive and ESBL negative P.
aeruginosa isolates (n = 106).
Antibiotic ESBL +ve n = 38 ESBL ve n = 68

Sensitive number (%) Resistant number (%) Sensitive number (%) Resistant number (%)

GTX 08 (21.05%) 30 (78.95%) 37 (54.41%) 31 (45.59%)

CIP 11 (28.95%) 27 (71.05%) 41 (60.29%) 27 (39.71%)
ENX 12 (31.58%) 26 (68.42%) 38 (55.88%) 30 (44.12%)
CN 09 (23.68%) 29 (76.32%) 16 (23.53%) 52 (76.47%)
AK 16 (42.11%) 22 (57.89%) 59 (86.76%) 09 (13.24%)
DO 09 (23.68%) 29 (76.32%) 14 (20.59%) 54 (79.41%)
SXT 05 (13.16%) 33 (86.84%) 12 (17.65%) 56 (82.35%)
SCF 16 (42.11%) 22 (57.89%) 50 (73.53%) 18 (26.47%)
TZP 09 (23.68%) 29 (76.32%) 44 (64.71%) 24 (35.29%)
MEM 32 (84.21%) 06 (15.79%) 67 (98.53%) 01 (01.47%)
IPM 31 (81.58%) 07 (18.42%) 65 (95.59%) 03 (04.41%)

Penicillins are bactericidal, inhibiting bacterial cell wall
synthesis [38]. These bacteria offer resistance to penicillins by
production of b-lactamases and by permeability barrier of the
cell surface [32]. High resistance has been noted to ampicillin
in various studies [25,39]. In this study we found 100 (94.34%)
isolates resistant to ampicillin. In a recent study from
Pakistan, Khan et al. [40] have reported 98% resistance to
ampicillin in P. aeruginosa.
Cephalosporins have been used in infections caused by P.
aeruginosa [4144] and new cephalosporins, which are now in
pipeline, also show good activity against P. aeruginosa [45,46].
Several studies have reported increased resistance of P.
aeruginosa isolates to cephalosporins [21,47]. In our isolates,
50% were susceptible to fourth generation cephalosporins,
cefpirome. While Chaudhary from India, in 2003, has recorded
32% susceptibility and Strateva et al., from Bulgaria have
found 42% susceptibility of P. aeruginosa isolates to cefpirome
[48,49]. Of the third generation cephalosporins, 54% isolates
were susceptible to ceftazidime and 42% to ceftriaxone. These
results are in agreement with other studies [6,48]. Most of the
isolates were resistant to first and second generation
cephalosporins. Overall, 25% isolates were susceptible to
cefaclor and 20% to cephradine.
Aminoglycosides have good activity against clinically
important gram negative bacilli [50]. Increased impermeability
and enzymatic modification are important mechanisms of
resistance to aminoglycosides in Pseudomonas [33,51]. Among
the non-beta-lactams, amikacin showed good activity with
70.75% isolates found susceptible in this study. This is lower
than reported from France by Cavallo et al. [52]. They recorded
86% susceptibility [52]. This may be due to increased use of
amikacin in Pakistan as compared to France. According to
Miller et al. [53], pattern of resistance to aminoglycosides is
affected by selective pressure in different regions. Gentamicin
has been used with excellent results in the treatment of sepsis
due to Pseudomonas in burn patients [54]. Resistance to
gentamicin was recorded in 76.42% isolates. Strateva et al.,
in 2007 [48], from Bulgaria reported 79.7% resistance to P.
aeruginosa.
Fluoroquinolones are most commonly used in burn wards
and are effective against Pseudomonas [47]. But resistance to
fluoroquinolones is increasing [21]. Resistance rates to
fluoroquinolones may vary and depends on local antibiotic
policies, origin of the strains, and geographic location [55].
Resistance to ciprofloxacin is correlated with its increased use
[56]. The observed resistance in our isolates to ciprofloxacin,
gatifloxacin and enoxacin was 48.11%, 46.23% and 45.28%
respectively. This is higher than reported in other studies from
Unites States, North America, Latin America and Europe
[57,58]. This may be due to their increased use in this part of
the world.
Generally, pathogens in hospitals are resistant to multiple
antibiotics (MDR) due to increased selection pressure of
antibiotics [59]. Multidrug Resistance (MDR) in Pseudomonas
is increasing throughout the world [33,48,58] and is a major
problem in the management of these pathogens [21,58]. We
found 31 (29.24%) isolates as MDR. This is in contrast to studies
by Japoni et al., Iran, 2006 and Strateva et al., Bulgaria, 2007.
They recorded 73% and 49.8% isolates being MDR in their
studies respectively [22,48].
Production of ESBL is frequently plasmid encoded and
bears clinical significance. Plasmids responsible for ESBL
producing bacteria frequently carry genes encoding resis-
tance to other drug classes also. Therefore, antibiotic
options in the treatment of ESBL producing organisms are
extremely limited [13]. We found 38 (35.85%) isolates as ESBL
producers. This is in agreement with another study from
Pakistan, conducted by Ali et al., in 2002, who reported
36.36% ESBL prevalence in P. aeruginosa [20]. To investigate
MDR, ESBL from other parts of Pakistan, further studies
using more isolates are required. Studies of molecular
epidemiology of these resistance genes can also be used for
comparison with genes already isolated from other parts of
the world.
Conflict of interest
We, all the authors, state that we have no conflict of interest.
references
[1] Atlas RM. Microbiology, Fundamentals and Applications.
New York: Macmillan; 1984.
[2] Van Eldere J. Multicentre surveillance of Pseudomonas
aeruginosa susceptibility patterns in nosocomial infections.
J Antimicrob Chemother 2003;51:34752.
1024 burns 35 (2009) 10201025
[3] Altoparlak U, Erol S, Akcay MN, Celebi F, Kadanali A. The
time-related changes of antimicrobial resistance patterns
and predominant bacterial profiles of burn wounds and
body flora of burned patients. Burns 2004;30:6604.
[4] Bloemsma GC, Dokter J, Boxma H, Oen IM. Mortality and
causes of death in a burn centre. Burns 2008;34:11037.
[5] Rastegar Lari A, Bahrami Honar H, Alaghehbandan R.
Pseudomonas infections in Tohid Burn Center, Iran. Burns
1998;24:63741.
[6] Revathi G, Puri J, Jain BK. Bacteriology of burns. Burns
1998;24:3479.
[7] Komolafe OO, James J, Kalongolera L, Makoka M.
Bacteriology of burns at the Queen Elizabeth Central
Hospital, Blantyre, Malawi. Burns 2003;29:2358.
[8] Tredget EE, Shankowsky HA, Rennie R, Burrell RE, Logsetty
S. Pseudomonas infections in the thermally injured patient.
Burns 2004;30:326.
[9] Aloush V, Navon-Venezia S, Seigman-Igra Y, Cabili S,
Carmeli Y. Multidrug-resistant Pseudomonas aeruginosa: risk
factors and clinical impact. Antimicrob Agents Chemother
2006;50:438.
[10] Armour AD, Shankowsky HA, Swanson T, Lee J, Tredget EE.
The impact of nosocomially-acquired resistant
Pseudomonas aeruginosa infection in a burn unit. J Trauma
2007;63:16471.
[11] Hancock REW. Resistance mechanisms in Pseudomonas
aeruginosa and other nonfermentative gram-negative
bacteria. Clin Infect Dis 1998;27:S939.
[12] Mesaros N, Nordmann P, Plesiat P, Roussell-Delvallez M,
Van Eldere J, Glupczynski Y, et al. Pseudomonas aeruginosa:
resistance and therapeutic options at the turn of the new
millennium. Clin Microbiol Infect 2007;13:56078.
[13] Paterson DL, Bonomo RA. Extended-spectrum beta-
lactamases: a clinical update. Clin Microbiol Rev
2005;18:65786.
[14] Philippon A, Labia R, Jacoby G. Extended-spectrum beta-
lactamases. Antimicrob Agents Chemother 1989;33:11316.
[15] Lucet JC, Decre D, Fichelle A, Joly-Guillou ML, Pernet M,
Deblangy C, et al. Control of a prolonged outbreak of
extended-spectrum beta-lactamase-producing
enterobacteriaceae in a university hospital. Clin Infect Dis
1999;29:14118.
[16] Pena C, Pujol M, Ardanuy C, Ricart A, Pallares R, Linares J,
et al. Epidemiology and successful control of a large
outbreak due to Klebsiella pneumoniae producing extended-
spectrum beta-lactamases. Antimicrob Agents Chemother
1998;42:538.
[17] Quale JM, Landman D, Bradford PA, et al. Molecular
epidemiology of a citywide outbreak of extended-spectrum
beta-lactamase-producing Klebsiella pneumoniae infection.
Clin Infect Dis 2002;35:83441.
[18] Meyer KS, Urban C, Eagan JA, Berger BJ, Rahal JJ.
Nosocomial outbreak of Klebsiella infection resistant to late-
generation cephalosporins. Ann Intern Med 1993;119:3538.
[19] Mathur P, Kapil A, Das B, Dhawan B. Prevalence of extended
spectrum beta lactamase producing gram negative bacteria
in a tertiary care hospital. Indian J Med Res 2002;115:1537.
[20] Ali AM, Rafi S, Hussain Z. ESBL producing Nosocomial
Enterobacteria isolated from clinical specimens detected by
Double Disc Diffusion Method. Infect Dis J 2003;12:1016.
[21] Singh NP, Goyal R, Manchanda V, Das S, Kaur I, Talwar V.
Changing trends in bacteriology of burns in the burns unit,
Delhi, India. Burns 2003;29:12932.
[22] Japoni A, Alborzi A, Kalani M, Nasiri J, Hayati M, Farshad S.
Susceptibility patterns and cross-resistance of antibiotics
against Pseudomonas aeruginosa isolated from burn patients
in the South of Iran. Burns 2006;32:3437.
[23] Walkty A, Decorby M, Nichol K, Mulvey MR, Hoban D,
Zhanel G. Antimicrobial susceptibility of Pseudomonas
aeruginosa isolates obtained from patients in Canadian
intensive care units as part of the Canadian National
Intensive Care Unit study. Diagn Microbiol Infect Dis
2008;61:21721.
[24] Karlowsky JA, Draghi DC, Jones ME, Thornsberry C,
Friedland IR, Sahm DF. Surveillance for antimicrobial
susceptibility among clinical isolates of Pseudomonas
aeruginosa and Acinetobacter baumannii from hospitalized
patients in the United States 1998 to 2001. Antimicrob
Agents Chemother 2003;47:16818.
[25] Gad GF, el-Domany RA, Ashour HM. Antimicrobial
susceptibility profile of Pseudomonas aeruginosa isolates in
Egypt. J Urol 2008;180:17681.
[26] Shahid M, Malik A. Resistance due to aminoglycoside
modifying enzymes in Pseudomonas aeruginosa isolates from
burns patients. Indian J Med Res 2005;122:3249.
[27] Jung R, Fish DN, Obritsch MD, MacLaren R. Surveillance of
multi-drug resistant Pseudomonas aeruginosa in an urban
tertiary-care teaching hospital. J Hosp Infect 2004;57:
10511.
[28] Oie S, Sawa A, Kamiya A, Mizuno H. In-vitro effects of a
combination of antipseudomonal antibiotics against multi-
drug resistant Pseudomonas aeruginosa. J Antimicrob
Chemother 1999;44:68991.
[29] Babini GS, Livermore DM. Antimicrobial resistance
amongst Klebsiella spp. collected from intensive care units
in Southern and Western Europe in 19971998. J Antimicrob
Chemother 2000;45:1839.
[30] Agnihotri N, Gupta V, Joshi RM. Aerobic bacterial isolates
from burn wound infections and their antibiogramsa
five-year study. Burns 2004;30:2413.
[31] Kaushik R, Kumar S, Sharma R, Lal P. Bacteriology of burn
woundsthe first three years in a new burn unit at the
Medical College Chandigarh. Burns 2001;27:5957.
[32] Suginaka H, Ichikawa A, Kotani S. Penicillin-resistant
mechanisms in Pseudomonas aeruginosa, binding of
penicillin to Pseudomonas aeruginosa KM 338. Antimicrob
Agents Chemother 1975;7:62935.
[33] Livermore DM. Multiple mechanisms of antimicrobial
resistance in Pseudomonas aeruginosa, our worst nightmare?
Clin Infect Dis 2002;34:63440.
[34] Nicolau DP. Carbapenems: a potent class of antibiotics.
Expert Opin Pharmacother 2008;9:2337.
[35] Shah PM. Parenteral carbapenems. Clin Microbiol Infect
2008;14(Suppl. 1):17580.
[36] Al-Jasser AM, Elkhizzi NA. Antimicrobial susceptibility
pattern of clinical isolates of Pseudomonas aeruginosa. Saudi
Med J 2004;25:7804.
[37] Ramakrishnan MK, Sankar J, Venkatraman J, Ramesh J.
Infections in burn patientsexperience in a tertiary care
hospital. Burns 2006;32:5946.
[38] Trevor AJ, Katzung BG, Masters SB. Katzungs
Pharmacology: Examination and Board Review. New York:
McGraw-Hill/Appleton & Lange; 2001.
[39] Astal Z. Susceptibility patterns in Pseudomonas aeruginosa
causing nosocomial infections. J Chemother 2004;16:2648.
[40] Khan JA, Iqbal Z, Rahman SU, Farzana K, Khan A. Report:
prevalence and resistance pattern of Pseudomonas aeruginosa
against various antibiotics. Pak J Pharm Sci 2008;21:3115.
[41] Hoogkamp-Korstanje JA, Westerdaal NA. In vitro
susceptibility of pseudomonas to four beta-lactam
antibiotics (ampicillin, cephalothin, carbenicillin,
piperacillin), to four aminoglycosides (kanamycin,
amikacin, gentamicin, tobramycin) and to colimycin.
Chemotherapy 1979;25:4853.
[42] Korvick J, Yu VL, Hilf M. Susceptibility of 100 blood isolates
of Pseudomonas aeruginosa to 19 antipseudomonal
antibiotics: old and new. Diagn Microbiol Infect Dis
1987;7:10711.
 burns 35 (2009) 10201025
[43] Cavallo JD, Fabre R, Leblanc F, Nicolas-Chanoine MH,
Thabaut A. Antibiotic susceptibility and mechanisms of
beta-lactam resistance in 1310 strains of Pseudomonas
aeruginosa: a French multicentre study (1996). J Antimicrob
Chemother 2000;46:1336.
[44] Gales AC, Jones RN, Turnidge J, Rennie R, Ramphal R.
Characterization of Pseudomonas aeruginosa isolates:
occurrence rates, antimicrobial susceptibility patterns, and
molecular typing in the global SENTRY Antimicrobial
Surveillance Program, 19971999. Clin Infect Dis
2001;32(Suppl. 2):S14655.
[45] Tsuji M, Takema M, Miwa H, Shimada J, Kuwahara S. In
vivo antibacterial activity of S-3578, a new broad-spectrum
cephalosporin: methicillin-resistant Staphylococcus aureus
and Pseudomonas aeruginosa experimental infection models.
Antimicrob Agents Chemother 2003;47:250712.
[46] Takeda S, Nakai T, Wakai Y, Ikeda F, Hatano K. In vitro and
in vivo activities of a new cephalosporin, FR264205, against
Pseudomonas aeruginosa. Antimicrob Agents Chemother
2007;51:82630.
[47] Khorasani G, Salehifar E, Eslami G. Profile of
microorganisms and antimicrobial resistance at a tertiary
care referral burn centre in Iran: emergence of Citrobacter
freundii as a common microorganism. Burns 2008;34:94752.
[48] Strateva T, Ouzounova-Raykova V, Markova B, Todorova A,
Marteva-Proevska Y, Mitov I. Problematic clinical isolates of
Pseudomonas aeruginosa from the university hospitals in
Sofia, Bulgaria: current status of antimicrobial resistance
and prevailing resistance mechanisms. J Med Microbiol
2007;56:95663.
[49] Chaudhury A. In vitro activity of cefpirome: a new fourth
generation cephalosporin. Indian J Med Microbiol
2003;21:525.
[50] Gonzalez 3rd LS, Spencer JP. Aminoglycosides: a practical
review. Am Fam Physician 1998;58:181120.
1025
[51] Poole K. Aminoglycoside resistance in Pseudomonas
aeruginosa. Antimicrob Agents Chemother 2005;49:47987.
[52] Cavallo JD, Hocquet D, Plesiat P, Fabre R, Roussel-Delvallez
M. Susceptibility of Pseudomonas aeruginosa to
antimicrobials: a 2004 French multicentre hospital study. J
Antimicrob Chemother 2007;59:10214.
[53] Miller GH, Sabatelli FJ, Hare RS, Glupczynski Y, Mackey P,
Shlaes D, et al. The most frequent aminoglycoside
resistance mechanismschanges with time and
geographic area: a reflection of aminoglycoside usage
patterns? Aminoglycoside Resistance Study Groups. Clin
Infect Dis 1997;24(Suppl. 1):S4662.
[54] Stone HH. Review of pseudomonas sepsis in thermal burns:
verdoglobin determination and gentamicin therapy. Ann
Surg 1966;163:297305.
[55] Acar JF, Goldstein FW. Trends in bacterial resistance to
fluoroquinolones. Clin Infect Dis 1997;24(Suppl. 1):S6773.
[56] Messadi AA, Lamia T, Kamel B, Salima O, Monia M, Saida
BR. Association between antibiotic use and changes in
susceptibility patterns of Pseudomonas aeruginosa in an
intensive care burn unit: a 5-year study, 20002004. Burns
2008;34:1098102.
[57] Fedler KA, Biedenbach DJ, Jones RN. Assessment of
pathogen frequency and resistance patterns among
pediatric patient isolates: report from the 2004 SENTRY
Antimicrobial Surveillance Program on 3 continents. Diagn
Microbiol Infect Dis 2006;56:42736.
[58] Karlowsky JA, Jones ME, Thornsberry C, Evangelista AT, Yee
YC, Sahm DF. Stable antimicrobial susceptibility rates for
clinical isolates of Pseudomonas aeruginosa from the 2001
2003 tracking resistance in the United States today
surveillance studies. Clin Infect Dis 2005;40(Suppl. 2):
S8998.
[59] Gold HS, Moellering Jr RC. Antimicrobial-drug resistance. N
Engl J Med 1996;335:144553.