Original Article

Detection of Methicillin-Resistant Staphylococcus aureus and Vancomycin-Resistant Enterococci on the Gowns and Gloves of Healthcare Workers

Graham M. Snyder, MD; Kerri A. Thom, MD; Jon P. Furuno, PhD; Eli N. Perencevich, MD, MS; Mary-Claire Roghmann, MD, MS; Sandra M. Strauss, BS MT(ASCP); Giora Netzer, MD, MSCE; Anthony D. Harris, MD, MPH  

From the Departments of Epidemiology and Preventive Medicine (G.M.S., K.A.T., J.P.F., E.N.P., M.-C.R., S.M.S., A.D.H.) and Internal Medicine, Division of Pulmonary and Critical Care Medicine (G.N.), University of Maryland School of Medicine, and the Veterans Affairs Maryland Health Care System (E.N.P., M.-C.R., A.D.H.), Baltimore, Maryland.

Objective. To assess the rate of and the risk factors for the detection of methicillin-resistant S. aureus (MRSA) and vancomycin-resistant enterococci (VRE) on the protective gowns and gloves of healthcare workers (HCWs).

Methods. We observed the interactions between HCWs and patients during routine clinical activities in a 29-bed medical intensive care unit at the University of Maryland Medical Center, an urban tertiary care academic hospital. Samples for culture were obtained from HCWs' hands prior to their entering a patient's room, from HCWs' disposable gowns and gloves after they completed patient care activities, and from HCWs' hands immediately after they removed their protective gowns and gloves.

Results. Of 137 HCWs caring for patients colonized or infected with MRSA and/or VRE, 24 (17.5%; 95% confidence interval, 11.6%–24.4%) acquired the organism on their gloves, gown, or both. HCW contact with the endotracheal tube or tracheostomy site of a patient (P < .05), HCW contact with the head and/or neck of a patient (P < .05), and HCW presence in the room of a patient with a percutaneous endoscopic gastrostomy and/or jejunostomy tube (P < .05) were associated with an increased risk of acquiring these organisms.

Conclusions. The gloves and gowns of HCWs frequently become contaminated with MRSA and VRE during the routine care of patients, and particularly during care of the patient's respiratory tract and any associated indwelling devices. As part of a larger infection control strategy, including high-compliance hand disinfection, they likely provide a useful barrier to transmitting antibiotic-resistant organisms among patients in an inpatient setting.

Received December 31, 2007; accepted April 1, 2008; electronically published June 12, 2008.

Nosocomial infections caused by methicillin-resistant S. aureus (MRSA) and vancomycin-resistant enterococci (VRE) result in significant morbidity and mortality among hospitalized patients. The Centers for Disease Control and Prevention and the Society for Healthcare Epidemiology of America recommend contact precautions (ie, the wearing of gloves and gowns) for healthcare workers (HCWs) caring for hospitalized patients colonized or infected with MRSA or VRE.1,2 Although studies have demonstrated that the inclusion of the use of gowns and gloves3-5 as a component of a broader infection control policy6-10 in an epidemic or endemic setting reduces transmission of MRSA and VRE, the reasons for this benefit are not well understood.

The rates of detection of MRSA or VRE on the gowns and/or gloves of HCWs involved in either standardized or routine clinical care have been reported as being as low as 4% and as high as 67%.11-15 To our knowledge, no study has investigated risk factors for the detection of MRSA on HCWs' gowns and/or gloves, and only one study has investigated risk factors for the detection of VRE on HCWs' gloves.11

In this study, we sought to evaluate the rates of detection of MRSA and VRE on HCWs' gowns and gloves during the routine clinical activities of HCWs and to evaluate risk factors for the detection of these organisms on the protective gowns and gloves of HCWs. To our knowledge, this is the largest such study to date.

Methods

 

Study Population

This study was conducted in a 29-bed medical intensive care unit at the University of Maryland Medical Center, an urban tertiary care academic hospital. HCWs were approached immediately before performing nonemergent, routine patient care for patients infected or colonized with MRSA and/or VRE during randomly chosen days and times in February, August, and September of 2007. Patients were identified as MRSA and/or VRE positive on the basis of active surveillance cultures performed on admission, clinical cultures performed during their index hospitalization, or past MRSA- or VRE-positive cultures performed at the index institution. The University of Maryland Medical Center's infection control policy includes providing a private room for patients identified as colonized or infected with MRSA or VRE; requiring hands to be washed with an antimicrobial soap or an alcohol-based hand-hygiene product (both are available) before entering or exiting a room; providing disposable gloves and gown for entry into the room; providing patient-dedicated, disposable patient-care equipment (eg, stethoscope, blood pressure cuff, and digital thermometer); prohibiting artificial nails or natural fingernails with tips longer than one-quarter inch (6.35 mm) for HCWs who have direct patient contact and who handle patient-care supplies; and requiring use of a standardized cleaning protocol, with particular procedures for isolation rooms, use of germicidal cleaning products, and room cleaning at discharge. The study was approved by the University of Maryland institutional review board.

Observations

Samples for culture were obtained from the hands of HCWs immediately before they donned their gowns and gloves. Routine HCW activities were then observed, and data on possible risk factors associated with detection of MRSA and VRE were collected, including type of HCW, time HCW spent in the room, patient variables, and the nature and location of HCW contact with patient. When uninterrupted routine activities were completed, the gloves and then the gown were sampled by the study investigator (G.M.S.) and subsequently removed by the HCW. The hands of the HCW were then sampled for culture a second time immediately after removal of gloves and gown and before hand cleansing. An observation was excluded if the initial hand sample was positive for either MRSA or VRE on culture. Data were collected on performance of hand hygiene before the donning of gloves and gown, on the method of removing gloves and gown, and on performance of hand hygiene after all culture samples were obtained, at the HCW's discretion, without documentation or instruction from the study investigator.

Microbiological Methods

HCWs' hands, gloves, and gowns were sampled in a standardized fashion with sterile cotton-tipped applicators (Puritan Medical Products) moistened with sterile water. Hand and glove samples were obtained using a standardized methodology with a single sample of each hand, first of the nondominant hand and then of the dominant hand. Hand and glove samples were obtained by swabbing the dorsum of each finger 3 times and the palm of each hand 2 times with a twirling motion of the swab. Gown samples were obtained by swabbing each forearm twice—first the nondominant arm and then the dominant arm—and then swabbing a “W” on the beltline, all with a single swab and performed with a twirling motion. If gloves or gowns were changed in the room (to either clean or sterile gloves, or over existing gloves), then the gloves and gown worn exiting the room were sampled for culture.

Specimens were cultured on blood agar plates and in trypticase soy broth supplemented with 6.5% sodium chloride. Colonies that were morphologically consistent with MRSA were isolated on chrome agar (CHROMagar; BBL Microbiology Systems; Becton Dickinson) and/or Mueller Hinton agar supplemented with 4% sodium chloride that contained 6 μg/mL of oxacillin (Becton Dickinson). Colonies that were morphologically consistent with VRE were isolated on bile esculin plates that contained 20 μg/mL of vancomycin (Becton Dickinson).

Environmental Cultures

To assess whether glove boxes and gowns were contaminated, the top glove from the first visible glove box in each of 8 rooms of MRSA- or VRE-positive patients was sampled for culture on the same day. Similarly, the first visible gown in each of the same 8 rooms was sampled on the same day. Specimens were obtained by use of a sterile saline-moistened swab, and cultures were performed as described above.

Data Analysis

All analyses were performed using SAS software, version 9.1 (SAS). All P values are 2 sided and were calculated using the Fisher exact test or χ2 analysis, as noted, except for the statistical significance of the duration of time spent in a room, which was calculated using the Wilcoxon rank-sum test.

Results

 

We approached 141 HCWs before their interactions with patients; 1 refused to participate, and 3 (2%) were excluded from the final analysis because cultures of the hand samples obtained prior to HCW-patient interactions were positive for MRSA. Of the 137 HCWs remaining, 38 interacted with patients cocolonized with MRSA and VRE, 43 interacted with patients colonized with MRSA only, and 56 interacted with patients colonized with VRE only. HCW interactions with cocolonized patients were evaluated as 2 observations: both as an interaction with a patient colonized with MRSA and as an interaction with a patient colonized with VRE. For some interactions, gown or glove samples could not be obtained, and this accounts for the variation in the reported number of observations.

Of 175 HCW-patient observations included in the final analysis, 96 involved registered nurses, 27 involved physicians or nurse practitioners, 18 involved patient care technicians, 16 involved respiratory therapists, 6 involved physical or occupational therapists, and 12 involved HCWs in miscellaneous fields.

Detection Rate

The rates of detection of MRSA and VRE on the hands, gloves, and gowns of HCWs are reported in Table 1. Of the 137 HCWs who entered a room to provide care for a patient with MRSA, VRE, or both, 24 (17.5%; 95% confidence interval, 11.6%–24.4%) acquired the antibiotic-resistant organism on their gloves, gown, or both.

Table 1. 
Table 1.  Rates of Detection of Methicillin-Resistant Staphylococcus aureus (MRSA) and Vancomycin-Resistant Enterococci (VRE) on the Gowns and Gloves Worn by Healthcare Workers Caring for Patients with MRSA and VRE Carriage

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Risk Factors for Detection

A univariate analysis of the presumed risk factors for acquiring MRSA or VRE on gloves and/or gowns is presented in Table 2. The statistically significant risk factors included presence of the HCW in the room of a patient with a percutaneous endoscopic gastrostomy and/or jejunostomy tube (P < .05), HCW contact with the endotracheal tube or tracheostomy site of a patient (P < .05), and HCW contact with the head and/or neck of a patient (P < .05). The time the HCW spent in the room (rounded to the nearest minute during observation) ranged from 1 minute to 73 minutes, with a mean of 8.3 minutes and median of 5 minutes. The time the HCW spent in the room was not statistically associated with detection of MRSA or VRE (P = .27).

Table 2. 
Table 2.  Rates of Detection of Methicillin-Resistant Staphylococcus aureus (MRSA) and/or Vancomycin-Resistant Enterococci (VRE) on the Gowns and Gloves Worn by Healthcare Workers (HCWs) Caring for Patients with MRSA and/or VRE Carriage and Univariate Analysis of Risk Factors for Detection.

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Table 3 presents univariate analyses of the presumed risk factors for detection of MRSA and VRE independently. For patients colonized with MRSA, detection of MRSA on the HCWs' gloves and/or gown was associated with presence of the HCW in the room of a patient with a percutaneous endoscopic gastrostomy and/or jejunostomy tube, HCW contact with the endotracheal tube or tracheostomy site of a patient, and HCW contact with the head and/or neck of a patient, compared with the overall analysis presented in Table 2. In addition, detection of MRSA was associated with HCW contact with the right lower extremity of a patient. For patients colonized with VRE, the small number of positive findings limited the analysis, but HCW use or care of a catheter or drain, HCW contact with the trunk of the patient, and HCW contact with the left lower extremity of the patient were significant factors for detection.

Table 3. 
Table 3.  Rates of Detection of Methicillin-Resistant Staphylococcus aureus (MRSA) and Vancomycin-Resistant Enterococci (VRE) on the Gowns and Gloves Worn by Healthcare Workers (HCWs) Caring for Patients with MRSA and VRE Carriage and Univariate Analyses of Risk Factors for Detection.

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Environmental Cultures

None of the 16 environmental cultures of samples from glove boxes or gowns grew MRSA or VRE.

Discussion

 

Our study demonstrated that gloves and gowns were frequently contaminated with MRSA and VRE during routine patient care: the rate of detection of MRSA and/or VRE on gowns and/or gloves was 18%. The detection rate for MRSA was higher than it was for VRE, and the detection of either organism was more frequent on gloves than on gowns. We found that patient-associated risk factors for detection include presence of the HCW in the room of a patient with a gastrostomy and/or jejunostomy feeding tube. Among risk factors related to the nature and location of contact between HCW and patient, HCW contact with the head or neck of a patient was associated with detection of organisms on the gown and/or glove of the HCW, as was care for an endotracheal tube or tracheostomy site (although, as a patient variable, presence of the HCW in the room of a patient with an endotracheal tube or a tracheostomy was not strongly associated with detection of a contaminating organism). The time spent in a patient's room was not significantly associated with an increased risk of acquiring either of the organisms. Hands were infrequently contaminated with VRE after routine clinical activities and after removal of gloves, but a significant number of HCWs acquired MRSA on their hands after removal of gowns and gloves that had become contaminated with MRSA.

In what is, to our knowledge, the largest study to date of MRSA and VRE contamination of gloves and gowns, we provide further evidence for a significant rate of detection of these organisms, particularly MRSA, on the gowns and/or gloves of HCWs during their routine care of patients. Given the general detection rate and the low rates of hand contamination after removal of gown and gloves, use of these infection control precautions likely serve as an important intervention in preventing transmission of these organisms. Although the population size of our study is small, 13% of HCWs who acquired MRSA and/or VRE on their gowns and/or gloves subsequently acquired it on their hands after removing their gowns and gloves, and this reinforces the importance of hand washing after all HCW-patient interactions, independent of contact precautions. It is also notable that even a short duration of time spent in a patient's room and limited activity or patient contact on the part of an HCW may result in detection of antibiotic-resistant organisms on the HCW or their protective clothing.

Furthermore, this study presents new information regarding risk factors associated with detection of MRSA and/or VRE on the HCW or their protective barriers—including an HCW having been in the room of a patient with an endotracheal tube or a tracheostomy—that may help guide further interventions for minimizing patient-to-HCW transmission. Transmission associated with these risk factors may be the result of HCW contact with respiratory secretions, which often have a high level of colonization with antibiotic-resistant organisms, such as MRSA or VRE.16 Although limited by the power of our study, the results of the independent analysis of risk factors associated with detection of MRSA remained very similar to the results of the overall analysis, whereas the risk factors associated with detection of VRE were limited to HCW care or use of a catheter and/or drain or HCW contact with body sites. Although the number of focused studies is limited, several demonstrate that there is a high rate of MRSA colonization of gastrostomy tubes17 and an association with infections at these sites.18,19 In one study, colonization with MRSA was found to be more common among patients with enteral feeding tubes or indwelling devices, in general, than among patients without (a finding not demonstrated with VRE).20 Although not the organisms most commonly isolated, multiple potential pathogens, including S. aureus and Enterococcus species, have been detected in endotracheal tube biofilm samples and tracheal aspirates.21,22 Taken together, these data and our current findings should encourage further investigation into the role played by indwelling devices in the transmission of antibiotic-resistant organisms, particularly MRSA.

No prior study, to our knowledge, has investigated risk factors for the detection of MRSA on HCW gowns or gloves. Tenorio et al.11 investigated risk factors for detection of VRE on gloves from 50 interactions among 5 HCWs and 10 patients: 39% of the HCWs acquired VRE on their gloves after interacting with a patient, and the risk factors for detection on gloves included contacting a patient who had diarrhea or who had a relatively high number of colonization sites.

There are several limitations to this study. Strain typing of MRSA and VRE isolates was not performed, thereby limiting our ability to be sure that the strain colonizing a patient was the same as that from the cultures for the HCW. The impact of this limitation was addressed by excluding observations for which culture of HCW hand samples obtained before patient interaction had positive results, which likely ensured that the MRSA or VRE strains recovered had been acquired from the patient. Informal attempts were made to randomly collect data from all rooms with MRSA- and VRE-positive patients. However, because patient-identifiable information was not collected, the possibility of bias from inclusion of multiple observations for the same patient cannot be excluded. Furthermore, some HCWs were observed more than once, and HCWs were aware that their routine activities were being observed. Therefore, HCW-patient interactions may not be statistically independent, and although we feel observation is unlikely to have changed the practice of routine clinical activities, there might have been an unrecognized impact on detection of organisms. While organism burden on patients may affect the rates of detection and transmission of antibiotic-resistant organisms, data on this variable were not collected and thus were not analyzed, partially because of our desire to not include patient-identifying information. Selection bias due to inadequately sensitive sampling techniques may have limited our ability to detect MRSA and VRE contamination. However, although there may be some improvement in sensitivity with use of polymerase chain reaction to detect MRSA23 and the Rodac imprint method to detect VRE,24 the moistened swab method has been demonstrated to be superior to the Rodac method for detecting gram-negative bacteria and only slightly less sensitive than the Rodac method for detecting gram-positive cocci, when compared directly.25 The enrichment broth method has been demonstrated to be similar or superior to other techniques for detection of both VRE26 and MRSA.27 Our technique is cost-effective, provides an optimal compromise for detection of both MRSA and VRE, and has been demonstrated successfully in a similar manner.28 Lastly, given the relatively low number of cultures positive for MRSA or VRE, risk factor analysis was limited by the power of the study.

Gowns and gloves, as infection control protective barriers, are frequently contaminated with MRSA and VRE, particularly during the care of a patient's respiratory tract. As part of a larger infection control strategy that includes a high rate of compliance with hand disinfection, they likely provide a useful barrier to transmission of antibiotic-resistant organisms among inpatients.

Acknowledgments

 

We thank all of the staff and clinicians of the medical intensive care unit who participated in the study for their support and participation.

Financial support. This study was supported by the Centers for Disease Control (grant CI000369-01) and the National Institutes of Health (research grants R01 AI60859-01A1 and 1K12RR023250-01).

Potential conflicts of interest. All authors report no conflicts of interest relevant to this study.

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  • (See the commentary by Mundy on pages 590–592)

  • Address reprint requests to Anthony Harris, MD, MPH, Department of Epidemiology and Preventive Medicine, University of Maryland School of Medicine, 100 N. Greene Street, Lower Level, Baltimore, MD 21201 ().

  • Presented in part: 47th Annual Interscience Conference on Antimicrobial Agents and Chemotherapy; Chicago, Illinois; September 17, 2007 (Abstract K-463).

© 2008 by The Society for Healthcare Epidemiology of America. All rights reserved.