Multicenter Intervention Program to Increase Adherence to Hand Hygiene Recommendations and Glove Use and to Reduce the Incidence of Antimicrobial Resistance
Objective. To determine whether a multimodal intervention could improve adherence to hand hygiene and glove use recommendations and decrease the incidence of antimicrobial resistance in different types of healthcare facilities.
Design. Prospective, observational study performed from October 1, 1999, through December 31, 2002. We monitored adherence to hand hygiene and glove use recommendations and the incidence of antimicrobial‐resistant bacteria among isolates from clinical cultures. We evaluated trends in and predictors for adherence and preferential use of alcohol‐based hand rubs, using multivariable analyses.
Setting. Three intervention hospitals (a 660‐bed acute and long‐term care hospital, a 120‐bed community hospital, and a 600‐bed public teaching hospital) and a control hospital (a 700‐bed university teaching hospital).
Intervention. At the intervention hospitals, we introduced or increased the availability of alcohol‐based hand rub, initiated an interactive education program, and developed a poster campaign; at the control hospital, we only increased the availability of alcohol‐based hand rub.
Results. We observed 6,948 hand hygiene opportunities. The frequency of hand hygiene performance or glove use significantly increased during the study period at the intervention hospitals but not at the control hospital; the maximum quarterly frequency of hand hygiene performance or glove use at intervention hospitals (74%, 80%, and 77%) was higher than that at the control hospital (59%). By multivariable analysis, preferential use of alcohol‐based hand rubs rather than soap and water for hand hygiene was more likely among workers at intervention hospitals compared with nonintervention hospitals (adjusted odds ratio, 4.6 [95% confidence interval, 3.3‐6.4]) and more likely among physicians (adjusted odds ratio, 1.4 [95% confidence interval, 1.2‐1.8]) than among nurses at intervention hospitals. A significantly reduced incidence of antimicrobial‐resistant bacteria among isolates from clinical culture was found at a single intervention hospital, which had the greatest increase in the frequency of hand hygiene performance.
Conclusions. During a 3‐year period, a multimodal intervention program increased adherence to hand hygiene recommendations, especially to the use of alcohol‐based hand rubs. In one hospital, a concomitant reduction was found in the incidence of antimicrobial‐resistant bacteria among isolates from clinical cultures.
Received March 11, 2006; accepted May 1, 2006; electronically published January 3, 2007.
Infection caused by antimicrobial‐resistant bacteria is common at many US hospitals.1 Despite evidence that hand antisepsis can reduce the frequency of pathogen transmission,2‐5 studies have consistently shown that hand hygiene performance by healthcare workers (HCWs) is woefully infrequent.6‐10 To overcome barriers to hand hygiene reported by HCWs, the Centers for Disease Control and Prevention (CDC) has promoted the use of alcohol‐based hand rubs.11 Compared with soap and water, alcohol‐based hand rubs are more efficient,12 effective,13 and less irritating to skin.14,15 These relative benefits have proved to be compelling in successful efforts to promote the use of alcohol‐based hand rub.2,16‐18
Because many interventions have not been shown to sustain improvements in adherence to hand hygiene recommendations when implemented alone, introduction of multimodal, bundled interventions has been recommended.2,4,19‐23 We designed a multimodal intervention program aimed at increasing the frequency of hand hygiene performance and glove use among HCWs and decreasing the incidence of recovery of antimicrobial‐resistant bacteria from clinical culture (hereafter, “incidence of antimicrobial‐resistant bacteria”). We implemented the entire intervention program at 3 of 4 hospitals that participated in the Chicago Antimicrobial Resistance Project and promoted a single intervention—use of alcohol‐based hand rub—at the fourth hospital.
Methods
Settings
The 4 hospitals comprised a 660‐bed acute and long‐term care hospital (hospital A), a 120‐bed community hospital (hospital B), a 600‐bed public teaching hospital (hospital C), and a 700‐bed university teaching hospital (hospital D). From October 1, 1999, through December 31, 2002, we observed hand hygiene performance and glove use by HCWs prospectively in 3 units at each hospital. The units represented different intensities in patient care. HCWs were not informed about the observations. We observed HCWs in 7 intensive care units (ICUs) (1 in hospital A, 2 in hospital B, 2 in hospital C, and 2 in hospital D), 3 medical and/or surgical units (hospitals A, B, and C), 1 skilled care unit (hospital A), and 1 rehabilitation unit (hospital D). At hospital D, after 4 quarters we changed 1 observation unit from the surgical ICU to the neonatal ICU. Because we did not monitor hand hygiene performance and glove use in both of these units throughout the study period, we performed 2 trend analyses: one analysis included data from the surgical ICU and the neonatal ICU, and the other analysis excluded data from both these units. Although the rate of hand hygiene performance or glove use among HCWs in the neonatal ICU was slightly higher than that among HCWs in the surgical ICU, the difference did not substantially or significantly change the results from the trend analyses; we report results of the analyses that include all observations.
Observation of Hand Hygiene Performance and Glove Use
Study personnel, not infection control staff, conducted at least 4 hours of observation in each unit per month (ie, 12 hours per month for each hospital). Observation lasted 60 minutes and was performed during all work shifts. To standardize observations, 3 observers were trained by the same person; we required 80% agreement among the observers about whether hand hygiene had occurred for an entire observation period before unsupervised observations were allowed. The training included tours of the observation units and discussions about each data element. We considered each HCW‐patient encounter as a single opportunity for hand hygiene (ie, we did not record all hand hygiene indications during these encounters). An encounter included HCW contact with any environmental surface in the patient’s room. We categorized each opportunity by whether the HCW touched the patient or an environmental surface only. Because we were concerned that multiple observations of a single HCW during an observation period could influence adherence and violate statistical assumptions of independence, we allowed only a single observation of a HCW during an observation period.
In addition to observing the frequency of hand hygiene performance, we recorded HCW type (ie, physician, nurse, or other), type of contact (ie, patient or environment only), use of gloves during contact and removal of gloves after contact, presence of isolation precautions, and agent used (ie, soap and water or alcohol‐based hand rub). To control for increased awareness of the observer by HCWs being observed, we also recorded the order in which HCWs were observed (eg, first HCW observed, second HCW observed, third HCW observed) during each observation period. We initiated observations at the study hospitals from October through December 1999, and we began implementing interventions in the first quarter of 2000.
Educational Intervention and Introduction of Alcohol‐Based Hand Rub
The content of our educational program was guided by responses to a survey we distributed during infection control sessions at the intervention hospitals.24 The survey queried participants about their understanding of pathogen transmission, opinions about hand hygiene practices, and perceived barriers to hand hygiene (eg, skin irritation and inadequate provision of hand hygiene infrastructure). The goal of the educational sessions was to increase HCW awareness of the value of alcohol‐based hand rubs; we also stressed the importance of wearing gloves to reduce hand contamination. The slides from the presentation were adapted by the CDC for distribution to HCWs or infection control professionals interested in improving hand hygiene at their healthcare facility.25
Starting in March 2000, we delivered 45‐minute educational sessions to personnel at hospitals A, B, and C during their annual mandatory infection control education programs. To engage audiences, we used an interactive audience‐response system, which allowed participants to respond anonymously to questions posed by the speaker and to compare their responses to those of the group. Components of the presentation included review of the CDC’s Healthcare Infection Control Practices Advisory Committee’s hand hygiene guidelines11 and hospital‐specific policies, current options for hand antisepsis, data on hospital‐specific hand hygiene adherence, benefits of using alcohol‐based hand rubs (eg, efficiency, efficacy, and improved skin condition), and value of wearing examination gloves. After the presentation, we distributed pocket‐sized bottles of alcohol‐based hand rub and a hand hygiene fact sheet. We revised the presentation each year; for example, after we noted poor hand hygiene practices by HCWs who touched an environmental surface only, we stressed the importance of hand hygiene in these situations. We continued to emphasize the benefits of alcohol‐based hand rub use and glove use during patient care.
From April through August 2000, we ensured that alcohol‐based hand rub (formulated with 62% ethyl alcohol) was readily available in all inpatient care areas of all 4 facilities. Wall‐mounted hand rub dispensers were installed at or near the entrance to each patient’s room. We solicited HCW input regarding the choice of alcohol‐based hand rub.
Poster Campaign
Between annual educational presentations, we used hospital‐wide poster campaigns at the intervention hospitals. The campaign featured humorous posters of high‐profile hospital administrative and clinical staff using and encouraging HCWs to use alcohol‐based hand rubs. During brief (10–15‐minute) ward‐based academic detailing sessions, a promotional handout that contained information on hand care, hand hygiene, benefits of wearing examination gloves, and hospital‐specific rates of hand hygiene performance was discussed with HCWs.
Surveillance for Antimicrobial‐Resistant Bacteria
From July 1, 1999, through December 31, 2002, we evaluated the incidence of recovery of the following antimicrobial‐resistant bacteria from clinical culture: methicillin‐resistant Staphylococcus aureus (MRSA), vancomycin‐resistant enterococci, third‐generation cephalosporin‐resistant Escherichia coli or Klebsiella species, fluoroquinolone‐resistant Escherichia coli, and Acinetobacter species or Pseudomonas aeruginosa resistant to either imipenem or amikacin. Our analysis excluded outpatient cultures and cultures performed only for screening purposes. We did not record duplicate isolates, defined as isolates with the same resistance phenotype and isolates recovered from the same patient within a 30‐day period. We calculated the overall and organism‐specific incidence as the number of antimicrobial‐resistant isolates recovered per 1,000 patient‐days and report the results aggregated by quarter.
At the intervention hospitals, surveillance for antimicrobial‐resistant isolates was performed by infection control professionals; they recorded their findings on forms that were subsequently scanned into a centralized data warehouse.26 The infection control professionals categorized isolates as either community acquired or hospital acquired, using CDC definitions.27 Comparable data from the control hospital were not collected.
Statistical Analysis
We calculated unit‐specific frequencies of hand hygiene performance and glove use and aggregated the results by quarter. For each hospital, we determined whether there was a significant departure from a linear trend of zero by modeling hand hygiene as the dependent variable and quarter as the explanatory variable. To adjust for unit‐specific effects, we included terms for each unit in our model. We performed similar analyses to assess the trend in hand hygiene practice according to type of contact, agent used, and whether hand hygiene was performed or gloves were used.
We evaluated HCW and facility characteristics by means of bivariable analyses to determine which characteristics were associated with performance of hand hygiene or use of gloves. We created indicator variables for each hospital and for hospital type (ie, intervention versus control), HCW type, observation sequence (dichotomized as first or second HCW observed vs other), and type of contact (ie, environment only, patient, or unknown). We identified factors associated with hand hygiene performance or glove use and factors associated with preference for alcohol‐based hand rub by constructing separate logistic regression models. We aggregated the incidence of infection with antimicrobial‐resistant bacteria quarterly and used linear regression methods to evaluate whether the time‐dependent trend was significantly different from zero. Statistical analyses were performed using Stata statistical software, version 9.0 (Stata).
Results
Hand Hygiene Performance and Glove Use
We observed 6,948 potential hand hygiene opportunities during 1,353 observation sessions. Most observations were of nurses, followed by physicians and other HCWs (Table 1). Adherence was better at intervention hospitals, after use of gloves during contact, and after patient contact (Table 1). Small increases in adherence were recorded for contact with patients under contact isolation precautions, during the middle of the day, and among HCWs observed later during the observation period (Table 1).
The frequency of hand hygiene performance by quarter increased significantly during the study period at hospitals A and B but not at hospital C: at hospital A, the frequency increased from 23% to 46% of hand hygiene opportunities (
); at hospital B, from 30% to 50% (
); and at hospital C, from 35% to 43% (
). The frequency of hand hygiene performance at the control hospital did not change during the study period (from 32% to 31% of opportunities;
) (Figure 1).
Figure 1. Trends in frequency of hand hygiene performance after patient or environmental contact or glove use without hand hygiene performance, by quarter (Q). During the study period, the frequency of hand hygiene performance or glove use without hand hygiene increased significantly at the intervention hospitals (hospitals A, B, and C;
for each hospital) but not at the control hospital (hospital D;
). Analysis of hand hygiene adherence alone revealed significant increases at hospitals A (
) and B (
) but not at hospitals C (
) and D (
).
The increase in the frequency of hand hygiene performance after patient contact was greatest at hospital A (from 32% to 56% of opportunities;
). Increases in the frequency of hand hygiene practice were more significant after contact with an environmental surface only: at hospital A, the frequency increased from 0% to 40% (
); at hospital B, from 0% to 51% (
); and at hospital C, from 5% to 38% (
).
To assess overall protection from microbial contamination of HCWs’ hands, we tallied the frequency of hand hygiene practice after patient care or glove use during care. Hand hygiene performance or glove use increased significantly at all 3 intervention hospitals (quarterly maximum by hospital: 74% of opportunities at hospital A, 80% at hospital B, and 77% at hospital C) but not at the control hospital (59%) (Figure 1). During the study period, HCWs at intervention hospitals were more likely to protect themselves from microbial contamination by wearing gloves or performing hand hygiene (67% of opportunities at hospital A, 74% at hospital B, and 67% at hospital C), compared with HCWs at the control hospital (50%).
The frequency of alcohol‐based hand rub use increased significantly at hospitals A, C, and D (
); the increase in the frequency of use at the community hospital (hospital B) initially was marked, but use then leveled off (
) (Figure 1). In contrast, the frequency of soap and water use was stable at all facilities except hospital C, where the frequency significantly decreased during the study period (
).
By multivariable analysis, hand hygiene performance was more likely among nurses, at intervention hospitals, after glove use, after patient contact, and later during the observation period (Table 2). Choice of alcohol‐based hand rub rather than soap and water was more likely at an intervention hospital and among physicians compared with nurses; HCWs preferentially used soap and water after a patient's skin was contacted and after gloves were worn (Table 2). Time of day and observation sequence had no effect on the choice of alcohol‐based hand rub over soap and water for hand hygiene.
Antimicrobial‐Resistant Clinical Isolates
At hospital A, a significant decrease in the overall incidence of hospital‐acquired, antimicrobial‐resistant bacteria occurred during the study period, despite a nonsignificant increase in the incidence of resistance among community‐acquired bacteria (Figure 2). A decreased incidence of antimicrobial resistance was evident for the following organisms: third‐generation cephalosporin–resistant E. coli (
), fluoroquinolone‐resistant E. coli (
), imipenem‐resistant P. aeruginosa (
), and MRSA (
). In contrast, the incidence of resistance among community‐acquired organisms (defined as antimicrobial‐resistant organisms recovered from culture of a specimen obtained within 48 after admission or transfer to hospital A) increased for MRSA (
) and imipenem‐resistant P. aeruginosa (
).
Figure 2. Trend in the incidence of antimicrobial‐resistant organisms among isolates recovered from clinical culture and trend in the percentage of hand hygiene opportunities for which healthcare workers (HCWs) used either soap and water or alcohol‐based hand rub after patient contract or used gloves during patient contact in hospital A. During the study period, we observed a significant increase in the frequency of hand hygiene or glove use (
), a significant decrease in the incidence of antimicrobial resistance among hospital‐acquired bacteria (
), and a nonsignificant increase in the incidence of antimicrobial resistance among community‐acquired bacteria (
). See Methods for antimicrobial‐resistant organisms for which surveillance was performed. Q, quarter.
No decreases in the incidence of antimicrobial‐resistant bacteria were detected at hospitals B and C.
Discussion
We observed a sustained increase in the frequency of hand hygiene practice during 3 years at 2 of 3 hospitals that implemented a multimodal intervention program. The increased hand hygiene adherence was primarily the result of increased use of alcohol‐based hand rubs, especially among physicians. Despite the increased availability of alcohol‐based hand rub, no increase in the frequency of hand hygiene practice was observed at the hospital that did not implement the intervention program. At the hospital that had the greatest increase in the frequency of hand hygiene practice, there was a concomitant reduction in the incidence of several antimicrobial‐resistant bacteria.
Although sustained improvements in hand hygiene have been reported by other investigators,2,4,18,21 our study adds to their findings by documenting improved adherence to hand hygiene recommendations at multiple institutions across the spectrum of health care during a 3‐year period. Although the overall increases may appear modest, the following factors need to be considered when interpreting our results: we included any contact with an environmental surface as a hand hygiene opportunity, we required that hand hygiene occur before contacting any object outside the patient’s room, and we did not include the significantly higher frequencies of hand hygiene performance recorded by the infection control department at the 2 intervention hospitals that submitted these data (these frequencies were 29% and 57% higher than those recorded by study personnel; data not shown). In addition to improved compliance with hand hygiene, we documented frequent use of examination gloves, which is an adjunct to hand cleansing.
Because isolated interventions, such as education or performance feedback, have only been successful for short periods, we modeled our program on recommendations that emphasized the importance of a multimodal approach.23 In addition, to improve retention of our educational message, we developed a program that facilitated audience participation through use of handheld keypads; the program was adapted by the CDC and is available for distribution.25 Of the 4 study hospitals, 3 incorporated the multimodal intervention; the fourth hospital increased access to alcohol‐based hand rubs without incorporating the other program features, and no increase in the frequency of hand hygiene practice occurred.
Use of alcohol‐based hand rub supplemented, rather than supplanted, use of soap and water. Alcohol‐based hand rubs were better accepted by physicians than by nurses, which is important because historically physicians have been less adherent to hand hygiene recommendations. When we surveyed HCWs,24 we found that nurses rather than physicians were more concerned about skin damage caused by alcohol‐based hand rubs. Despite addressing this concern in our presentations, we had less success changing nurses’ behavior. In addition to increased use of alcohol‐based hand rubs after patient care, overall hand hygiene was improved by increased use of gloves during patient care.
Our greatest success at increasing hand hygiene practice was at the acute and long‐term care facility (hospital A) and community hospital (hospital B). Although use of alcohol‐based hand rubs increased at the large public teaching hospital (hospital C), the increase in the rate of hand hygiene performance was not significant. The relative success at hospitals A and B may be due to the stability of their work forces: because they had few house staff members or students and few or no physicians in private practice, it was easier to educate HCWs with episodic educational sessions. To achieve significant improvements in hand hygiene adherence at teaching hospitals, we would need to ensure good penetration of our educational efforts to rotating students, house staff members, and attending physicians.
Coincident with the largest increase in the frequency of hand hygiene practice, hospital A had significant decreases in the overall incidence of antimicrobial‐resistant bacteria recovered from clinical culture. This decrease occurred despite a stable or increasing incidence of resistance among community‐acquired bacteria. Because of the observational study design, there was no randomized control group; our findings must therefore be interpreted with caution. Although the decrease in antimicrobial‐resistant organisms at hospital A may have been the result of reduced hand contamination, other factors may have contributed to the decrease. For example, there may have been unmeasured changes in the patient population, and there was a separate intervention (initiated in November 2000) to improve antimicrobial prescribing practices at hospital A28; however, the decrease in antimicrobial‐resistant organisms preceded the intervention to improve prescribing practices. Because the frequency of culture performance at hospital A was unchanged during the study (data not shown), the decrease in antimicrobial‐resistant organisms was unlikely to be the result of changes in the frequency of testing. Our study adds to the seminal work of Pittet et al.2 and to the growing body of evidence that increased frequency of hand hygiene performance, especially by means of alcohol‐based hand rubs, is associated with a decreased incidence of antimicrobial‐resistant bacteria2‐4,29 and of hospital‐acquired infection.5,21 Incorporation of other interventions into a multimodal strategy, such as active surveillance culture,30,31 environmental decontamination,32 and patient decolonization,33 could provide an additional level of control of the spread of antimicrobial resistance.
Theoretical models suggest that, to interrupt transmission of antimicrobial‐resistant organisms in settings where colonization pressure is high, hand hygiene needs to occur after 60%‐80% of patient contacts34; however, the frequent use of gloves can notably reduce HCW hand carriage of vancomycin‐resistant enterococci35 and may have contributed to the decreased incidence of antimicrobial‐resistant bacteria.
Our study has several limitations. First, we selected observation units from our study hospitals that represented both ICUs and non‐ICUs and allowed for relatively inconspicuous observations of hand hygiene behavior; we did not match units by type of care delivered. Second, we did not control for workload by monitoring the ratio of nurses to patients. Third, our observations of hand hygiene performance, glove use, and antimicrobial resistance rates suffer from the limitations of ecological studies in which associations are not made at the level of the individual. Fourth, we performed a prospective, observational study because our staffing patterns precluded randomizing the intervention by unit or HCW type; however, we included a control hospital that introduced alcohol‐based hand rub but did not implement the intervention; we also observed hand hygiene behavior over several years to evaluate the sustainability of our intervention. Finally, observer bias is also a possible limitation. In fact, we found that the rate of hand hygiene practice improved later in the observation period, especially outside ICUs (data not shown); however, our findings were unchanged when we controlled for observation sequence.
In conclusion, we found that implementation of a multimodal intervention program resulted in a sustained increase in adherence to hand hygiene recommendations and use of alcohol‐based hand rub. The provision of an alcohol‐based hand rub in the absence of an aggressive educational intervention was insufficient to improve hand hygiene rates. At one hospital, the increased rate of hand hygiene practice was associated with a decreased incidence of antimicrobial‐resistant bacteria recovered from clinical culture.
Acknowledgments
We thank participants from the Chicago Antimicrobial Resistance Project; Stroger, Oak Forest, and Provident hospitals; Rush University Medical Center; and the CDC. We thank Ellen Holfels for help with editing figures and manuscript preparation.
This work was funded by the Centers for Disease Control and Prevention (cooperative agreement U50/CCU515853‐03).
References
- 1. Fridkin SK, Steward CD, Edwards JR, et al. Surveillance of antimicrobial use and antimicrobial resistance in United States hospitals: project ICARE phase 2. Project Intensive Care Antimicrobial Resistance Epidemiology (ICARE) hospitals. Clin Infect Dis 1999; 29:245‐252.
- 2. Pittet D, Hugonnet S, Harbarth S, et al. Effectiveness of a hospital‐wide programme to improve compliance with hand hygiene: Infection Control Programme. Lancet 2000; 356:1307‐1312.
- 3. MacDonald A, Dinah F, MacKenzie D, Wilson A. Performance feedback of hand hygiene, using alcohol gel as the skin decontaminant, reduces the number of inpatients newly affected by MRSA and antibiotic costs. J Hosp Infect 2004; 56:56‐63.
- 4. Larson EL, Early E, Cloonan P, Sugrue S, Parides M. An organizational climate intervention associated with increased handwashing and decreased nosocomial infections. Behav Med 2000; 26:14‐22.
- 5. Rosenthal VD, Guzman S, Safdar N. Reduction in nosocomial infection with improved hand hygiene in intensive care units of a tertiary care hospital in Argentina. Am J Infect Control 2005; 33:392‐397.
- 6. Bischoff WE, Reynolds TM, Sessler CN, Edmond MB, Wenzel RP. Handwashing compliance by health care workers: the impact of introducing an accessible, alcohol‐based hand antiseptic. Arch Intern Med 2000; 160:1017‐1021.
- 7. Pittet D, Simon A, Hugonnet S, Pessoa‐Silva CL, Sauvan V, Perneger TV. Hand hygiene among physicians: performance, beliefs, and perceptions. Ann Intern Med 2004; 141:1‐8.
- 8. Pittet D, Mourouga P, Perneger TV. Compliance with handwashing in a teaching hospital: Infection Control Programme. Ann Intern Med 1999; 130:126‐130.
- 9. Lankford MG, Zembower TR, Trick WE, Hacek DM, Noskin GA, Peterson LR. Influence of role models and hospital design on hand hygiene of healthcare workers. Emerg Infect Dis 2003; 9:217‐223.
- 10. Larson E, Kretzer EK. Compliance with handwashing and barrier precautions. J Hosp Infect 1995; 30:S88‐S106.
- 11. Boyce JM, Pittet D. Guideline for Hand Hygiene in Health‐Care Settings: recommendations of the Healthcare Infection Control Practices Advisory Committee and the HICPAC/SHEA/APIC/IDSA Hand Hygiene Task Force. Infect Control Hosp Epidemiol 2002; 23:S3‐S40.
- 12. Voss A, Widmer AF. No time for handwashing!? Handwashing versus alcoholic rub: can we afford 100% compliance? Infect Control Hosp Epidemiol 1997; 18:205‐208.
- 13. Trick WE, Vernon MO, Hayes RA, et al. Impact of ring wearing on hand contamination and comparison of hand hygiene agents in a hospital. Clin Infect Dis 2003; 36:1383‐1390.
- 14. Boyce JM, Kelliher S, Vallande N. Skin irritation and dryness associated with two hand‐hygiene regimens: soap‐and‐water hand washing versus hand antisepsis with an alcohol hand gel. Infect Control Hosp Epidemiol 2000; 21:442‐448.
- 15. Larson EL, Aiello AE, Bastyr J, et al. Assessment of two hand hygiene regimens for intensive care unit personnel. Crit Care Med 2001; 29:944‐951.
- 16. Girard R, Amazian K, Fabry J. Better compliance and better tolerance in relation to a well‐conducted introduction to rub‐in hand disinfection. J Hosp Infect 2001; 47:131‐137.
- 17. Harbarth S, Pittet D, Grady L, et al. Interventional study to evaluate the impact of an alcohol‐based hand gel in improving hand hygiene compliance. Pediatr Infect Dis J 2002; 21:489‐495.
- 18. Hugonnet S, Perneger TV, Pittet D. Alcohol‐based handrub improves compliance with hand hygiene in intensive care units. Arch Intern Med 2002; 162:1037‐1043.
- 19. Larson EL, Bryan JL, Adler LM, Blane C. A multifaceted approach to changing handwashing behavior. Am J Infect Control 1997; 25:3‐10.
- 20. Pittet D. Improving adherence to hand hygiene practice: a multidisciplinary approach. Emerg Infect Dis 2001; 7:234‐240.
- 21. Lam BC, Lee J, Lau YL. Hand hygiene practices in a neonatal intensive care unit: a multimodal intervention and impact on nosocomial infection. Pediatrics 2004; 114:565‐571.
- 22. Johnson PDR, Martin R, Burrell LJ, et al. Efficacy of an alcohol/chlorhexidine hand hygiene program in a hospital with high rates of nosocomial methicillin‐resistant Staphylococcus aureus (MRSA) infection. Med J Aust 2005; 183:509‐514.
- 23. Kretzer EK, Larson EL. Behavioral interventions to improve infection control practices. Am J Infect Control 1998; 26:245‐253.
- 24. Wisniewski MF, Kim S, Trick WE, Welbel SF, Weinstein RA. The effect of education on hand hygiene beliefs and practices: a five‐year experience. Infect Control Hosp Epidemiol. In press.
- 25. Materials to promote hand hygiene in your healthcare facility. Available at: http://www.cdc.gov/handhygiene/. Accessed March 2, 2006.
- 26. Wisniewski MF, Kieszkowski P, Zagorski BM, Trick WE, Sommers M, Weinstein RA. Development of a data warehouse for hospital infection control. J Am Med Inform Assoc 2003; 10:454‐462.
- 27. Garner JS, Jarvis WR, Emori TG, Horan TC, Hughes JM. CDC definitions for nosocomial infections, 1988. Am J Infect Control 1988; 16:128‐140.
- 28. Schwartz DSL, DeMarais P, Trick W, Weinstein R. Beneficial effect of a training intervention based on IDSA and SHEA guidelines for antibiotic use in long term care facilities. In: Program and abstracts of the 39th Annual Meeting of the Infectious Diseases Society of America; 2001; San Francisco, CA. Abstract 490.
- 29. Gordin FM, Schultz ME, Huber RA, Gill JA. Reduction in nosocomial transmission of drug‐resistant bacteria after introduction of an alcohol‐based handrub. Infect Control Hosp Epidemiol 2005; 26:650‐653.
- 30. Jernigan JA, Clemence MA, Stott GA, et al. Control of methicillin‐resistant Staphylococcus aureus at a university hospital: one decade later. Infect Control Hosp Epidemiol 1995; 16:686‐696.
- 31. Ostrowsky BE, Trick WE, Sohn AH, et al. Control of vancomycin‐resistant enterococcus in health care facilities in a region. N Engl J Med 2001; 344:1427‐1433.
- 32. Hayden MK, Bonten MJ, Blom DW, Lyle EA, van de Vijver D, Weinstein RA. Reduction in acquisition of vancomycin‐resistant enterococcus after enforcement of routine environmental cleaning measures. Clin Infect Dis 2006; 42:1552‐1560.
- 33. Vernon MO, Hayden MK, Trick WE, Hayes RA, Blom DW, Weinstein RA. Chlorhexidine gluconate to cleanse patients in a medical intensive care unit: the effectiveness of source control to reduce the bioburden of vancomycin‐resistant enterococci. Arch Intern Med 2006; 166:306‐312.
- 34. Austin DJ, Bonten MJ, Weinstein RA, Slaughter S, Anderson RM. Vancomycin‐resistant enterococci in intensive‐care hospital settings: transmission dynamics, persistence, and the impact of infection control programs. Proc Natl Acad Sci U S A 1999; 96:6908‐6913.
- 35. Tenorio AR, Badri SM, Sahgal NB, et al. Effectiveness of gloves in the prevention of hand carriage of vancomycin‐resistant enterococcus species by health care workers after patient care. Clin Infect Dis 2001; 32:826‐829.



