Spread of extended-spectrum β-lactamase genes of bla OXA-10, bla PER-1 and bla CTX-M in Pseudomonas aeruginosa strains isolated from burn patients

JBUR-4301; No. of Pages 6

Spread of extended-spectrum b-lactamase genes ofbla OXA-10, bla PER-1 and bla CTX-M in Pseudomonasaeruginosa strains isolated from burn patients

Zahra Farshadzadeh a, Azar Dokht Khosravi a,b,*,Seyed Mohammad Alavi a, Najmeh Parhizgari a, Hajar Hoveizavi a

aHealth Research Institute, Infectious and Tropical Diseases Research Center, Ahvaz Jundishapur University of

Medical Sciences, Ahvaz, IranbDepartment of Microbiology, School of Medicine, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran

b u r n s x x x ( 2 0 1 4 ) x x x – x x x

a r t i c l e i n f o

Article history:

Accepted 12 February 2014

Keywords:

P. aeruginosa

ESBL producing

Burn

DDST

PCR

a b s t r a c t

Background: Pseudomonas aeruginosa is resistant to many antibiotics due to production of

different classes of extended spectrum b-lactamases (ESBLs). Prevalence of ESBLs among P.

aeruginosa has been increased in recent years, demonstrate a serious health problem

especially in burn units worldwide.

Objective: Present study was designed to determine the ESBL producing strains and identify

the genes encoding three different ESBLs of bla PER-1, bla OXA-10 and bla CTX-M genes in P.

aeruginosa isolates from burn patients.

Methods: In total 185 clinical isolates of P. aeruginosa were collected from infectious wounds

of hospitalized burn patients. Antimicrobial susceptibility testing and phenotypic detection

of ESBL were performed by disk diffusion method and Double disk Synergy Test (DDST).

Polymerase Chain Reaction (PCR) was done for detection of bla OXA-10, bla PER-1 and bla

CTX-M ESBL encoding genes.

Results: In total, 176 (95.13%) isolates were multidrug resistant. The DDST demonstrated 96

(51.9%) isolates as putative ESBL producers with 100% or highly resistance to ofloxacin,

cephalexin, aztreonam (97.57%) and ceftriaxone (91.6%). By PCR amplification, bla PER-1, bla

OXA-10 and bla CTX-M genes were detected in 52 (54.16%), 66 (68.75%) and 1 (1.04%) isolates

of ESBL producers respectively. Forty-three isolates (44.79%) were simultaneously positive

for both bla OXA-10 and bla PER-1 related genes.

Conclusion: The rate of ESBL producing P. aeruginosa was notable in present study. Since

there are only limited effective antibiotics against the bacterium, therefore all isolates must

be investigated by antimicrobial susceptibility testing, which limits resistance development

in burn units and helps the management of treatment strategy.

# 2014 Elsevier Ltd and ISBI. All rights reserved.

* Corresponding author at: Health Research Institute, Infectious and Tropical Diseases Research Center, Ahvaz Jundishapur University ofMedical Sciences, Ahvaz, Iran. Tel.: +98 6113330074; fax: +98 611 3332036.

E-mail addresses: [email protected], [email protected] (A.D. Khosravi).

Available online at www.sciencedirect.com

ScienceDirect

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

Please cite this article in press as: Farshadzadeh Z, et al. Spread of extended-spectrum b-lactamase genes of bla OXA-10, bla PER-1 and bla CTX-M inPseudomonas aeruginosa strains isolated from burn patients. Burns (2014), http://dx.doi.org/10.1016/j.burns.2014.02.008

http://dx.doi.org/10.1016/j.burns.2014.02.0080305-4179/# 2014 Elsevier Ltd and ISBI. All rights reserved.

http://dx.doi.org/10.1016/j.burns.2014.02.008

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b u r n s x x x ( 2 0 1 4 ) x x x – x x x2

1. Introduction

Gram-negative pathogens have long been known to cause the

most severe infections in burn patients. Among them,

Pseudomonas aeruginosa is the second leading cause of

nosocomial infection and increasingly recognized as the

etiological agent of serious infections in burn hospitalized

patients [1–3].

P. aeruginosa is physiologically resistant to many antibio-

tics, disinfectants and against extended-spectrum cephalos-

porins, such as cefotaxime, ceftriaxone and ceftazidime due to

produce different class of extended spectrum b-lactamases

(ESBLs) and prevalence of the ESBLs among P. aeruginosa has

been increased [1,4,5]. The broad spectrum antibiotics such as

ceftazidime and other third generation cephalosporins are

used in hospitals excessively and exerts selective pressure on

bacteria, thereby promoting infections by multi-drug resistant

strains [6].

Among ESBLs reported in P. aeruginosa, Ambler class A are

of medical significance and comprises several enzymes

including Pseudomonas extended resistance (PER-1). PER-1

which is produced only by P. aeruginosa, was initially detected

from a Turkish patient hospitalized in France in 1993 [7]. This

enzyme has strong hydrolytic activity against cephalosporins

and confers resistance to penicillins, cefotaxime, ceftazidime,

and aztreonam but, like most ESBLs of the TEM and SHV type,

cannot hydrolyze carbapenems and cephamycins, its activity

is well inhibited by clavulanate, sulbactam and tazobactam

[7,8].

Oxacillinase (OXA ESBL), class D b-lactamases, which

hydrolyses oxacillin, is reported in P. aeruginosa but have

been detected in many other gram-negative bacteria, includ-

ing Enterobacteriaceae. The ESBLs including OXA-11, OXA-14,

OXA-16, OXA-17, OXA-19 and OXA-28 are related structurally

to OXA-10. OXA ESBLs exhibit appreciable diversity in their

enzymic activities. OXA-10 and OXA-13 weakly hydrolyse

cefotaxime, ceftriaxone and aztreonam, thus providing most

organisms with reduced susceptibility to these antibiotics.

Most OXA-10-derived ESBLs confer greater resistance to

cefotaxime, and confer significant resistance to ceftazidime

and aztreonam. The majority of OXA-type enzymes are

resistant to b-lactamase inhibitors [8].

Another class of ESBL enzyme is cefotaximase-Munich

(CTX-M), class A b-lactamase, which is active against

cefotaxime and by hydrolyzing that confer resistance to

cefotaxime preferentially over ceftazidime and exhibit a

higher susceptibility to tazobactam than to clavulanic acid.

Since 1995 a rapid increase in the number of variants

producing CTX-M has been reported, especially among

enterobacterial isolates from hospitalized patients. In 1989,

the CTX-M type was reported as a new ESBL family member

not belonging to either the TEM or SHV types and was reported

among E. coli isolates from Greece [9,10]. Recently, PCR and

sequence analysis revealed the presence of the blaCTX-M-1

gene in the P. aeruginosa [11].

Due to increasing resistance of P. aeruginosa to several

ESBLs, the objectives of present study were to determine

antibiotic susceptibility patterns against different antibiotics,

detection of ESBL producing strains by double disk synergy test

Please cite this article in press as: Farshadzadeh Z, et al. Spread of extendPseudomonas aeruginosa strains isolated from burn patients. Burns (2014)

(DDST) and identify the prevalence of genes encoding three

different ESBLs including bla PER-1, bla OXA-10 and bla CTX-M in

clinical isolates of P. aeruginosa from infected hospitalized

burn patients.

2. Materials and methods

2.1. Bacterial isolates

A total of 185 non-duplicated clinical isolates of P. aeruginosa

were collected from infected wounds of burn patients in the

Taleghani burn Hospital, Ahvaz, Iran, during one year period

(2010–2011). The study was approved by Institutional Ethics

Committee after submission of preliminary proposal of the

study. All samples were collected from wounds of burn

patients and were transferred to the laboratory of Infectious

and Tropical diseases research center. The sampling proce-

dure from wound included swabs that were taken from

clinically deep areas of the burn wounds when clinical signs of

wound infection occurred.

The isolates were identified as P. aeruginosa by application

of culture (cultivation on McConkey agar and Blood agar for

preliminary isolation) and standard biochemical tests includ-

ing SIM, MRVP, grow aerobically in Oxidation Fermentation

(OF) medium and pigment production in Mueller Hinton agar

[12]. All culture media were purchased from Himedia, India. P.

aeruginosa ATCC 27853 was used as a control strain.

2.2. Antimicrobial susceptibility testing

Antimicrobial susceptibility testing of isolates were performed

by disk diffusion method according to Clinical and Laboratory

Standards Institute (CLSI) guidelines [13], using following

antibiotic disks: piperacillin-tazobactam (PTZ; 100/10), oflox-

acin (OFX; 5 mg), cephalexin (CN; 30 mg), cefepime (CPM; 30 mg),

cefotaxime (CTX; 30 mg), ceftazidime (CAZ; 30 mg), cefteriaxone

(CTR; 30 mg), ciprofeloxacin (CIP; 30 mg), imipenem (IMI; 10 mg),

meropenem (MEM; mg), and aztreonam (ATM; 30 mg) (MAST

Co., UK). The test were performed by preparation of standard

bacterial suspension equal to 0.5 McFarland and inoculated in

Muller Hinton agar and the antibiotic disks were placed in the

plate at identical distances. Plates were incubated for 16–24 h

at 35 8C. The diameter of zone of growth inhibition were

measured and compared with standard values.

2.3. Phenotypic detection of ESBL

Isolates with intermediate susceptibility or resistance to

ceftazidime, cefotaxime, cefepime, cefteriaxone or aztreonam

were selected to identify the ESBL production. Detection of

ESBL production was performed by combined double disk

synergy test (DDST) as per CLSI guideline [13]. Disks containing

ceftazidime and ceftazidime/clavulanic acid (30/10 mg), cefo-

taxime and cefotaxime/clavulanic acid (30/10 mg) and cefe-

pime and cefepime/clavulanic acid (30/10 mg) were placed at a

distance of 15 mm center to center on Muller Hinton agar

plate. Plates were incubated overnight at 35 8C. A positive test

result was defined as a �5 mm increase in zone diameter

compared to a disk without clavulanic acid.

ed-spectrum b-lactamase genes of bla OXA-10, bla PER-1 and bla CTX-M in, http://dx.doi.org/10.1016/j.burns.2014.02.008


Table 1 – Primers used for detection of ESBL genes by PCR.

Primer name 50-Sequence-30 Detected gene Molecular weight References

CTX-M F: CGCTTTGCGATGTGCAG bla CTX-M 552 bp [22]

R: ACCGCGATATCGTTGGT

OXA-10 ABD1: TAT CGC GTG TCT TTC GAG TA bla OXA-10 760 bp [23]

ABD4: TTA GCC ACC AAT GAT GCC

PER-1 F: ATG AAT GTC ATT ATA AAA GC bla PER-1 927 bp [24]

R: TTA ATT TGG GCT TAG GG

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2.4. Polymerase Chain Reaction (PCR) for detection of bla

OXA-10, bla PER-1 and bla CTX-M genes

DNA extracted from colonies of all confirmed P. aeruginosa

isolates by simple boiling method as described elsewhere [14].

PCR amplification was carried out in a final volume of 25 ml,

using the previously reported primers based on bla CTX-M, bla

OXA-10, and bla PER-1 genes as presented in Table 1. The accuracy

of primers were initially confirmed using NCBI/nucleotide

blast at: www.ncbi.nlm.nih.gov/tools/primer-blast/. The com-

position of PCR mixture was: 10X PCR Buffer, 50 mM MgCl2,

10 mM dNTPs, 10 mM of each primer, 500Unit Taq DNA

Polymerase, and 2 ml of template DNA. The amplification

program was consisted of initial denaturation at 95 8C for

5 min, 30 cycles of denaturation at 94 8C for 1 min, annealing at

48 8C for bla PER-1, 57 8C for bla OXA-10 and 55 8C for bla CTX-M for

1 min, extension at 72 8C for 1 min and a final extension at

72 8C for 5 min. SPSS software (SPSS Inc no. 13) was used for

data analysis.

3. Results

Antimicrobial susceptibility test revealed that 176 (95.13%) P.

aeruginosa isolates, were multidrug resistant by simultaneous

resistance to cephalexin, ofloxacin, aztreonam, cefotaxime

and ceftriaxone. The DDST demonstrated 96 (51.9%) isolates as

putative ESBL producers. These isolates were 100% resistant to

ofloxacin and cephalexin and were highly resistant to

aztreonam (97.57%) and ceftriaxone (91.6%). The remaining

89 (48.1%) isolates were ESBL negative. These were 100% or

Table 2 – Frequency of ESBLs producing strains and susceptib

Antimicrobial agents ESBL positive (96)

R (%) I (%)

ATM 94 (97.57) 1 (1.04)

CIP 22 (22.9) 15 (15.62)

OFX 96 (100) 0

CAZ 70 (72.9) 3 (3.12)

CPM 75 (78.12) 6 (6.25)

IMI 39 (40.6) 15 (15.62)

MEM 69 (71.8) 0

CTX 82 (85.4) 4 (4.16)

CTR 88 (91.6) 3 (3.12)

PTZ 74 (77) 5 (5.2)

CN 96 (100) 0

R, resistance; S, sensitive; I, intermediate, ATM, aztreonam; CIP, cipr

imipenem; MEM, meropenem; CTX, cefotaxime; CTR, cefteriaxone; PTZ,

Please cite this article in press as: Farshadzadeh Z, et al. Spread of extendPseudomonas aeruginosa strains isolated from burn patients. Burns (2014),

highly resistant to ofloxacin, cephalexin, aztreonam, cefotax-

ime, and cefepime (Table 2). By PCR amplification, all 96

isolates were confirmed for comprising ESBL encoding genes.

Based on the results, 66 (68.75%) and 52 (54.16%) of ESBL

producer isolates comprised bla OXA-10 (Fig. 1) and bla PER-1

(Fig. 2) related genes respectively.

Forty three isolates (44.79%), were simultaneously positive

for both bla OXA-10 and bla PER-1 related genes. The isolates with

bla OXA-10 gene, were 100% resistant to aztreonam, ofloxacin,

meropenem, ceftriaxone, cephalexin and showed high to

moderate resistance to other tested antibiotics except for

ciprofloxacin, while isolates with bla PER-1 gene, were 100%

resistant to all antibiotics except for ciprofloxacin (Table 3).

Three genes of bla OXA-10, bla PER-1 and bla CTX-M (Fig. 3), were

discovered in only one isolate (1.04%), which was resistant to

ceftazidime, cefotaxime, cefepime, imipenem, meropenem

and aztreonam.

4. Discussion

The current study demonstrated a high antibiotic resistance

among P. aeruginosa strains isolated from infectious burn

patients in the burn center of Ahvaz, Iran. The majority of

antibiotics comprised less than 50% effectiveness against P.

aeruginosa isolates except for ciprofloxacin with 61.45% and

51.6% sensitivity among ESBL positive and ESBL negative

strains (based on DDST) respectively. All isolates were entirely

resistant to cephalexin, ofloxacin and aztreonam. Though

piperacillin-tazobactam is an effective antibiotic against P.

aeruginosa infections [15], but in this study, isolates showed

ility patterns to antimicrobial agents.

ESBL negative (89)

S (%) R (%) I (%) S (%)

1 (1.04) 88 (98.8) 0 1 (1.18)

59 (61.45) 30 (33.7) 13 (14.6) 46 (51.6)

0 89 (100) 0 0

23 (23.9) 79 (88.76) 0 10 (11.23)

15 (15.62) 82 (92.13) 0 7 (7.86)

42 (43.75) 16 (17.9) 28 (31.46) 45 (50.56)

27 (28.12) 42 (47.19) 6 (6.74) 41 (46)

10 (10.41) 85 (95.5) 1 (1.12) 3 (3.37)

5 (5.2) 77 (86.5) 1 (1.12) 11 (12.35)

17 (17.7) 69 (77.52) 3 (3.37) 17 (19.1)

0 89 (100) 0 0

ofeloxacin; OFX, ofloxacin; CAZ, ceftazidime; CPM, cefepime; IMI,

piperacillin-tazobactam; CN, cephalexin.

ed-spectrum b-lactamase genes of bla OXA-10, bla PER-1 and bla CTX-M in http://dx.doi.org/10.1016/j.burns.2014.02.008

http://www.ncbi.nlm.nih.gov/tools/primer-blast/


Fig. 1 – Agarose gel electrophoresis of PCR products of bla

CTX-M gene. Lanes: 1, molecular size marker; 2, negative

control; 3, positive control; 4, 5, positive samples for bla

CTX-M gene; 6, negative sample.


OXA-10 gene. Lanes: 1, molecular size marker; 2, negative

control; 3, positive control; 4–6 positive samples for bla

OXA-10 gene; 7, 8, negative samples.

b u r n s x x x ( 2 0 1 4 ) x x x – x x x4


high resistance to this antibiotic (77%). The resistance rates

obtained in this study were slightly different from those

recently reported by Mirsalehian et al. form Iran [16]. In their

study, the rate of multidrug resistance was reported as 87%,

and the rate of ESBL producers was 39.41%, which was both

lower than our study. Although in concordant to them, the

isolates showed high resistance to meropenem and cefotax-

ime.

Though carbapenems such as imipenem, meropenem, and

b-lactams such as pipracillin-tazobactam are useful in their

antipseudomonal behavior [17], however in our study, ESBL

producing strains with bla OXA-10, bla PER-1 and bla CTX-M genes

showed high level of resistance to meropenem, and pipra-

cillin-tazobactam and moderate sensitivity to imipenem.

These findings suggest that resistance to cephalosporins

and carbapenemases could be associated with other mecha-

nisms of resistance. These mechanisms are included overpro-

duction of AmpC, a cephalosporinase expressed by

chromosomal gene of P. aeruginosa, which causes the most

common mechanism of resistance to b-lactams including

Table 3 – Frequency of ESBLs producing strains and susceptibiand bla PER-1.

Antimicrobial agents bla OXA-10 positive (66)

R (%) I (%)

ATM 66 (100) 0

CIP 0 6 (9)

OFX 66 (100) 0

CAZ 46 (69.9) 3 (4.54)

CPM 37 (56) 11 (16.66)

IMI 59 (89.4) 7 (10.6)

MEM 66 (100) 0

CTX 56 (84.8) 5 (7.57)

CTR 66 (100) 0

PTZ 49 (74.2) 3 (4.54)

CN 66 (100) 0

R, resistance; S, sensitive; I, intermediate, ATM, aztreonam; CIP, cipr

imipenem; MEM, meropenem; CTX, cefotaxime; CTR, cefteriaxone; PTZ,


ESBLs (e.g., ceftazidime) and penicillins, and decreased outer-

membrane permeability via loss or alteration of the outer

membrane porin protein such as OprD, which is the most

common mechanism of resistance to the carbapenems

(including imipenem) in P. aeruginosa [14]. Since carbapenems

(e.g., imipenem) interestingly, have excellent activity against

AmpC+ P. aeruginosa strains, so, existence of other mecha-

nisms of resistance such as loss of OprD could be the reason of

high to moderate resistance to carbapenemes among P.

aeruginosa strains in current study [18]. This explanation

may be true for 89 remaining non-ESBL producing isolates as

well, which showed high antibiotic resistance in this study.

The overall detection rate of bla OXA-10, bla PER-1 and bla CTX-M

were as 68.75%, 54.16% and 2.3% respectively. Even higher

resistance was observed in isolates comprising bla PER-1 gene.

The results were slightly different from prevalence of bla OXA-10

and bla PER-1 have demonstrated by other investigators from

Iran. In study of Shahcheraghi et al. [3], which the P. aeruginosa

isolates from Kerman city were screened, the rate of bla OXA-10

and bla PER-1 reported as 92.7% and 68.3% respectively, which

lity patterns to antimicrobial agents in relation to bla OXA-10

bla PER-1 positive (52)

S (%) R (%) I (%) S (%)

0 52 (100) 0 0

60 (90.9) 4 (7.6) 13 (25) 35 (67.3)

0 52 (100) 0 0

17 (25.75) 52 (100) 0 0

18 (27.27) 48 (92.3) 4 (7.7) 0

0 52 (100) 0 0

0 52 (100) 0 0

5 (7.57) 52 (100) 0 0

0 52 (100) 0 0

14 (21.2) 52 (100) 0 0

0 52 (100) 0 0

ofeloxacin; OFX, ofloxacin; CAZ, ceftazidime; CPM, cefepime; IMI,

piperacillin-tazobactam; CN, cephalexin.




PER-1 gene. Lanes: 1, molecular size marker; 2, negative

control; 3, positive control; 4, 5, 7, positive samples for bla

PER-1 gene; 6, 8, negative samples.

b u r n s x x x ( 2 0 1 4 ) x x x – x x x 5


was higher than our findings. However the lower rate of bla PER-

1 was previously reported from isolates collected in Tehran

hospitals by the same investigators [19]. Besides in another

study conducted by Mirsalehian et al. [16], compared to us,

lower rates of bla OXA-10 and bla PER-1 as 39.11% and 49.25%

respectively were reported from Tehran. This variation in

prevalence of ESBL encoding genes shows that the distribution

of such resistance may be different in various settings.

Moreover, the prevalence of bla PER-1 (62.75%) in Ahvaz, Iran,

was higher than Italy (34.61%) [20], Hungary (1.3%) and

Belgium (2%) [21], and lower than Turkey (86%) [7].

In conclusion, the rate of ESBL producing P. aeruginosa is

notable in present study and demonstrates a significant health

problem and deserves merits more attention. Since there are

only limited effective antibiotics against the bacterium, all

isolates must be investigated by antimicrobial susceptibility

testing. Performance of this test limits indiscriminately use of

antibiotics and resistance development in burn units and

helps management of treatment strategy.

Conflict of interest

The authors declare that there is no conflict of interest.

Acknowledgements

This work has been approved in Infectious and Tropical

Diseases Research Center of our University and financially

supported by a grant (no. 88103) from Ahvaz Jundishapur

University of Medical Sciences, Ahvaz, Iran. Special thanks to

research affairs of the university, for their continues support.

Our appreciation goes to the laboratory staff of Taleghani Burn

hospital of Ahvaz for providing the samples.

Please cite this article in press as: Farshadzadeh Z, et al. Spread of extendPseudomonas aeruginosa strains isolated from burn patients. Burns (2014),

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Spread of extended-spectrum β-lactamase genes of bla OXA-10, bla PER-1 and bla CTX-M in Pseudomonas aeruginosa strains isolated from burn patients