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To Gown or Not to Gown: The Effect on Acquisition of Vancomycin-Resistant Enterococci

  1. Laura A. Puzniak1,
  2. Terry Leet1,
  3. Jennie Mayfield2,
  4. Marin Kollef3, and
  5. Linda M. Mundy4
  1. 1Department of Community Health, St. Louis University School of Public Health, St. Louis, Missouri
  2. 2Infection Control Department, Barnes-Jewish Hospital, St. Louis, Missouri
  3. 3Divisions of Pulmonary and Critical Care Medicine, St. Louis, Missouri
  4. 4Divisions of Infectious Diseases, Washington University School of Medicine, St. Louis, Missouri
  1. Reprints or correspondence: Dr. Linda M. Mundy, Div. of Infectious Diseases, Washington University School of Medicine, 660 S. Euclid Ave., Campus Box 8051, St. Louis, MO 63110 (lmundy{at}imgate.wustl.edu).
 
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Abstract

Infection-control recommendations include the use of gowns and gloves to prevent horizontal transmission of vancomycin-resistant enterococci (VRE). This study sought to determine whether the use of a gown and gloves gives greater protection than glove use alone against VRE transmission in a medical intensive care unit (MICU). From 1 July 1997 through 30 June 1998 and from 1 July 1999 through 31 December 1999, health care personnel and visitors were required to don gloves and gowns upon entry into rooms where there were patients infected with nosocomial pathogens. From 1 July 1998 through 30 June 1999, only gloves were required under these same circumstances. During the gown period, 59 patients acquired VRE (9.1 cases per 1000 MICU-days), and 73 patients acquired VRE during the no-gown period (19.6 cases per 1000 MICU-days; P < .01). The adjusted risk estimate indicated that gowns were protective in reducing VRE acquisition in an MICU with high VRE colonization pressure.

Vancomycin-resistant enterococci (VRE) have emerged as prominent nosocomial pathogens despite efforts to prevent and control the spread in hospital settings [1–3]. Of note, in 1999, 25% of enterococcal isolates recovered from patients in the intensive care unit were vancomycin resistant [1]. The increasing incidence of VRE is problematic because of the limitations of effective treatment and eradication strategies and the potential transfer of vancomycin resistance genes to more-virulent organisms, such as methicillin-resistant Staphylococcus aureus [2–6].

In 1994, the Hospital Infection Control Practices Advisory Committee responded to the increase in the incidence of VRE with prevention and infection-control recommendations [7]. These recommendations included the use of gloves and a gown upon entrance into the room of any patient colonized or infected with VRE and the removal of gloves and gowns before leaving the patient's room. Although this practice is recommended, few data have suggested that gowns are effective in preventing VRE transmission in settings where it is endemic. Montecalvo et al. [8] reported a reduction in VRE rates with enhanced infection-control procedures in an oncology inpatient setting where VRE were endemic; these procedures included wearing a gown. In another study, an outbreak of multidrug-resistant Enterococcus faecium was interrupted when glove and gown use was required [9]. It remains uncertain whether the potential protection caused by gown use occurred because of an additional barrier against environmental contamination or because of multiple enhanced behaviors as the outbreak evolved over time.

Conversely, another study reported that use of both gloves and gowns had no additional protective effect when compared with use of gloves alone in an intensive care unit with endemic VRE [10]. Nonetheless, the investigators concluded that gowns had a potential benefit, because use of gowns may enhance compliance with other infection-control measures, especially glove use. Additional studies from neonatal units failed to show the added benefits of gown use on reducing nosocomial infections in settings where infection is endemic [11–13].

The purpose of this study was to determine whether enteric VRE acquisition rates were affected when gowns were and were not a component of contact precautions for interaction with patients infected or colonized with VRE in a medical intensive care unit (MICU).

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Patients and Methods

Desig. A quasi experimental study was used to assess VRE acquisition rates during 18 months of gown and glove use and during 12 months of glove use only. Patients admitted to the MICU were screened for enteric VRE acquisition at admission, every 7 days thereafter, and at discharge from the MICU. Additional data were obtained from hospital databases and from medical information services [14]. The study was approved by the Human Studies Committee at Washington University Medical Center (St. Louis) and the institutional review board at St. Louis University.

Participant. All patients admitted to the 19-bed MICU at Barnes-Jewish Hospital (BJH) from 1 July 1997 through 31 December 1999 were eligible for the study. BJH is a 1287-bed tertiary care facility located in St. Louis. Patients were excluded from the analyses if the duration of their MICU stay was <24 h. Data from patients with multiple admissions were combined if the multiple admissions occurred within 30 days. If multiple admissions occurred µ30 days apart, only the first admission during the study period was included in the analysis.

Intervention strateg. From 1 July 1997 through 30 June 1998, and again from 1 July 1999 through 31 December 1999, health care personnel and visitors were required to wear both gloves and gowns before entry into rooms with patients who were colonized or infected with the following pathogens: VRE; methicillin-resistant S. aureus; multidrug-resistant, gram-negative pathogens; or Clostridium difficile. From 1 July 1998 through 30 June 1999, health care personnel and visitors were required only to wear gloves before entry into the rooms of patients who were colonized or infected with the aforementioned pathogens.

Nurses obtained stool samples or rectal swabs from the patients for culture. Bile esculin azide agar with vancomycin (6 µg/mL; Remel), followed by a subculture on a 30-µg vancomycin disk, was used for isolation, identification, and characterization of enteric VRE, as described elsewhere [15]. Because VanA and VanB fail to produce inhibition zones of µ6 mm, whereas VanC isolates primarily produce inhibition zones of µ15 mm during subculturing on a 30-µg vancomycin disk, this method reliably differentiates clinically and epidemiologically relevant species [15]. In addition, stool samples submitted for C. difficile testing were routinely tested for enteric VRE [16].

The study physician, MICU director, and infection-control specialist consistently informed and educated physicians, nurses, and support staff in the MICU of new infection-control policies throughout the study period. Infection-control specialists monitored compliance with isolation procedures during April 1998 and April—June 1999. Violations of infection-control policies were noted, but no interventions or corrective actions were undertaken during this study period.

Housekeeping practices were altered during the study period. From July 1997 through April 1998, the housekeeping staff included 2 staff members during the day and none in the evening. From May 1998 through December 1999, housekeeping responsibilities were switched to patient service representatives (technicians trained in comprehensive service delivery), and the staff comprised 3 staff members during the day and 1 staff member during the evening.

During the first 18 months of this study, another intervention was tested in the same MICU to assess the effect of the scheduled rotation of preferred agents active against gram-negative bacteria on VRE acquisition. Compliance with the preferred agent active against gram-negative bacteria was low (25%) [17]. There was no additional beneficial or adverse effect on VRE acquisition as a result of this practice [17]. The hospital formulary was unchanged throughout the study periods.

Outcom. A patient was considered to have nosocomial enteric VRE colonization if, before discharge from the MICU, a surveillance or clinical culture of a rectal swab or stool sample was positive for VRE after a documented negative specimen had been obtained. Acquisition rates were calculated by dividing the number of cases of enteric VRE by the total MICU patient-days for the 2 study periods. VRE bacteremia and mortality rates were calculated as described elsewhere [17, 18]. MICU patient-days for all rates were calculated from the time of MICU admission to the time of detection of VRE colonization or infection for patients with VRE; for patients without VRE, MICU patient-days were calculated from the time of MICU admission to the time of discharge.

Patients with a culture positive for enteric VRE before or at admission to the MICU were classified as “colonized at admission.” Point prevalence was calculated by dividing the number of patients colonized with enteric VRE at admission by the total number of admissions.

Potential confounding variable. Additional data were collected to assess potential confounding bias. Demographic characteristics included age, race, and sex. Severity of illness was assessed via the Acute Physiology and Chronic Health Evaluation (APACHE) II score [19]. Length of hospital stay was computed from the time of hospital admission to the time of enteric VRE colonization detection for patients with VRE and from time of hospital admission to time of discharge for patients without VRE.

Other potential risk factors were categorized as being present or absent during the MICU stay. Antimicrobial agent receipt was classified by the agent's spectrum of activity on the gastrointestinal flora, as reported elsewhere [16]. Data for receipt of antimicrobial agents, receipt of vancomycin specifically, and duration of treatment were collected from the time of hospital admission until a culture positive for enteric VRE was obtained or, for non—VRE-colonized patients, until discharge from the hospital. Colonization pressure, initially defined by Bonten et al. [20], quantifies the burden of VRE in a geographic unit. We used a modified method to calculate colonization pressure, as described elsewhere [17].

Statistical method. Demographic characteristics, severity of illness, nosocomial exposures, and acquisition variables were compared for patients during both gown periods with patients during the no-gown period by the χ2 test for categorical variables and analysis of variance for continuous variables. Logistic regression was used to determine whether VRE acquisition risks were different between periods with and without use of gowns and to control for confounding bias. Potential confounding variables were added to the model independently to determine whether the variable modified the size of the OR for study period by ⩾10% [17, 21]. Variables that changed the risk for the primary exposure by ⩾10% were retained in the final model. Two-way interactions were assessed between the primary exposure and potential confounding variables. Regression diagnostics were used to ascertain outlying or influential cases. Log likelihood analysis was used to assess the fit of the model. P < .05 was considered statistically significant, and all tests were 2 tailed. SPSS software, version 9.0 for Windows (SPSS), was used to perform all statistical analyses.

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Results

Patient. There were 2631 patients admitted to the MICU during the 30-month study period. Seven hundred forty-eight patients (28.4%) had an MICU stay of <24 h and were excluded from the analysis. The 185 patients (7.0%) who were colonized with VRE at admission to the hospital were retained to calculate point prevalence and colonization pressure, but this group was excluded from further analyses because they were not at risk for acquiring enteric VRE while in the MICU. Eleven VRE-positive patients (0.4%) were excluded from the analyses because of the absence of a previous VRE-negative culture. Three patients (0.1%) were excluded because they did not have discharge cultures performed and because previous VRE cultures performed during their MICU stay were negative, despite there having been VRE-positive cultures <48 h before the patients left the MICU. Eighty patients (3.0%) had multiple admissions to the hospital within a 30-day period that were considered to be a single episode of care. The final study population consisted of 1684 patients.

VRE prevalence estimates at admission to the MICU were 52 (6.6%) of 779 patients, 87 (12.2%) of 709 patients, and 46 (12.0%) of 381 patients for first gown, no gown, and second gown periods, respectively. The VRE acquisition rates were 9.0 cases per 1000 MICU-days in both of the gown periods and 19.6 cases per 1000 MICU-days in the no-gown period (table 1). Demographic and clinical characteristics of patients in the MICU during the 3 study periods are listed in table 1.

Table 1
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Table 1

Demographic and clinical characteristics of patients in the medical intensive care unit (MICU) during periods when gowns were or were not required.

Logistic regression analysi. The risk of acquiring enteric VRE for each study period was assessed by logistic regression analysis. The demographic and clinical characteristics of patients in the MICU, according to VRE acquisition status, are listed in table 2. The unadjusted protective effect of gown use relative to no use of gowns was 0.44 (95% CI, 0.31–0.63). To control for confounding bias, each variable from table 2 was added independently to the model to determine whether the risk estimate for gown use was modified by ⩾10%. Although there were other risk factors consistent with the literature that were significant independent predictors of VRE acquisition in this study population, only 2 variables (colonization pressure stratified by the median number of patient-days of exposure, and duration of anaerobic antimicrobial therapy) were needed to provide the best-fitting model for these data.

Table 2
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Table 2

Demographic and clinical characteristics of patients in the medical intensive care unit (MICU), according to vancomycin-resistant enterococci (VRE)–acquisition status.

Two-way interactions were assessed, and the interaction between colonization pressure and gown use was significant (table 3). Figure 1 illustrates VRE acquisition and colonization pressure for the 30-month period. Gown use had a protective effect on VRE acquisition for patients who had µ15 patient-days of VRE exposure (adjusted OR, 0.43; 95% CI, 0.27–0.68). When the colonization pressure was ⩽15 VRE-positive patient-days of exposure, gown use did not confer protection against VRE acquisition (adjusted OR, 1.50; 95% CI, 0.57–3.98).

Table 3
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Table 3

Logistic regression analysis for vancomycin-resistant enterococci acquisition by gown use, anaerobic agent exposure, and colonization pressure.

Figure 1
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Figure 1

Colonization pressure and number of patients with acquired vancomycin-resistant enterococci (VRE) in the medical intensive care unit from July 1997 through December 1999. PSRs, patient service representatives.

Observations of compliance and environmental culture. Observations of health care workers' compliance with infection-control procedures were performed during April 1998 (the gown period) and April—June 1999 (the no-gown period). There were 22 health care workers and visitors observed during the gown period and 105 observed during the no-gown period. Better compliance with a majority of the infection-control procedures occurred during the gown period. Specifically, a greater percentage of persons wore gloves when entering an isolation room (78% vs. 66%; P = .01), maintained use of isolation apparel while in the room (83% vs. 66%; P < .01), performed clean tasks before dirty tasks within the patient's room (100% vs. 82%; P < .01), and cleaned equipment (i.e., the pulse oximeter) appropriately (17% vs. 0%; P < .01) in the gown period compared with the no-gown period. However, the percentages of persons who removed and discarded gloves before leaving the room (65% vs. 67%; P = .57) and who discarded gloves appropriately (60% vs. 76%; P < .01) were lower during the gown period than they were during the no-gown period. Frequency of compliance with handwashing protocols (i.e., washing for a minimum of 15 s immediately after removing gloves) was similar in the 2 study periods (48% vs. 49%; P = .91)

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Discussion

The use of gowns by health care workers and visitors was protective against the acquisition of enteric VRE in this MICU when VRE colonization pressure was high. Although the findings of Slaughter et al. [10] suggested that gowns do not offer added protection against VRE infection over glove use alone, our data show that they have a protective effect, even after adjusting for known risk factors. Furthermore, Slaughter et al. [10] suggested that gown use might provide enhanced awareness of transmission dynamics and increase compliance with infection-control procedures. Additional studies have shown that enhanced infection-control strategies were associated with increased compliance [8, 22]. Without extensive behavioral analysis, it is difficult to determine whether gowns provide a direct, physical barrier to reduce VRE transmission or whether gowns provide an indirect effect by enhancing compliance with infection-control procedures. Regardless of the mechanism, this study provides evidence that the use of gowns may be protective against the acquisition of VRE.

Similar to other studies, the most prominent risk factor associated with an increased risk of acquisition was colonization pressure [17, 20]. Specifically, as the colonization pressure from VRE increased, the risk for acquiring VRE increased. Until now, the interaction between colonization pressure and gown use has not been evaluated. Our data show that, when a patient had µ15 patient-days of VRE exposure, the added barrier of gown use was protective. These results are similar to the findings of Boyce et al. [9] that a clonal outbreak of VRE was contained after requiring the additional barrier of gowns. In addition, Boyce et al. [9] also found 2 risk factors for acquiring the epidemic VRE strain during the outbreak: (1) proximity to a case patient with VRE, and (2) exposure to a nurse assigned to case patients with VRE. These 2 factors coincide with the fundamental principal of colonization pressure and horizontal transmission. These findings suggest that active VRE surveillance systems should be a component of infection-control protocols aimed at the control of VRE acquisition due to high colonization pressure.

Duration of anaerobic antimicrobial therapy was an independent predictor of VRE acquisition and altered the risk associated with gown use for MICU patients in our study. Because administration of antimicrobial agents affects gastrointestinal flora, receipt of antimicrobial agents presumably altered the gastrointestinal ecology conducive to enterococcal growth [3, 23–25]. Donskey et al. [25] found that administration of anaerobic antimicrobials was associated with higher levels of enteric VRE colonization. Our data support a more judicious use of antimicrobials, which may prevent transmission or reduce detectable levels of enteric VRE.

Another possible explanation is enhanced overall compliance with infection-control practices and increased emphasis on VRE control during the gown period. Except for glove removal, there was better overall compliance with infection-control practices during the gown period, which is consistent with the findings of Slaughter et al. [10]. Whether the protective effect of gown use was direct or indirect (i.e., through enhanced glove use) remains to be studied; we observed low compliance rates with isolation practices, similar to those of most other studies reported in the literature [10, 26–28].

As in most clinical investigations, our study has recognized limitations. As in our earlier work, we relied on a modified measure of colonization pressure, which most likely resulted in an underestimation of colonization pressure and the risk of acquiring enteric VRE [17]. Furthermore, we may have misclassified some patients as having acquired VRE during their MICU stay who were colonized with undetectable levels of VRE before their MICU admission and who were subsequently identified in the MICU as a result of the receipt of antibiotics. Third, we were unable to monitor health care workers' and visitors' compliance with infection-control procedures throughout the entire study. The trend for compliance with most components of the isolation procedures to be better during the gown period may or may not represent what occurred throughout the entire study period. Fourth, we were unable to determine the environmental burden of VRE in this unit for the entire study period. Because VRE persists on a variety of environmental surfaces, identifying these isolates can lead to more-conclusive results concerning modes of transmission. Fifth, we did not confirm horizontal transmission of a single or few clones with molecular testing of the VRE isolates. Although molecular characterization of the VRE clinical isolates might provide further support of the epidemiologic link between VRE acquisition and higher colonization pressure, resources for such testing were not available. Furthermore, if a heterogeneous group of VRE isolates were identified, our conclusion about gown use, given the association between gown use and enteric VRE acquisition, would remain unchanged.

Overall, this study demonstrates the beneficial effect of wearing gowns to reduce the risk of enteric VRE acquisition when colonization pressure is high. Although there are conflicting data regarding the efficacy of gowns on VRE acquisition [8–10, 13, 29], eradication of VRE from a geographic unit is extremely difficult. Strategies to prevent endemic VRE are essential. Therefore, active surveillance is essential to facilitate early detection of patients with VRE and periods of high colonization pressure. The additional barrier of gowns, whether a direct or indirect effect in areas of high colonization pressure, can aid in containing VRE by decreasing the potential for horizontal transmission.

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Acknowledgments

We thank the 65 staff members of the MICU who collected enteric VRE specimens; the BJH medicine residents and attending physicians who facilitated the ongoing surveillance program; Donna Prentice, for managing the intervention, J. Russell Little, Lou Polish, and Roger Lewis, for manuscript review; Kathy Gillespie, for statistical consultation; and Jordana Stewart, for assistance with the preparation of the manuscript.

  • Received November 1, 2001.
  • Revision received February 7, 2002.
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  1. Clin Infect Dis. (2002) 35 (1): 18-25. doi: 10.1086/340739
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