ORIGINAL CONTRIBUTIONS
Higher nasal carriage rate of
methicillin-resistant Staphylococcus
aureus among dental students who
have clinical experience
Yoo Sang Baek, MD; Seung-Ho Baek, DDS, PhD;
Yeon-Jee Yoo, DDS, PhD
S
ince its isolation in the early 1960s, methicillin-
resistant Staphylococcus aureus (MRSA) has
been a cause of great concern.1 The Asia-Pacific
region in particular has a relatively high rate
of S. aureus methicillin resistance.2 MRSA is considered
to be one of the most important nosocomial pathogens
and is associated with multidrug resistance.2,3 In addition
to hospital-acquired MRSA (HA-MRSA), community-
associated MRSA
(CA-MRSA) emerged
in the 1990s and has
spread worldwide.3,4
Investigators have reported that some people have
nasal MRSA colonization.5 Theoretically, nasal MRSA
colonization can serve as a reservoir for transmission and
as a risk factor for the development of MRSA infection.6
There is increasing evidence that MRSA also is present in
dental patients, on dental clinical surfaces, and in dental
health care professionals (DHCPs), including students.7-11
Although there has been limited documentation of the
transmission of MRSA infection from DHCPs to patients
during conventional dental therapy,11,12 DHCPs should
not disregard the possibility of MRSA colonization. In a
case report by Martin and Hardy,12 the dentist involved
in the transmission described by the authors did not
routinely use gloves and had recently been hospitalized
for emergency surgery when the hospital was dealing
with an MRSA outbreak. In a report by Kurita and
colleagues,11 8 of 140 patients who had no evidence of
MRSA when they were admitted to a hospital ward for
special dental care and oral surgery became MRSA car-
riers during their hospitalization. Kurita and colleagues11
Copyright ª 2016 American Dental Association. All rights reserved.
ABSTRACT
Background. Methicillin-resistant Staphylococcus
aureus (MRSA) has been isolated from dental clinical
surfaces, dental patients, and dental health care pro-
fessionals. The authors conducted a study to determine the
prevalence rate of nasal MRSA colonization among dental
school students and to identify the characteristics of the
isolated strains.
Methods. The authors collected nasal samples from
159 dental students. The authors performed mecA gene
detection, staphylococcal cassette chromosome mec
(SCCmec) typing, and antimicrobial susceptibility tests on
each sample. The authors compared the results of 2 groups
(students who had clinical experience and students who did
not have clinical experience).
Results. Five (3.1%) dental students had MRSA coloni-
zation, as confirmed by the presence of the mecA gene in
the nasal cavity. Prior clinical experience was associated
significantly with nasal MRSA carriage (P < .05). Four of
the strains were SCCmec type IV, and 1 strain was SCCmec
type I. All isolates were resistant to amoxicillin and clav-
ulanic acid, imipenem, and oxacillin, but were susceptible
to several antimicrobial agents including mupirocin,
trimethoprim and sulfamethoxazole, and rifampin. The
nasal MRSA colonization was eradicated with the use of
mupirocin ointment.
Conclusions. Nasal MRSA colonization occurs in some
dental students, especially those who have clinical
experience.
Practical Implications. Education about MRSA colo-
nization and transmission, as well as infection prevention
and control measures is necessary for dental students,
especially when they participate in clinical practice.
Key Words. Methicillin-resistant Staphylococcus aureus;
MRSA; dental student; nasal carriage; colonization.
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 ORIGINAL CONTRIBUTIONS
suggested that the MRSA-contaminated surfaces of the
dental operatory were the reservoirs for MRSA trans-
mission. After appropriate infection prevention practices
were implemented at both of these studies’ sites, the
investigators found no subsequent instances of MRSA
transmission.11,12
Compared with the medical field, proper studies of
MRSA carriage in the dental field are relatively sparse.
The aim of our study was to investigate the nasal MRSA
carriage rate among dental students and to identify the
characteristics of isolated strains. In addition, we aimed
to support the hypothesis that dental students who had
clinical practice experience would have a higher risk of
being an MRSA carrier compared with students who did
not have clinical practice experience.
METHODS
Participants. The institutional review board of Seoul
National University Dental Hospital, Seoul, South Korea,
approved the protocol of this study (CRI14040). We
conducted the survey during a 2-week period from
December 2014 to January 2015. First- to third-year
dental students at the Seoul National University School
of Dentistry participated in this study. Each dental stu-
dent volunteer provided informed consent, and the
participants did not receive any compensation.
Each participant completed a questionnaire
(Appendix, available online at the end of this article) that
included sex, age, school year, duration of clinical
training, and a brief medical history (for example, hy-
pertension, diabetes mellitus, hepatitis, and asthma). We
excluded from the study participants who had a history
of hospitalization, participants who had taken antibiotics
within 30 days, and participants who were undergoing
immunosuppressive or chemotherapeutic treatment.
Sample collection and processing. We inserted a
sterile swab moistened with normal saline into each
participant’s anterior nostril to a depth of approximately
1.5 centimeters and rotated the swab 5 times. For each
specimen, we sampled both nostrils consecutively using
the same swab.
We took all swab samples to the Seoul National
University Clinical Research Institute to be screened for
MRSA growth using chromID MRSA agar (bioMérieux).
Detection of mecA gene and staphylococcal cassette
chromosome mec typing. We extracted and amplified
genomic DNA from each culture with presumptive
MRSA growth by polymerase chain reaction (PCR) to
detect the mecA gene. We determined the staphylococcal
cassette chromosome mec (SCCmec) type (that is, type I
to type V) of each strain consecutively using PCR assay.
Antimicrobial susceptibility testing of isolated
MRSA strains. Using an automated MicroScan Walk-
Away 96 system (Siemens Healthcare Diagnostics), we
measured the minimal inhibitory concentration of each
antimicrobial agent to determine each agent’s resistance
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or susceptibility. We tested the following 22 antimicro-
bials: amoxicillin and clavulanic acid, azithromycin,
ciprofloxacin, clindamycin, daptomycin, erythromycin,
fosfomycin, fusidic acid, gentamicin, imipenem, levo-
floxacin, linezolid, moxifloxacin, mupirocin, nitro-
furantoin, oxacillin, quinupristin and dalfopristin
(Synercid, Pfizer), rifampin, teicoplanin, tetracycline,
trimethoprim and sulfamethoxazole (TMP-SMX), and
vancomycin. We considered resistance to oxacillin to be
equivalent to resistance to methicillin.13 We performed
quality control by testing a standard S. aureus strain
(American Type Culture Collection 29213).
Decolonization of nasal MRSA carriers. We advised
all students with nasal MRSA colonization to see a
clinician to discuss possible decolonization. To achieve
decolonization, these students applied mupirocin oint-
ment twice daily for 7 consecutive days. We retested all
students who had undergone decolonization for MRSA
colonization.
Statistics. We carried out statistical comparisons us-
ing SPSS software 20.0 (IBM). We applied the c2 test or
the Fisher exact test to determine the significance of
differences between 2 dental student groups (that is,
students who had clinical experience and students who
did not have clinical experience). We considered a
P value of < .05 to be statistically significant.
RESULTS
Demographic characteristics of participants. Initially,
160 dental students participated in our study. However,
we excluded 1 student from the study because the student
had been hospitalized within 30 days of the study.
Therefore, we included a total of 159 dental students.
Among these students were 38 (23.9%) first-year, 44
(27.7%) second-year, and 77 (48.4%) third-year dental
students. There were 109 (68.6%) male students, and the
mean age was 26.8 years (range, 22-35).
Microbiological results. Of the 159 students, 5 (3.1%)
students’ nasal cultures contained MRSA isolates. We
confirmed this by determining the presence of the mecA
gene. All isolates occurred in third-year male students,
who had a mean age of 29.4 years (range, 26-32). Sub-
sequently, we determined the SCCmec types and found
that 4 strains were SCCmec type IV, and 1 strain was
SCCmec type I (Table 1).
ABBREVIATION KEY. CA-MRSA: Community-associated
methicillin-resistant Staphylococcus aureus. CDC: Centers for
Disease Control and Prevention. DHCP: Dental health care
professional. HA-MRSA: Hospital-associated methicillin-
resistant Staphylococcus aureus. HCP: Health care professional.
MRSA: Methicillin-resistant Staphylococcus aureus. NA: Not
applicable. PCR: Polymerase chain reaction. PPE: Personal
protective equipment. R: Resistant. S: Susceptible. SCCmec:
Staphylococcal cassette chromosome mec. TMP-SMX:
Trimethoprim and sulfamethoxazole.
 ORIGINAL CONTRIBUTIONS

All 5 strains were resistant to TABLE 1

amoxicillin and clavulanic acid, SCCmec* type and antimicrobial susceptibility
imipenem, and oxacillin. They †
were all susceptible to daptomycin, results of MRSA isolates.
fosfomycin, fusidic acid, linezolid, CHARACTERISTIC STRAIN 1 STRAIN 2 STRAIN 3 STRAIN 4 STRAIN 5
mupirocin, nitrofurantoin, quinu- Age (y) 32 26 31 32 26
pristin and dalfopristin (Synercid), Sex Male Male Male Male Male
rifampin, teicoplanin, tetracycline, School Year Third Third Third Third Third
TMP-SMX, and vancomycin. Length of Clinical Experience 6 mo 6 mo 6 mo 6 mo 6 mo
Table 1 shows the resistance or mecA Gene +‡ + + + +
susceptibility of each strain to other SCCmec Type IV IV IV IV I
antimicrobials. Antimicrobial Susceptibility Results
Decolonization results. One Amoxicillin and clavulanic acid R§ R R R R
student refused to undergo decolo- Azithromycin R R R S¶ R
nization, and the remaining 4 Ciprofloxacin R S S S S
students completed decolonization. Clindamycin R R R S R
After applying mupirocin ointment Daptomycin S S S S S
for 7 days, all 4 of these students Erythromycin R R R S R
tested negative for MRSA Fosfomycin S S S S S
colonization. Fusidic acid S S S S S
Comparison between dental Gentamicin R S S S S
students who had clinical experi- Imipenem R R R R R
ence and dental students who Levofloxacin R S S S S
did not have clinical experience. Linezolid S S S S S
According to Seoul National Uni- Moxifloxacin R S S S S
versity School of Dentistry’s cur- Mupirocin S S S S S
riculum, students do not participate Nitrofurantoin S S S S S
in clinical practice during their first Oxacillin R R R R R
2 years of the program. Beginning Quinupristin and dalfopristin# S S S S S
in the third year, students have the Rifampin S S S S S
opportunity to participate in clin- Teicoplanin S S S S S
ical dental practice at the Seoul Tetracycline S S S S S
National University Dental Hospi- Trimethoprim and sulfamethoxazole S S S S S
tal. We divided the students in our Vancomycin S S S S S
study into 2 groups (that is, stu- * SCCmec: Staphylococcal cassette chromosome mec.
dents who had clinical experience † MRSA: Methicillin-resistant Staphylococcus aureus.
and students who did not have ‡ +: Positive.
§ R: Resistant.
clinical experience). The group who ¶ S: Susceptible.
had clinical experience had partic- # Brand name is Synercid (Pfizer).
ipated in approximately 6 months
of clinical practice. When we
compared the 2 groups, we noted that the group who had a nationwide surveillance study of noninstitutionalized
clinical experience had a significantly higher rate of nasal US residents reported that 28.6% of the study partici-
MRSA carriage (P < .05). We noted no significant dif- pants were nasal carriers of S. aureus and that 1.5% of the
ferences in sex between the 2 groups, but we found that study participants carried MRSA.5 Although having a
the group who had clinical experience was significantly nasal colonization of S. aureus or MRSA itself is not
older than the group who did not have clinical experi- clinically equivalent to having an infectious disease, re-
ence (Table 2). searchers have reported that carriers are at risk of
experiencing self-contamination and transmission.6,9,16,17
DISCUSSION Study results have shown that, among health care
Staphylococcus aureus (S. aureus) is part of the normal professionals (HCPs) followed by investigators in 104
flora in the nose, throat, and oral cavity.6,9 Approxi- studies, the mean rate of nasal carriage of MRSA was
mately 25% to 30% of the general population are nasal 4.1%.18 However, carriage rates varied by geographical
5,14,15
carriers of S. aureus at any given time. Among these location, time of study, hospital type, ward type, and
people, a low percentage (less than 2%) has a colonized occupation.4,18 Investigators have shown that the MRSA
case of MRSA.4,5,15 In 2003 and 2004, the investigators of carriage rate among DHCPs is relatively lower than the

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 ORIGINAL CONTRIBUTIONS
TABLE 2
Comparison between dental students
who had clinical experience and dental
students who did not have clinical
experience.
CHARACTERISTIC DENTAL STUDENTS DENTAL STUDENTS
WHO DID NOT HAVE WHO HAD
CLINICAL EXPERIENCE CLINICAL EXPERIENCE
(n [ 82) (n [ 77)
Age (y) 26.0 (range, 22-32) 27.6 (range, 24-35)
Sex, No. (%)
Male 62 (82.5) 47 (62.0)
Female 20 (17.5) 30 (38.0)
Nasal Colonization
of MRSA,† No. (%)
Positive 0 (0) 5 (6.4)
* NA: Not applicable.
† MRSA: Methicillin-resistant Staphylococcus aureus.
rate of MRSA carriage among HCPs and that the MRSA
carriage rate for DHCPs is close to the MRSA carriage
rate of the general population.4
MRSA is most frequently transmitted via the
transiently contaminated hands of HCPs, including
DHCPs.11,18,19 Investigators have suggested that contam-
inated environmental surfaces can play a minor role
in MRSA transmission.8,9,11,15,19 Thus, direct or indirect
contact with a patient or the environment are the main
routes of MRSA transmission.11,20 Other investigators
have indicated that MRSA can be isolated from saliva
and dental plaque.21,22 Also, investigators have docu-
mented aerial dispersal of MRSA from patients with
MRSA colonization.23 MRSA transmission via a droplet
or an airborne route in dental settings is theoretically
possible, but no investigators have reported actual
transmissions. However, DHCPs should be aware of
the possibility of transmission via these routes because
investigators have reported that the dental health care
environment can be contaminated by microbial aerosol
and splashes from patients produced by dental
devices.4,24
Few studies have been published on the topic of nasal
carriage of MRSA among dental school students. The
results of a 2014 study by Martinez-Ruiz and colleagues7
at the National University of Mexico showed that 20% of
dental school students who had 5 to 6 years of cumula-
tive clinical exposure to patients carried MRSA. In
addition, Roberts and colleagues9 showed that 21% of
dental students at the University of Washington were
MRSA carriers. These results are important because they
show that not only are dental students at risk of expe-
riencing self-infection, but that many dental patients and
other DHCPs also are exposed to the risk of experiencing
MRSA through transmission. In our study, we found that
3.1% of dental school students at the Seoul National
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University were nasal carriers of MRSA.
Although this rate is relatively higher than that
of the general population, it is much lower than
the results found in other dental schools.7,9
This might be owing to the relatively short
duration (that is, 0-6 months) of the clinical
experience of the students who were included
P VALUE
in our study. Further studies are needed to
provide a more accurate explanation for the
relatively low rate of nasal carriage of MRSA in
< .05 dental students in South Korea compared with
dental students in other nations.
NA* Interestingly, our study results demon-
strated that dental students who had clinical
experience (6.4%) had a significantly higher
rate of nasal carriage of MRSA compared with
< .05
students who did not have clinical experience
(0%). Roberts and colleagues9 also showed that
the carriage rate of fourth-year dental students
(26%) differed from that of first-year students
(6.6%). These data indicate that clinical exposure to
patients is an important risk factor for becoming a nasal
carrier of MRSA.
Typically, HA-MRSA infection is associated with
SCCmec types I, II, and III, whereas CA-MRSA infection
is associated with SCCmec type IV.25 In South Korea,
the most common HA-MRSA strain is type IV, and the
most common CA-MRSA strain is type II.3 However, the
results of some studies have shown that a substantial
percentage of CA-MRSA infections were caused by types
II and III and that HA-MRSA infections were caused by
type IV.3,26 Therefore, SCCmec typing alone cannot be
used to classify a strain as CA-MRSA or HA-MRSA. In
our study, 4 isolated MRSA strains were type IV and 1
was type I. It is difficult to verify whether these isolated
MRSA strains were CA-MRSA or HA-MRSA owing to
the lack of information.
According to the results of the antimicrobial sus-
ceptibility tests we performed in our study, all 5 strains
of isolated MRSA were susceptible to several antimi-
crobial agents, including mupirocin, rifampin, and
TMP-SMX. The strains were resistant to multiple other
antimicrobial agents, including amoxicillin and clav-
ulanic acid, which is a commonly used antibiotic in the
dental field.
To eradicate the nasal carriage of MRSA, the use of
nasal mupirocin 2% ointment twice daily for 7 days is
common and has been proven to be safe and effective.18,27
If this treatment method fails, clinicians can consider
prescribing oral rifampin with TMP-SMX.18 We tested all
of the MRSA isolates in our study and found them to be
susceptible to mupirocin; 4 of the 5 students in our study
with nasal carriage of MRSA successfully achieved
decolonization by using mupirocin ointment.
Because our study results showed that some dental
school students had MRSA colonization, we believe it is
 ORIGINAL CONTRIBUTIONS
necessary to provide education on MRSA colonization
and transmission control. There are no published
guidelines on MRSA transmission control that are
specifically targeted to clinicians in dental health care
settings. Instead, the standard precautions recommended
by the Centers for Disease Control and Prevention
(CDC) are considered to be generally adequate for pre-
venting the transmission of MRSA in outpatient dental
clinics.6,20 Standard precautions are recommended for
clinicians in all health care settings to prevent trans-
mission from patients who potentially have coloniza-
tion.6,28 These precautions are based on the principle that
blood, body fluids, secretions, excretions (except sweat),
skin that is not intact, and mucous membranes may
contain transmissible infectious agents.28 These standard
precautions consist of general practice protocols such as
hand hygiene; use of personal protective equipment
(PPE); appropriate handling of contaminated equipment,
materials, and surfaces; safe handling of sharps; safe
injection practices; and respiratory hygiene and cough
etiquette.28,29 Although most DHCPs routinely use PPE
such as single-use gloves and are aware of infection
control guidelines,4,30 some DHCPs may neglect per-
forming some of the standard precautions during daily
practice. For example, a DHCP may inadvertently touch
his or her nose or skin, which could lead to MRSA
exposure, because the exterior of a gloved hand can
become contaminated with MRSA.6 Therefore, it is
important for DHCPs to appropriately review the stan-
dard precautions and strictly adhere to these protocols.
As for caring for patients with uncontrolled wound
drainage, DHCPs should refer to the CDC’s contact
precautions in addition to the standard precautions.6,20
These additional measures include applying PPE when
entering a patient’s room, placing patients in single-
patient rooms when available or placing patients in
cohorts, and limiting patient transport.6,20,28
A limitation of our study results is that we did not
perform additional molecular typing, such as pulsed-field
gel electrophoresis or multilocus sequence typing, to
provide the detailed genotypes of isolated strains. Also,
we did not collect additional information regarding
students’ personal hand hygiene or their interactions
with patients or other DHCPs in clinical practice.
CONCLUSIONS
According to the results of our study, we found that 3.1%
of dental school students in Seoul National University
School of Dentistry had nasal colonization of MRSA. In
addition, dental students who had clinical experience had
a significantly higher rate of being a nasal carrier of
MRSA compared with students who did not have clinical
experience. Therefore, clinical exposure to patients is an
important risk factor of becoming a nasal carrier of
MRSA. In addition, it is necessary for dental students
participating in clinical practice to receive education
about MRSA colonization and transmission as well as to
follow infection prevention and control measures. Most
of the MRSA isolates from dental students were SCCmec
type IV. Eradication of nasal MRSA colonization can be
accomplished by applying mupirocin ointment. n
SUPPLEMENTAL DATA
Supplemental data related to this article can be found at
http://dx.doi.org/10.1016/j.adaj.2015.12.004.
Dr. Yoo Sang Baek is a captain, Department of Dermatology, Armed
Forces Seoul Hospital, Seoul, and a doctoral student, College of Medicine,
Korea University, Seoul, South Korea.
Dr. Seung-Ho Baek is a professor, Department of Conservative Dentistry,
Dental Research Institute, Seoul National University School of Dentistry,
Seoul National University Dental Hospital, Seoul, South Korea.
Dr. Yoo is a clinical professor, Department of Conservative Dentistry,
Dental Research Institute, Seoul National University School of Dentistry,
and Department of Comprehensive Treatment Center, Seoul National
University Dental Hospital, 101 Daehak-ro, Jongro-Gu, Seoul, South Korea
03080, e-mail duswl0808@hanmail.net. Address correspondence to Dr. Yoo.
Disclosures. None of the authors reported any disclosures.
This study was funded by The Seoul National University Dental Hospital
Research Fund grant 04-20140078.
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