Prevalence of nasal carriage of methicillin-resistant
Staphylococcus aureus and its antibiotic susceptibility
pattern in healthcare workers at Namazi Hospital,
Mehrdad Askariana,*, Alihosein Zeinalzadeha, Aziz Japonib,
Abdolvahab Alborzic, Ziad A. Memishd
aDepartment of Community Medicine, Shiraz University of Medical Sciences, PO Box 71345-1737, Shiraz, Iran
bMolecular Bacteriology, Professor Alborzi Clinical Microbiology Research Center, Shiraz University of Medical Sciences, Shiraz, Iran
cDepartment of Pediatrics, Shiraz University of Medical Sciences, Shiraz, Iran
dDepartment of Medicine and Infection Prevention & Control Program, King Abdulaziz Medical City, King Fahad National Guard
Hospital, Riyadh, Saudi Arabia
Received 15 February 2008; received in revised form 28 October 2008; accepted 17 November 2008
International Journal of Infectious Diseases (2009) 13, e241—e247
resistant Staphylococcus aureus (MRSA) among healthcare workers (HCWs) at Namazi Hospital,
Methods: This cross-sectional study was conducted from July to November 2006. Nasal swabs
were taken from 600 randomly selected HCWs. The isolates were identified as S. aureus based on
morphology, Gram stain, catalase test, coagulase test, and mannitol salt agar fermentation. To
analyze sensitivity patterns of MRSA strains more precisely, minimum inhibitory concentrations
(MICs) of antibiotics were determined by the E-test method. All methicillin-resistant isolates
were examined for the existence of the mecA gene by total DNA extraction and PCR.
Results: The prevalence of nasal carriage of methicillin-sensitive S. aureus (MSSA) was 25.7% and
of MRSA was 5.3%, with the highest nasal carriage of MRSA in surgical wards and the emergency
department. There was no significant difference between the sexes (p = 0.247), age (p = 0.817),
and years of healthcare service (p = 0.15) with regard to the nasal carriage of MRSA and MSSA. In
the univariate analysis, a statistically significant difference was only found for occupation
(p = 0.032) between the carriage of MSSA and MRSA. In the multivariate analysis, the occupation
‘nurse’ was independently associated with MRSA carriage (p = 0.012, odds ratio 3.6, 95%
confidence interval 1.3—9.7). The highest resistance rate for both gentamicin and clindamycin
(69%) was noted among the MRSA strains. None of the MRSA strains were resistant to mupirocin,
* Corresponding author. Tel.: +98 917 1125777; fax: +98 711 2354431.
E-mail address: firstname.lastname@example.org (M. Askarian).
1201-9712/$36.00 # 2009 International Society for Infectious Diseases. Published by Elsevier Ltd. All rights reserved.
Staphylococcus aureus has been recognized as an epide-
miologically important pathogen. Despite antibiotic ther-
hospitalized patients and have severe consequences.1Fol-
lowing the introduction of penicillin in the 1940 s, strains
of S. aureus unaffected by penicillin were reported in
1945.2,3Methicillin was introduced in 1959 to treat these
infections, but in 1961, shortly after the introduction of
methicillin, S. aureus isolates that had acquired resistance
to methicillin (methicillin-resistant S. aureus, MRSA) were
reported.4The bacterial cell wall contains penicillin-bind-
ing proteins (PBPs), which have an enzymatic role in the
synthesis of peptidoglycan. Normally, PBPs have a high
affinity for beta-lactam antibiotics; in MRSA this affinity
is reduced resulting in antibiotic resistance. In MRSA, a
low-antibiotic affinity PBP known as PBP2a is encoded by
the mecA gene.2,3,5—7
Several studies worldwide have reported the rate of nasal
carriage of S. aureus strains varying from 16.8% to 90%.1,8—10
In Iran the prevalence of nasal carriage of S. aureus among
hospital personnel has varied between 28.2% and 44.5% in
different studies.11—18In studies conducted by Goyal et al.9
and Alghaithy et al.,106.6% and 18.3% were MRSA carriers,
respectively. We have recently reported rates of 42.4% for
MRSA and 23.5% for MSSA in our hospital patients infected
with S. aureus.19
MRSA is a major nosocomial pathogen that causes severe
morbidity and mortality worldwide.20Initially, MRSA was
limited to hospitals, however it is now increasingly recovered
from nursing homes and the community.21The emergence of
MRSA, which is also often multidrug-resistant, renders the
treatment of staphylococcal infections more challenging.22
The aim of this study was to determine the prevalence of
nasal carriage of MRSA among HCWs at Namazi Hospital,
Shiraz, Iran, and to determine the susceptibility of the
recovered isolates to various antibiotics.
Setting and design
The study hospital (Namazi Hospital) is a 750-bed, tertiary-
per year, which serves about one fourth of the Iranian
population. This cross-sectional study was carried out from
July to November 2006 among HCWs from intensive care
units, neurosurgery, general, pediatric, cardiovascular sur-
gery, operating room, hemodialysis, internal medicine,
pediatrics, laundry, and kitchen.
Half of all staff members (600/1200) from all wards were
asked to undergo screening for nasal carriage of S. aureus
this hospital. Doctors and medical students were excluded
from the study. All personnel included in the study were full-
time workers at Namazi Hospital. Personnel who worked part
time at our hospital were excluded from the study.
Data collected included: sex, age, ward, years of healthcare
service, level of education (university graduate, high school
graduate, or secondary school), occupation (nurse, auxiliary
nurse, or non-medical personnel), history of hospitalization
or antibiotic therapy during last three months, smoking
habits, nasal abnormalities (sinusitis, allergic rhinitis, nasal
septal deviation), and history of underlying diseases such as
hypertension, ischemic heart disease (IHD), chronic obstruc-
tive pulmonary disease (COPD), and diabetes mellitus (DM).
Specimens were taken from the subjects in the following
way: a sterile moistened swab was inserted into each nostril
in turn, to a depth of approximately 1 cm, and rotated five
times.23For each specimen, both nostrils were sampled using
the same swab. Trypticase soy broth (TSB) was used as the
transport medium. The samples were quickly sent to the
laboratory and were inoculated onto mannitol salt agar
plates and incubated at 35 8C for 48 h. The isolates were
identified as S. aureus based on morphology, Gram stain,
catalase test, coagulase test, and mannitol salt agar fermen-
tation. Methicillin-susceptible S. aureus strains (MSSA) were
differentiated from MRSA using agar screen plates (Mueller—
Hinton agar) containing 2 mg/ml oxacillin with 4% NaCl.
Isolates with growths on the plates with 2 mg/ml of oxacillin
the antibiotic-containing medium were considered as MSSA.
Antibiotic susceptibility determination
The sensitivity patterns of MSSA and MRSA strains were
determined by disk diffusion method (Kirby—Bauer). The
panel of antibiotics used in sensitivity tests included: oxa-
cillin, vancomycin, mupirocin, gentamicin, linezolid, clinda-
mycin, ciprofloxacin, rifampin, tetracycline, and fusidic
acid. American type culture collection (ATCC) 29213 S. aur-
eus was used as the control strain in antibacterial suscept-
ibility determination. To analyze sensitivity patterns of MRSA
linezolid, fusidic acid, or vancomycin. The existence of the mecA gene in all 32 methicillin-
resistant isolates was observed by PCR.
Conclusions: This study revealed the prevalence of nasal carriage of S. aureus strains among
HCWs tobelower thanthat found in otherstudies from Iran. The antibiotic susceptibility patterns
also differed, perhaps as a result of the excessive use of antibiotics at our hospital. Only the
occupation of nurse was an independent risk factor for MRSA carriage.
# 2009 International Society forInfectious Diseases. Published by ElsevierLtd. All rights reserved.
e242 M. Askarian et al.
strains more precisely, minimum inhibitory concentrations
(MICs) of methicillin (oxacillin) were determined by the E-
test method (AB Biodisk, Sweden). The isolates were incu-
bated overnight, following which the sensitivity breakpoints
for MICs were determined. The sensitivity breakpoints for
MICs and the antibiotic disk diffusion method were inter-
preted according to the manufacturer’s instructions (AB
Biodisk, Sweden) and the BSAC (British Society for Antimi-
crobial Chemotherapy) guidelines, respectively.24
Detection of mecA gene by PCR
All methicillin-resistant isolates were examined for the exis-
tence of the mecA gene by total DNA extraction and PCR.
Briefly, the isolates were swabbed on trypticase soy agar
(TSA) and the surface of the agar medium was covered with
standard vancomycin disks, followed by incubation over-
night. The vancomycin disk was used to weaken the thick
cell wall of S. aureus. The weakened bacterial cell wall was
then rapidly lysed simply by heating.25The bacterial colonies
from the edges of the inhibition zone were then resuspended
in sterile distilled water and matched to 0.5 McFarland
standards (approximately 108cfu/ml). The bacterial suspen-
sion was heated at 95 8C for 15 min and cooled at room
temperature. The crude lysate (2.5 ml) was used as a DNA
template for all isolates when PCR tests were carried out. To
detect methicillin-resistant genes, the 147-bp band from
mecA genes was amplified using two specific primers.26
Data were analyzed using SPSS 11.5 software. Qualitative
variables were compared using the Chi-square or Fisher’s
exact test and quantitative variables were compared by one-
way ANOVA. All p-values were two-sided with p < 0.05 being
considered significant. A logistic regression model was built
toidentify risk factors. Variables with p < 0.25 were retained
in the final model.
Informed oral consent was obtained from all study staff prior
to specimen collection. The study was approved by the Ethics
Committee of Shiraz University of Medical Sciences. Ethical
considerations including privacy of personal data were con-
sidered during all steps of the research.
(600/1220) were screened for S. aureus carriage. The mean
age of participants was 32.36 ? 8.3 years (range 19—74 years)
186 (31%) S. aureus carriers. Of the 186 nasal carriers of S.
aureus, 154 (82.8%) carried MSSA and 32 (17.2%) carried MRSA
(25.7% and 5.3% of all HCWs, respectively).
The frequency of MRSA and MSSA carriage also varied
according to the ward (Table 1). The highest prevalence of
nasal carriage of MRSAwas in the surgical wards. The staff of
the general, pediatric, cardiovascular and orthopedic sur-
gery wards together with the emergency department
accounted for 43.8% of all MRSA carriers. This study showed
the highest rate of nasal carriage of MSSA (53.3%) in laundry
and kitchen workers without any carriage of MRSA. In uni-
variate analysis we divided the hospital departments into:
emergency, internal medicine, pediatrics, intensive care
units (ICUs), surgery and operating room, and non-medical
(laboratory, laundry, kitchen, and paramedical staff) units
and found no significant difference between MSSA and MRSA
carriers (p = 0.224).
Table 2 shows the results of univariate and logistic regres-
sion analysis of potential risk factors for nasal carriage of
MSSA and MRSA. There was no significant difference between
the sexes (p = 0.247), age (p = 0.817), and years of health-
care service (p = 0.15) between those with nasal carriage of
MRSA and MSSA.
The other variables studied were level of education (uni-
versity graduate, high school graduate, and secondary
school) and occupation (nurse, auxiliary nurse, and non-
medical personnel) of HCWs. There was a significant differ-
ence between nasal carriage of MRSA and MSSA (p = 0.032)
between level of education and nasal carriers (p = 0.23).
We also studied the probable risk factors related to nasal
carriage of MSSA and MRSA, such as previous hospitalization,
antibiotic therapy during the last three months, smoking
habits, nasal abnormalities, and underlying diseases (hyper-
tension, IHD, COPD, and DM). There was no association
between these and nasal carriage.
In the multivariate analysis, the only significant indepen-
dent risk factor for nasal carriage of MRSA versus MSSA was
tive and methicillin-resistant Staphylococcus aureus among
healthcare workers at Namazi Hospital by ward (N = 600)
Prevalence of nasal carriage of methicillin-sensi-
MSSA, n (%)MRSA, n (%)
Intensive care unit
Laundry and kitchen
MSSA, methicillin-sensitive Staphylococcus aureus; MRSA, methi-
cillin-resistant Staphylococcus aureus.
aThe total consists of three groups: nasal carriers (MRSA and
MSSA) and non-carriers.
Nasal carriage of MRSA, Shiraz, Irane243
resistant Staphylococcus aureus among healthcare workers at Namazi Hospital
Univariate and multivariate analysis of potential factors for nasal carriage of methicillin-sensitive and methicillin-
Variable Carrier statusp-Value Logistic regression
MSSA, n (%)MRSA, n (%)ORa(95% CI)p-Value
Age (years), mean ? SD
Stratified age (years)
33.16 ? 9.3 33.56 ? 7.2 0.817
Years of working, mean ? SD
Stratified years of working
8.85 ? 7.410.98 ? 8.20.15
Internal medicine and pediatrics
Surgery and operating room
Level of education
High school graduate
Antibiotic use in previous 3 months
aOR is comparing the odds of having MSSA to the odds of having MRSA.
e244 M. Askarian et al.
the occupation ‘nurse’ (odds ratio 3.6, 95% confidence inter-
val 1.3—9.7; p = 0.012).
The sensitivity of S. aureus isolates (MSSA and MRSA) to
the tested antibiotics is shown in Table 3. In addition, the
MICs for oxacillin are listed in Table 4. Overall, 154 (25.7%)
isolates were methicillin-sensitive (MSSA) and 32 (5.3%) were
methicillin-resistant (MRSA). The highest resistance rate for
both gentamicin and clindamycin (69%) was noted among the
MRSA strains, while the highest resistance in MSSA strains was
to gentamicin (55%). None of the MRSA strains (0%) were
as follows: one (3%) to vancomycin, three (9%) togentamicin,
two (6%) to ciprofloxacin, and one (3%) to tetracycline. All
MSSA strains were sensitive to mupirocin, linezolid, fusidic
acid, rifampin, and vancomycin. The existence of the mecA
gene in all 32 methicillin-resistant isolates was observed by
PCR (Figure 1).
The prevalence of nasal carriage of MRSA among HCWs at our
hospital has not been determined to date. This study
revealed that 31% of HCWs were carriers of S. aureus strains.
Of these, 17.2% were MRSA (i.e., 5.3% of all HCWs). However,
the carriage rate of S. aureus and MRSA in the present study
cannot be generalized. The estimated prevalence in our
study was significantly lower than that found in the studies
of Rahbar et al.,11Mosavi,12Ghasemian et al.,13Khoddami,14
Mansuri and Khaleghi,15and Rashidian et al.16Differences in
the prevalence of nasal carriage of S. aureus strains may be
due in part to differences in the quality and size of samples
and the use of different techniques and different interpreta-
The frequency of MRSA and MSSA carriage also varies
between hospital wards. In the present study, 43.8% of the
MRSA carriers were working in several surgical units and the
emergency department. An important finding of this study is
that the highest prevalence of nasal carriage of MSSA (53.3%)
was found in laundry and kitchen workers without any car-
riage of MRSA. A reason for this may be the lack of direct
contact between these personnel and patients. This finding
confirms the effect of close contact on the transmission of
bacteria from patients to personnel.
The only occupation found to have an association with
carrier status was having a nursing job, which increased the
for 32 isolates of MRSA from Namazi Hospital personnel by E-
Frequency and range of methicillin (oxacillin) MICs
MIC (mg/ml) Number
MIC, minimum inhibitory concentration; MRSA, methicillin-resis-
tant Staphylococcus aureus.
Antibiotic susceptibility of Staphylococcus aureus isolates (MSSA and MRSA) from Namazi Hospital personnel by Kirby—
AntibioticMSSA (N = 154), n (%)MRSA (N = 32), n (%)
MSSA, methicillin-sensitive Staphylococcus aureus; MRSA, methicillin-resistant Staphylococcus aureus; S, sensitive; R, resistant; I,
control MSSA strain ATCC 29213; lanes 2—9, eight representative
MRSA strains isolated from personnel (amplicon size 147 bp); M,
Detection of the mecA gene by PCR. Lane 1, negative
Nasal carriage of MRSA, Shiraz, Irane245
risk of nasal carriage of MRSA 3.6-fold. We found that the
other variables studied were not risk factors for nasal car-
riage of S. aureus strains. We noticed high rates of MRSA
among patients who were infected with S. aureus at our
hospital. This may indicate cross-contamination of MRSA
between personnel and patients. However, further molecular
epidemiologystudies suchasDNAsequencingand pulsedfield
gel electrophoresis are needed to clarify the existence of any
To our knowledge, the present study is the first from Iran
to evaluate the susceptibility of S. aureus strains from HCWs
to linezolid and fusidic acid. All the S. aureus isolates recov-
ered from nasal carriers, both MRSA and MSSA, were suscep-
tible to linezolid, fusidic acid, rifampin and mupirocin,
In view of the high resistance rates of MRSA to gentamicin,
clindamycin, tetracycline, and ciprofloxacin, empirical
treatment of MRSA infections at our hospital with these
antibiotics may not be effective. The full susceptibility of
S. aureus to linezolid, fusidic acid, rifampin, and mupirocin
observed in this study indicates that these antibacterial
agents are effective for the treatment of S. aureus infections
at our hospital. To date, mupirocin has not been used for the
therapy with mupirocin ointment has been shown to elim-
inate MRSA nasal colonization in both patients and hospital
There was a relationship between methicillin resistance
and resistance to other antibiotics, as noted in previous
investigations.30—33Thus, this is a major problem in the
treatment of S. aureus infections. Our study also supports
the observation of a relationship between oxacillin and
aminoglycoside resistance in S. aureus. More than 69% of
MRSA were resistant to gentamicin, while the frequency of
MRSA resistance to the tetracyclines was 41%. In the last few
years, understanding of the genetic basis for methicillin
resistance has advanced significantly. So far, staphylococcal
cassette chromosome mec (SCCmec) elements are the only
resistance in staphylococci.34PCR testing confirmed that all
MRSA strains isolated from our HCWs were mecA gene-posi-
tive. This study was preliminary and the initiation of further
molecular studies is required to track mecA in our isolates.
As shown by Shitrit et al.,35contact isolation precautions
can prevent new colonization and infection and lead to a
significant reduction in morbidity and healthcare costs. How-
ever, active surveillance culture is important for identifying
hidden reservoirs of MRSA. Currently there is no such active
surveillance and policy for MRSA at our hospital. Previous
studies at our university hospitals have shown that compli-
ance with contact isolation precautions is not well accepted
among nurses,36medical students,37and physicians.38
In conclusion, this study revealed that the prevalence of
nasal carriage of S. aureus strains among HCWs was lower
than that found in other studies in our country. Univariate
analysissuggests thatonly occupation isa risk factorfornasal
carriage of MRSA among HCWs. Logistic regression showed
that having a nursing occupation is independently associated
with MRSA carriage. Antibiotic susceptibility patterns were
different to those of the other studies, which could be as a
result of the excessive use of antibiotics at our hospital. All S.
aureus isolates that we recovered from nasal carriage were
susceptible to mupirocin. Hence, topical mupirocin could be
used to eradicate nasal staphylococcal colonization and
Our study was funded by the Deputy of Research at the Shiraz
University of Medical Sciences and Professor Alborzi Clinical
Microbiology Research Center.
Ethical approval: The Ethics Committee of Shiraz Univer-
sity of Medical Sciences approved this study.
Conflict of interest: No conflict of interest to declare.
1. Kluytmans J, van Belkum A, Verbrugh H. Nasal carriage of
Staphylococcus aureus: epidemiology, underlying mechanism
and associated risks. Clin Microbiol Rev 1997;10:505—20.
2. Shehabel-Din SA, El-Shafey E, El-Hadidy M, Bahaa El-Din A, El-
Hadidy M, Zaghloul H. Methicillin-resistant Staphylococcus aur-
eus: a problem in the burns unit. Egypt J Plast Reconstr Surg
3. Korn GP, Martino MD, Mimica IM, Mimica LJ, Chiavone PA, Muso-
lino LR. High frequency of colonization and absence of identifi-
able risk factors for methicillin-resistant Staphylococcus aureus
(MRSA) in intensive care units in Brazil. Braz J Infect Dis
BG. The evolutionary history of methicillin-resistant Staphylo-
coccus aureus (MRSA). Proc Natl Acad Sci USA 2002;99:7687—92.
5. Silvana M, Emmanuel R, Carlos C. Prevalence of Staphylococcus
aureus introduced into intensive care units of a university hos-
pital. Braz J Infect Dis 2005;9:1—12.
6. Hardy KJ, Hawkey PM, Gao F, Oppenheim BA. Methicillin-resis-
tant Staphylococcus aureus in the critically ill. Br J Anaesth
7. Johnson A, Pearson A, Duckworth G. Surveillance and epidemiol-
ogy of MRSA bacteraemia in the UK. J Antimicrob Chemother
8. Bolyard EA, Tablan OC, Williams WW, Pearson ML, Shapiro CN,
Deitchmann SD. Guideline for infection control in health care
personnel, 1998. Hospital Infection Control Practices Advisory
Committee. Infect Control Hosp Epidemiol 1998;19:407—63.
9. Goyal R, Das S, Mathur M. Colonisation of methicillin-resistant
Staphylococcus aureus among health care workers in a tertiary
care hospital of Delhi. Indian J Med Sci 2002;56:321—4.
10. Alghaithy AA, Bilal NE, Gedebou M, Weily AH. Nasal carriage and
antibiotic resistance of Staphylococcus aureus isolates from
hospital and non-hospital personnel in Abha, Saudi Arabia. Trans
R Soc Trop Med Hyg 2000;94:504—7.
11. Rahbar M, Karamiyar M, Gra-Agaji R. Nasal carriage of methi-
cillin-resistant Staphylococcus aureus among healthcare worker
12. Mosavi M. Positive Staphylococcus-coagulase carriers in Qazvin
Hospital staff. J Qazvin Univ Med Sci Health Serv 1996;1:29—37.
13. Ghasemian R, Najafi N, Shojaifar A. Nasal carriage and antibiotic
resistance of Staphylococcus aureus isolates of Razi Hospital
personnel, Qaemshahr, 1382. J Mazandaran Univ Med Sci
14. Khoddami E. A survey on nasal carriers of Staphylococcus aureus
among hospital staff. J Babol Univ Med Sci 2000;10:52—5.
15. Mansuri SH, Khaleghi M. Nose and throat carrier rate of S. aureus
inthe staff of fouruniversity hospitalsinKermanand comparison
with the control and patients group. J Tehran Fac Med
e246M. Askarian et al.
16. Rashidian M, Taherpoor A, Goodarzi S. Nasal carrier rates and Download full-text
antibiotic resistance of Staphylococcus aureus isolates of Beasat
Hospital staff. Sci J Kurdistan Univ Med Sci 2000;21:1—8.
17. Jazayeri Moghadas A. Frequency of nasal carriers of coagulase-
positive staphylococci in medical personnelof teaching hospitals
in Semnan. Koomesh — J Semnan Univ Med Sci 1999;3:49—55.
18. Hashemi S, Aghi H. Nasal carrier rate of Staphylococcus aureus in
J Hamadan Univ Med Sci Health Serv 1998;5:10—5.
19. Japoni A, Alborzi A, Orafa F, Rasouli. Farshad S. Distribution
patterns of methicillin resistance genes (mecA) in Staphylococ-
cus aureus isolated from clinical specimens. Iranian Biomed J
20. Haddadin AH, Fappiano SA, Lipset PA. Methicillin-resistant Sta-
phylococcus aureus (MRSA) in the intensive care unit. Postgrad
Med J 2002;78:385—92.
21. Mainous AG, Hueston WJ, Everett CJ, Diaz VA. Nasal carriage of
Staphylococcus aureus and methicillin-resistant S. aureus in the
United States, 2001—2002. Ann Fam Med 2006;4:132—7.
22. Choi CS, Yin CS, Bakar AA, Sakewi Z, Naing NN, Jamal F, et al.
Nasal carriage of Staphylococcus aureus among healthy adults. J
Microbiol Immunol Infect 2006;39:458—64.
23. Scarnato F, Mallaret MR, Croize ´ J. Incidence and prevalence of
among healthcare workers in geriatric departments: relevance
24. MacGowan AP, Wise R. Establishing MIC breakpoints and the
interpretation of in vitro susceptibility tests. J Antimicrob Che-
25. Japoni A, Alborzi A, Rasouli M, Pourabbas B. Modified DNA
extraction for rapid PCR detection of methicillin-resistant sta-
phylococci. Iranian Biomed J 2004;8:161—5.
26. Zhang K, McClure JA, Elsayed S, Louie T, Conly JM. Novel multi-
plex PCR assay for characterization and concomitant subtyping
of staphylococcal cassette chromosome mec types I to V in
methicillin-resistant Staphylococcus aureus. J Clin Microbiol
27. Harbarth S, Dharan S, Liassine N, Herrault P, Auckenthaler R,
Pittet A. Randomized, placebo-controlled, double-blind trial to
evaluate the efficacy of mupirocin for eradicating carriage of
methicillin-resistant Staphylococcus aureus. Antimicrob Agents
28. Martin JN, Perdreau-Remington F, Kartalija M, Pasi OG, Webb M,
Gerberding JL, et al. A randomized clinical trial of mupirocin in
the eradication of Staphylococcus aureus nasal carriage in
human immunodeficiency virus disease. J Infect Dis 1999;180:
29. Coia JE, Duckworth GJ, Edwards DI, Farrington M, Fry C, Hum-
phreys H, et al. Guidelines for the control and prevention of
methicillin-resistant Staphylococcus aureus (MRSA) in health-
care facilities. J Hosp Infect 2006;63(Suppl 1):S1—44.
30. Kim HB, Jang HC, NamHJ, Lee YS, Kim BS, Park WB, et al. In vitro
activities of 28 antimicrobial agents against Staphylococcus
aureus isolates from tertiary-care hospitals in Korea: a nation-
wide survey. Antimicrob Agents Chemother 2004;48:1124—7.
31. Zinn CS, Westh H, Rosdahl VT. An international multicenter study
of antimicrobial resistance and typingof hospitalStaphylococcus
aureus isolates from 21 laboratories in 19 countries or states.
Microb Drug Resist 2004;10:160—8.
32. Diekema DJ, Pfaller MA, Schmitz FJ, Smayevsky J, Bell J, Jones
RN, et al. Survey of infections due to Staphylococcus species:
frequency of occurrence and antimicrobial susceptibility of iso-
lates collected in the United States, Canada, Latin America,
Europe and the Western Pacific Region for the SENTRY Antimi-
crobial Surveillance Program, 1997—1999. Clin Infect Dis
33. Fluit AC, Wielders CL, Verhoef J, Schmitz FJ. Epidemiology and
susceptibility of 3051 Staphylococcus aureus isolates from 25
university hospitals participating in the European SENTRY study.
J Clin Microbiol 2001;39:3727—32.
34. Hanssen AM, Ericson Sollid JU. SCCmec in staphylococci: genes
on the move. FEMS Immunol Med Microbiol 2006;46:8—20.
35. Shitrit P, Gottesman BS, Katzir M, Kilman A, Ben-Nissan Y,
Chowers M. Active surveillance for methicillin-resistant Staphy-
lococcus aureus (MRSA) decreases the incidence of MRSA bacter-
emia. Infect Control Hosp Epidemiol 2006;27:1004—8.
36. Askarian M, Shiraly R, McLaws ML. Knowledge, attitudes, and
practices of contact precautions among Iranian nurses. Am J
Infect Control 2005;33:486—8.
37. Askarian M, Aramesh K, Palenik CJ. Knowledge, attitude, and
practice toward contact isolation precautions among medical
students in Shiraz, Iran. Am J Infect Control 2006;34:593—4.
38. Askarian M, Shiraly R, Aramesh K, McLaws ML. Knowledge, atti-
tude, and practices regarding contact precautions among Iranian
physicians. Infect Control Hosp Epidemiol 2006;27:868—72.
Nasal carriage of MRSA, Shiraz, Iran e247