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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; ABSTRACT
Yeon-Jee Yoo, DDS, PhD
Background. Methicillin-resistant Staphylococcus
aureus (MRSA) has been isolated from dental clinical

S
ince its isolation in the early 1960s, methicillin- surfaces, dental patients, and dental health care pro-
resistant Staphylococcus aureus (MRSA) has fessionals. The authors conducted a study to determine the
been a cause of great concern.1 The Asia-Pacific prevalence rate of nasal MRSA colonization among dental
region in particular has a relatively high rate school students and to identify the characteristics of the
of S. aureus methicillin resistance.2 MRSA is considered isolated strains.
to be one of the most important nosocomial pathogens Methods. The authors collected nasal samples from
and is associated with multidrug resistance.2,3 In addition 159 dental students. The authors performed mecA gene
to hospital-acquired MRSA (HA-MRSA), community- detection, staphylococcal cassette chromosome mec
associated MRSA (SCCmec) typing, and antimicrobial susceptibility tests on
(CA-MRSA) emerged each sample. The authors compared the results of 2 groups
in the 1990s and has (students who had clinical experience and students who did
spread worldwide.3,4 not have clinical experience).
Investigators have reported that some people have Results. Five (3.1%) dental students had MRSA coloni-
nasal MRSA colonization.5 Theoretically, nasal MRSA zation, as confirmed by the presence of the mecA gene in
colonization can serve as a reservoir for transmission and the nasal cavity. Prior clinical experience was associated
as a risk factor for the development of MRSA infection.6 significantly with nasal MRSA carriage (P < .05). Four of
There is increasing evidence that MRSA also is present in the strains were SCCmec type IV, and 1 strain was SCCmec
dental patients, on dental clinical surfaces, and in dental type I. All isolates were resistant to amoxicillin and clav-
health care professionals (DHCPs), including students.7-11 ulanic acid, imipenem, and oxacillin, but were susceptible
Although there has been limited documentation of the to several antimicrobial agents including mupirocin,
transmission of MRSA infection from DHCPs to patients trimethoprim and sulfamethoxazole, and rifampin. The
during conventional dental therapy,11,12 DHCPs should nasal MRSA colonization was eradicated with the use of
not disregard the possibility of MRSA colonization. In a mupirocin ointment.
case report by Martin and Hardy,12 the dentist involved Conclusions. Nasal MRSA colonization occurs in some
in the transmission described by the authors did not dental students, especially those who have clinical
routinely use gloves and had recently been hospitalized experience.
for emergency surgery when the hospital was dealing Practical Implications. Education about MRSA colo-
with an MRSA outbreak. In a report by Kurita and nization and transmission, as well as infection prevention
colleagues,11 8 of 140 patients who had no evidence of and control measures is necessary for dental students,
MRSA when they were admitted to a hospital ward for especially when they participate in clinical practice.
special dental care and oral surgery became MRSA car- Key Words. Methicillin-resistant Staphylococcus aureus;
riers during their hospitalization. Kurita and colleagues11 MRSA; dental student; nasal carriage; colonization.
JADA 2016:-(-):---
http://dx.doi.org/10.1016/j.adaj.2015.12.004
Copyright ª 2016 American Dental Association. All rights reserved.

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suggested that the MRSA-contaminated surfaces of the or susceptibility. We tested the following 22 antimicro-
dental operatory were the reservoirs for MRSA trans- bials: amoxicillin and clavulanic acid, azithromycin,
mission. After appropriate infection prevention practices ciprofloxacin, clindamycin, daptomycin, erythromycin,
were implemented at both of these studies’ sites, the fosfomycin, fusidic acid, gentamicin, imipenem, levo-
investigators found no subsequent instances of MRSA floxacin, linezolid, moxifloxacin, mupirocin, nitro-
transmission.11,12 furantoin, oxacillin, quinupristin and dalfopristin
Compared with the medical field, proper studies of (Synercid, Pfizer), rifampin, teicoplanin, tetracycline,
MRSA carriage in the dental field are relatively sparse. trimethoprim and sulfamethoxazole (TMP-SMX), and
The aim of our study was to investigate the nasal MRSA vancomycin. We considered resistance to oxacillin to be
carriage rate among dental students and to identify the equivalent to resistance to methicillin.13 We performed
characteristics of isolated strains. In addition, we aimed quality control by testing a standard S. aureus strain
to support the hypothesis that dental students who had (American Type Culture Collection 29213).
clinical practice experience would have a higher risk of Decolonization of nasal MRSA carriers. We advised
being an MRSA carrier compared with students who did all students with nasal MRSA colonization to see a
not have clinical practice experience. clinician to discuss possible decolonization. To achieve
decolonization, these students applied mupirocin oint-
METHODS ment twice daily for 7 consecutive days. We retested all
Participants. The institutional review board of Seoul students who had undergone decolonization for MRSA
National University Dental Hospital, Seoul, South Korea, colonization.
approved the protocol of this study (CRI14040). We Statistics. We carried out statistical comparisons us-
conducted the survey during a 2-week period from ing SPSS software 20.0 (IBM). We applied the c2 test or
December 2014 to January 2015. First- to third-year the Fisher exact test to determine the significance of
dental students at the Seoul National University School differences between 2 dental student groups (that is,
of Dentistry participated in this study. Each dental stu- students who had clinical experience and students who
dent volunteer provided informed consent, and the did not have clinical experience). We considered a
participants did not receive any compensation. P value of < .05 to be statistically significant.
Each participant completed a questionnaire
(Appendix, available online at the end of this article) that RESULTS
included sex, age, school year, duration of clinical Demographic characteristics of participants. Initially,
training, and a brief medical history (for example, hy- 160 dental students participated in our study. However,
pertension, diabetes mellitus, hepatitis, and asthma). We we excluded 1 student from the study because the student
excluded from the study participants who had a history had been hospitalized within 30 days of the study.
of hospitalization, participants who had taken antibiotics Therefore, we included a total of 159 dental students.
within 30 days, and participants who were undergoing Among these students were 38 (23.9%) first-year, 44
immunosuppressive or chemotherapeutic treatment. (27.7%) second-year, and 77 (48.4%) third-year dental
Sample collection and processing. We inserted a students. There were 109 (68.6%) male students, and the
sterile swab moistened with normal saline into each mean age was 26.8 years (range, 22-35).
participant’s anterior nostril to a depth of approximately Microbiological results. Of the 159 students, 5 (3.1%)
1.5 centimeters and rotated the swab 5 times. For each students’ nasal cultures contained MRSA isolates. We
specimen, we sampled both nostrils consecutively using confirmed this by determining the presence of the mecA
the same swab. gene. All isolates occurred in third-year male students,
We took all swab samples to the Seoul National who had a mean age of 29.4 years (range, 26-32). Sub-
University Clinical Research Institute to be screened for sequently, we determined the SCCmec types and found
MRSA growth using chromID MRSA agar (bioMérieux). that 4 strains were SCCmec type IV, and 1 strain was
Detection of mecA gene and staphylococcal cassette SCCmec type I (Table 1).
chromosome mec typing. We extracted and amplified
genomic DNA from each culture with presumptive
MRSA growth by polymerase chain reaction (PCR) to ABBREVIATION KEY. CA-MRSA: Community-associated
detect the mecA gene. We determined the staphylococcal methicillin-resistant Staphylococcus aureus. CDC: Centers for
cassette chromosome mec (SCCmec) type (that is, type I Disease Control and Prevention. DHCP: Dental health care
professional. HA-MRSA: Hospital-associated methicillin-
to type V) of each strain consecutively using PCR assay. resistant Staphylococcus aureus. HCP: Health care professional.
Antimicrobial susceptibility testing of isolated MRSA: Methicillin-resistant Staphylococcus aureus. NA: Not
MRSA strains. Using an automated MicroScan Walk- applicable. PCR: Polymerase chain reaction. PPE: Personal
Away 96 system (Siemens Healthcare Diagnostics), we protective equipment. R: Resistant. S: Susceptible. SCCmec:
measured the minimal inhibitory concentration of each Staphylococcal cassette chromosome mec. TMP-SMX:
antimicrobial agent to determine each agent’s resistance Trimethoprim and sulfamethoxazole.

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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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TABLE 2 University were nasal carriers of MRSA.


Comparison between dental students Although this rate is relatively higher than that
of the general population, it is much lower than
who had clinical experience and dental the results found in other dental schools.7,9
students who did not have clinical This might be owing to the relatively short
experience. duration (that is, 0-6 months) of the clinical
experience of the students who were included
CHARACTERISTIC DENTAL STUDENTS DENTAL STUDENTS P VALUE
WHO DID NOT HAVE WHO HAD in our study. Further studies are needed to
CLINICAL EXPERIENCE CLINICAL EXPERIENCE provide a more accurate explanation for the
(n [ 82) (n [ 77) relatively low rate of nasal carriage of MRSA in
Age (y) 26.0 (range, 22-32) 27.6 (range, 24-35) < .05 dental students in South Korea compared with
Sex, No. (%) dental students in other nations.
Male 62 (82.5) 47 (62.0) NA* Interestingly, our study results demon-
Female 20 (17.5) 30 (38.0) strated that dental students who had clinical
Nasal Colonization experience (6.4%) had a significantly higher
of MRSA,† No. (%)
rate of nasal carriage of MRSA compared with
Positive 0 (0) 5 (6.4) < .05
students who did not have clinical experience
* NA: Not applicable.
† MRSA: Methicillin-resistant Staphylococcus aureus.
(0%). Roberts and colleagues9 also showed that
the carriage rate of fourth-year dental students
(26%) differed from that of first-year students
rate of MRSA carriage among HCPs and that the MRSA (6.6%). These data indicate that clinical exposure to
carriage rate for DHCPs is close to the MRSA carriage patients is an important risk factor for becoming a nasal
rate of the general population.4 carrier of MRSA.
MRSA is most frequently transmitted via the Typically, HA-MRSA infection is associated with
transiently contaminated hands of HCPs, including SCCmec types I, II, and III, whereas CA-MRSA infection
DHCPs.11,18,19 Investigators have suggested that contam- is associated with SCCmec type IV.25 In South Korea,
inated environmental surfaces can play a minor role the most common HA-MRSA strain is type IV, and the
in MRSA transmission.8,9,11,15,19 Thus, direct or indirect most common CA-MRSA strain is type II.3 However, the
contact with a patient or the environment are the main results of some studies have shown that a substantial
routes of MRSA transmission.11,20 Other investigators percentage of CA-MRSA infections were caused by types
have indicated that MRSA can be isolated from saliva II and III and that HA-MRSA infections were caused by
and dental plaque.21,22 Also, investigators have docu- type IV.3,26 Therefore, SCCmec typing alone cannot be
mented aerial dispersal of MRSA from patients with used to classify a strain as CA-MRSA or HA-MRSA. In
MRSA colonization.23 MRSA transmission via a droplet our study, 4 isolated MRSA strains were type IV and 1
or an airborne route in dental settings is theoretically was type I. It is difficult to verify whether these isolated
possible, but no investigators have reported actual MRSA strains were CA-MRSA or HA-MRSA owing to
transmissions. However, DHCPs should be aware of the lack of information.
the possibility of transmission via these routes because According to the results of the antimicrobial sus-
investigators have reported that the dental health care ceptibility tests we performed in our study, all 5 strains
environment can be contaminated by microbial aerosol of isolated MRSA were susceptible to several antimi-
and splashes from patients produced by dental crobial agents, including mupirocin, rifampin, and
devices.4,24 TMP-SMX. The strains were resistant to multiple other
Few studies have been published on the topic of nasal antimicrobial agents, including amoxicillin and clav-
carriage of MRSA among dental school students. The ulanic acid, which is a commonly used antibiotic in the
results of a 2014 study by Martinez-Ruiz and colleagues7 dental field.
at the National University of Mexico showed that 20% of To eradicate the nasal carriage of MRSA, the use of
dental school students who had 5 to 6 years of cumula- nasal mupirocin 2% ointment twice daily for 7 days is
tive clinical exposure to patients carried MRSA. In common and has been proven to be safe and effective.18,27
addition, Roberts and colleagues9 showed that 21% of If this treatment method fails, clinicians can consider
dental students at the University of Washington were prescribing oral rifampin with TMP-SMX.18 We tested all
MRSA carriers. These results are important because they of the MRSA isolates in our study and found them to be
show that not only are dental students at risk of expe- susceptible to mupirocin; 4 of the 5 students in our study
riencing self-infection, but that many dental patients and with nasal carriage of MRSA successfully achieved
other DHCPs also are exposed to the risk of experiencing decolonization by using mupirocin ointment.
MRSA through transmission. In our study, we found that Because our study results showed that some dental
3.1% of dental school students at the Seoul National school students had MRSA colonization, we believe it is

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necessary to provide education on MRSA colonization about MRSA colonization and transmission as well as to
and transmission control. There are no published follow infection prevention and control measures. Most
guidelines on MRSA transmission control that are of the MRSA isolates from dental students were SCCmec
specifically targeted to clinicians in dental health care type IV. Eradication of nasal MRSA colonization can be
settings. Instead, the standard precautions recommended accomplished by applying mupirocin ointment. n
by the Centers for Disease Control and Prevention
(CDC) are considered to be generally adequate for pre- SUPPLEMENTAL DATA
venting the transmission of MRSA in outpatient dental Supplemental data related to this article can be found at
clinics.6,20 Standard precautions are recommended for http://dx.doi.org/10.1016/j.adaj.2015.12.004.
clinicians in all health care settings to prevent trans-
mission from patients who potentially have coloniza- Dr. Yoo Sang Baek is a captain, Department of Dermatology, Armed
tion.6,28 These precautions are based on the principle that Forces Seoul Hospital, Seoul, and a doctoral student, College of Medicine,
blood, body fluids, secretions, excretions (except sweat), Korea University, Seoul, South Korea.
Dr. Seung-Ho Baek is a professor, Department of Conservative Dentistry,
skin that is not intact, and mucous membranes may Dental Research Institute, Seoul National University School of Dentistry,
contain transmissible infectious agents.28 These standard Seoul National University Dental Hospital, Seoul, South Korea.
precautions consist of general practice protocols such as Dr. Yoo is a clinical professor, Department of Conservative Dentistry,
hand hygiene; use of personal protective equipment Dental Research Institute, Seoul National University School of Dentistry,
and Department of Comprehensive Treatment Center, Seoul National
(PPE); appropriate handling of contaminated equipment, University Dental Hospital, 101 Daehak-ro, Jongro-Gu, Seoul, South Korea
materials, and surfaces; safe handling of sharps; safe 03080, e-mail duswl0808@hanmail.net. Address correspondence to Dr. Yoo.
injection practices; and respiratory hygiene and cough
etiquette.28,29 Although most DHCPs routinely use PPE
Disclosures. None of the authors reported any disclosures.

such as single-use gloves and are aware of infection This study was funded by The Seoul National University Dental Hospital
control guidelines,4,30 some DHCPs may neglect per- Research Fund grant 04-20140078.
forming some of the standard precautions during daily 1. Kim HB, Jang HC, Nam HJ, et al. In vitro activities of 28 antimicrobial
practice. For example, a DHCP may inadvertently touch agents against Staphylococcus aureus isolates from tertiary-care hospitals in
his or her nose or skin, which could lead to MRSA Korea: a nationwide survey. Antimicrob Agents Chemother. 2004;48(4):
1124-1127.
exposure, because the exterior of a gloved hand can 2. Diekema DJ, Pfaller MA, Schmitz FJ, et al. Survey of infections due
become contaminated with MRSA.6 Therefore, it is to Staphylococcus species: frequency of occurrence and antimicrobial
important for DHCPs to appropriately review the stan- susceptibility of isolates collected in the United States, Canada, Latin
dard precautions and strictly adhere to these protocols. America, Europe, and the Western Pacific region for the SENTRY Anti-
microbial Surveillance Program, 1997-1999. Clin Infect Dis. 2001;32(suppl 2):
As for caring for patients with uncontrolled wound S114-S132.
drainage, DHCPs should refer to the CDC’s contact 3. Song JH, Hsueh PR, Chung DR, et al. Spread of methicillin-resistant
precautions in addition to the standard precautions.6,20 Staphylococcus aureus between the community and the hospitals in Asian
countries: an ANSORP study. J Antimicrob Chemother. 2011;66(5):1061-
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entering a patient’s room, placing patients in single- 4. Petti S, Polimeni A. Risk of methicillin-resistant Staphylococcus aureus
patient rooms when available or placing patients in transmission in the dental healthcare setting: a narrative review. Infect
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5. Gorwitz RJ, Kruszon-Moran D, McAllister SK, et al. Changes in the
A limitation of our study results is that we did not prevalence of nasal colonization with Staphylococcus aureus in the United
perform additional molecular typing, such as pulsed-field States, 2001-2004. J Infect Dis. 2008;197(9):1226-1234.
gel electrophoresis or multilocus sequence typing, to 6. Klevens RM, Gorwitz RJ, Collins AS. Methicillin-resistant Staphylo-
coccus aureus: a primer for dentists. JADA. 2008;139(10):1328-1337.
provide the detailed genotypes of isolated strains. Also, 7. Martinez-Ruiz FJ, Carrillo-Espindola TY, Bustos-Martinez J, Hamdan-
we did not collect additional information regarding Partida A, Sanchez-Perez L, Acosta-Gio AE. Higher prevalence of
students’ personal hand hygiene or their interactions meticillin-resistant Staphylococcus aureus among dental students. J Hosp
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According to the results of our study, we found that 3.1% resistant Staphylococcus aureus from dental school clinic surfaces and
students. Am J Infect Control. 2011;39(8):628-632.
of dental school students in Seoul National University 10. Apolonio-Alonso AN, Acosta-Gio AE, Bustos-Martinez J, Sanchez-
School of Dentistry had nasal colonization of MRSA. In Perez L, Hamdan-Partida A. Methicillin-resistant Staphylococcus aureus
addition, dental students who had clinical experience had among dental patients. Am J Infect Control. 2011;39(3):254-255.
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