Risk of Hand or Glove Contamination After Contact With Patients Colonized With Vancomycin‐Resistant Enterococcus or the Colonized Patients' Environment
Objective. To estimate the level of hand or glove contamination with vancomycin‐resistant enterococci (VRE) among healthcare workers (HCWs) who touch a patient colonized with VRE and/or the colonized patient’s environment during routine care.
Design. Structured observational study.
Setting. Medical intensive care unit of a 700‐bed, tertiary‐care teaching hospital.
Participants. VRE‐colonized patients and their caregivers.
Methods. We obtained samples from sites on the intact skin of 22 patients colonized with VRE and samples from sites in the patients’ rooms, before and after routine care, during 27 monitoring episodes. A total of 98 unique HCWs were observed during 131 HCW observations. Observers recorded the sites touched by HCWs. Culture samples were obtained from HCWs’ hands and gloves before and after care.
Results. VRE were isolated from a mean (±SD) of 
of patient sites (
) and 
of environmental sites (
). Most HCWs (131 [56%]) touched both the patient and the patient's environment; no HCW touched only the patient. Of 103 HCWs whose hand samples were negative for VRE when they entered the room, 52% contaminated their hands or gloves after touching the environment, and 70% contaminated their hands or gloves after touching the patient and the environment (
). In a univariate logistic regression model, the risk of hand or glove contamination was associated with the number of contacts made (odds ratio, 1.1 [95% confidence interval, 1.01‐1.19). In a multivariate model, the effect of the number of contacts could not be distinguished from the effect of type of contact (ie, touching the environment alone or touching both the patient and the environment). Overall, 37% of HCWs who did not wear gloves contaminated their hands, and 5% of HCWs who wore gloves did so (an 86% difference).
Conclusion. HCWs were nearly as likely to have contaminated their hands or gloves after touching the environment in a room occupied by a patient colonized by VRE as after touching the colonized patient and the patient's environment. Gloves were highly protective with respect to hand contamination.
Received July 9, 2007; accepted September 4, 2007; electronically published December 31, 2007.
Cross‐transmission of vancomycin‐resistant Enterococcus (VRE) between patients in hospitals occurs primarily via the contaminated hands of healthcare workers (HCWs). This process requires several sequential steps, including the transfer of VRE from a contaminated site on a patient or in the environment to an HCW’s hand.1 Because the density of VRE on patients’ skin is usually greater than that found on environmental surfaces,2 hand contamination might be assumed to occur more frequently after direct contact with a patient colonized with VRE than after contact with the environment. Touching a VRE‐contaminated inanimate surface has been shown to result in glove contamination, however, in both experimental and clinical settings.3‐5 In a previous study, we found that HCWs transferred VRE from a contaminated site on a patient’s body or in the environment to a clean site via their inadvertently contaminated hands even when very few colony‐forming units of VRE were identified at the transfer source.6 In the present study, we reevaluated those data and studied related information to estimate the risk of contamination of gloved or ungloved hands after contact with a VRE‐colonized patient and/or the patient’s environment during routine clinical care.
Methods
Setting and Study Design
The study took place over a 9‐month period in the medical intensive care unit (MICU) of Rush University Medical Center, a 700‐bed tertiary care teaching hospital in Chicago, Illinois. The MICU comprises 21 beds, 17 in single rooms and 4 in double rooms. The study was evaluated and approved by the Rush University institutional review board.
All patients were screened for rectal carriage of VRE within 24 hours after admission and twice per week thereafter. Colonized patients were placed under contact precautions. The demographic and clinical information recorded for each patient included age, sex, ethnicity, medical diagnoses, Acute Physiology and Chronic Health Evaluation (APACHE) II score, antibiotics received, presence of loose stools or diarrhea, use of a fecal incontinence bag, mobility, and whether VRE grew in a clinical culture. Informed consent for patients was waived.
We studied HCWs providing routine clinical care in the rooms of VRE‐colonized patients during specified monitoring periods lasting from 2 to 4 hours (hereafter, “monitoring episode”). Before each monitoring episode, we used a selective broth enrichment method to culture samples from up to 12 sites on patients’ intact skin (eg, antecubital fossae, inguinal region, chest, back, and/or wound) and samples from up to 34 environmental sites (eg, blood pressure cuff, bed linen, bed rails, countertops, monitor dials, door handles, telephone handset, and bedside record), if present.6 Subsequently, each HCW who entered the patient’s room was invited to participate in the study; informed consent was obtained from all participating HCWs. The information collected from each HCW included age, sex, job category, and use of systemic or topical antibiotics or topical corticosteroids in the past month. A research staff member (D.W.B. or E.A.L.) recorded the following information about each participating HCW: whether the HCW was wearing artificial nails, nail polish, rings, bracelets, and/or a watch; nail length (dichotomized as long [ie, nail extended past the finger tip] or short [nail extended to end of finger tip or less]), the presence of cuts or abrasions on the hands, and the skin condition of the hands.7 After this assessment, and before the HCW touched the patient or the patient's environment, the research staff member obtained culture samples from both of the HCW’s hands by use of a modified “glove juice” technique.8 The HCW was then observed during the entire episode of patient care; we noted whether gloves were donned. Each environmental site or patient body site touched by the HCW was recorded on a standardized data collection form as a contact. After the HCW had completed patient care activities, but before hand washing, culture samples were obtained from his/her hands again; if the HCW wore gloves, we obtained culture samples from the hands before and after glove removal. Up to 6 HCWs were studied per room per day; individual HCWs were studied no more than once per day.
Rooms were cleaned daily after each monitoring episode. Daily cleaning comprised wiping or mopping all accessible surfaces—except windows, walls, ceiling, and drapes—with a clean cloth or mop soaked in the standard hospital quaternary ammonium detergent disinfectant (Virex; SC Johnson). Bed rails, infusion pumps, countertops, door handles, telephone handsets, and other items were cleaned similarly. Housekeepers used 8‐12 cloths per room. Separate buckets of cleaning solution were used for the floor. Buckets of cleaning solution and mop heads were changed every 3 rooms and after every isolation room. Isolation rooms were cleaned last.9
VRE were identified as described elsewhere.6 Pulsed‐field gel electrophoresis (PFGE) of all unique colony morphotypes was done according to a standard method.10 Only Enterococcus faecium and Enterococcus faecalis strains harboring the vanA or vanB gene were included in the epidemiologic analysis.
Statistical Methods
We used descriptive statistics (mean ± SD, frequency, and/or percentage) to characterize the patients sampled. Statistical analysis was done with SAS for Windows, version 8.1 (SAS Institute). VRE colonization status was compared using the χ2 or Fisher exact test.11 We used the Spearman correlation to test the association between the proportion of body and environmental sites that were positive for VRE on culture, and between the proportion of body or environmental sites positive for VRE on culture and contamination of HCWs' hands or gloves.12 We used logistic regression models to estimate the association between the number of contacts, type of contacts, and contamination of gloved or ungloved hands. We employed general estimating equations to control for repeated collection of culture samples from patients and HCWs.13
Results
There were 27 monitoring episodes involving 22 unique patients (Figure 1 and Table 1). Samples from a total of 256 patient and 1,572 environmental sites were cultured. For each monitoring episode, a mean (±SD) of 
of samples from body sites and 
of samples from environmental sites grew VRE on culture.6 The proportions of body sites and environmental sites positive for VRE were highly correlated (
; 
). The PFGE patterns of the VRE isolates recovered from colonized patients matched those found in the environment in all episodes. In 4 episodes, an additional pulsotype was recovered from 1 or more environmental sites; in no episode were any of these 4 additional strains isolated from HCWs' hands or gloves.
Figure 1. Flow diagram summarizing the observational study design. HCW, healthcare worker; VRE (+), sample grew vancomycin‐resistant Enterococcus (VRE) on culture; VRE (−), sample did not grow VRE on culture.
We obtained samples for 131 pairs of hand cultures from 98 unique HCWs (Figure 2); the largest categories of HCWs studied were nurses (43%) and resident physicians (30%). HCWs made an average of 7 environmental or patient contacts per episode of care (total contacts, 916). A total of 58 (44%) of the HCWs touched only the patient's environment, and 73 (56%) touched both the patient and the patient's environment. No HCW touched only the patient.
Figure 2. Rates of vancomycin‐resistant Enterococcus (VRE) contamination on healthcare workers' gloved and ungloved hands after touching a colonized patient and the patient’s environment or after touching only the environment. None of the 29 healthcare workers (HCWs) who wore gloves and touched only the environment had VRE isolated from their hands after glove removal. Our analysis included only HCWs who provided hand samples on room entry that were negative for VRE on culture. *
; **
.
HCWs who touched only the environment made an average of 5.1 contacts, whereas those who touched both the patient and the environment made an average of 8.5 contacts (
). Among HCWs who touched only the environment, 36 (62%) wore gloves, whereas 66 (90%) of the HCWs who touched both the patient and the environment wore gloves (
). One HCW who touched only the environment and 5 HCWs who touched both the patient and the environment had the same VRE pulsotype on their gloves when they exited the patient’s room as when they entered. Of the remaining HCWs who wore gloves, 20 (57%) of 35 contaminated them after touching only the environment, and 43 (69%) of 61 contaminated their gloves after touching both the patient and the environment (
).
A total of 28 (21%) of the HCWs’ hands were contaminated with VRE when culture samples were first obtained, prior to patient care; these HCWs were excluded from further analysis. Of 103 (79%) HCWs who provided hand samples on room entry that tested negative for VRE, 44 (43%) touched only the environment, and 59 (57%) touched both the patient and the environment (Figure 1). There was a trend toward increased hand or glove contamination among HCWs who touched both the patient and the environment (41 [70%] of 59), compared with HCWs who touched only the environment (23 [52%] of 44), but the difference was not statistically significant (Table 2).
The median number of patient and environmental contacts made by HCWs who contaminated their gloved or ungloved hands was 6.5, compared to 5.0 contacts for HCWs who did not contaminate their hands or gloves (
). In an unadjusted logistic regression model, the risk of gloved or ungloved hand contamination was significantly associated with the number of contacts made (odds ratio [OR], 1.1 [ 95% confidence interval {CI}, 1.01– 1.19]; 
); each contact resulted in a 10% risk of hand contamination. In multivariable logistic regression analysis, the effect of the number of contacts (OR, 1.07 [95% CI, 0.97‐1.18]) and the effect of the type of contact (ie, touching a patient and the environment or touching only the environment) (OR, 1.65 [95% CI, 0.58‐4.62]), were so closely related that they could not be distinguished. After controlling for the number of contacts and the type of contact, no HCW variable examined, including job category, skin condition, or the wearing of rings, was significantly associated with hand or glove contamination.
As expected, HCWs who wore gloves were significantly less likely to contaminate their hands, despite touching more sites than HCWs who did not wear gloves (mean, 7.9 vs 3.4 contacts; 
). Overall, 37% of HCWs who did not wear gloves contaminated their hands, and 5% of HCWs who wore gloves did so (an 86% difference). Gloves were effective at protecting hands from contamination regardless of whether HCWs touched both the patient and the environment or touched only the environment (Figure 2).
When we further evaluated the 19 monitoring episodes during which 3 or more HCWs were studied, we observed a correlation between the proportion of culture‐positive patient or environmental sites and gloved or ungloved hand contamination (
; 
). We found no association between any patient characteristic, including the presence of diarrhea or growth of VRE in a clinical culture, and gloved or ungloved hand contamination.
Discussion
In this structured observational study, HCWs performing routine clinical care were nearly as likely to have contaminated their gloved or ungloved hands after touching an environmental surface in the room of a VRE‐colonized patient as they were after touching both the patient and the patient's environment; rates of contamination were 52% and 70%, respectively. These results are consistent with findings of a previous study in which each of 3 HCWs who manipulated items in a VRE‐colonized patient’s room contaminated their gloves with VRE,3 and with the results of another investigation in which 46% of subjects contaminated their gloves after deliberately touching bed rails and bedside tables in staged evaluations in VRE‐colonized patients’ rooms.4 Our study adds to those investigations by analyzing a larger number of HCWs, by estimating the contamination risk in an actual work setting during routine patient care, and by quantifying differences in hand contamination rates between those HCWs with patient contact and those with only environmental contact.
The rates of hand or glove contamination were comparable between the 2 groups, that is, between HCWs who touched only the environment and HCWs who touched both the patient and the environment, despite HCWs making more contacts with the patient and the environment than with the environment alone. Previous studies have found that HCWs' hands became progressively more contaminated with potential pathogens during patient care and that longer duration of care was associated with greater levels of contamination.14,15 The number of contacts measured in our study likely serves as a surrogate measure for duration of care. Although we found that the number of contacts was significantly associated with hand contamination in a univariate logistic regression model, in a multivariate analysis, the effect of number of contacts could not be distinguished from the effect of the type of contact (ie, touching the environment alone versus touching the environment and the patient). After controlling for the number and type of contacts, we were unable to show an association between hand contamination and any of several factors that have been found to be associated with hand contamination in some other studies, including patients having diarrhea or HCWs wearing rings.3,16,17 This may have been a result of the relatively small number of patients that we studied or differences in our study design; for example, we cultured samples from both hands together, whereas the study that found rings to be a risk factor for hand contamination cultured each hand separately.16
As expected, gloves were highly protective: the risk of VRE hand contamination was 5% for gloved hands and 37% for ungloved hands. Of concern, HCWs who touched only the environment, and who made fewer contacts, were less likely to wear gloves than were other HCWs. This suggests that HCWs may not appreciate the risk of hand contamination (4 [27%] of 15) from brief contact with environmental surfaces in the rooms of VRE‐colonized patients, which may help to explain our high (21%) baseline rate of VRE hand contamination among HCWs. Our findings support recommendations for HCWs to wear gloves when entering the room of a VRE‐colonized patient,18 to perform hand hygiene after removing gloves,18,19 and to view touching an inanimate surface in the patient’s room as an activity that poses a high risk for hand contamination.1
The limitations of our study include the modest number of HCWs studied; the apparent trend toward differences in gloved or ungloved hand contamination may not have reached statistical significance because of the sample size. The observational study design allowed us to compare hand and glove contamination during real clinical work, but may have introduced unmeasured bias. Nevertheless, we observed high rates of hand contamination. We excluded from primary analysis those HCWs whose hands were already contaminated with VRE when they entered the patient's room. However, the activities of these HCWs and their rates of gloved hand contamination (57% contaminated their gloves after touching only the environment, vs 69% who contaminated their gloves after touching both the environment and the patient) were similar to those of the subset that was studied more intensively (52% vs 70%), and so their exclusion is unlikely to have biased results.
Recently published data suggest that the inanimate environment serves as a reservoir for VRE transmission in hospitals.6,9,20‐22 Our study adds support to those findings, extends our understanding of the mechanism of transmission by demonstrating that HCWs performing routine clinical care readily contaminated their gloved or ungloved hands with VRE after touching environmental surfaces near patients colonized with VRE, and provides quantified risks of hand contamination that may be useful for educating HCWs and for creating models to assess the role of environmental contamination in the spread of nosocomial pathogens. Gloves provided good but imperfect protection against hand contamination. VRE control programs should emphasize effective environmental disinfection, interventions that may limit environmental contamination (eg, patient cleansing with chlorhexidine gluconate23), and diligent hand hygiene.
Acknowledgements
We thank the patients and staff members of the medical intensive care unit at Rush University Medical Center for their assistance and cooperation.
Financial support. This study was supported in part by a grant from the Centers for Disease Control and Prevention (U50/CCU516573).
Potential conflicts of interest. M.K.H. and R.A.W. report receiving research grants from Sage Products. All other authors report no potential conflicts of interest relevant to this article.
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Presented in part: 41st Interscience Conference on Antimicrobial Agents and Chemotherapy; Chicago, Illinois; December 16‐19, 2001 (Abstract K‐1334).