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Higher nasal carriage rate of methicillin-resistant Staphylococcus aureus among dental students who have clinical experience
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, methicillinresistant 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), communityassociated 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 carriers during their hospitalization. Kurita and colleagues11
ABSTRACT Background. Methicillin-resistant Staphylococcus aureus (MRSA) has been isolated from dental clinical surfaces, dental patients, and dental health care professionals. 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 colonization, 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 clavulanic 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 colonization 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. 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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ORIGINAL CONTRIBUTIONS
suggested that the MRSA-contaminated surfaces of the dental operatory were the reservoirs for MRSA transmission. 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 student 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, hypertension, 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 WalkAway 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 antimicrobials: amoxicillin and clavulanic acid, azithromycin, ciprofloxacin, clindamycin, daptomycin, erythromycin, fosfomycin, fusidic acid, gentamicin, imipenem, levofloxacin, linezolid, moxifloxacin, mupirocin, nitrofurantoin, 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 ointment twice daily for 7 consecutive days. We retested all students who had undergone decolonization for MRSA colonization. Statistics. We carried out statistical comparisons using 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). Subsequently, 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 methicillinresistant 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
TABLE 1 All 5 strains were resistant to 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, quinuAge (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 R S¶ 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 experiImipenem 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 UniMoxifloxacin R S S S S versity School of Dentistry’s curMupirocin 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 S S S S S Quinupristin and dalfopristin# in the third year, students have the Rifampin S S S S S opportunity to participate in clinTeicoplanin S S S S S ical dental practice at the Seoul Tetracycline S S S S S National University Dental HospiTrimethoprim 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. ‡ +: Positive. and students who did not have § R: Resistant. clinical experience). The group who ¶ S: Susceptible. # Brand name is Synercid (Pfizer). had clinical experience had participated 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 particiMRSA carriage (P < .05). We noted no significant difpants 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 expericlinically equivalent to having an infectious disease, reence (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 Approxistudies, 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 Among these location, time of study, hospital type, ward type, and carriers of S. aureus at any given time. 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
Comparison between dental students who had clinical experience and dental students who did not have clinical experience. CHARACTERISTIC
DENTAL STUDENTS DENTAL STUDENTS WHO HAD WHO DID NOT HAVE CLINICAL EXPERIENCE CLINICAL EXPERIENCE (n [ 77) (n [ 82) 26.0 (range, 22-32)
Age (y)
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 contaminated 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 documented 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 cumulative 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 experiencing 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 demonstrated 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 susceptibility tests we performed in our study, all 5 strains of isolated MRSA were susceptible to several antimicrobial agents, including mupirocin, rifampin, and TMP-SMX. The strains were resistant to multiple other antimicrobial agents, including amoxicillin and clavulanic 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 preventing the transmission of MRSA in outpatient dental clinics.6,20 Standard precautions are recommended for clinicians in all health care settings to prevent transmission from patients who potentially have colonization.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 performing 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 standard 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 singlepatient 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 [email protected]. 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. 1. Kim HB, Jang HC, Nam HJ, et al. In vitro activities of 28 antimicrobial agents against Staphylococcus aureus isolates from tertiary-care hospitals in Korea: a nationwide survey. Antimicrob Agents Chemother. 2004;48(4): 1124-1127. 2. Diekema DJ, Pfaller MA, Schmitz FJ, et al. Survey of infections due to Staphylococcus species: frequency of occurrence and antimicrobial susceptibility of isolates collected in the United States, Canada, Latin America, Europe, and the Western Pacific region for the SENTRY Antimicrobial Surveillance Program, 1997-1999. Clin Infect Dis. 2001;32(suppl 2): S114-S132. 3. Song JH, Hsueh PR, Chung DR, et al. Spread of methicillin-resistant Staphylococcus aureus between the community and the hospitals in Asian countries: an ANSORP study. J Antimicrob Chemother. 2011;66(5):10611069. 4. Petti S, Polimeni A. Risk of methicillin-resistant Staphylococcus aureus transmission in the dental healthcare setting: a narrative review. Infect Control Hosp Epidemiol. 2011;32(11):1109-1115. 5. Gorwitz RJ, Kruszon-Moran D, McAllister SK, et al. Changes in the prevalence of nasal colonization with Staphylococcus aureus in the United States, 2001-2004. J Infect Dis. 2008;197(9):1226-1234. 6. Klevens RM, Gorwitz RJ, Collins AS. Methicillin-resistant Staphylococcus aureus: a primer for dentists. JADA. 2008;139(10):1328-1337. 7. Martinez-Ruiz FJ, Carrillo-Espindola TY, Bustos-Martinez J, HamdanPartida A, Sanchez-Perez L, Acosta-Gio AE. Higher prevalence of meticillin-resistant Staphylococcus aureus among dental students. J Hosp Infect. 2014;86(3):216-218. 8. Horiba N, Yoshida T, Suzuki K, et al. Isolation of methicillin-resistant staphylococci in the dental operatory. J Endod. 1995;21(1):21-25. 9. Roberts MC, Soge OO, Horst JA, Ly KA, Milgrom P. Methicillinresistant Staphylococcus aureus from dental school clinic surfaces and students. Am J Infect Control. 2011;39(8):628-632. 10. Apolonio-Alonso AN, Acosta-Gio AE, Bustos-Martinez J, SanchezPerez L, Hamdan-Partida A. Methicillin-resistant Staphylococcus aureus among dental patients. Am J Infect Control. 2011;39(3):254-255. 11. Kurita H, Kurashina K, Honda T. Nosocomial transmission of methicillin-resistant Staphylococcus aureus via the surfaces of the dental operatory. Br Dent J. 2006;201(5):297-300. 12. Martin MV, Hardy P. Two cases of oral infection by methicillinresistant Staphylococcus aureus. Br Dent J. 1991;170(2):63-64. 13. Clinical and Library Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing; Twenty-First Informational Supplement. Wayne, PA: Clinical Laboratory Standards Institute; 2011.
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14. Graham PL 3rd, Lin SX, Larson EL. A U.S. population-based survey of Staphylococcus aureus colonization. Ann Intern Med. 2006;144(5):318-325. 15. Trochesset DA, Walker SG. Isolation of Staphylococcus aureus from environmental surfaces in an academic dental clinic. JADA. 2012;143(2): 164-169. 16. Davis KA, Stewart JJ, Crouch HK, Florez CE, Hospenthal DR. Methicillin-resistant Staphylococcus aureus (MRSA) nares colonization at hospital admission and its effect on subsequent MRSA infection. Clin Infect Dis. 2004;39(6):776-782. 17. Wertheim HF, Walsh E, Choudhurry R, et al. Key role for clumping factor B in Staphylococcus aureus nasal colonization of humans. PLoS Med. 2008;5(1):e17. 18. Albrich WC, Harbarth S. Health-care workers: source, vector, or victim of MRSA? Lancet Infect Dis. 2008;8(5):289-301. 19. Zimmerli M, Widmer AF, Dangel M, Filippi A, Frei R, Meyer J. Methicillin-resistant Staphylococcus aureus (MRSA) among dental patients: a problem for infection control in dentistry? Clin Oral Investig. 2009;13(4):369-373. 20. Harte JA. Standard and transmission-based precautions: an update for dentistry. JADA. 2010;141(5):572-581. 21. de Carvalho MJ, Pimenta FC, Hayashida M, et al. Prevalence of methicillin-resistant and methicillin-susceptible S. aureus in the saliva of health professionals. Clinics (Sao Paulo). 2009;64(4):295-302. 22. Scannapieco FA, Stewart EM, Mylotte JM. Colonization of dental plaque by respiratory pathogens in medical intensive care patients. Crit Care Med. 1992;20(6):740-745. 23. Gehanno JF, Louvel A, Nouvellon M, Caillard JF, Pestel-Caron M. Aerial dispersal of meticillin-resistant Staphylococcus aureus in hospital
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rooms by infected or colonised patients. J Hosp Infect. 2009;71(3): 256-262. 24. Micik RE, Miller RL, Mazzarella MA, Ryge G. Studies on dental aerobiology, part I: bacterial aerosols generated during dental procedures. J Dent Res. 1969;48(1):49-56. 25. Cohen PR. Community-acquired methicillin-resistant Staphylococcus aureus skin infections: a review of epidemiology, clinical features, management, and prevention (published correction appears in Int J Dermatol. 2007;46[2]:230). Int J Dermatol. 2007;46(1):1-11. 26. Park SH, Park C, Yoo JH, et al. Emergence of community-associated methicillin-resistant Staphylococcus aureus strains as a cause of healthcareassociated bloodstream infections in Korea. Infect Control Hosp Epidemiol. 2009;30(2):146-155. 27. Vasquez JE, Walker ES, Franzus BW, Overbay BK, Reagan DR, Sarubbi FA. The epidemiology of mupirocin resistance among methicillinresistant Staphylococcus aureus at a Veterans’ Affairs hospital. Infect Control Hosp Epidemiol. 2000;21(7):459-464. 28. Siegel JD, Rhinehart E, Jackson M, Chiarello L; Healthcare Infection Control Practices Advisory Committee. Management of multidrugresistant organisms in health care settings, 2006. Am J Infect Control. 2007; 35(10 suppl 2):S165-S193. 29. Siegel JD, Rhinehart E, Jackson M, Chiarello L; Health Care Infection Control Practices Advisory Committee. 2007 guideline for isolation precautions: preventing transmission of infectious agents in health care settings. Am J Infect Control 2007;35(10 suppl 2):S65-S164. 30. Al Negrish A, Al Momani AS, Al Sharafat F. Compliance of Jordanian dentists with infection control strategies. Int Dent J. 2008;58(5): 231-236.
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, methicillinresistant 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), communityassociated 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 carriers during their hospitalization. Kurita and colleagues11
ABSTRACT Background. Methicillin-resistant Staphylococcus aureus (MRSA) has been isolated from dental clinical surfaces, dental patients, and dental health care professionals. 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 colonization, 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 clavulanic 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 colonization 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. 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 dental operatory were the reservoirs for MRSA transmission. 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 student 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, hypertension, 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 WalkAway 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 antimicrobials: amoxicillin and clavulanic acid, azithromycin, ciprofloxacin, clindamycin, daptomycin, erythromycin, fosfomycin, fusidic acid, gentamicin, imipenem, levofloxacin, linezolid, moxifloxacin, mupirocin, nitrofurantoin, 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 ointment twice daily for 7 consecutive days. We retested all students who had undergone decolonization for MRSA colonization. Statistics. We carried out statistical comparisons using 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). Subsequently, 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 methicillinresistant 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
TABLE 1 All 5 strains were resistant to 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, quinuAge (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 R S¶ 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 experiImipenem 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 UniMoxifloxacin R S S S S versity School of Dentistry’s curMupirocin 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 S S S S S Quinupristin and dalfopristin# in the third year, students have the Rifampin S S S S S opportunity to participate in clinTeicoplanin S S S S S ical dental practice at the Seoul Tetracycline S S S S S National University Dental HospiTrimethoprim 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. ‡ +: Positive. and students who did not have § R: Resistant. clinical experience). The group who ¶ S: Susceptible. # Brand name is Synercid (Pfizer). had clinical experience had participated 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 particiMRSA carriage (P < .05). We noted no significant difpants 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 expericlinically equivalent to having an infectious disease, reence (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 Approxistudies, 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 Among these location, time of study, hospital type, ward type, and carriers of S. aureus at any given time. 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
Comparison between dental students who had clinical experience and dental students who did not have clinical experience. CHARACTERISTIC
DENTAL STUDENTS DENTAL STUDENTS WHO HAD WHO DID NOT HAVE CLINICAL EXPERIENCE CLINICAL EXPERIENCE (n [ 77) (n [ 82) 26.0 (range, 22-32)
Age (y)
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 contaminated 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 documented 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 cumulative 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 experiencing 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 demonstrated 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 susceptibility tests we performed in our study, all 5 strains of isolated MRSA were susceptible to several antimicrobial agents, including mupirocin, rifampin, and TMP-SMX. The strains were resistant to multiple other antimicrobial agents, including amoxicillin and clavulanic 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 preventing the transmission of MRSA in outpatient dental clinics.6,20 Standard precautions are recommended for clinicians in all health care settings to prevent transmission from patients who potentially have colonization.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 performing 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 standard 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 singlepatient 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 [email protected]. 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. 1. Kim HB, Jang HC, Nam HJ, et al. In vitro activities of 28 antimicrobial agents against Staphylococcus aureus isolates from tertiary-care hospitals in Korea: a nationwide survey. Antimicrob Agents Chemother. 2004;48(4): 1124-1127. 2. Diekema DJ, Pfaller MA, Schmitz FJ, et al. Survey of infections due to Staphylococcus species: frequency of occurrence and antimicrobial susceptibility of isolates collected in the United States, Canada, Latin America, Europe, and the Western Pacific region for the SENTRY Antimicrobial Surveillance Program, 1997-1999. Clin Infect Dis. 2001;32(suppl 2): S114-S132. 3. Song JH, Hsueh PR, Chung DR, et al. Spread of methicillin-resistant Staphylococcus aureus between the community and the hospitals in Asian countries: an ANSORP study. J Antimicrob Chemother. 2011;66(5):10611069. 4. Petti S, Polimeni A. Risk of methicillin-resistant Staphylococcus aureus transmission in the dental healthcare setting: a narrative review. Infect Control Hosp Epidemiol. 2011;32(11):1109-1115. 5. Gorwitz RJ, Kruszon-Moran D, McAllister SK, et al. Changes in the prevalence of nasal colonization with Staphylococcus aureus in the United States, 2001-2004. J Infect Dis. 2008;197(9):1226-1234. 6. Klevens RM, Gorwitz RJ, Collins AS. Methicillin-resistant Staphylococcus aureus: a primer for dentists. JADA. 2008;139(10):1328-1337. 7. Martinez-Ruiz FJ, Carrillo-Espindola TY, Bustos-Martinez J, HamdanPartida A, Sanchez-Perez L, Acosta-Gio AE. Higher prevalence of meticillin-resistant Staphylococcus aureus among dental students. J Hosp Infect. 2014;86(3):216-218. 8. Horiba N, Yoshida T, Suzuki K, et al. Isolation of methicillin-resistant staphylococci in the dental operatory. J Endod. 1995;21(1):21-25. 9. Roberts MC, Soge OO, Horst JA, Ly KA, Milgrom P. Methicillinresistant Staphylococcus aureus from dental school clinic surfaces and students. Am J Infect Control. 2011;39(8):628-632. 10. Apolonio-Alonso AN, Acosta-Gio AE, Bustos-Martinez J, SanchezPerez L, Hamdan-Partida A. Methicillin-resistant Staphylococcus aureus among dental patients. Am J Infect Control. 2011;39(3):254-255. 11. Kurita H, Kurashina K, Honda T. Nosocomial transmission of methicillin-resistant Staphylococcus aureus via the surfaces of the dental operatory. Br Dent J. 2006;201(5):297-300. 12. Martin MV, Hardy P. Two cases of oral infection by methicillinresistant Staphylococcus aureus. Br Dent J. 1991;170(2):63-64. 13. Clinical and Library Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing; Twenty-First Informational Supplement. Wayne, PA: Clinical Laboratory Standards Institute; 2011.
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14. Graham PL 3rd, Lin SX, Larson EL. A U.S. population-based survey of Staphylococcus aureus colonization. Ann Intern Med. 2006;144(5):318-325. 15. Trochesset DA, Walker SG. Isolation of Staphylococcus aureus from environmental surfaces in an academic dental clinic. JADA. 2012;143(2): 164-169. 16. Davis KA, Stewart JJ, Crouch HK, Florez CE, Hospenthal DR. Methicillin-resistant Staphylococcus aureus (MRSA) nares colonization at hospital admission and its effect on subsequent MRSA infection. Clin Infect Dis. 2004;39(6):776-782. 17. Wertheim HF, Walsh E, Choudhurry R, et al. Key role for clumping factor B in Staphylococcus aureus nasal colonization of humans. PLoS Med. 2008;5(1):e17. 18. Albrich WC, Harbarth S. Health-care workers: source, vector, or victim of MRSA? Lancet Infect Dis. 2008;8(5):289-301. 19. Zimmerli M, Widmer AF, Dangel M, Filippi A, Frei R, Meyer J. Methicillin-resistant Staphylococcus aureus (MRSA) among dental patients: a problem for infection control in dentistry? Clin Oral Investig. 2009;13(4):369-373. 20. Harte JA. Standard and transmission-based precautions: an update for dentistry. JADA. 2010;141(5):572-581. 21. de Carvalho MJ, Pimenta FC, Hayashida M, et al. Prevalence of methicillin-resistant and methicillin-susceptible S. aureus in the saliva of health professionals. Clinics (Sao Paulo). 2009;64(4):295-302. 22. Scannapieco FA, Stewart EM, Mylotte JM. Colonization of dental plaque by respiratory pathogens in medical intensive care patients. Crit Care Med. 1992;20(6):740-745. 23. Gehanno JF, Louvel A, Nouvellon M, Caillard JF, Pestel-Caron M. Aerial dispersal of meticillin-resistant Staphylococcus aureus in hospital
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rooms by infected or colonised patients. J Hosp Infect. 2009;71(3): 256-262. 24. Micik RE, Miller RL, Mazzarella MA, Ryge G. Studies on dental aerobiology, part I: bacterial aerosols generated during dental procedures. J Dent Res. 1969;48(1):49-56. 25. Cohen PR. Community-acquired methicillin-resistant Staphylococcus aureus skin infections: a review of epidemiology, clinical features, management, and prevention (published correction appears in Int J Dermatol. 2007;46[2]:230). Int J Dermatol. 2007;46(1):1-11. 26. Park SH, Park C, Yoo JH, et al. Emergence of community-associated methicillin-resistant Staphylococcus aureus strains as a cause of healthcareassociated bloodstream infections in Korea. Infect Control Hosp Epidemiol. 2009;30(2):146-155. 27. Vasquez JE, Walker ES, Franzus BW, Overbay BK, Reagan DR, Sarubbi FA. The epidemiology of mupirocin resistance among methicillinresistant Staphylococcus aureus at a Veterans’ Affairs hospital. Infect Control Hosp Epidemiol. 2000;21(7):459-464. 28. Siegel JD, Rhinehart E, Jackson M, Chiarello L; Healthcare Infection Control Practices Advisory Committee. Management of multidrugresistant organisms in health care settings, 2006. Am J Infect Control. 2007; 35(10 suppl 2):S165-S193. 29. Siegel JD, Rhinehart E, Jackson M, Chiarello L; Health Care Infection Control Practices Advisory Committee. 2007 guideline for isolation precautions: preventing transmission of infectious agents in health care settings. Am J Infect Control 2007;35(10 suppl 2):S65-S164. 30. Al Negrish A, Al Momani AS, Al Sharafat F. Compliance of Jordanian dentists with infection control strategies. Int Dent J. 2008;58(5): 231-236.