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Prevalence and antimicrobial resistance

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Volume 6 Number 3 (June 2014) 163-168

Prevalence and antimicrobial resistance pattern of methicillin resistant

Staphylococcus aureus (MRSA) strains isolated from clinical specimens
in Ardabil, Iran

Solmaz Dibah1, Mohsen Arzanlou2*, Elham Jannati3, Reza Shapouri1

1
Department of Microbiology, Zanjan Branch, Islamic Azad University, Zanjan, Iran. 2Department of Microbiology,
School of Medicine, Ardabil University of Medical Sciences, Ardabil, Iran. 3Young Researchers Club, Ardabil
Branch, Islamic Azad University, Ardabil, Iran.

Received: December 2013, Accepted: April 2014.

ABSTRACT

Background and Objective: Reports on MRSA strains are increasing worldwide. The aim of this study was to find the
prevalence of MRSA strains isolated from clinical specimens and to evaluate their resistance profile. Additionally we
compared the phenotypic and genotypic methods for detection of methicillin resistance.
Materials and Methods: In this cross-sectional study, a total of 41 isolates of S. aureus were collected from clinical
specimens at two teaching hospitals in Ardabil, Iran. All isolates were identified at the species level by standard biochemical
tests. The methicillin resistance were evaluated using three methods: PCR for mecA gene, agar dilution for determination
of oxacillin MIC and disk diffusion test to detect methicillin, oxacillin and cefoxitin resistance. Antimicrobial resistance
patterns were determined by disk diffusion method.
Results: The results identified 19 (46.3 %) out of 41 isolates as MRSA. Most of the MRSA strains (68.4%) were isolated
from patients hospitalized in ICU. All isolates were susceptible to vancomycin, mupirocin and linezolid. Among other
antibiotics co-trimoxazole was more active against MRSA isolates. Using PCR as reference method all the phenotypic tests
showed 100% specificity. The sensitivity for MIC test and cefoxitin was 100% and for methicillin and oxacillin disks was
77.7% and 89.5%, respectively.
Conclusion: The prevalence of MRSA strains in our hospitals especially in ICU ward was high and disk diffusion testing
using cefoxitin or oxacillin MIC test as an alternative to PCR for detection of MRSA is recommended.

Keywords: Staphylococcus aureus, Methicillin resistance, Antibiotic resistance

INTRODUCTION infections as a major therapeutic challenge (2).

Initially MRSA infections were observed in
Staphylococcus aureus is one of the most important hospitalized patients and those with chronic illnesses.
and frequent cause of nosocomial infections These types of infections are caused by strains named
worldwide (1). Emergence of methicillin-resistant S. as hospital-associated MRSA (HA-MRSA) (3). In
aureus strain (MRSA) in 1961 made staphylococcal 1990s another type of MRSA strain was emerged
that primarily causes skin and soft tissue infections
in healthy people. It is called community-associated
*Corresponding Author: Dr. Mohsen Arzanlou MRSA (CA-MRSA) (3). MRSA strains show
Address: Department of Microbiology, School of Medicine, distinct microbiological, therapeutic and clinical
Ardabil University of Medical Sciences, Ardabil, Iran. features compared to their methicillin-susceptible
Tel: +98-451-5512788 (MSSA) counterparts. From microbiological aspect,
E-mail: [email protected] HA-MRSA strains are resistant to multiple classes

163
Dibah ET AL .

of antibiotics. This characteristic limits proper Himedia (Himedia Laboratories, Pvt. Ltd., Mumbai,
therapeutic options against staphylococcal infections India) and oxacilllin powder for MIC determination
(4). Clinically, infections caused by HA-MRSA strains was purchased from Sigma-Aldrich (St. Louis, MO,
are associated with higher mortality and morbidity USA). All tests were compared for sensitivity and
(5). Some CA-MRSA strains express additional specificity with PCR for mecA gene as reference
virulence factors that enable them to causes more method. Sensitivity was calculated by dividing
serious diseases (6). the number of mecA-positive isolates detected as
Currently, MRSA strains account for many of resistant using phenotypic methods by the total
staphylococcal infections and reports of MRSA strains number of mecA-positive strains (ether susceptible or
are increasing worldwide (7). There are also several resistant). Specificity was calculated through dividing
reports from Iran showing the prevalence of methicillin the number of mecA-negative isolates classified as
resistance among clinical isolates of S. aureus (8-11). sensitive based on phenotypic criteria by the total
A meta-analysis study recently carried out in Iran by number of mecA-negative isolates (15).
Askari et al., showed that the average prevalence rate
of MRSA isolates among clinical specimens were Antimicrobial susceptibility testing. The isolates
52.7% (12). Understanding the prevalence, antibiotic were tested for antibiotic sensitivity using the Kirby
resistance patterns and information on accurate and Bauer disk diffusion method by employing the
reliable detection methods of MRSA strains are following disks (disk); penicillin (10) co-amoxiclav
necessary for appropriate antibiotic treatment and (30), chloramphenicol (30), tetracycline (30),
effective infection control. Considering these, the ciprofloxacin (10), ceftriaxone (100), cefazolin (30),
current study was performed to find the prevalence clindamycin (2), imipenem (10), co-trimoxazole (25),
and evaluate the antimicrobial resistance profile of rifampicin (30), gentamicin (10) pristinamycin (15),
MRSA strains isolated from clinical specimens in linezolid (30) and mupirocin (5). MICs of oxacillin
Ardabil, the northwest region of Iran. Additionally and vancomycin to the both MRSA and MSSA
we compared the phenotypic and genotypic methods isolates were determined by agar dilution method. All
for detection of methicillin resistance. procedures were carried out and interpreted according
to CLSI guideline (13). S. aureus ATCC 25923, ATCC
MATERIALS AND METHODS 29213 and ATCC 33591 were used as control strains in
disk diffusion and agar dilution methods.
Bacterial Isolates. From July to December 2011,
a total of 41 S. aureus isolates were collected from PCR amplification of mecA gene. Total bacterial
patients admitted to two teaching hospitals affiliated DNA was extracted from S. aureus using
to Ardabil University of Medical Sciences. Isolates DNP Genomic DNA Extraction Kit (Cinagen,
were examined by conventional methods such as Tehran, Iran). Oligonucleotide primers (14):
colony morphology on blood agar, Gram stain 5- AAAATCGATGGTAAAGGTTGGC-3(forward)
characteristics and catalase production then identified and 5- AGTTCTGCAGTACCGGATTTGC-3 (revers)
as S. aureus by tube coagulase and DNase tests. were synthesized by Bioneer company (Daejon, South
Identified strains were stored at -80C in Mueller- Korea). PCR was performed in a 20 L AccuPower
Hinton broth containing 15% glycerol. PCR PreMix (Bioneer) with 10pmol of each primers
under the following conditions: initial denaturation at
Determination of methicillin resistance. Methicillin 95C for 5min, followed by 34 cycles of 95C for 1
resistance was evaluated using three methods: 1) min, 55C for 1min and 72C for 1min, and a final
Disk diffusion test using 30 g cefoxitin disk ( 21 incubation at 72C for 5min. The amplified DNA
mm indicated MRSA), 1 g oxacillin disk ( 10 mm fragments (PCR product: 533 bp) were separated on
indicated MRSA), and 5 g methicillin disk ( 9 1% (w/v) agarose gel, stained with ethidium bromide
mm indicated MRSA); 2) Oxacillin MIC (Minimum and visualized under ultraviolet light. S. aureus ATCC
Inhibition Concentration) test ( 4 g/ml indicated 29213 and ATCC 33591were used as mecA negative
MRSA); and 3) Polymerase chain reaction (PCR) and positive controls respectively.
for the detection of mecA gene (positive indicated
MRSA) (13,14). Antibiotic disks were obtained from Statistical analysis. Chi-square test was used to

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 METHICILLIN RESISTANT SATPHYLOCOCCUS AUREUS IN ARDABI

Table 1. Prevalence of S. aureus among clinical specimens in relationship with specimen type.
Specimen type MSSA n (%) MRSA n (%) Total
Sputum 6 (27.3) 11 (57.8) 17
Blood 6 (27.3) 3 (15.7) 9
Urine 9 (40.9 ) 1(5.2) 10
Wound 1 (4.5) 3 (15.7) 4
Cerebral spinal fluid - 1(5.2) 1
Total 22 (100) 19 (100) 41

Table 2. Prevalence of S. aureus among clinical specimens in relationship with hospital wards.
Ward MSSA n (%) MRSA n (%)
Emergency 2 (13.3) 2 (11.1)
Surgery 1 (6.6) 3 (16.6)
Infectious 4 (26.6) -
Intensive care unit 3 (20) 13 (68.4)
Outpatient (Clinic) 4 (26.6) -
Total 22 (100) 19 (100)

compare the prevalence of MRSA and MSSA strains The MICs for oxacillin and vancomycin are listed
between specimen type and hospital wards. in Table 3. The MICs for oxacillin were between
64 to 512 g/mL and 0.25 to 1 g/mL for
RESULTS MRSA and MSSA strains respectively. The MICs for
vancomycin against both MRSA and MSSA strains
A total of 41 non duplicate S. aureus isolates were 1 g/mL. Only, 1 MRSA strain showed MIC
including 22 (53.6%) MSSA and 19 (46.3%) MRSA equal to 2 g/mL. These strains did not fall into
were isolated from different clinical specimens that vancomycin resistant category according to CLSI (13).
have been sent to the Microbiology Laboratory. Table 4 represents the resistance pattern of S. aureus
The prevalence of MRSA was significantly higher isolates (MRSA and MSSA) to the tested antibiotics. In
(P = 0.0001) in sputum (n = 11, 57.8%) than other this study the entire S. aureus isolates were susceptible
specimens respectively (Table 1). The majority of to vancomycin, mupirocin and linezolid. Among other
isolates with MSSA phenotype were cultured from antibiotics imipenem and co-trimoxazole showed to be
urine specimens (n = 9, 40.9%). the most effective antibiotics against MRSA isolates.
Table 2 shows the distribution of isolate in PCR testing revealed the presence of mecA gene in all
relationship with hospital wards. The prevalence of isolates (Fig 1) which were determined as methicillin
MRSA isolates (68.4%) were significantly higher resistant by the phenotypic methods. The sensitivities
(P = 0.0001) in patients from intensive care unit of oxacillin MIC test and cefoxitin disk were 100%,
(ICU). MRSA accounted for about 81.25% of S. whereas the sensitivities of methicillin and oxacillin
aureus strains from patients at ICU. disks were 77.7% and 89.5% respectively.

Table 3. Frequency and range of oxacillin and vancomycin MICs of S. aureus (MRSA and MSSA) isolated from clinical
specimens by agar dilution method.
MIC Oxacillin MIC Vancomycin
g/ml MRSA, n (%) MSSA, n (%) g/ml MRSA, n (%) MSSA, n (%)
0.25 - 14 (63.6) 1 18 (94.7) 22 (100)
0.5 - 2 (9) 2 1 (5.3) -
1 - 6 (27.2)
64 2 (25)
128 1(12.5 )
512 16 (62.5)

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Dibah ET AL .

prevalence reported for MRSA infection in the

different studies. The heterogeneity is probably due
to applying different infection control measures,
antibiotic administration, human population, study
design and laboratory testing for determining
methicillin resistance (12). In this study methicillin
and oxacillin disks could not detect all MRSA isolates
but cefoxitin disk and oxacillin MIC test showed the
Fig1. PCR detection of mecA gene among S. aureus
sensitivity equal to PCR. These results are similar to
isolates. Lane M: 50 pb DNA size marker, Lane 1: positive
the previous reports (16). However, the emergence
control strain ATCC 33591. Lane 2: negative control strain
ATCC 29213. Lanes 3, 5, 6 and 9 mecA positive isolates. of mecA positive oxacillin susceptible and mecA
Lanes: 4, 7 and 8 mecA negative isolates. negative oxacillin resistantMRSA strains reduces
the sensitivities of both the phenotypic and genotypic
DISCUSSION methods (17-19). Thus, combination of genotypic and
phenotypic tests is necessary to detect the methicillin
Since the emergence of MRSA in 1961, there resistance in S. aureus accurately.
has been a steady increase in the prevalence of this MRSA infections pose a significant concern for
type of S. aureus strains worldwide (7). Currently, ICU patients (19). In this study, the incidence rate
more than 50% of S. aureus infections are caused of MRSA infection in ICU patients was significantly
by MRSA strains in the US (3). The reports from higher than other wards, with an estimated prevalence
Iran also indicate the increasing incidence of MRSA as high as 68.4% and within ICU MRSA strains were
in clinical specimens over the time (8-12). In this responsible for about 81% of S. aureus infections.
study out of 41, 19 (46.3%) of isolates were MRSA Previously it has been documented that MRSA
strains. Worldwide, HA-MRSA prevalence varies accounted for 57% of all ICU acquired S. aureus
considerably, from <1 percent in Scandinavia to infections (19). However, recent reports indicate
>50 percent in other countries (7). The estimated declining ICU acquired MRSA infections with
prevalence in our study locates in upper limits of applying appropriate infection control measures,
the reported ranges. However there is not a uniform rapid and reliable detection of methicillin resistance

Table 4. Antibiotic susceptibility profiles of S. aureus strains isolated from clinical specimens by disk diffusion method.
MSSA (N = 22), n (%) MRSA (N = 19), n (%)
Antibiotic Susceptible Intermediate Resistant Susceptible Intermediate Resistant
Vancomycina 22 (100) - - 19 (100) - -
Penicillin 6 (27.2) - 16 (72.7) - - 19 (100)
Co-amoxiclav 10 (45.4) - 12 (54.5) 2 (10.5) - 17 (89.4)
Chloramphenicol 22 (100) - - - - 19 (100)
Tetracycline 20 (90.9) - 2 (9) 3 (15.7) 16 (84.2)
Ciprofloxacin 22 (100) - - 1 (5.2) 5 (26.3) 13 (68.4)
Ceftriaxone 16 (72.7) 6 (27.2) - 2 (10.5) - 17 (89.4)
Cefazolin 21 (95.4) - 1 (4.5) 3 (15.7) 1 (5.2) 15 (78.9)
Clindamycin 20 (90.9) - 2 (9) 1 (5.2) - 18 (94.7)
Imipenem 22 (100) - - 14 (73.6) 3 (15.7) 2 (10.5)
Co-trimoxazole 18 (81.8) 1 (4.5) 3 (13.6) 17 (89.4) - 2 (10.5)
Erythromycin 20 (90.9) - 2 (9) 3 (15.7) - 16 (84.2)
Gentamicin 22 (100) - - 4 (21) - 15 (78.9)
Rifampicin 22 (100) - - 3 (15.7) - 16 (84.2)
Pristinamycin 18 (81.8) 1 (4.5) 3 (13.6) 5 (26.3) - 14 (73.6)
Linezolid 22 (100) - - 19 (100) - -
Mupirocin 22 (100) - - 19 (100) - -
a. Vancomycin susceptibility profile was determined using agar dilution method.

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 METHICILLIN RESISTANT SATPHYLOCOCCUS AUREUS IN ARDABI

and effective antibiotic therapy (2, 20). low. Several studies reported a decrease in resistance
In this study, all isolates were susceptible to of MRSA to co-trimoxazol over the time (31-32).
vancomycin, mupirocin, linezolid. The absence of In conclusion, the frequency of MRSA infection in
resistance to mupirocin may be related to the low our hospitals was found to be high and this finding
usage of this antibiotic in the study setting. However highlights the need for applying appropriate infection
others have recently reported the incidence of high- control measures and effective antibiotic therapy.
level mupirocin resistant S. aureus strains isolated Moreover results emphasize the use of cefoxitin
from patients in Iran (11). Mupirocin is topical agent disk diffusion or oxacillin MIC tests as accurate
often used to eradicate nasal carriage and control phenotypic methods in clinical laboratories if PCR
outbreaks of methicillin-resistant S. aureus (11). for mecA gene detection is not feasible.
The vancomycin is the drug of choice for the
treatment of infections due to MRSA (21). Several ACKNOWLEDGMENT
studies reported emergence of vancomycin resistant
clinical MRSA isolates around the world (22-24). This work was performed in partial fulfilment of
In our study all of the isolates displayed MICs of the requirements for M.Sc thesis in Microbiology
2 g/ml to vancomycin and were susceptible to (Solmaz Dibah, Zanjan Branch, Islamic Azad
vancomycin. University). We gratefully acknowledge Ardabil
Multiple-drug resistant characteristics of MRSA University of Medical Sciences for providing
and emergence of glycopeptide resistant strains laboratory facilities for this work.
have been frequently caused treatment failure of
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