Abdul Jabbar et al. / International Journal of Advances in Pharmaceutical Research
IJAPR
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Research Paper
ISSN: 2230 – 7583
PREVALENCE AND ANTIMICROBIAL SUSCEPTIBILITY PATTERN OF
METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS ISOLATES IN
LAHORE
Abdul Jabbar2 , Saeedullah Khan1, Shahzad Munir2, Najmul Hasan3,
Hamid Rasool Niazi2
1
2
Institute of Molecular Biology and Biotechnology, University of Lahore, Pakistan
Department of Microbiology, Kohat University of Science and Technology, Kohat, Pakistan
3
Department of Microbiology, University of Karachi, Karachi, Pakistan.
Received on 13 – 02 - 2013
Revised on 27 – 03- 2013
Accepted on 21– 04 – 2013
ABSTRACT
The emphasis of this study was on the sensitivity of the antibiotics to pathogenic bacterial strains of methicillin
resistant Staphylococcus aureus (MRSA). Total of 280 samples were collected in microbiology laboratory of
Sheikh Zayed Hospital, Lahore. Staphyloccus aureus was isolated by using Blood agar, Nutrient agar, Mannitol
salt agar, Catalase, Coagulase and Dnase tests. Anti PBP-2a latex agglutination test was used to identify MRSA.
Out of 139 Staphylococcus aureus strains isolated from various clinical samples, 43.16% were found to be
methicillin resistant. The efficacies of these isolates were tested by paper disc diffusion method on Mueller Hinton
agar. All MRSA isolates were resistant to penicillin. Among MRSA isolates, 44.82% were from different inpatient
departments, whereas, 40.43% of the MRSA isolates were from outpatients. This preliminary report showed a high
prevalence of MRSA in the hospital. To reduce the prevalence of MRSA, regular surveillance of hospital acquired
infections is the need of the hour.
Keywords: Methicillin resistant, Staphylococcus aureus, Anti PBP-2a, latex agglutination test, Paper disc
diffusion method
INTRODUCTION
Staphylococcus aureus has been recognized as the
most important virulent and frequently encountered
pathogen in clinical practices. It is an endogenous
microorganism colonizing the nasal cavity, skin,
gastrointestinal, anus and vaginal vulvae of healthy
women1.
Author for Correspondence
Abdul Jabbar,
Department of Microbiology,
Kohat University of Science and Technology,
Kohat, Pakistan.
ajswati22@gmail.com
Cell # + 92 333 9483707
Fax # +92 91 9211663
IJAPR /June 2013/ Vol. 4 /Issue. 6 / 1810 – 1816
Clinically MRSA is a major healthcare associatedMethicillin Resistant Staphylococcus aureus (HAMRSA) as well as a community associatedMethicillin Resistant Staphylococcus aureus (CAMRSA) infection causing a wide range of diseases,
including endocarditis, osteomyelitis, toxic-shock
syndrome, pneumonia, food poisoning, impetigo and
carbuncles. These infections may occur in wounds or
skin, burns and other sites where tubes enter the
body, as well as in the eyes, bones, heart and blood2.
The proportion of nosocomial infections caused by
MRSA augmented strongly, and MRSA is now a
leading cause of such infections3. Appearance of
MRSA in animals has been shown by previous
studies4. Epidemiological studies suggest that
hospitals of all sizes are facing the problem of
MRSA. The problem occurs to be increasing
regardless of hospital size and control measures for
MRSA. MRSA has become the commonest hospital
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Abdul Jabbar et al. / International Journal of Advances in Pharmaceutical Research
acquired infection causing agent throughout the
world, causing a wide range of hospital infections5.
Resistance to methicillin mediated by mecA gene,
responsible for production of PBP2a, which have
been observed in MRSA. mecA located on a region
of chromosome called SCC mec. Five different types
of SCC mec have been characterized as I, II, III, IV,
V6. The mecA gene complex also contains insertion
sites for plasmids and transposons that facilitate
acquisition of resistance to other antibiotics. Thus,
cross-resistance to non-β-lactam antibiotics such as
erythromycin,
clindamycin,
gentamicin,
cotrimoxazole and ciprofloxacin is common2.
The past few decades have seen an alarming increase
in the prevalence of antimicrobial resistant
pathogens in serious infections7.
Increasing
resistance to penicillin has led to the development of
semi-synthetic groups of penicillin such as
methicillin, that are resistant to many genetic
variations of the beta-lactamase enzyme. For years,
infection by Staphylococcus aureus was controlled
using methicillin and its analogues. However, in
1961 the first strain of MRSA was isolated8 since
then, MRSA has been found worldwide especially
in hospitals and nursing homes9. Hospital-acquired
infections due to MRSA have been associated with
an increase in length of hospital stays, mortality
rates, and health-care costs10.
Objectives
1. Isolation
and
identification
of
Staphylococcus aureus from different
clinical samples.
2. Prevalence of MRSA
METHODOLOGY
Sample collection and processing
A total of 280 samples were collected from different
sites including pus, wound swabs, sputum, blood,
throat swabs, high vaginal swabs and urine, during
the period of May to July 2012, and submitted at
microbiology laboratory of Sheikh Zayed Hospital,
Lahore. Blood samples were collected in a sterile
thioglicolate broth, sputum and urine were collected
in sterile containers, pus in sterile syringes while
vaginal, throat and wound samples were collected by
sterile swabs. Staphylococcus aureus were isolated
and identified by growing on Nutrient agar, Blood
agar and Mannitol salt agar. These were incubated at
37ºC for 18 to 24 hours and the growth of organisms
then confirmed by Gram staining, Catalase test,
Coagulase test, Mannitol fermentation test and
Dnase test, following standard microbiological
procedures11.
IDENTIFICATION OF STAPHYLOCOCCI
Gram staining
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A smear of bacteria was prepared by placing a drop
of distilled water on a clean slide to perform Gram
staining. Smear was allowed to air-dry and then heat
fixed by gliding slide 2-3 times over Bunsen’s
burner flame. The smear was stained with crystal
violet (primary) for one minute and washed with tap
water. Gram’s Iodine (mordant) was added for one
minute and washed with tap water. The slides were
decolorized with 95% ethanol until no stain came out
and washed with tap water. Safranin (counter)
solution was added for a half minute and washed
with tap water. Stained slides were examined under
oil immersion objective (100X) of the bright field
compound microscope. Staining character and
microscopic morphological appearance of individual
bacteria were recorded.
Identification of Staphylococcus aureus
Catalase test was used for the biochemical
identification of this nosocomial pathogen. One drop
of 3% hydrogen peroxide was placed on a clean
slide. The suspected isolate was picked by using
sterile inoculating loop and put into 3% hydrogen
peroxide. The presence of bubbles was indicative for
positive results11. Coagulase test (Clumping factor)
was performed by placing a drop of distilled water
on each end of a slide or on two separate slides.
Emulsify a colony of the test organism in each of the
drops to make thick suspensions. Add a loopfuls of
plasma to one of the suspensions, and mixed gently.
Look for clumping of the organisms within 10
seconds11. DNase test was carried out by dividing
DNase plate into the required numbers of strips by
marking the underside of the plates. Using a sterile
loop or swab, spot-inoculate the test and control
organisms. Incubated the plate at 35-37°C overnight.
Covered the surface of the plate with
1mol/hydrochloric acid solution. Tip off the excess
acid and looked for clearing around the colonies
within 5 minutes of adding the acids11.
SCREENING OF MRSA
PBP-2a latex agglutination kit
MRSA were confirmed by PBP-2a latex
agglutination kit (Oxoid). Extraction reagent 1 (four
drops) and sufficient bacterial growth (filling 5 μl
bacterial loop) were added in an Eppendorf tube to
make homogeneous suspension. It was placed in a
boiling water bath (over 95 ºC) for three minutes and
then allowed to cool at room temperature. Extraction
reagent 2 (one drop) was added in the same
eppendorf and mixed well. Mixture was centrifuged
at 3,000 rpm for five minutes and supernatant was
used for the test. Kit is provided with two bottles of
latex particles i.e. test latex and control latex. On the
test card one drop of test latex and control latex was
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Abdul Jabbar et al. / International Journal of Advances in Pharmaceutical Research
added to the respective circles. Supernatant was
added on test latex and control latex and mixed
thoroughly with a separate mixing stick for three
minutes and agglutination was noted. Results were
interpreted according to following two possibilities.
a. Agglutination in test latex but not in control latex
within 3 minutes-----MRSA
b. Agglutination in neither test latex nor control latex
within 3 minutes----MSSA
Antimicrobial susceptibility testing
Antimicrobial susceptibility was determined by the
Disc Diffusion method, referred to the Clinical and
Laboratory Standard Institute (CLSI, 2009). The
antibiotic discs including Oxacillin (1μg), Penicillin
(10μg), Erythromycin (30μg), Gentamycin (10μg),
Tetracycline
(30μg)
amikacin
(30μg),
Chloramphenicol (30μg), cefotaxime (30μg),
vancomycin (10μg) ciprofloxacin (5μg), were placed
on the surface of Mueller Hinton agar plates and
were incubated for 18 to 24 hours at 37ºC. The
antibiogram was read and recorded the diameter of
zone of the inhibition.
RESULTS
Identification of Staphylococci
Staphylococci produced characteristic yellow to
cream color colonies on blood agar after overnight
incubation. Pigments were less pronounced in young
colonies. Colonies were slightly raised and easily
emulsified. Microscopic study revealed gram
positive cocci, occurring characteristically in groups
like grapes but also singly and in pairs. These were
non motile, non capsulated and appeared blue purple
under oil immersion objective (100X) of the bright
field compound microscope.
Identification of Staphylococcus aureus
Catalase test
This test was performed to differentiate
Staphylococci from Streptococci. Staphylococci
produced bubbles and it was concluded that the
organism makes catalase. A lack of bubbles indicates
the absence of catalase.
Coagulase test
This was used to identify Staphylococcus aureus.
Coagulase enzymes are present in Staphylococcus
aureus which convert fibrinogen into fibrin clot
while absent in the other species of Staphylococcus.
DNase test
This test was used to identify Staphylococcus aureus
which produces deoxyribonuclease (DNase)
enzymes. The clearing around the colonies shows
DNase positive strains.
Mannitol fermentation test
IJAPR /June 2013/ Vol. 4 /Issue. 6 / 1810 – 1816
Staphylococcus aureus ferments mannitol and
produced yellow colour 1-2mm in diameter colonies
after overnight incubation at 37°C.
IDENTIFICATION OF MRSA
PBP-2a latex agglutination test
This test was used to identify methicillin resistant
Staphylococcus aureus (MRSA). Agglutination in
test latex but not in control latex within 3 minutes
was confirmed as MRSA as shown in figure 1.
Isolation of MRSA
The isolates were from different parts of the body.
Out of 280 samples 139 strains were found as
Staphylococcus aureus of which 60 (43.16%) were
found to be methicillin resistant MRSA (Table 1).
Maximum number of Staphylococcus was found in
pus isolates. Out of 32 Staphylococcus aureus
56.25% were MRSA, followed by wound swabs in
which 54.54% were MRSA. The prevalence of
MRSA and Staphylococcus aureus was higher in
Inpatient (Wards and ICU) department as 39
(44.82%) and Staphylococcus aureus was 48
(55.17%) as compared to Outpatient (OPD)
department which was 21 (40.38%) and
Staphylococcus aureus was 31 (59.61%). Hence, the
overall prevalence of MRSA and Stapylococcus
auerus was 43.16% and 56.83% respectively as
shown in figure 2.
Antimicrobial susceptibility pattern
All the strains of MRSA were found to be resistant
to Penicillin. Among MRSA, resistance to oxacilline
was 100%, ciprofloxacin 68.33%, erythromycin
63.33%, gentamicin 51.66%, cefotoxime 100%,
Chloromphenicol 38.33%, fusidic acid 45%,
amikacin 48.33%, and tetracycline were resistant to
41.66% of the MRSA strains. Many MRSA strains
were multidrug resistant shown in table 2. Many of
the MRSA strains were resistant to all the antibiotics
tested except Vancomycin as shown in figure 3. The
diameter for zone of inhibition for test drugs was
according to the standard zone of inhibition chart
(NCCLS, 2007) as shown in table 2.
DISCUSSION
Methicillin resistant Staphylococcus aureus (MRSA)
is a serious threat to hospitalized patients globally
and it now represents a challenge for public health,
as community associated infections appear to be on
the increase in both adults and children in different
regions and countries12.
Epidemiological studies suggest that hospitals of all
sizes are facing the problem of MRSA. The problem
occurs to be increasing regardless of hospital size
and control measures for MRSA. Prevalence is
constantly mounting in many countries, and in some
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Abdul Jabbar et al. / International Journal of Advances in Pharmaceutical Research
hospitals, more than half of all Staphylococcus
aureus disease isolates are MRSA13.
In Pakistan, the prevalence of MRSA was reported
up to 42% in 2007 by Ali et al14. In Nepal, Sanjana
et al., 201015 founded the prevalence of MRSA
39.6%. Prevalence of MRSA was higher among
inpatients (41.1%) than outpatients (37.4%). A
comparable prevalence rate of 34.7%, 31.0% and
38.5% were also reported from Assam, Tamil Nadu
and Delhi by Rajaduraipandi et al., 200616.These
results were consisted with the finding of our results.
We found the prevalence rate of methicillin
resistance Staphylococcus aureus (MRSA) 43.16%.
Prevalence of MRSA was higher among inpatients
(44.82%) than outpatients (40.38%) in Shaikh Zayed
Hospital, Lahore. In a study by Kumari et al., 200817,
in Eastern part of Nepal in Dharan, reported the rate
of MRSA was (26.4%), which was low as compared
to our finding; this difference could be due to
prolonged hospital stay, instrumentation and other
invasive procedures.
MRSA are often multidrug-resistant. A study form
Tehran, Iran by Vadhani et al., 200418 reported that,
from the 90 MRSA isolates, approximately half of
them displayed resistance to one or more
antimicrobial
agents,
including
penicillin,
cephalosporins, tetracycline and aminoglycosides.
We found multidrug resistant MRSA 61.84%. If we
look into the Indian literature, it seems the burden of
multidrug resistant MRSA is increasing over time:
for instance, 23.2% was reported by Majumder et al.,
200119, 32% by Anuparba et al., 200320 and 63.6%
by Rajaduraipandi et al., 200616. The lesson is clear,
MRSA surveillance and strict drug policy are of
more importance or else the threat will increase.
Vancomycin seems to be the only antimicrobial
agent which showed 100% sensitivity and so may be
used as the drug of choice for treating multidrugresistant MRSA infections as we found it in the
susceptibility pattern of MRSA. This result is similar
with previous studies, as Alborzi et al.,200021, in
Shiraz, Iran, reported that, 100 percent of isolates
were sensitive to vancomycin and recently in
Qassim, Saudi Arabia, Mohammad et al., 201122,
reported the similar value. But in Tehran, Vidhani et
al., 200418, reported 7% of isolates were resistant to
Source
Pus
Sputum
Blood
Throat swab
Wound swab
vancomycin. This report is an early warning that
Staphylococcus aureus strains with full resistance to
vancomycin might emerge in future because of
widespread use of antibiotics and changing trends of
defence acquired by MRSA.
Gentamycin is an aminoglycoside most often used
because of it slow cost and reliable activity against
gram positive bacteria. In the present study 51.66%
of MRSA showed resistance towards gentamycin
which is higher than reported earlier 34% in
Islamabad by Yameen et al., 200923.
Beta-lactam antibiotics like penicillin and cephalexin
were not found to be effective against MRSA.
Penicillin and cephalexin resistance were 100% and
88.7% respectively. Resistance to quinolones
(ciprofloxacin) was also found to be very high i.e.
84.1%. This correlates with an earlier finding where
it has been shown that the resistance to ciprofloxacin
is steadily increasing from 39% in 1992 to 68% in
1996 as reported Delhi by Mehta et al., 199824.
All these studies were in agreement with this
research because we found the resistance pattern of
Penicillin 100%. Resistance to quinolones
(ciprofloxacin) was also found to be very high i.e.
68.33%. This correlates with an earlier finding where
it has been shown 68% by Mehta et al., 199824. This
high resistance may due to increases pressure of
antibiotics. Vancomycin is not a commonly
prescribed drug, which is almost certainly due to the
higher price of the antibiotic and its unavailability in
many parts of the country.
In the study, Penicillin-resistance was observed to be
100% against the organism. This corroborates with
the finding of Anupurba et al., 200320. This result is
in agreement with our finding, where we found
cefotaxime 100% resistance because of the presence
of beta lactams ring in this antibiotic.
We found such strains of multidrug resistant MRSA
with increasing resistance to ciprofloxacin,
chloramphenicol, fusidic acid and erythromycin.
This is due to high pressure of antibiotics usages.
This observation is in agreement with Schito, 200225,
in his study of MRSA reported that, MRSA were
generally multidrug resistant with increasing
resistance to ciprofloxacin, chloramphenicol, fusidic
acid and erythromycin.
Table 1: Isolation of MRSA (%) from different specimens.
Total Staphylococcus aureus
MRSA
32
18
20
7
18
3
25
11
22
12
IJAPR /June 2013/ Vol. 4 /Issue. 6 / 1810 – 1816
%
56.25
35
16.16
44
54.54
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Abdul Jabbar et al. / International Journal of Advances in Pharmaceutical Research
High vaginal swab
Urine
Total
15
7
139
6
3
60
Table 2: Antimicrobial resistant Pattern of MRSA% Strains.
Diameter for sensitive zone of MRSA (%)
inhibition
100
>14mm
Antibiotics
Oxacillin
Penicillin
>18mm
100
Cefotaxime
>23mm
100
Ciprofloxacin
Erythromycin
Gentamycin
Vancomycin
63.33
>23mm
51.66
45
>15mm
Chloramphenicol
Tetracycline
68.33
>21mm
>18mm
Fusidic acid
Amikacin
40
42
43.16
38.33
>18mm
48.33
>17mm
41.66
>15mm
00
>15mm
mm = millimeter
Figure 1: Positive PBP-2a Latex agglutination test
Figure 2: Percentage of S. aureus and MRSA in inpatient and outpatient department
IJAPR /June 2013/ Vol. 4 /Issue. 6 / 1810 – 1816
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Abdul Jabbar et al. / International Journal of Advances in Pharmaceutical Research
Figure 3: Percentage of resistant pattern of MRSA isolates.
CONCLUSION
From this study it was concluded that, the prevalence
of MRSA is increases amongst clinical isolates of
Staphylococcus aureus. Out of 139 Staphylococcus
aureus strains isolated from various clinical samples,
60 (43.16%) were found to be MRSA. Among
MRSA isolates, 39(44.82%) were from different
inpatient departments, whereas, 21(40.43%) of the
isolates were from outpatient department. All MRSA
were resistant to penicillin. Active screening and
compliance with recommended infection control
practices play an important role in the control of
MRSA. Attention should be paid to stop the
transmission of MRSA by health care taker by very
careful hand washing. There is a need for
surveillance of MRSA and its antimicrobial profile.
The hospital infection control policy and guidelines
that already exists should be strictly followed so as
to enable the clinicians to deliver better and proper
health care to the patients.
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