- Email: [email protected]
Prevalence of Staphylococcus aureus Nasal Colonization in Emergency Department Personnel
INFECTIOUS DISEASE/BRIEF RESEARCH REPORT
Prevalence of Staphylococcus aureus Nasal Colonization in Emergency Department Personnel Brian P. Suffoletto, MD Eliot H. Cannon, MD Kaveh Ilkhanipour, MD Donald M. Yealy, MD
From the University of Pittsburgh Department of Emergency Medicine, Pittsburgh, PA.
Study objective: Nasal colonization with Staphylococcus aureus and methicillin-resistant Staphylococcus aureus (MRSA) can precede infection in patients and contacts. Although general population S aureus/MRSA rates are well described, the prevalence of S aureus and MRSA nasal colonization in emergency department health care workers is not defined. We seek to determine the prevalence of S aureus and MRSA nasal colonization among ED health care workers without evidence of an active site of staphylococcal infection and identify variables associated with colonization. Methods: We prospectively studied a convenience sample of ED health care workers from 5 urban teaching hospitals in Pittsburgh, PA. Each participant completed a questionnaire and nasal culturing. We tested susceptibility with the oxacillin disc diffusion method. We analyzed data with descriptive statistics and univariate regression, with ␣ set at 0.05. Results: Of 255 subjects, 23% were physicians; 62% were nurses, nursing assistants, or patient care technicians; and 15% were clerical staff or social service workers. Of 81 (31.8%) S aureus isolates, 11 (13.6%) were MRSA, an overall prevalence of 4.3%. All positive MRSA samples were from nurses, nursing assistants, or patient care technicians. No other covariate had an association with S aureus or MRSA colonization. Conclusion: In this urban ED health care worker population, the prevalence of S aureus is similar but MRSA nasal colonization is higher than previously reported estimates in the general population of the United States. Physicians and nonpatient contact ED health care workers did not have MRSA colonization. [Ann Emerg Med. 2008;52:529-533.] 0196-0644/$-see front matter Copyright © 2008 by the American College of Emergency Physicians. doi:10.1016/j.annemergmed.2008.03.020
SEE EDITORIAL, P. 534. INTRODUCTION Background Staphylococcus aureus is a major source of skin and soft tissue infections.1 The emergence and spread of multidrug-resistant strains, especially methicillin-resistant S aureus (MRSA), is associated with an increased morbidity and mortality and a higher frequency of infections.2-4 Given that up to 38% of healthy subjects who have nasal colonization with MRSA develop subsequent infection5,6 and that elimination of carriage reduces infection rates,7 colonization likely plays a key role in its pathogenesis. National estimates from 2001 to 2002 suggested that the prevalence of S aureus and MRSA colonization was 31.6% and 0.84%, respectively.8 Among health care workers in a single ICU, the prevalence of nasal colonization of S aureus and MRSA was Volume , . : November
28% and 2%, respectively.9 In local outbreaks, health care worker colonization has been reported to be as high as 50%.10 Among hospitalized patients, the prevalence of colonization is higher among subjects with previous MRSA infections, previous hospitalizations, and high-risk behaviors.11 The risk factors for colonization among healthy subjects, including health care workers, remain largely unknown but are likely influenced by environmental exposures. Given that S aureus and MRSA strains have been isolated from stethoscopes, pagers, bed spaces, and workstations, health care workers may have increased risk for self-inoculation from workplace exposure.12 Importance Nationally, 7% or more of patients admitted to the hospital are colonized with MRSA,13 and approximately 40% of all admissions to a hospital come through the ED. Thus, the ED is a potential bacteriologic mixing ground where the transfer of organisms among a clustered population with varying illness burden is likely. Annals of Emergency Medicine 529
Staphylococcus aureus Nasal Colonization
Editor’s Capsule Summary
What is already known on this topic The prevalence of community-associated methicillin-resistant Staphylococcus aureus (MRSA) skin and soft tissue infections observed in emergency departments (EDs) has substantially increased in the last few years, leading to greater exposure of ED staff. What question this study addressed What is the prevalence of MRSA nasal colonization among ED providers? What this study adds to our knowledge Of 255 ED staff tested at the beginning of their shift, 11 (4.3%; 95% confidence interval 0% to 9.3%) had MRSA cultured from their nares. How this might change clinical practice The prevalence of nasal MRSA among staff in this ED is higher than in the general population. It remains unknown whether these are community- or health care–associated strains and whether colonization increases subsequent infection in these individuals or their contacts. Emergency department (ED) personnel could be vessels for nasal carriage of MRSA and inadvertently spread the pathogen. The prevalence of MRSA colonization among ED health care workers is not known. It is important to identify which ED personnel are at the highest risk of colonization. Information about ED health care worker MRSA prevalence also could assist in the development of guidelines for infection control. Goals of This Investigation We sought to determine the prevalence of S aureus and MRSA in ED health care workers. We also sought to identify demographic and exposure variables associated with MRSA in our population. We hypothesized that the prevalence of nasal carriage of MRSA was greater than previously reported estimates in the general population of the United States because of the frequency of exposure to infected or colonized patients.
MATERIALS AND METHODS Study Design We use a prospective, observational study design of a convenience sample of ED health care workers. Setting Volunteers from 5 urban teaching hospital EDs in Pittsburgh, PA, consented to participate. The annual ED census at the 5 hospitals ranged from approximately 31,000 to 48,000 530 Annals of Emergency Medicine
Suffoletto et al per year. We obtained approval from all medical center institutional review boards. Selection of Participants We announced the study in an e-mail to ED staff and placed flyers in staff areas. Volunteers gave written consent, completed the questionnaire, and had nasal culture samples taken by 2 authors (B.P.S., E.C.) from October 2006 through December 2006. We included ED health care workers on all shifts and collected nasal samples at the beginning of each shift to reduce selection bias and to identify persistent colonization, as opposed to transient colonization from recent self-inoculation. We included only ED health care workers working in a single ED and without a known recent S aureus/MRSA infection or colonization. Additionally, we excluded anyone hospitalized in the last year. Data Collection and Processing The questionnaire included an assessment of limited demographics and recent antibiotic and MRSA exposure. At initial enrollment in the ED, we sampled each participant’s anterior nares with sterile Dacron swabs. The swabs were coded and transported within 6 hours to the Allegheny County Health Department. Laboratory analysis at the Allegheny County Health Department consisted of bacterial culture and antibiotic susceptibility/resistance assays, using standardized methods. The swab samples were rolled on sheep blood agar then incubated inverted for 16 to 24 hours at 35°C in air. Laboratory technicians Gram stained and coagulase tested all colonies. We tested antibiotic resistance with oxacillin disc diffusion with the BBL Prompt kit (Beckton Dickinson, Sparks, NC). As a quality control measure, known S aureus/MRSA strain testing occurred on Mueller-Hinton agar plates and with antibiotic discs diffusion tests. For samples that grew S aureus (coagulase-positive staphylococcus), we reported the results as “oxacillin-resistant” (MRSA), intermediate-resistance S aureus, or “MRSA not found.” Primary Data Analysis All volunteers were healthy and without evidence of an active site of staphylococcal infection at the testing time; we therefore defined isolation of S aureus and MRSA from the nares as colonization.14 We compiled the subject number and culture results from the 5 testing sites. A priori we calculated a sample size of 223 needed to compare a known proportion of MRSA-positive of 0.0084 in the US population7 to a hypothesized proportion of 0.03 in our cohort. We entered all questionnaire and bacteriology data into an Excel 2007 database (Microsoft, Redmond, WA). Prevalence and 95% confidence intervals (CIs) were calculated. We tested potential predictor variables associated with MRSA colonization, using univariate analysis with ␣ set at 0.05 and using Stata 9.0. Volume , . : November
Suffoletto et al
Staphylococcus aureus Nasal Colonization
Table 1. Selected demographic and antibiotic/infection-related characteristics of study subjects. Characteristic
Total Participants, No. (%)
S aureus Present, No. (% [95% CI])
Total 255 (100) Hospital 1 60 (23.5) 2 60 (23.5) 3 60 (23.5) 4 32 (12.6) 5 43 (16.9) Age, y ⱕ30 54 (22.3) 31–45 126 (49.4) 46–60 72 (28.3) Sex Male 101 (39.6) Female 154 (60.4) Job Title Physician/PA 58 (23.1) RN/NA/PCT 159 (62.4) Clerical/Soc Svc 38 (14.5) Antibiotic use in past 6 mo No 211 (82.8) Yes 44 (17.2) Past MRSA infection No 252 (98.8) Yes 3 (1.2) MRSA infection in household No 244 (95.7) Yes 11 (4.3) Other health care worker in household No 194 (76.1) Yes 61 (23.9)
MRSA Present, No. (% [95% CI])
81 (31.8)
11 (4.31)
18 (30.0 [19.0–43.0]) 19 (31.7 [20.3–45.0]) 20 (33.3 [21.7–46.8]) 9 (28.1 [13.7–46.7]) 15 (34.9 [21.0–50.9])
2 (3.3 [0.4–11.5]) 3 (5.0 [1.0–13.9]) 2 (3.3 [0.4–11.5]) 1 (3.1 [0.1–16.2]) 3 (7.0 [1.5–19.1])
11 (20.3 [10.6–33.5]) 48 (38.1 [29.6–47.2]) 22 (30.6 [20.2–42.5])
1 (1.9 [0.05–9.9]) 7 (5.6 [2.3–11.1]) 3 (4.2 [0.87–11.7])
34 (33.7 [24.6–43.8]) 47 (30.5 [23.4–38.4])
4 (4.0 [1.1–9.8]) 7 (4.5 [1.8–9.1])
22 (37.9 [25.5–51.6]) 48 (30.2 [23.2–38.0]) 11 (28.9 [15.4–45.9])
0 11 (6.9 [3.5–12.0]) 0
69 (32.7 [26.4–39.5]) 12 (27.3 [15.0–42.8])
8 (3.8 [1.7–7.3]) 3 (6.8 [1.4–18.7])
80 (31.7 [26.0–37.9]) 1 (33.3 [0.8–90.6])
11 (4.4 [2.2–7.7]) 0
79 (32.4 [26.5–38.6]) 2 (18.2 [2.3–51.8])
10 (4.1 [2.0–7.4]) 1 (9.1 [0.2–41.3])
59 (30.4 [24.0–37.4]) 22 (36.1 [24.2–49.4])
10 (5.2 [2.5–9.3]) 1 (1.6 [0.04–8.8])
PA, Physician assistant; RN, registered nurse; NA, nurses assistant; PCT, patient care technician. Household denied as a frequent, personal contact.
RESULTS During a 3-month period, we enrolled 255 subjects. The absolute number and demographics of those who refused to participate were not systematically recorded. Subject demographics and antibiotic/infection-related characteristics as they relate to culture results are in Table 1. The majority (68.2%) of nasal cultures were negative for S aureus. Of the 81 S aureus isolates, 11 (13.6%; 95% CI 0% to 28.5%) were MRSA. Overall, the prevalence of MRSA was 4.3% (95% CI 0% to 9.3%). Variables associated with MRSA colonization are presented in Table 2, identified by univariate logistic regression analysis. In short, nurses, nursing assistants, and radiology and respiratory technicians composed the entire MRSA colonization group.
Table 2. Selected characteristics associated with MRSA colonization.
Predictor Variable Age, y ⱕ30 31-45 46-60 Female sex Antibiotic use in past 6 mo MRSA infection in household Other health care worker in household
No. of Colonized Subjects No. (%) 54 126 72 154 44 11 61
1 (1.9) 7 (5.6) 3 (4.2) 7 (4.5) 3 (6.8) 1 (9.1) 1 (1.6)
Colonized Odds Ratio (95% CI) Reference 3.12 (0.37-26.0) 2.31 (0.23-22.8) 1.15 (0.32-4.05) 1.86 (0.47-7.30) 2.34 (0.27-20.1) 0.31 (0.04-2.44)
All variables potentially associated with MRSA colonization are presented, except job title, where nursing, nursing assistants, and radiology and respiratory technicians predicted colonization perfectly. No covariate presented was significantly associated with MRSA colonization.
LIMITATIONS We identified MRSA colonization in a single urban region and in teaching hospitals, which may limit the external validity of this work. We attempted to minimize local effects by sampling from 5 different ED environments. There is a potential for selection bias, given that ED health care workers who worked more and had greater contact with patients had a greater likelihood to be approached and agree to participate. Volume , . : November
Also, those who were either less or more likely to be colonized may have refused to participate. We collected nasal samples at a single point in time, potentially identifying those with transient exposure, not persistent carriers. We took steps to minimize identifying transient carriers by collecting samples before clinical exposure on the day of sampling. Annals of Emergency Medicine 531
Staphylococcus aureus Nasal Colonization
Suffoletto et al
We focused on work demographics and did not collect other potential predictors of MRSA such as race, ethnicity, health status, or intravenous drug abuse history because of privacy issues. We did not perform multiple antibiotic sensitivity studies or genotype the colonies, limiting the ability to biologically classify them as community-acquired strains. Given the amount of time that ED health care workers care for patients who have considerable health care setting exposures, we also did not attempt to clinically classify MRSA strains as community acquired or hospital acquired. We were unable to contemporaneously compare the prevalence of colonization in ED health care workers to that of our local nonED health care worker population and therefore had to use previously reported estimates from the Health and Nutrition Examination Survey 2001 to 2002, representing the noninstitutionalized US population. Given that the prevalence of S aureus and MRSA skin infections has increased over time,4 there is a chance that current estimates of US colonization prevalence are not significantly greater than that of ED health care workers.
Drs. Talan and Callaham were the supervising editors on this article. Dr. Yealy did not participate in the editorial review or decision to publish this article.
DISCUSSION
REFERENCES
The colonization prevalence reported in this study is greater than previously reported estimates in the general population of the United States but less than colonization of health care workers during outbreaks.10 There have been no reported MRSA outbreaks at any of the participating hospitals during the period of sampling; therefore, we believe that our findings reflect a nonepidemic carrier state. Data from outbreaks of community-associated MRSA infection suggest that skin-skin and skin-fomite contact represent important and common routes of acquisition of MRSA colonization.12 It is possible that the frequency and duration of contacts among nursing-related duties puts them at increased risk for MRSA transfer. In summary, MRSA is more prevalent in ED health care workers than previously reported estimates in the general population of the United States, especially those with a greater frequency and duration of patient contact. If affirmed, these data might help guide MRSA infection control measures in the ED. We thank Tom Campbell, MD, Fred Harchelroad, Jr, MD, and Rick Wadas, MD, for the recruitment of subjects and Bruce Dixon, MD, and the staff of the Allegheny Department of Health for laboratory support. We would also like to thank Pam Cockley, RN, for data collection. Supervising editors: David A. Talan, MD; Michael L. Callaham, MD Author contributions: BPS, EHC, KI, and DMY were responsible for data collection, analysis, and interpretation and article preparation and revision. KI and DMY were responsible for conception of the study. BPS takes responsibility for the paper as a whole.
532 Annals of Emergency Medicine
Funding and support: By Annals policy, all authors are required to disclose any and all commercial, financial, and other relationships in any way related to the subject of this article, that might create any potential conflict of interest. See the Manuscript Submission Agreement in this issue for examples of specific conflicts covered by this statement. Dr. Suffoletto is supported by the Society for Academic Emergency Medicine Institutional Training grant. Publication dates: Received for publication February 29, 2008. Revision received March 14, 2008. Accepted for publication March 21, 2008. Available online April 24, 2008. Reprints not available from the authors. Address for correspondence: Brian Suffoletto, MD, Department of Emergency Medicine, University of Pittsburgh, 230 McKee Place, Suite 400, Pittsburgh, PA 15213; 412-9016892, fax 412-647-6669; E-mail [email protected].
1. Moran GJ, Krishnadasan A, Gorwitz RJ, et al. Methicillin-resistant S aureus infections among patients in the emergency department. N Engl J Med. 2006;355:666-674. 2. Cosgrove SE, Sakoulas G, Perencevich EN, et al. Comparison of mortality associated with methicillin-resistant and methicillinsusceptible Staphylococcus aureus bacteremia: a meta-analysis. Clin Infect Dis. 2003;36:53-59. 3. Delaney JA, Schneider-Lindner V, Brassard P, et al. Mortality after infection with methicillin resistant Staphylococcus aureus (MRSA) diagnosed in the community. BMC Med. 2008;6:2-10. 4. Pallin DJ, Egan DJ, Pelletier AJ, et al. Increased US emergency department visits for skin and soft tissue infections, and changes in antibiotic choices, during the emergence of communityassociated methicillin-resistant Staphylococcus aureus. Ann Emerg Med. 2008;51:291-298. 5. Ellis MW, Hospenthal DR, Dooley DP, et al. Natural history of community-acquired methicillin-resistant Staphylococcus aureus colonization and infection in soldiers. Clin Infect Dis. 2004;39:971-979. 6. Ellis MW, Griffith ME, Dooley DP, et al. Targeted intranasal mupirocin to prevent colonization and infection by communityassociated methicillin-resistant Staphylococcus aureus strains in soldiers: a cluster randomized controlled trial. Antimicrob Agents Chemother. 2007;51:3591-3598. 7. Kluytmans J, van Belkum A, Verbrugh H. Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin Microbiol Rev. 1997;10:505-520. 8. Graham PL 3rd, Lin SX, Larson EL. A U.S. population-based survey of Staphylococcus aureus colonization. Ann Intern Med. 2006;144:318-325. 9. Johnston CP, Stokes AK, Ross T, et al. Staphylococcus aureus colonization among healthcare workers at a tertiary care hospital. Infect Control Hosp Epidemiol. 2007;28:1404-1407. 10. Cookson B, Peters B, Webster M, et al. Staff carriage of epidemic methicillin-resistant Staphylococcus aureus. J Clin Microbiol. 1989;27:1471-1476. 11. Hidron AI, Kourbatova EV, Halvosa JS, et al. Risk factors for colonization with methicillin-resistant Staphylococcus aureus (MRSA) in patients admitted to an urban hospital: emergence of community-associated MRSA nasal carriage. Clin Infect Dis. 2005;41:159-166.
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Suffoletto et al 12. Miller LG, Diep BA. Clinical practice: colonization, fomites, and virulence: rethinking the pathogenesis of community-associated methicillin-resistant Staphylococcus aureus infection. Clin Infect Dis. 2008;46:752-760. 13. Jarvis WR, Schlosser J, Chinn RY, et al. National prevalence of methicillin-resistant Staphylococcus aureus in inpatients at US
Staphylococcus aureus Nasal Colonization health care facilities, 2006. Am J Infect Control. 2007;35:631-637. 14. Naimi TS, LeDell KH, Como-Sabetti K, et al. Comparison of community- and health care–associated methicillinresistant Staphylococcus aureus infection. JAMA. 2003;290: 2976-2984.
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Volume , . : November
Annals of Emergency Medicine 533
Prevalence of Staphylococcus aureus Nasal Colonization in Emergency Department Personnel Brian P. Suffoletto, MD Eliot H. Cannon, MD Kaveh Ilkhanipour, MD Donald M. Yealy, MD
From the University of Pittsburgh Department of Emergency Medicine, Pittsburgh, PA.
Study objective: Nasal colonization with Staphylococcus aureus and methicillin-resistant Staphylococcus aureus (MRSA) can precede infection in patients and contacts. Although general population S aureus/MRSA rates are well described, the prevalence of S aureus and MRSA nasal colonization in emergency department health care workers is not defined. We seek to determine the prevalence of S aureus and MRSA nasal colonization among ED health care workers without evidence of an active site of staphylococcal infection and identify variables associated with colonization. Methods: We prospectively studied a convenience sample of ED health care workers from 5 urban teaching hospitals in Pittsburgh, PA. Each participant completed a questionnaire and nasal culturing. We tested susceptibility with the oxacillin disc diffusion method. We analyzed data with descriptive statistics and univariate regression, with ␣ set at 0.05. Results: Of 255 subjects, 23% were physicians; 62% were nurses, nursing assistants, or patient care technicians; and 15% were clerical staff or social service workers. Of 81 (31.8%) S aureus isolates, 11 (13.6%) were MRSA, an overall prevalence of 4.3%. All positive MRSA samples were from nurses, nursing assistants, or patient care technicians. No other covariate had an association with S aureus or MRSA colonization. Conclusion: In this urban ED health care worker population, the prevalence of S aureus is similar but MRSA nasal colonization is higher than previously reported estimates in the general population of the United States. Physicians and nonpatient contact ED health care workers did not have MRSA colonization. [Ann Emerg Med. 2008;52:529-533.] 0196-0644/$-see front matter Copyright © 2008 by the American College of Emergency Physicians. doi:10.1016/j.annemergmed.2008.03.020
SEE EDITORIAL, P. 534. INTRODUCTION Background Staphylococcus aureus is a major source of skin and soft tissue infections.1 The emergence and spread of multidrug-resistant strains, especially methicillin-resistant S aureus (MRSA), is associated with an increased morbidity and mortality and a higher frequency of infections.2-4 Given that up to 38% of healthy subjects who have nasal colonization with MRSA develop subsequent infection5,6 and that elimination of carriage reduces infection rates,7 colonization likely plays a key role in its pathogenesis. National estimates from 2001 to 2002 suggested that the prevalence of S aureus and MRSA colonization was 31.6% and 0.84%, respectively.8 Among health care workers in a single ICU, the prevalence of nasal colonization of S aureus and MRSA was Volume , . : November
28% and 2%, respectively.9 In local outbreaks, health care worker colonization has been reported to be as high as 50%.10 Among hospitalized patients, the prevalence of colonization is higher among subjects with previous MRSA infections, previous hospitalizations, and high-risk behaviors.11 The risk factors for colonization among healthy subjects, including health care workers, remain largely unknown but are likely influenced by environmental exposures. Given that S aureus and MRSA strains have been isolated from stethoscopes, pagers, bed spaces, and workstations, health care workers may have increased risk for self-inoculation from workplace exposure.12 Importance Nationally, 7% or more of patients admitted to the hospital are colonized with MRSA,13 and approximately 40% of all admissions to a hospital come through the ED. Thus, the ED is a potential bacteriologic mixing ground where the transfer of organisms among a clustered population with varying illness burden is likely. Annals of Emergency Medicine 529
Staphylococcus aureus Nasal Colonization
Editor’s Capsule Summary
What is already known on this topic The prevalence of community-associated methicillin-resistant Staphylococcus aureus (MRSA) skin and soft tissue infections observed in emergency departments (EDs) has substantially increased in the last few years, leading to greater exposure of ED staff. What question this study addressed What is the prevalence of MRSA nasal colonization among ED providers? What this study adds to our knowledge Of 255 ED staff tested at the beginning of their shift, 11 (4.3%; 95% confidence interval 0% to 9.3%) had MRSA cultured from their nares. How this might change clinical practice The prevalence of nasal MRSA among staff in this ED is higher than in the general population. It remains unknown whether these are community- or health care–associated strains and whether colonization increases subsequent infection in these individuals or their contacts. Emergency department (ED) personnel could be vessels for nasal carriage of MRSA and inadvertently spread the pathogen. The prevalence of MRSA colonization among ED health care workers is not known. It is important to identify which ED personnel are at the highest risk of colonization. Information about ED health care worker MRSA prevalence also could assist in the development of guidelines for infection control. Goals of This Investigation We sought to determine the prevalence of S aureus and MRSA in ED health care workers. We also sought to identify demographic and exposure variables associated with MRSA in our population. We hypothesized that the prevalence of nasal carriage of MRSA was greater than previously reported estimates in the general population of the United States because of the frequency of exposure to infected or colonized patients.
MATERIALS AND METHODS Study Design We use a prospective, observational study design of a convenience sample of ED health care workers. Setting Volunteers from 5 urban teaching hospital EDs in Pittsburgh, PA, consented to participate. The annual ED census at the 5 hospitals ranged from approximately 31,000 to 48,000 530 Annals of Emergency Medicine
Suffoletto et al per year. We obtained approval from all medical center institutional review boards. Selection of Participants We announced the study in an e-mail to ED staff and placed flyers in staff areas. Volunteers gave written consent, completed the questionnaire, and had nasal culture samples taken by 2 authors (B.P.S., E.C.) from October 2006 through December 2006. We included ED health care workers on all shifts and collected nasal samples at the beginning of each shift to reduce selection bias and to identify persistent colonization, as opposed to transient colonization from recent self-inoculation. We included only ED health care workers working in a single ED and without a known recent S aureus/MRSA infection or colonization. Additionally, we excluded anyone hospitalized in the last year. Data Collection and Processing The questionnaire included an assessment of limited demographics and recent antibiotic and MRSA exposure. At initial enrollment in the ED, we sampled each participant’s anterior nares with sterile Dacron swabs. The swabs were coded and transported within 6 hours to the Allegheny County Health Department. Laboratory analysis at the Allegheny County Health Department consisted of bacterial culture and antibiotic susceptibility/resistance assays, using standardized methods. The swab samples were rolled on sheep blood agar then incubated inverted for 16 to 24 hours at 35°C in air. Laboratory technicians Gram stained and coagulase tested all colonies. We tested antibiotic resistance with oxacillin disc diffusion with the BBL Prompt kit (Beckton Dickinson, Sparks, NC). As a quality control measure, known S aureus/MRSA strain testing occurred on Mueller-Hinton agar plates and with antibiotic discs diffusion tests. For samples that grew S aureus (coagulase-positive staphylococcus), we reported the results as “oxacillin-resistant” (MRSA), intermediate-resistance S aureus, or “MRSA not found.” Primary Data Analysis All volunteers were healthy and without evidence of an active site of staphylococcal infection at the testing time; we therefore defined isolation of S aureus and MRSA from the nares as colonization.14 We compiled the subject number and culture results from the 5 testing sites. A priori we calculated a sample size of 223 needed to compare a known proportion of MRSA-positive of 0.0084 in the US population7 to a hypothesized proportion of 0.03 in our cohort. We entered all questionnaire and bacteriology data into an Excel 2007 database (Microsoft, Redmond, WA). Prevalence and 95% confidence intervals (CIs) were calculated. We tested potential predictor variables associated with MRSA colonization, using univariate analysis with ␣ set at 0.05 and using Stata 9.0. Volume , . : November
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Table 1. Selected demographic and antibiotic/infection-related characteristics of study subjects. Characteristic
Total Participants, No. (%)
S aureus Present, No. (% [95% CI])
Total 255 (100) Hospital 1 60 (23.5) 2 60 (23.5) 3 60 (23.5) 4 32 (12.6) 5 43 (16.9) Age, y ⱕ30 54 (22.3) 31–45 126 (49.4) 46–60 72 (28.3) Sex Male 101 (39.6) Female 154 (60.4) Job Title Physician/PA 58 (23.1) RN/NA/PCT 159 (62.4) Clerical/Soc Svc 38 (14.5) Antibiotic use in past 6 mo No 211 (82.8) Yes 44 (17.2) Past MRSA infection No 252 (98.8) Yes 3 (1.2) MRSA infection in household No 244 (95.7) Yes 11 (4.3) Other health care worker in household No 194 (76.1) Yes 61 (23.9)
MRSA Present, No. (% [95% CI])
81 (31.8)
11 (4.31)
18 (30.0 [19.0–43.0]) 19 (31.7 [20.3–45.0]) 20 (33.3 [21.7–46.8]) 9 (28.1 [13.7–46.7]) 15 (34.9 [21.0–50.9])
2 (3.3 [0.4–11.5]) 3 (5.0 [1.0–13.9]) 2 (3.3 [0.4–11.5]) 1 (3.1 [0.1–16.2]) 3 (7.0 [1.5–19.1])
11 (20.3 [10.6–33.5]) 48 (38.1 [29.6–47.2]) 22 (30.6 [20.2–42.5])
1 (1.9 [0.05–9.9]) 7 (5.6 [2.3–11.1]) 3 (4.2 [0.87–11.7])
34 (33.7 [24.6–43.8]) 47 (30.5 [23.4–38.4])
4 (4.0 [1.1–9.8]) 7 (4.5 [1.8–9.1])
22 (37.9 [25.5–51.6]) 48 (30.2 [23.2–38.0]) 11 (28.9 [15.4–45.9])
0 11 (6.9 [3.5–12.0]) 0
69 (32.7 [26.4–39.5]) 12 (27.3 [15.0–42.8])
8 (3.8 [1.7–7.3]) 3 (6.8 [1.4–18.7])
80 (31.7 [26.0–37.9]) 1 (33.3 [0.8–90.6])
11 (4.4 [2.2–7.7]) 0
79 (32.4 [26.5–38.6]) 2 (18.2 [2.3–51.8])
10 (4.1 [2.0–7.4]) 1 (9.1 [0.2–41.3])
59 (30.4 [24.0–37.4]) 22 (36.1 [24.2–49.4])
10 (5.2 [2.5–9.3]) 1 (1.6 [0.04–8.8])
PA, Physician assistant; RN, registered nurse; NA, nurses assistant; PCT, patient care technician. Household denied as a frequent, personal contact.
RESULTS During a 3-month period, we enrolled 255 subjects. The absolute number and demographics of those who refused to participate were not systematically recorded. Subject demographics and antibiotic/infection-related characteristics as they relate to culture results are in Table 1. The majority (68.2%) of nasal cultures were negative for S aureus. Of the 81 S aureus isolates, 11 (13.6%; 95% CI 0% to 28.5%) were MRSA. Overall, the prevalence of MRSA was 4.3% (95% CI 0% to 9.3%). Variables associated with MRSA colonization are presented in Table 2, identified by univariate logistic regression analysis. In short, nurses, nursing assistants, and radiology and respiratory technicians composed the entire MRSA colonization group.
Table 2. Selected characteristics associated with MRSA colonization.
Predictor Variable Age, y ⱕ30 31-45 46-60 Female sex Antibiotic use in past 6 mo MRSA infection in household Other health care worker in household
No. of Colonized Subjects No. (%) 54 126 72 154 44 11 61
1 (1.9) 7 (5.6) 3 (4.2) 7 (4.5) 3 (6.8) 1 (9.1) 1 (1.6)
Colonized Odds Ratio (95% CI) Reference 3.12 (0.37-26.0) 2.31 (0.23-22.8) 1.15 (0.32-4.05) 1.86 (0.47-7.30) 2.34 (0.27-20.1) 0.31 (0.04-2.44)
All variables potentially associated with MRSA colonization are presented, except job title, where nursing, nursing assistants, and radiology and respiratory technicians predicted colonization perfectly. No covariate presented was significantly associated with MRSA colonization.
LIMITATIONS We identified MRSA colonization in a single urban region and in teaching hospitals, which may limit the external validity of this work. We attempted to minimize local effects by sampling from 5 different ED environments. There is a potential for selection bias, given that ED health care workers who worked more and had greater contact with patients had a greater likelihood to be approached and agree to participate. Volume , . : November
Also, those who were either less or more likely to be colonized may have refused to participate. We collected nasal samples at a single point in time, potentially identifying those with transient exposure, not persistent carriers. We took steps to minimize identifying transient carriers by collecting samples before clinical exposure on the day of sampling. Annals of Emergency Medicine 531
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We focused on work demographics and did not collect other potential predictors of MRSA such as race, ethnicity, health status, or intravenous drug abuse history because of privacy issues. We did not perform multiple antibiotic sensitivity studies or genotype the colonies, limiting the ability to biologically classify them as community-acquired strains. Given the amount of time that ED health care workers care for patients who have considerable health care setting exposures, we also did not attempt to clinically classify MRSA strains as community acquired or hospital acquired. We were unable to contemporaneously compare the prevalence of colonization in ED health care workers to that of our local nonED health care worker population and therefore had to use previously reported estimates from the Health and Nutrition Examination Survey 2001 to 2002, representing the noninstitutionalized US population. Given that the prevalence of S aureus and MRSA skin infections has increased over time,4 there is a chance that current estimates of US colonization prevalence are not significantly greater than that of ED health care workers.
Drs. Talan and Callaham were the supervising editors on this article. Dr. Yealy did not participate in the editorial review or decision to publish this article.
DISCUSSION
REFERENCES
The colonization prevalence reported in this study is greater than previously reported estimates in the general population of the United States but less than colonization of health care workers during outbreaks.10 There have been no reported MRSA outbreaks at any of the participating hospitals during the period of sampling; therefore, we believe that our findings reflect a nonepidemic carrier state. Data from outbreaks of community-associated MRSA infection suggest that skin-skin and skin-fomite contact represent important and common routes of acquisition of MRSA colonization.12 It is possible that the frequency and duration of contacts among nursing-related duties puts them at increased risk for MRSA transfer. In summary, MRSA is more prevalent in ED health care workers than previously reported estimates in the general population of the United States, especially those with a greater frequency and duration of patient contact. If affirmed, these data might help guide MRSA infection control measures in the ED. We thank Tom Campbell, MD, Fred Harchelroad, Jr, MD, and Rick Wadas, MD, for the recruitment of subjects and Bruce Dixon, MD, and the staff of the Allegheny Department of Health for laboratory support. We would also like to thank Pam Cockley, RN, for data collection. Supervising editors: David A. Talan, MD; Michael L. Callaham, MD Author contributions: BPS, EHC, KI, and DMY were responsible for data collection, analysis, and interpretation and article preparation and revision. KI and DMY were responsible for conception of the study. BPS takes responsibility for the paper as a whole.
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Funding and support: By Annals policy, all authors are required to disclose any and all commercial, financial, and other relationships in any way related to the subject of this article, that might create any potential conflict of interest. See the Manuscript Submission Agreement in this issue for examples of specific conflicts covered by this statement. Dr. Suffoletto is supported by the Society for Academic Emergency Medicine Institutional Training grant. Publication dates: Received for publication February 29, 2008. Revision received March 14, 2008. Accepted for publication March 21, 2008. Available online April 24, 2008. Reprints not available from the authors. Address for correspondence: Brian Suffoletto, MD, Department of Emergency Medicine, University of Pittsburgh, 230 McKee Place, Suite 400, Pittsburgh, PA 15213; 412-9016892, fax 412-647-6669; E-mail [email protected].
1. Moran GJ, Krishnadasan A, Gorwitz RJ, et al. Methicillin-resistant S aureus infections among patients in the emergency department. N Engl J Med. 2006;355:666-674. 2. Cosgrove SE, Sakoulas G, Perencevich EN, et al. Comparison of mortality associated with methicillin-resistant and methicillinsusceptible Staphylococcus aureus bacteremia: a meta-analysis. Clin Infect Dis. 2003;36:53-59. 3. Delaney JA, Schneider-Lindner V, Brassard P, et al. Mortality after infection with methicillin resistant Staphylococcus aureus (MRSA) diagnosed in the community. BMC Med. 2008;6:2-10. 4. Pallin DJ, Egan DJ, Pelletier AJ, et al. Increased US emergency department visits for skin and soft tissue infections, and changes in antibiotic choices, during the emergence of communityassociated methicillin-resistant Staphylococcus aureus. Ann Emerg Med. 2008;51:291-298. 5. Ellis MW, Hospenthal DR, Dooley DP, et al. Natural history of community-acquired methicillin-resistant Staphylococcus aureus colonization and infection in soldiers. Clin Infect Dis. 2004;39:971-979. 6. Ellis MW, Griffith ME, Dooley DP, et al. Targeted intranasal mupirocin to prevent colonization and infection by communityassociated methicillin-resistant Staphylococcus aureus strains in soldiers: a cluster randomized controlled trial. Antimicrob Agents Chemother. 2007;51:3591-3598. 7. Kluytmans J, van Belkum A, Verbrugh H. Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin Microbiol Rev. 1997;10:505-520. 8. Graham PL 3rd, Lin SX, Larson EL. A U.S. population-based survey of Staphylococcus aureus colonization. Ann Intern Med. 2006;144:318-325. 9. Johnston CP, Stokes AK, Ross T, et al. Staphylococcus aureus colonization among healthcare workers at a tertiary care hospital. Infect Control Hosp Epidemiol. 2007;28:1404-1407. 10. Cookson B, Peters B, Webster M, et al. Staff carriage of epidemic methicillin-resistant Staphylococcus aureus. J Clin Microbiol. 1989;27:1471-1476. 11. Hidron AI, Kourbatova EV, Halvosa JS, et al. Risk factors for colonization with methicillin-resistant Staphylococcus aureus (MRSA) in patients admitted to an urban hospital: emergence of community-associated MRSA nasal carriage. Clin Infect Dis. 2005;41:159-166.
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Suffoletto et al 12. Miller LG, Diep BA. Clinical practice: colonization, fomites, and virulence: rethinking the pathogenesis of community-associated methicillin-resistant Staphylococcus aureus infection. Clin Infect Dis. 2008;46:752-760. 13. Jarvis WR, Schlosser J, Chinn RY, et al. National prevalence of methicillin-resistant Staphylococcus aureus in inpatients at US
Staphylococcus aureus Nasal Colonization health care facilities, 2006. Am J Infect Control. 2007;35:631-637. 14. Naimi TS, LeDell KH, Como-Sabetti K, et al. Comparison of community- and health care–associated methicillinresistant Staphylococcus aureus infection. JAMA. 2003;290: 2976-2984.
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