Prevalence and antibiotic susceptiblity of methicillin resistant staphylococcus aureus, collected at thammasat university hospital, Thailand, august 2012- july 2015

Abstract

We analyzed data of Staphylococcus aureus isolated from patients attending
Thammasat University Hospital, Thailand from August 2012 to July 2015. In
total, 232/502 (46%) S. aureus isolates were methicillin-resistant S. aureus (MRSA).
There was a declining trend of proportion of MRSA infection, but the prevalence
of MRSA in the last year of study remained high (38%). All 32 MRSA-infected
outpatients had history of exposure to healthcare facilities during the previous two
months and thus were not considered as having community-associated MRSA.
In addition, all these strains were negative for pvl, suggesting that these strains
were hospital-associated MRSA. All MRSA stains were susceptible to linezolid,
teicoplanin and vancomycin, but resistance to erythromycin and clindamycin
were nearly 100%. Fifty-two percent and 87% of MRSA strains were susceptible
to tetracycline and trimethoprim-sulfamethoxazole, respectively. These results
emphasize the necessity of long-term surveillance and monitoring of antimicrobial
susceptibility pattern of MRSA.

Full text

Prevalence and antibiotic Profiles of Mrsa, thailand
Vol 48 No. 2 March 2017 351
Correspondence: Sumalee Kondo, Department
of Preclinical Science, Faculty of Medicine,
Thammasat University, Rangsit campus, Klong
Luang, Pathum Thani 12120, Thailand.
Tel: +66 (0) 2926 9756; Fax: +66 (0) 2926 9755
E-mail: ksumalee@alpha.tu.ac.th
PREVALENCE AND ANTIBIOTIC SUSCEPTIBLITY OF
METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS,
COLLECTED AT THAMMASAT UNIVERSITY HOSPITAL,
THAILAND, AUGUST 2012 - JULY 2015
Pimonwan Phokhaphan1, Pholawat Tingpej1, Anucha Apisarnthanarak2
and Sumalee Kondo1
1Department of Pre-Clinical Sciences, 2Department of Internal Medicine, Faculty of
Medicine, Thammasat University, Pathum Thani, Thailand
Abstract. We analyzed data of Staphylococcus aureus isolated from patients attend-
ing Thammasat University Hospital, Thailand from August 2012 to July 2015. In
total, 232/502 (46%) S. aureus isolates were methicillin-resistant S. aureus (MRSA).
There was a declining trend of proportion of MRSA infection, but the prevalence
of MRSA in the last year of study remained high (38%). All 32 MRSA-infected
outpatients had history of exposure to healthcare facilities during the previous two
months and thus were not considered as having community-associated MRSA.
In addition, all these strains were negative for pvl, suggesting that these strains
were hospital-associated MRSA. All MRSA stains were susceptible to linezolid,
teicoplanin and vancomycin, but resistance to erythromycin and clindamycin
were nearly 100%. Fifty-two percent and 87% of MRSA strains were susceptible
to tetracycline and trimethoprim-sulfamethoxazole, respectively. These results
emphasize the necessity of long-term surveillance and monitoring of antimicrobial
susceptibility pattern of MRSA.
Keywords: Staphylococcus aureus, antimicrobial susceptibility, MRSA, Thailand
and to an increase in healthcare burden.
The pandemic of both hospital-associated
MRSA (HA-MRSA) and community-
associated MRSA (CA-MRSA) instigates a
global concern. In Asia, a high prevalence
of MRSA infection, where the proportion
is greater than 70%, has been observed in
several countries, including Japan, Korea,
Taiwan, and Vietnam (Chen and Huang,
2014). Those countries also experience
a high incidence of CA-MRSA infection
(Chen and Huang, 2014).
In Thailand, data from two multi-
center studies revealed MRSA prevalence
of 53-57%, the majority being HA-MRSA
INTRODUCTION
Resistant strains of Staphylococcus
aureus especially methicillin-resistant S.
aureus (MRSA) have become a worldwide
threat to public health (Boucher and Co-
rey, 2008). Infections with these strains are
more dicult and expensive to treat, lead-
ing to signicant morbidity and mortality

SoutheaSt aSian J trop Med public health
352 Vol 48 No. 2 March 2017
with only 2.5% CA-MRSA (Song et al, 2011;
Mendes et al, 2013). MRSA is usually re-
sistant to all beta-lactams, but resistance
to other antibiotic classes varies among
strains (Chua et al, 2011). Predominant
MRSA strains isolated from different
geographic regions may manifest dier-
ences in antibiotic susceptibility patterns
(antibiograms) (Chua et al, 2011). Given
the diversity of MRSA strains and their
evolving antibiogram, it is crucial to moni-
tor the emergence of CA-MRSA and to
conduct an antibiotic surveillance study.
Currently, there is limited information of
antibiotic susceptibility of MRSA isolated
from Thammasat University Hospital.
Thus, this study investigated the
epidemiology of S. aureus and MRSA
infections among patients visiting Tham-
masat University Hospital (a tertiary-
care, academic hospital), Pathum Thani,
Thailand and determined antibiograms of
MRSA isolates. The data provide essential
information for infection control moni-
toring and for establishing institutional
guidelines for staphylococcal treatment.
MATERIALS AND METHODS
Study setting
Thammasat University Hospital,
Pathum Thani is located approximately 40
km from Bangkok Metropolitan and pro-
vides tertiary medical care in all service
sectors to an average of 1,000 outpatients
per day, with 500 beds for inpatients.
Data collection
All S. aureus-positive clinical speci-
mens sent to the Microbiology Laboratory,
Thammasat University Hospital from
August 2012 to July 2015 were included
in the analysis. Conventional methods of
strain identication included coagulase
test, PR-glucose and PR-mannitol fermen-
tation (Ishii et al, 2006). If all three tests
were positive, the strain was identied
as S. aureus.
Screening of MRSA strains
Cefoxitin disk diusion test was used
to screen all S. aureus isolates (CLSI, 2013).
Isolates with a zone of growth inhibition
≥ 22 mm are dened as methicillin-sen-
sitive S. aureus (MSSA), and those with
a zone diameter < 22 mm as methicillin-
resistant S. aureus (MRSA).
Criterion of CA-MRSA and HA-MRSA
Patients infected with CA-MRSA are
dened by culture-conrmed MRSA in-
fection when presenting at an outpatient
clinic or within 48 hours of hospitalization
without history of exposure to healthcare
facilities during the previous two months.
HA-MRSA-infected patients are dened
as those whose history did not meet the
denition of CA-MRSA.
PCR detection of S. aureus mecA and pvl
Total DNA was isolated from an
inoculum of an overnight S. aureus
culture using Genomic DNA Extrac-
tion Mini Kit (RBC Bioscience, New
Taipei City, Taiwan). The primer pair
used for mecA amplication was 5′-TC-
CAGATTACAACTTCACCAGG-3′ and
5′-CCACTTCATATCTTGTAACG-3′, and
for pvl 5′-ATCATTAGGTAAAATGTCTG-
GACATGATCC-3′ and 5′-GCATCAASTG-
TATTGGATAGCAAAAGC-3′ (Integrated
DNA Technologies, Singapore). PCR
mixture consisted of 50-µl mixture of 10X
PCR buer, 50 mM MgCl2, 10 mM dNTPs,
100 µM specic primer pair and 1.25 U Taq
polymerase (RBC Bioscience). Thermo-
cycling was conducted in a MyCyclertm
Thermal Cycler (Bio-Rad, Hercules, CA)
as follows: 94°C for 2 minutes; followed
by 30 cycles of 94°C for 30 seconds, 51°C
(for mecA) or 56°C (for pvl) for 30 seconds,

Prevalence and antibiotic Profiles of Mrsa, thailand
Vol 48 No. 2 March 2017 353
and 72°C for 1 minute; with a nal heat-
ing at 72°C for 5 minutes. Amplicons (162
bp and 433 bp of mecA and pvl, respec-
tively) were analyzed by 1% agarose gel-
electrophoresis, stained with GelStarTM
Nucleic Acid Gel Stain (Lonza Rockland,
Rockland, ME) and visualized under
UV light. S. aureus N315 and KKU-MS14
strains, kindly provided by Dr Aroonlug
Lulitanond, Faculty of Associated Medical
Sciences, Khon Kaen University, Thailand,
were used as mecA- and pvl-positive con-
trol, respectively.
Antibiogram determination
MRSA isolates were tested for antibi-
otic susceptibility using a standard disk
diusion method (CLSI, 2013), employing
clindamycin (CD), erythromycin (E), fos-
fomycin (FOS), fusidic acid (FD), linezolid
(LZD), teicoplanin (TEC), tetracycline
(TE), trimethoprim-sulfamethoxazole
(SXT), and vancomycin (VAN) (Lio-
lchem®, Arezzo, Italy).
Statistical analysis
Difference of proportion between
MRSA and MSSA was tested using chi-
square test (SPSS Statistics 22.0) (IBM, Ar-
monk, NY). A p-value < 0.05 is considered
signicantly dierent.
Ethical considerations
The study was approved by the Hu-
man Research Ethics Committee of Tham-
masat University (approval no. MTU-EC-
DS-6-015/57). All patients gave informed
consent prior to the study.
RESULTS
S. aureus isolates
A total of 536 S. aureus isolates were
obtained from clinical specimens of 502
patients during the 3-year study period.
Only the rst isolate from a patient with
recurrent infections was used. Over the
3-year survey period, in the rst (August
2012 - July 2013), second (August 2103 -
July 2014) and third (August 2014 - July
2015) year there were 118 (57% MRSA),
150 (51% MRSA) and 234 (38% MRSA)
S. aureus isolates, respectively. Although
the incidence of S. aureus infection nearly
doubled over the 3-year period, the pro-
portion of MRSA signicantly declined.
All MRSA isolates harbored mecA encod-
ing penicillin binding protein 2A (data not
shown) (Ubukata et al, 1989). Distribution
of S. aureus isolates according specimen
types were as follows: sputum, 244 (67%
MRSA); pus, 160 (18% MRSA); blood,
81 (37% MRSA); urine, 7 (86% MRSA);
body uid, 6 [4 synovial and 2 ascitic,
17% MRSA (from ascetic)]; and vaginal
discharge, 4.
As regards the distribution of S.
aureus among clinical wards, 109 (22%)
isolates were from the Outpatient De-
partment: Outpatient clinics, 63 samples
(14% MRSA); Emergency room (ER), 42
(55% MRSA) and Hemodialysis center, 4.
Among the Inpatient Departments, high-
est number of S. aureus samples was from
Internal Medicine wards (239 isolates,
62% MRSA), followed by Surgery (78,
42% MRSA), Operation theaters (39, 23%
MRSA), Pediatrics (34, 26% MRSA), and
Obstetrics-Gynecology (3, 0% MRSA).
Review of outpatients’ illness history
and based on the criterion for CA-MRSA,
all 32 outpatients could be ruled out as
putative CA-MRSA cases. All inpatients
with culture-positive MRSA were de-
tected after 48 hours of admission. No
MRSA isolate in this study carried pvl,
often associated with CA-MRSA (data not
shown) (David and Daum, 2010).
Antibiotic susceptibility of MRSA isolates
According to antibiogram proles,
the 232 MRSA isolates can be classied

SoutheaSt aSian J trop Med public health
354 Vol 48 No. 2 March 2017
Table 1
Antibacterial susceptibility patterns of MRSA isolates collected at Thammasat University Hospital, Thailand during 2012-2015.
Pattern E TE FOS CD SXT FD VAN TEC LZD Number
(15 µg/ml) (30 µg/ml) (200 µg/ml) (2 µg/ml) (1.25/ 23.75 (10 µg/ml) (30 µg/ml) (30 µg/ml) (30 µg/ml) of isolates
µg/ml) (%)
I NS S S NS S S S S S 109 (47)
II NS NS NS NS S S S S S 74 (32)
III NS NS S NS NS S S S S 14 (6)
IV NS NS S NS S S S S S 11 (5)
V NS NS NS NS NS S S S S 11 (5)
VI NS S NS NS S S S S S 3 (1)
VII NS S S NS NS S S S S 3 (1)
VIII NS NS NS NS NS NS S S S 1 (< 1)
IX NS S NS NS NS S S S S 1 (< 1)
X NS S S NS S NS S S S 1 (< 1)
XI NS S NS S S S S S S 1 (< 1)
XII NS S S S S S S S S 1 (< 1)
XIII S NS NS NS S NS S S S 1 (< 1)
XIV S S S S S S S S S 1 (< 1)
Number of susceptible 2 (1%) 120 (52%) 140 (60%) 3 (1%) 202 (87%) 229 (99%) 232 (100%) 232 (100%) 232 (100%)
isolates (%)
CD, clindamycin; E, erythromycin; FOS, fosfomycin; FD, fusidic acid; LZD, linezolid; STX, trimethoprim-sulfamathoxazole; TE, tetracyclin;
TEC, tecoplanin; VAN, vanconycin; NS, not susceptible; S, susceptible.
Table 2
Antibiotic susceptibility of MRSA isolates classied by period of collection, Thammasat University Hospital, Thailand.
Period Number of Number of susceptible MRSA isolates (%)a
MRSA isolates
E TE FOS CD SXT FD
1st year 67 1 (1) 27 (40) 34 (51) 2 (3) 58 (87) 66 (99)
2nd year 77 0 (0) 35 (45) 40 (52) 1 (1) 65 (84) 76 (99)
3rd year 88 1 (1) 58 (66) 66 (75) 0 (0) 79 (90) 87 (99)
aAll samples were susceptible to LZD, TEC and VAN.

Prevalence and antibiotic Profiles of Mrsa, thailand
Vol 48 No. 2 March 2017 355
Table 3
Antibiotic susceptibility of MRSA isolated from dierent specimen types, collected at Thammasat University Hospital,
Thailand during 2013-2015.
Sample type Total number of Number of MRSA susceptible isolates (%)a
MRSA isolates
E TE FOS CD SXT FD
Sputum 164 1 (1) 87 (53) 100 (61) 1 (1) 143 (87) 164 (100)
Pus 31 1 (3) 15 (48) 19 (61) 2 (6) 26 (84) 28 (90)
Blood 30 0 (0) 14 (47) 17 (57) 0 (0) 27 (90) 30 (100)
Urine 6 0 (0) 4 (67) 4 (67) 0 (0) 5 (83) 6 (100)
Body uid 1 0 (0) 0 (0) 0 (0) 0 (0) 1 (100) 1 (100)
aAll samples were susceptible to LZD, TEC and VAN.
into 14 patterns, pattern I being the most
common (109 isolates) and VIII-XIV being
represented by 1 sample each (Table 1).
All 232 MRSA isolates were susceptible
to LZD, TEC and VAN, followed by 229
(99%) to FD with only 1 isolate (pattern
XIV) sensitive to all 9 antimicrobials
tested. On the other hand, no isolate was
resistant to all 9 drugs, but 229 (99%)
and 230 (99%) isolates were resistant to
CD and E, respectively. The proportion
of MRSA isolates susceptible to FOS and
TE increased in the third year of study
compared to the rst and the second years
(p <0.01), but the proportion to other an-
tibiotics remained unchanged (Table 2).
Antibiogram patterns I and II were
predominant in MRSA isolates from Out-
patient Clinics and ER and in all inpatient
wards except the Pediatric wards, from
which antibiogram patterns III, IV and
V were obtained. It is noteworthy that
all 32 putative non-CA-MRSA isolates
from outpatients were susceptible to SXT
whereas 170/200 (85%) isolates from the
Inpatient Departments were susceptible
to this antibiotic. Also all 9 MRSA isolates
from the Pediatric wards were TE resis-
tant while the overall TE susceptible rate
was 52%.
There was no specic MRSA antibio-
gram pattern associated with a specimen
type (Table 3). Three MRSA isolates from
pus specimens were found resistant to FD,
an antibiotic often used in topical form.
DISCUSSION
It is notable that the proportion of
MRSA isolates detected at Thammasat
University Hospital declined over 3-year
study period (August 2013 - July 2015).
Similar trends regarding MRSA infection
were observed in the USA and Europe
during the past decade (Johnson, 2011;

SoutheaSt aSian J trop Med public health
356 Vol 48 No. 2 March 2017
Dantes et al, 2013; Song et al, 2013). Never-
theless, despite the declining trend, MRSA
constituted nearly 40% of S. aureus infec-
tions in the last year of the study.
The spread of CA-MRSA strains in
many countries has created global con-
cern (David and Daum, 2010). Thus, close
monitoring of the emergence of CA-MRSA
remains important. In this study, we did
not nd any instance of CA-MRSA infec-
tion among the inpatients. This suggests
that HA-MRSA was most likely responsi-
ble for these community-onset infections.
Molecular means were applied to
distinguish between CA- and HA-MRSA.
CA-MRSA strains usually carry staphy-
lococcal chromosomal cassette mec (SCC-
mec) type IV and V as well as Panton-Val-
entine leukocidin (PVL) genes, whereas
HA-MRSA strains carry SCCmec type I,
II and III and seldom have pvl (David
and Daum, 2010). No MRSA isolates in
our study carried pvl, a nding consistent
with previous reports (Song et al, 2011;
Mendes et al, 2013). Overall data indicate
that the prevalence of CA-MRSA infection
remains very low in Thailand (Mekviwat-
tanawong et al, 2006).The spread of vari-
ous MRSA clones has already occurred
between community and hospital and
also between Asian nations (Song et al,
2011). Thai university students appear
to have a prevalence of MRSA of around
1% (Kitti et al, 2011). Tertiary government
hospitals in Thailand have also reported
signicant levels of MRSA nosocomial
infections (Jariyasethpong et al, 2010). It
was suggested that CA-MRSA found in
an animal hospital might have come from
humans and/or sick animals (Patchanee
et al, 2014).
All MRSA strains tested were suscep-
tible to LZD, TEC and VAN, indicating
that these antibiotics are still eective.
Interestingly, nearly all MRSA strains
were resistant to CD and E; thus, both
drugs are no longer recommended for
managing MRSA infection in our institute.
In particular, all MRSA specimens from
the Pediatric Wards were TE resistant
and 2/3 to SXT. The sporadic outbreak of
MRSA strains isolated from four regions
during 1996-1998 were also resistant to
TE but less susceptible to SXT (81.5%),
as compared to the tested strains in this
study (Wongwanich et al, 2000). Resistance
to at least 5 antimicrobial agents includ-
ing cefazolin, erythromycin, gentamicin,
ooxacin and tetracycline was reported
in a university hospital (Lulitanond et al,
2010). Multidrug resistance to MRSA was
also found in a small animal hospital,
Faculty of Veterinary Medicine, Chiang
Mai University, Thailand (Patchanee et al,
2014). The strains were 100% susceptible
to vancomycin but were 92% resistant to
tetracycline, 69% to trimethoprim-sulfa-
methoxazoles, and 62% to ceftriaxone. In
comparison, the antibiogram of MRSA iso-
lated from India during the same period
(Abbas et al, 2015) showed all of its MRSA
isolates were also sensitive to vancomycin
and linezolid; however, resistance to E,
TE and SXT was found to be less than in
our study. This implies that good clinical
practices in using antibiotics for MRSA
infection treatment must be intensively
monitored among physicians and medical
personnel in order to reduce the spread of
multidrug-resistant MRSA infections. In
addition, HA-MRSA has a wider antimi-
crobial resistance pattern than CA-MRSA
(Huang et al, 2006; Vysakh and Jeya, 2013;
Abass et al, 2015).
The three FD-resistant MRSA isolates
were from pus specimens of surgery
patients. Frequent usage of this drug for
topical applications in surgery patients
may contribute to the emergence of FD-
resistant MRSA strains. In New Zealand,

Prevalence and antibiotic Profiles of Mrsa, thailand
Vol 48 No. 2 March 2017 357
increased prevalence of FD-resistant
MRSA was found in the youngest age
group (< 5 years) with impetigo (Vogel
et al, 2016). In addition, in Norway a
growth in FD-resistance among S. aureus
was reported in children with impetigo
bullosa-like skin disease in the summer
months (Tveten et al, 2002).
The most common specimen contain-
ing MRSA was sputum, consistent with
previous report (Ray et al, 2012). Pro-
longed mechanical ventilation is known as
one of the risks for nosocomial pneumonia
(Lynch, 2001). In addition, more than 1/3
of all S. aureus bloodstream infections
were MRSA, and they expressed various
antibiogram patterns. However, there
were no associations among antibiogram
patterns and MRSA strains categorized
according to clinical origins. Vancomycin
is thus still the drug of choice for treating
MRSA irrespective of site of infection. An
active surveillance of vancomycin suscep-
tibility is therefore encouraged. Moreover,
meta-analysis data of vancomycin treat-
ment indicated that high vancomycin
trough levels are associated with risk of
nephrotoxicity; however, the high vanco-
mycin trough levels are not signicantly
dierent in mortality rate compared to the
low vancomycin trough levels (Tongsai
and Koomanachai, 2016). After vancomy-
cin was introduced for MRSA infection
treatment, MRSA with reduced suscepti-
bility to vancomycin including VISA and
hVISA were reported in 1997 (Hiramatsu
et al, 1997a,b) and has increased globally.
The isolates from Thammasat University
Hospital will be further investigated for
reduced susceptibility to vancomycin in
order to prevent and control spread of
the MRSA infection as recently described
(Sirichoat et al, 2016).
In summary, this research reveals a re-
cent situation of MRSA infection at Tham-
masat University Hospital. Although a
declining trend in the proportion of MRSA
among S. aureus infection was observed,
the prevalence of MRSA infection in 2015
remained nearly 40%. CA-MRSA was not
found in our institute, suggesting a low
prevalence of this strain in the region.
While linezolid, teicoplanin and vanco-
mycin, still remained eective antibiotics
for treatment of MRSA infection, vigilance
of possible emerging resistance must be
maintained. In addition, greater aware-
ness of antibiogram profiles of MRSA
strains prevailing in the various clinical
wards should provide guidance in the
appropriate choice of antimicrobial regi-
men in treating MRSA-infected patients.
ACKNOWLEDGEMENTS
The authors thank Dr Aroonlug Luli-
tanond, Faculty of Associated Medical Sci-
ences, Khon Kaen University, Thailand for
kindly providing mecA- and pvl-positive
control strains, Narissara Mungkornkaew
and all sta of the Microbiology Labora-
tory, Thammasat University Hospital for
assistance with collecting microbiology
data, and Debra Kim Liwiski for help in
editing the paper. This study was funded
by the National Research Council of
Thailand.
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