Hand hygiene is the single most important measure to prevent healthcare-associated infections. Since the late 1960s and their first commercial availability, alcohol-based hand rubs (ABHRs) have been increasingly used for hand hygiene.Reference Kampf 1 Many in vitro and in vivo studies have shown their preventive potential, and both the US Centers for Disease Control and Prevention (CDC)Reference Boyce and Pittet 2 and the World Health Organization (WHO) Guidelines for Hand Hygiene in HealthcareReference Pittet, Allegranzi and Boyce 3 favor ABHR over hand washing with antimicrobial soaps.Reference Rotter, Kampf, Suchomel and Kundi 4 – Reference Pittet and Boyce 8 Alcohol-based hand rubs have additional benefits over antimicrobial soaps, such as no necessity for using sinks with water supply for washing and rinsing,Reference Boyce 9 better dermal tolerance, and higher acceptability by healthcare professionals,Reference Pittet, Allegranzi, Sax, Chraiti, Griffiths and Richet 10 – Reference Souweine, Lautrette and Aumeran 12 as well as a significantly shorter time to carry out the procedure.Reference Voss and Widmer 13 , Reference Rotter 14 Although there is consensus on the importance of hand hygiene and general agreement on the use of ABHR, the major challenge today remains healthcare worker compliance with this practice, which is generally reported to be low.Reference Pittet, Allegranzi and Boyce 3 , Reference Pittet 15 One frequently given reason for noncompliance is lack of time for this action.Reference Boyce 16 – Reference Allegranzi and Pittet 24 Although recommendations for the application time of ABHRs have decreased over the past years from several minutes to a minimum of 30 seconds,Reference Kramer, Rudolph, Kampf and Pittet 25 even this short time still seems to be too long in clinical practice. The actual time spent on a hand antisepsis action was reported to range between 5 and 24 seconds,Reference Boyce and Pittet 2 , Reference Pittet, Allegranzi and Boyce 3 and the WHO Guideline on Hand Hygiene in Health Care recommends a duration of 20–30 seconds. 26 However, concerns have been raised that application times that are too short may decrease ABHR antimicrobial efficacy, and it remains unproven that further shortening the application time will encourage healthcare workers to perform hand antisepsis actions more frequently.Reference Pittet 27
We investigated whether shortening the required application time from 30 seconds to 15 seconds may alter the antimicrobial efficacy of ABHRs and simultaneously influence healthcare worker compliance with the recommended frequency of hand antisepsis actions under real working conditions in a neonatal intensive care unit (NICU).
MATERIALS AND METHODS
In total, 10 commercially available ABHRs were included in the in vitro and in vivo tests. The evaluated ABHRs were based on the following compositions: (1) 70% (weight/weight [w/w]) ethanol, (2) 76.7% (w/w) ethanol, (3) 79.9% (w/w) ethanol, (4) 15% (w/w) ethanol+55% (w/w) propan-1-ol, (5) 45% (w/w) ethanol+18% (w/w) propan-1-ol, (6) 53.9% (w/w) ethanol+21.6% (w/w) propan-1-ol, (7) 54% (w/w) ethanol+10% (w/w) propan-1-ol, (8) 73.4% (w/w) ethanol+10% (w/w) propan-2-ol, (9) 14.3% (w/w) propan-1-ol+63.1% (w/w) propan-2-ol, 70% (w/w) propan-2-ol, and (10) 30% (w/w) propan-1-ol+45% (w/w) propan-2-ol+0.2% mecetroniumetile sulfate. Additionally, the 2 ABHRs based on the WHO formulation were tested: (1) 80% (w/w) ethanol+1.45% glycerol+0.125% H2O2 and (2) 75% (w/w) propan-2-ol+1.45 glycerol+0.125% H2O2.
The study was approved by the Ethic Committee of the University Hospital of Greifswald (Reg. No. BB 109/10).
In Vitro Antimicrobial Efficacy of Hand Rubs
The bactericidal and yeasticidal efficacy of a representative sample of ethanol- and propanol- based commercially available hand rubs was tested in quantitative suspension essays following the European norms (EN) 13727 28 and EN 13624. 29 All tested products were liquid ABHRs; gel formulations were not included because their drying times were longer than those of liquid rubs, thus potentially confounding comparisons.Reference Kramer, Rudolph, Kampf and Pittet 25
Efficacy of Artificially Contaminated Hands of Volunteers
The antimicrobial efficacy of ABHRs was evaluated following the EN 1500. 30 Alcohol-based hand rubs were tested against the reference alcohol propan-2-ol 60% (volume/volume [v/v]) in a blinded, controlled, crossover design with 15 volunteers for the in vivo test. Briefly, fingertips, including thumbs, were sampled in soy broth with the addition of Tween 80 3% (weight/weight [w/w]), saponine 3% (w/w), histidine 1% (w/w), and cysteine 1% (w/w) to eliminate the residual effect of a potential bacteriostatic detergent or compound. The fingertips of each hand were tested separately in a petri dish filled with sample fluid. The initial number of colonies (ie, pretreatment value) was determined, followed by a standardized hand-rubbing motion 30 at the respective observation time (15 seconds or 30 seconds). The result (ie, posttreatment value) was then recorded.
Sampling Culture and Calculation of Efficacy in Reducing Microorganisms
A volume of 0.1 mL sample fluid from hands was plated within 30 minutes after sampling in serial dilutions on Columbia blood agar plates. Culture plates were incubated for 48 hours at 36°C±1°C under aerobic conditions, and the number of colony-forming units (CFUs) was determined thereafter. The log reduction factor (log RF) was calculated by subtracting the log posttreatment values from the log pretreatment values. Log RFs were calculated separately for each participant, and the arithmetic mean of all samples was calculated.
Efficacy Under Practical Working Conditions
In a second step, a clinical observation trial was performed including 14 registered nurses working at the NICU of the University Hospital of Greifswald, Greifswald, Germany. Inclusion criteria were healthy skin condition, and short and clean fingernails without artificial or gelled fingernails and without nail polish. Exclusion criteria were open wounds and skin irritations on hands and lower forearms. All 14 participants underwent training on correct hand-rubbing technique using a pictogram according to EN 1500 30 and practical training using fluorescent dye together with the use of an ultraviolet light to control correct application. In addition, on-site training was repeated individually with each participant before the trial. Pictograms demonstrating the correct hand-rubbing technique were placed next to each hand rub dispenser.
For the clinical observation trial, an ABHR containing the active ingredients 45% (w/w) propan-2-ol+30% (w/w) propan-1-ol+0.2% mecetroniumetile sulfate was used. This product showed noninferiority when tested at 15 seconds compared to the reference alcohol 60% (v/v) propan-2-ol tested at 30 seconds. Furthermore, it was available as routine ABHR at the NICU under observation. Before the beginning of each shift and before the first hand rubbing, the initial bacterial colony count on fingertips of both hands of participating nurses was determined. This procedure was repeated hourly during the entire shift.
Frequency of ABHR Use
Participant compliance with hand antisepsis recommendations in terms of frequency was monitored during a complete working shift of 8 hours, starting at the beginning of a shift. Registered nurses were randomly allocated to a 15-second (group A) or 30-second (group B) hand antisepsis cohort. During the shift, a trained, independent observer monitored the frequency of hand antisepsis actions and recorded whether the assigned application time (15 seconds or 30 seconds) was followed. Parts of the WHO hand hygiene observation methodReference Sax, Allegranzi, Chraïti, Boyce, Larson and Pittet 31 , Reference Pittet, Mourouga and Perneger 32 were used to measure compliance in terms of frequency of hand antisepsis moments. The overall consumption of ABHR and the count of hand antisepsis actions in each group were used to determine the average use of ABHR for each hand antisepsis action.
Statistical Analysis
Bacterial counts were logarithmically transformed and expressed as means±standard deviation (SD) before statistical analysis. Viable CFU log10 differences were calculated as log10 CFU of the tested ABHR product minus log10 CFU of a reference alcohol for each corresponding pair. Continuous variables such as frequency of hand antisepsis action were calculated as the mean of all separate counts±SD. For the in vivo experiments on artificially contaminated hands, means±SD of test and the reference group were compared using a matched Wilcoxon’s matched-pairs signed-ranks test. To assess differences of the antimicrobial efficacy or the frequency of use under practical working conditions between group A (15 seconds) and group B (30 seconds), an unpaired 2-tailed t test was applied. All tests for significance were run as 2-sided tests, with α set at the 5% level.
RESULTS
In Vitro Antimicrobial Efficacy of ABHRs and Efficacy on Artificially Contaminated Hands
The in vitro suspension test demonstrated log RF of >5 for Staphylococcus aureus, Enterococcus hirae, Escherichia coli, Pseudomonas aeruginosa, and Proteus mirabilis and >4 for Candida albicans within 15 seconds of application time for all tested commercially available ABHRs (Table 1). All tested ABHRs fulfilled within 15 seconds the requirement of the EN 1500 as being equal or even more effective than the reference alcohol 60% (v/v) propan-2-ol within 30 seconds (Table 2).
TABLE 1 Antimicrobial Efficacy of Commercially Available Alcohol-Based Hand Rubs at 15-Second Application Time
TABLE 2 Log Reduction Factors of Commercially Available and WHO-Recommended ABHRs Within 15 Seconds Compared to the EN 1500 Reference Alcohol at 30 Seconds After Artificial Contamination With Eschericha coli K12
NOTE. WHO, World Health Organization; ABHR, alcohol-based hand rub; SD, standard deviation.
a EN 1500 reference alcohol: propan-2-ol 60% (v/v).
b WHO-recommended ABHR formulations.
c P < .05 (Wilcoxon test).
Efficacy Under Practical Working Conditions
No significant differences between CFUs retrieved from hands before hand rubbing was observed in the groups rubbing hands for 15 seconds and 30 seconds (P=.73, Wilcoxon test, asymptotic significance; Table 3) or in terms of antimicrobial log RF of ABHRs applied for 15 seconds or 30 seconds (P=.59, Wilcoxon test). These results indicate that the application of ABHRs for 15 seconds has antimicrobial efficacy similar to that at 30 seconds. On average, 3.4 mL ABHR was used for each hand antisepsis action, with no difference in ABHR consumption between the 2 different application times (3.4 mL, group A vs 3.3 mL, group B; P>.05). Furthermore, there was no difference between the 2 groups in terms of retrievable CFU counts from hands before, during, and at the end of shifts. During the entire shifts, the mean retrievable CFU counts ranged from 0.2 to 4.4 log (15-second group: 2.13±1.1 log CFU; 30-second group: 2.26±1.3 log CFU; P=.87, Wilcoxon test). These results indicate that reducing the ABHR application time to 15 seconds had no influence on a possible accumulation of bacteria on hands.
TABLE 3 Comparison of the Efficacy of an ABHRFootnote a at 15-Second and 30-Second Application Times Before and After Hand Rubbing During Clinical Practice in a NICU
NOTE. ABHR, alcohol-based hand rub; NICU, neonatal intensive care unit; SD, standard deviation.
a Content (% v/v) of tested formulation: propan-1-ol (30.0), propan-2-ol (45.0), mecetroniumetile sulfate (0.2).
When hands were rubbed with an application time of 15 seconds, the frequency of hand antisepsis action was significantly higher (7.9±4.3 times per hour) than with the application time of 30 seconds (5.8±2.9 times per hour; P < .05). These results indicate that shortening the application time for hand antisepsis significantly increased the frequency of hand antisepsis actions.
DISCUSSION
The results of this investigation are based on clinical practice and provide evidence for the feasibility and safety of shortening the time required for hand antisepsis from 30 seconds to 15 seconds during real patient care. The prerequisite for such an approach is the proof of the efficacy of ABHRs fulfilling the requirements of the EN 1500 within an application time of 15 seconds. Our results also show increased frequency of hand antisepsis action in the group of healthcare workers at a 15-second application time compared to a 30-second hand antisepsis application time. This finding may suggest that the recommendation of the application time of ABHR alone seems to influence clinicians’ willingness to use ABHRs more frequently. Notably, there was no difference in duration for hand antisepsis action between both groups in our observation. Although time recommendation did not practically shorten the hand antisepsis action, it encouraged the healthcare workers to follow hand antisepsis recommendations more frequently.
The precondition for investigating a shortened application time of 15 seconds for ABHRs in comparison to the currently recommended 30 seconds in a clinical setting was the assessment of their antimicrobial efficacy in vitro and under practical experimental conditions on artificially contaminated hands. Our in vitro experiments confirmed that the shorter application time was not associated with a statistically significant reduction in antimicrobial efficacy of ABHRs, as recently demonstrated by Pires et alReference Pires, Soule, Bellissimo-Rodrigues, Gayet-Ageron and Pittet 33 in a laboratory based study in conditions closely mimicking clinical practice. In our study, all tested ABHRs fulfill this precondition according to one of the most stringentReference Pittet, Allegranzi and Boyce 3 standard testing norms (ie, EN 1500). 30
For the study under practical clinical conditions, the shortened application time was the only different factor applied during the study period. All participants were registered nurses and performed all procedures without any dropout. To achieve standardization under clinical conditions, all participants were carefully supervised by a trained infection-control nurse. Indeed, direct observation of staff during their clinical work is the preferred method to assess compliance with hand antisepsis recommendations.Reference Pittet, Allegranzi and Boyce 3 , Reference Sax, Allegranzi, Chraïti, Boyce, Larson and Pittet 31 , Reference Pittet, Mourouga and Perneger 32 , Reference Pittet, Hugonnet and Harbarth 34 Because there were no differences in antimicrobial efficacy of the ABHRs among both groups and because the reduction of the recommended application time was associated with a significantly increased frequency of hand antisepsis actions, a reduction of the time for hand rubbing can be recommended to encourage healthcare workers to perform hand antisepsis, provided that the ABHR in use has proven efficacy after 15 seconds. This efficacy does not extend to all available ABHRs, and particularly not gel formulations of ABHRs. Many available commercial products may not fulfill the requirements of the EN 1500 within 15 seconds.Reference Kramer, Rudolph, Kampf and Pittet 25 , Reference Dharan, Hugonnet, Sax and Pittet 35
Although they are encouraging, our results must be regarded with some caution. This study lacked monitoring compliance with hand hygiene practices in full accordance with the definition proposed by the WHO in 2009.Reference Pittet, Allegranzi and Boyce 3 , 26 , Reference Pittet, Mourouga and Perneger 32 Although the strength of our study is that the observer was physically present in the NICU and directly observed hand antisepsis actions, the quality of performance was not assessed. However, all 14 participants were trained to perform the correct hand-rubbing technique using appropriate approach and repeated practical training before the trial to control correct ABHR application. Nevertheless, we report only the frequency of hand antisepsis actions, which technically does not equal compliance as defined by the WHO.Reference Pittet and Donaldson 36 This gap should be closed in future studies.
In conclusion, shortening the application time of ABHRs from 30 seconds to 15 seconds showed no statistically significant difference in the antimicrobial efficacy of applied ABHR products on the hands of healthcare workers, but it significantly increased the frequency of hand antisepsis actions under clinical conditions. Because time pressure and workload are recognized barriers to compliance,Reference De Wandel, Maes, Labeau, Vereecken and Blot 17 , Reference Dunn-Navarra, Cohen, Stone, Pogorzelska, Jordan and Larson 20 – Reference Allegranzi and Pittet 24 reducing the currently recommended 20–30 seconds duration of ABHR application, 26 using tested and well evaluated hand rub formulations, may constitute a further step toward improving compliance with hand hygiene recommendations in clinical practice.Reference Pittet and Donaldson 36
ACKNOWLEDGMENTS
Financial support: This study was conducted with funds from the routine departmental research budgets of the Institute of Hygiene and Environmental Medicine, University Hospital of Greifswald, Greifswald, Germany. No external funds from sources outside the institution were received.
Potential conflicts of interest: Prof. Ojan Assadian was member of the medical advisory boards of Hutchinson santé, Beckon Dickenson, and Mölnlycke Health Care until end of 2016, and he declares having received consulting and lecture fees, travel compensation, and speaker’s honoraria from Altrazeal Europe, Ltd., Antiseptica Chemical GmbH, Bode GmbH Germany, B. Braun Melsungen AG, Ethicon, Ltd., Kinetic Concepts, Inc., Lohmann & Rauscher, Smith & Nephew, Ltd., Quantum Management & Service GmbH, and Schulke & Mayr GmbH in the past. All other authors report no potential conflicts of interest relevant to this article.
