Original Article
Comparative Efficacy of Alternative Hand-Washing Agents in Reducing Nosocomial Infections in Intensive Care Units
N Engl J Med 1992; 327:88-93July 9, 1992
- Abstract
- Abstract
Background.
Effective hand-washing can prevent nosocomial infections, particularly in high-risk areas of the hospital. There are few clinical studies of the efficacy of specific hand-cleansing agents in preventing the transmission of pathogens from health care workers to patients.
Methods.
For eight months, we conducted a prospective multiple-crossover trial involving 1894 adult patients in three intensive care units (ICUs). In a given month, the ICU used a hand-washing system involving either chlorhexidine, a broad-spectrum antimicrobial agent, or 60 percent isopropyl alcohol with the optional use of a nonmedicated soap; in alternate months the other system was used. Rates of nosocomial infection and hand-washing compliance were monitored prospectively.
Results.
When chlorhexidine was used, there were 152 nosocomial infections, as compared with 202 when the combination of alcohol and soap was used (adjusted incidence-density ratio [IDR], 0.73; 95 percent confidence interval, 0.59 to 0.90). The largest reduction with chlorhexidine was in gastrointestinal infections (IDR, 0.19; 95 percent confidence interval, 0.05 to 0.64). When chlorhexidine was available, the rates of nosocomial infection declined in each of the ICUs, and health care workers washed their hands more often than when alcohol and soap were used (relative risk, 1.28; 95 percent confidence interval, 1.02 to 1.60). The total volume of alcohol and soap used was 46 percent that of chlorhexidine (P<0.001).
Conclusions.
A hand-disinfection system using an antimicrobial agent (chlorhexidine) reduces the rate of nosocomial infections more effectively than one using alcohol and soap. The improvement may be explained at least in part by better compliance with hand-washing instructions when chlorhexidine was used. (N Engl J Med 1992;327: 88–93.)
Media in This Article
Table 1
Characteristics of Patients in the Two Study Arms.Table 2
Rates of Hand-Washing According to ICU.Article Activity
- Article
NOSOCOMIAL infections represent major sources of morbidity and mortality for patients in the intensive care unit (ICU).1 2 3 4 5 Important risk factors for such infections include life-threatening medical or surgical conditions, the immunocompromised state, alterations in flora due to exposure to multiple antibiotics, and the disruption of skin and mucous membrane by the use of invasive devices.6 7 8 9 The organisms causing these infections include antibiotic-resistant gram-negative bacilli, staphylococci, enterococci, and candida species.10 Most endemic infections are transmitted by the hands of health care workers.11 Similarly, outbreaks of infection due to the transmission of a specific pathogen from patient to patient or from a contaminated device to a patient are well documented.12 Pathogenic gram-negative bacilli may survive on the hands for over two hours.13 Since the time of Semmelweis, hand-washing has been shown to reduce the incidence of nosocomial infections.14 15 16 17 18 Thus, it appears that many infections can be prevented by interrupting their transmission on the hands.19
Various antimicrobial chemicals have been incorporated into hand-washing agents, including chlorhexidine, iodophors, quaternary ammonium compounds, and alcohols.20 The efficacy of many of these agents has been tested experimentally, although carefully conducted field testing would be desirable. Some have assumed that clinical trials of alternative hand-cleansing agents would be too difficult to perform, because of insufficient statistical power and multiple confounding variables.21 22 23 24 Thus, current choices are based on in vitro testing and experimental models of hand-washing.
Chlorhexidine gluconate is frequently recommended because of its broad antimicrobial spectrum, low toxicity, and residual activity. Isopropyl alcohol, also effective in removing nontransient bacterial flora from the hands, is relatively inexpensive and is widely used in Europe.22 , 25 26 27 28 29 We report the results of an eight-month crossover study comparing the effects of these two agents on nosocomial-infection rates in the ICUs at our hospital.
Methods
Hospital
The University of Iowa Hospital is a 902-bed teaching facility providing tertiary care to residents of Iowa and the surrounding region. During the study period, 46 beds were available for adult critical care: 23 beds in the surgical ICU (50 percent), 12 in the medical ICU (26 percent), and 11 in the cardiovascular ICU (24 percent). There were 27,854 hospital admissions from July 1987 through June 1988, and a patient's mean stay was 8.5 days. During this period, adult admissions to the ICU totaled 3420, with a mean stay of 3.3 days.
Study Design
A four-month pilot investigation was performed from July through October 1987 in a single ICU to evaluate the feasibility of the project and determine the number of patients required for adequate study power. The periods when alcohol and soap were used were associated with a trend toward lower nosocomial-infection rates. Subsequently, an eight-month clinical trial was performed from July 3, 1988, through February 28, 1989, to compare the effect of the two hand-washing systems on nosocomial-infection rates in the three adult ICUs. A study design involving a monthly crossover was used.
Definition of Nosocomial Infection
For the purposes of the study, an infection was defined as nosocomial if it developed more than 72 hours after the patient was admitted to the ICU. Infection-control nurses and technicians used a modified version of the criteria of the Centers for Disease Control30 to classify the infections.31
Surveillance
Prospective surveillance of nosocomial infections in the ICUs has been performed continuously at the University of Iowa since 1976. Each critical care unit is evaluated by a member of the infection-control team every weekday. Recently, the university's hospitalwide system of nosocomial surveillance was validated by standard methods and was shown to have a sensitivity of 81 percent and a specificity of 98 percent.32
Hand-Washing Systems
Two hand-washing systems were used in the study, one involving a 4 percent solution of chlorhexidine gluconate (Hibiclens, Stuart Pharmaceuticals, Wilmington, Del.) and the other involving a 60 percent isopropyl alcohol hand-rinsing agent (Cal-Stat, Calgon—Vestal, St. Louis) with the optional use of a separate nonmedicated soap with a neutral pH (Kindest Kare, Calgon—Vestal). During July, the chlorhexidine system was introduced in the surgical ICU, and the alcohol—soap system was introduced in the medical and cardiovascular ICUs. In each subsequent month, the system in use in a given ICU was switched to the alternate system. When the alcohol—soap combination was available, health care personnel were instructed to use the alcohol routinely. The soap was to be used if the hands were visibly contaminated, in which case the hands were to be washed, rinsed with tap water, and dried, after which the alcohol product was to be used. Dispensers for the hand-cleansing agents were located at all the sinks in the ICU, as well as in all the lavatories. In addition, individual dispensers containing the alcohol product were mounted on the wall at each patient's bedside.
The soap and alcohol were dispensed in a metered dose (mean doses, 1.4 and 0.8 ml per pump stroke, respectively). Chlorhexidine was delivered by unmetered hand and foot pumps (mean dose, 3.7 ml from the hand pump and 4.0 ml from the foot pump); the amount dispensed depended on the operator and required priming of the pump.
The presence of any other, unauthorized hand-cleansing agents on an ICU was reported by housekeeping personnel, and the agents were immediately removed. At the beginning of each month of the study, the amount of hand-cleansing agents distributed to each unit was recorded. At the end of the month, the remaining amount was measured and replaced with the opposite agent, allowing an aggregate measure of use.
Comparability of Treatment Groups
The variables used to assess the comparability of the two study populations included the age and sex of the patient, the Major Diagnostic Categories classification used in the diagnosis-related-groups reimbursement scheme, the risk score of the American Society of Anesthesiology in the case of surgical patients, and the Unit Acuity Score. The Unit Acuity Score represented a weighted classification system routinely used by the nursing service to determine the intensity of staffing requirements for the ICU. This score reflected the frequency of patient—nurse interactions in relation to such needs as the taking of vital signs, invasive monitoring devices, mechanical ventilation, medical procedures, parenteral nutrition, isolation precautions, and the presence of incontinence or behavioral dysfunction. High scores reflect frequent care interactions and thus presumably frequent opportunities for hand-washing, although the scores have not been prospectively validated for that purpose. A mean acuity score per patient was determined monthly for each ICU.
Education about Hand-Washing
A special education program on the appropriate use of each hand-cleansing agent was provided by a videotaped demonstration, written instructions, and frequent presentations in the ICUs. The videotape was distributed to each ICU and viewed at regularly scheduled sessions by the nursing staff on all shifts during the week before the study began. The videotape was required viewing at general staff meetings in the departments of radiology, physical therapy, and respiratory therapy and was included in the orientation of new personnel. Staff members who failed to view the tape were mailed written instructions with a content similar to that of the film. Resident and staff physicians received written instructions about the study protocol before their ICU rotations. A formal refresher program was provided at the midpoint of the study. Moreover, a monthly summary of the results of hand cultures and of compliance with hand-washing instructions was posted in each ICU in the middle of each month.
Compliance with Hand-Washing Instructions
To assess compliance with hand-washing instructions, two observers monitored the hand-washing practices of health care workers in each ICU. The total number of potential opportunities for hand-washing and the actual number of episodes of hand-washing were recorded during 30-minute observation periods at random intervals throughout the day and night. The observations were distributed equally over the eight months of the study and in proportion to the total bed capacity of the three ICUs. All the staff members providing care to a given patient in a randomly selected bed during each 30-minute observation period were monitored to determine their compliance with the hand-washing protocols defined in the educational material provided at the beginning of the study. Variations between observers in the assessment of compliance with hand-washing instructions were recorded during five simultaneous monitoring sessions. Both observers identified 96 percent of 23 potential opportunities for hand-washing identified by a third observer with experience in such determinations.
Hand Cultures
Cultures were obtained randomly from the hands of health care workers in each unit after they had cared for the patient selected for observation. Each hand was placed in a separate sterile polyethylene bag (Dow Chemical, Indianapolis) with 15 ml of tryptic soy broth (Difco, Detroit) supplemented with Tween 80 (0.5 percent; Fisher Scientific, Fairlawn, N.J.), lecithin (2 percent; Fisher), sodium oleate (0.5 percent; J.T. Baker Chemical, Phillipsburg, N.J.), and sodium sulfite (0.1 percent; J.T. Baker) as neutralizing agents and agitated vigorously for 30 seconds. An aliquot of 0.1 ml was pipetted onto a trypticase soy agar plate (BBL, Cockeysville, Md.) containing 6 μg of gentamicin per milliliter and an equal volume pipetted onto a MacConkey agar plate (BBL). All the plates were incubated at 35°C for 24 hours. After incubation, colonies were identified by standard microbiologic techniques.
Toxicity
At the completion of the trial, a brief questionnaire was distributed to all ICU personnel about the acceptability and side effects of each hand-washing agent. In addition, anyone with dermatitis was interviewed by one of the investigators.
Statistical Analysis
The primary measure of the efficacy of the hand-washing system was the rate of nosocomial infection in the study patients. Each month, during a 72-hour period after the crossover to the alternate hand-washing system, any new nosocomial infection was attributed to the previous month's washing system. Seven additional variables were monitored: site-specific infection rates, crude mortality rates, lengths of stay in the ICU, compliance with hand-washing instructions, types of microbial species recovered from patients' nosocomial infections and health care workers' hands, amounts of hand-cleansing agents used, and the presence or absence of dermatitis.
Comparisons between treatment groups were performed by the chi-square statistic for categorical variables and by Student's t-test for normally distributed continuous variables. When the data were not distributed normally, the Wilcoxon rank-sum test was used. A MantelHaenszel summary adjusted risk ratio was calculated to compare relative degrees of compliance with hand-washing instructions in all the ICUs. The Breslow-Day test for the heterogeneity of the odds ratios was used to determine whether there was more than chance variation in compliance among units.33 Infection rates for the two populations were evaluated with the incidence-density ratio (IDR) to compare the rates at which patients were infected and the rates of infection per 1000 patient-days.33 The number of infections per group was compared with use of MantelHaenszel summary adjusted IDRs, stratified according to the sequence of infections (e.g., first, second, and third) and the number of days at risk for each.34 The MantelHaenszel adjusted chi-square statistic was used to test for the effect over all the strata. All P values are two-sided, and the alpha level of significance was set at 0.05. Ninety-five percent confidence intervals were calculated.35
Results
Characteristics of the Study Population
During the eight-month study, 1894 patients were admitted to the three ICUs and were cared for by 577 health care workers. The mean stay in the ICU was 3.4 days. Four hundred twenty patients (22 percent) were in the ICUs at the time of a crossover between treatments. There were 932 patients in the chlorhexidine group and 962 patients in the alcohol—soap group who were in the ICU at a time when only one agent was used. As a result, 1352 patients were included in the chlorhexidine group and 1382 in the alcohol—soap group for the comparison of base-line characteristics. It is important to note that the two treatment groups did not differ appreciably with respect to age, sex, length of stay in the ICU, nursing Unit Acuity Scores, major diagnostic categories, American Society of Anesthesiology scores (for those undergoing an operative procedure), or surgical rates (Table 1Table 1
Characteristics of Patients in the Two Study Arms.).Compliance with Hand-Washing Instructions
The hand-washing behavior of the professional staff was monitored over a 152-hour period during which there were 1233 opportunities for hand-washing (579 with chlorhexidine and 654 with alcohol—soap). The proportion of such opportunities in which the hands were washed was 42 percent during chlorhexidine use and 38 percent when the alcohol—soap combination was available (Table 2Table 2
Rates of Hand-Washing According to ICU.). Hand-washing was significantly more frequent during observation in the cardiovascular ICU when chlorhexidine was available than when alcohol and soap were available (48 percent vs. 30 percent; relative risk, 2.14; 95 percent confidence interval, 1.32 to 3.46; P = 0.002). Overall compliance with hand-washing instructions in the three units was significantly better during periods when chlorhexidine was available (relative risk by the MantelHaenszel test, 1.28; 95 percent confidence interval, 1.02 to 1.60).Significantly more chlorhexidine was used monthly than soap and alcohol combined (median, 165.3 vs. 75.2 liters per 1000 patient-days, respectively; P<0.001, by the Wilcoxon rank-sum test). In each ICU, approximately twice as much chlorhexidine was used as alcohol and soap combined. The overall volume of alcohol used was 42 percent that of nonmedicated soap.
Nosocomial Infection
Ninety-six patients initially became infected while the chlorhexidine hand-washing system was in use (Table 3Table 3
Nosocomial Infections in the Two Study Groups.). In contrast, 116 patients initially became infected while the alcohol and soap were being used. A stratified analysis for the number of patients with multiple infections according to the agent in use at the time of the initial infection demonstrated a nonsignificant trend in favor of chlorhexidine (summary adjusted IDR, 0.87; 95 percent confidence interval, 0.67 to 1.15). Overall, 152 nosocomial infections occurred in the chlorhexidine group, as compared with 202 in the alcohol—soap group (IDR, 0.73; 95 percent confidence interval, 0.59 to 0.90). When infection rates were stratified according to unit, the rate was significantly lower in the cardiovascular ICU with chlorhexidine than with alcohol—soap (34.8 vs. 59.9 infections per 1000 patient-days, respectively; IDR, 0.58; 95 percent confidence interval, 0.36 to 0.92). Similarly, rates of infection were lower in both the surgical ICU (IDR, 0.75; 95 percent confidence interval, 0.58 to 0.99) and the medical ICU during periods of chlorhexidine use, although differences in the latter unit did not reach statistical significance (IDR, 0.72; 95 percent confidence interval, 0.45 to 1.13).The analysis of site-specific infections revealed that there were significantly fewer gastrointestinal infections when chlorhexidine was available (IDR, 0.19; 95 percent confidence interval, 0.05 to 0.64). Although at those times the rates of infection of skin and soft tissue (IDR, 0.56; 95 percent confidence interval, 0.27 to 1.13) and of infection at the site of intravenous catheters (IDR, 0.43; 95 percent confidence interval, 0.17 to 1.08) were approximately half those observed when alcohol and soap were available, these differences were not statistically significant. Similarly, there was a nonsignificant trend toward fewer urinary tract infections and primary bacteremias during periods of chlorhexidine use.
Nosocomial infections due to gram-negative bacilli, gram-positive cocci, and fungi occurred in similar proportions with each hand-washing system (Table 4Table 4
Organisms Isolated from 212 Patients with Nosocomial Infections.). Most bacterial infections were caused by staphylococci and gram-negative enteric bacilli (Enterobacteriaceae). Interestingly, the patients in units where the alcohol—soap hand-washing system was used had more infections with Xanthomonas maltophilia (9 vs. 0, P = 0.012), although epidemiologically these infections did not appear to be related to each other. Stratified analyses of the odds of infection in the two treatment groups according to ICU, the need for surgery, and number of infections per patient demonstrated no evidence of confounding and showed a consistent effect in favor of chlorhexidine.The overall rates of nosocomial infection (the number of infected patients per 1000 patient-days) in the three ICUs studied were not significantly different from the rates during the previous eight months (IDR, 1.03; 95 percent confidence interval, 0.87 to 1.24). Nor were they significantly different during the eight months after the completion of the study (IDR, 1.01; 95 percent confidence interval, 0.85 to 1.20). Thus, the study itself did not appear to influence the overall infection rates (i.e., there was no evidence of a Hawthorne effect).
Cultures of Hands
A total of 328 cultures from hands were obtained after hand-washing, in a pattern distributed evenly over the eight-month study period; they were stratified according to the number of beds in each ICU. The rate of hand carriage was 2.25 organisms per pair of hands from which cultures were obtained after periods of chlorhexidine use, as compared with 2.51 organisms per pair of hands after the use of alcohol and soap. Gram-positive organisms were isolated most frequently, accounting for 87.6 percent and 82.4 percent of isolates associated with the respective agents. Gram-negative organisms were relatively uncommon, accounting for 10.7 percent of the isolates obtained after chlorhexidine use and 15.3 percent of those obtained after alcohol—soap use. Fungi were recovered infrequently, from 1.7 percent of the isolates obtained during chlorhexidine use and 2.3 percent of those obtained during alcohol—soap use.
Toxicity
Fewer than 1 percent of health care personnel (5 of 577) reported skin irritation after using any of the hand-washing products. Four people reported dry skin (associated in three with chlorhexidine and in one with alcohol and soap), and one person reported an urticarial rash (with alcohol—soap). These symptoms all resolved with the use of a replacement soap. None of those who had skin irritation sought medical attention or therapy other than the discontinuation of the agent in question.
Mortality and Length of Stay
The data on mortality and length of stay in the ICU are complex, since patients may have received care from a number of persons who used both hand-washing agents. Patients who were in the ICU only during a period of chlorhexidine use had a mean stay of 2.9 days, as compared with 2.7 days for those in the ICU only during a period of alcohol-soap use. The mortality rate among patients cared for only during a period of chlorhexidine use was 47.9 deaths per 1000 patient-days, as compared with 50.9 deaths per 1000 patient-days for those cared for only during a period of alcohol—soap use (IDR, 0.94; 95 percent confidence interval, 0.68 to 1.30).
Discussion
The consequences of nosocomial infection add dramatically to the morbidity and mortality expected from underlying diseases alone and may greatly increase hospital costs because of extended hospital stays.1 , 3 , 36 37 38 Nationally, the annual direct costs of nosocomial infection are estimated to range from $5 billion to $10 billion.39 Nosocomial infections occur disproportionately in patients in the ICU1 , 2 , 4 5 6 7 8 , 12 and are thought to originate in part with health care workers who transmit bacteria by their hands to patients.13 , 16 17 18 19 20 The magnitude of the problem and the likelihood of preventing certain infections mandate effective control measures.
Hand-washing remains one of the simplest and most important interventions. Despite its apparent simplicity, several studies, including our own, have documented poor compliance with hand-washing procedures, particularly in the ICU.40 41 42 Improvements either in the frequency of hand-washing or in the use of gloves and gowns have resulted in decreased infection rates in ICUs, providing further evidence of the role of transmission on hands.43 Other data also suggest that infection rates are reduced by the use of antiseptic hand-washing products as compared with the use of plain (nonmedicated) soap or with no hand-washing.44 , 45
Although the present study was neither randomized nor blinded, we have shown that a monthly-crossover clinical trial is efficient and statistically powerful for the study of alternative hand-washing systems. Using this approach, we have shown significantly lower rates of nosocomial infection when ICUs have a system that uses chlorhexidine as opposed to one that uses alcohol and soap. There was consistency in our data, since the effect favoring chlorhexidine was observed in all three critical care units. Although the number of patients with nosocomial infections did not differ significantly between the two hand-washing groups, there were more infections in the alcohol—soap group. These differences in rates of infection could not be explained by differences in the underlying characteristics of the two populations of patients or in the distribution of microbial species isolated from the hands of personnel involved in patient care.
There were also consistently lower rates of infection in the chlorhexidine groups according to anatomical site. An examination of infections according to site revealed significantly higher rates of gastrointestinal infection in the alcohol—soap group. Black and colleagues have previously demonstrated a decreased rate of diarrhea in day-care centers at which strict hand-washing was enforced.18 These findings are consistent with those of previous studies documenting the enhanced potency of chlorhexidine as compared with soap for removing Staphylococcus aureus from the hands.22 , 25 , 46 In addition, chlorhexidine has been shown to have a greater residual activity than soap or alcohol,15 which may be important in preventing infections in the ICU. The trend in the chlorhexidine group toward lower rates of infection of skin and soft tissue, infection at the sites of insertion of intravenous catheters, urinary tract infection, and primary bacteremia may partly reflect the higher compliance with hand-washing instructions during the periods when chlorhexidine was available. The reasons for the difference are unclear; however, it is noteworthy that 38 percent of the wound infections in the alcohol—soap group (6 of 16) were due to staphylococcus species (3 each to S. aureus and coagulase-negative staphylococci), as compared with none of 6 in the chlorhexidine group.
As reported by others,40 41 42 compliance with hand-washing procedures was quite low, regardless of the hand-washing system used. In our study, significantly more chlorhexidine than alcohol and soap was used during the study. The delivery system for chlorhexidine had hand and foot pumps that frequently resulted in considerable waste of the agent into the sink as the pump was primed, whereas the alcohol—soap system deposited the agents directly on the hands. Recently, Larson46 reviewed several studies that demonstrated a dose–response effect with either chlorhexidine or alcohol, suggesting that the volume of antiseptic agent used may be an important determinant of the efficacy of hand-washing in reducing the number of organisms on the hands. Thus, the differences in the volumes of the two hand-washing agents used in the present study may partly explain the observed differences in infection rates. In addition, Rotter reported that the efficacy of hand decontamination when a rinsing agent containing alcohol was used in an experimental setting was decreased slightly when the hands were already wet.27 Although this may have been a factor in our clinical trial, it is likely that its effect was small, since the distribution of the organisms recovered from the hands was similar in the two study groups.
Although it is difficult to estimate the relative importance of improvement in compliance as compared with the use of an antibacterial hand-cleansing agent in reducing nosocomial infections in our study, we would assume that both are of equal importance. The results of our study and those reported in abstract form by Maki and Hecht44 and Massanari and Hierholzer45 suggest that a reduction in rates of 25 to 50 percent is achievable if an antiseptic hand-cleansing agent is used rather than a nonmedicated soap. Although it is difficult to change hand-washing behavior, we think that infection rates might be similarly reduced through the use of an effective approach to increase compliance by 50 to 100 percent.
Future strategies to increase the effectiveness of hand-washing must address issues of compliance and of the amount of antiseptic used, as well as those of the antimicrobial potency of the various hand-washing approaches. Useful approaches to test alternative hand-washing agents for efficacy may be applied in the design of crossover studies in critical care units.
Supported in part by a grant from Calgon—Vestal, St. Louis.
Source Information
From the Department of Internal Medicine, Division of General Medicine, Clinical Epidemiology and Health Services Research (B.N.D., G.L.S., C.T.S., A.K.H., L.A., R.P.W.), the Department of Pathology (M.A.P.), and the Department of Preventive Medicine and Environmental Health (N.L.), the University of Iowa College of Medicine; the Program of Epidemiology, the University of Iowa Hospitals and Clinics (R.P.W.); and the Veterans Affairs Medical Center (M.A.P.) — all in Iowa City. Address reprint requests to Dr. Wenzel at the Department of Internal Medicine. C41, GH, The University of Iowa College of Medicine, Iowa City, IA 52242.
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