Hand contamination before and after different hand hygiene techniques: a randomized clinical trial
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1 Journal of Hospital Infection (2002) 50: 276±280 doi: /jhin , available online at on Hand contamination before and after different hand hygiene techniques: a randomized clinical trial J.-C. Lucet*, M.-P. Rigaud*, F. Mentrey, N. Kassisz, C. Deblangy* A. Andremontzx and E. Bouvetx *Infection Control Unit, ydepartment of Biostatistics and Epidemiology, zbacteriology Laboratory and x Infection Control Committee, Bichat-Claude Bernard Hospital, Paris, France Summary: The efficacy of alcohol-based handrubs (ABH) for hand hygiene (HH) compared with handwashing (HW) remains to be established in the clinical setting. Factors associated with severe hand contamination before HH techniques were medical ward, physician and not wearing gloves. Forty-three healthcare workers [HCW, 26 nurses (N), nine nurse assistants (NA) and eight physicians (P)] each performed six HH techniques in random order, immediately after a patient care activity: HW with non-antiseptic soap for 10 (US10) and 30 (US30) s; HW with antiseptic (polyvidone iodine- or chlorhexidine-based) soap for 10 (AS10), 30 (AS30) or 60 (AS60) s; and ABH (Sterillium, Bode Chemie, Germany). The fingertips of the dominant hand were pressed on to agar for culture before and after each HH technique. Five hundred and sixteen specimens were obtained. Log 10 -transformed bacterial count reductions after HH were 0.74, 0.51, 1.13, 1.14, 1.21 and 1.40 for US10, US30, AS10, AS30, AS60 and ABH, respectively; both AS and ABH were significantly better than US. Qualitative assessment showed that 11 of the 256 pre-hh specimens (4.3%) had pathogenic bacteria, and that two of these 11 remained positive after HH (US in both instances). & 2002 The Hospital Infection Society Introduction Handwashing is recognized as a basic measure for preventing nosocomial infections. 1 However, compliance with handwashing in hospital environments is generally less than 50%. 2 Furthermore, correct handwashing technique, particularly in respect of duration, is often not practiced. Reasons for insufficient compliance have recently been Received 17 August 2001; revised manuscript accepted 5 February 2002; published online 18 March Author for correspondence: Dr J. C. Lucet, Unite d'hygieá ne et de Lutte contre l'infection Nosocomiale, GH Bichat-Claude Bernard, F Paris Cedex 18, France. Fax: 33 (0) ; jean-christophe.lucet@bch.ap-hop-paris.fr studied. 3 Problems include insufficient facilities, lack of training and information, a lack of time and a high patient care load, as well as cutaneous intolerance of soaps. Alcohol-based hand disinfectant solutions are used increasingly as an alternative to handwashing 4,5 and may enable many obstacles in the way of handwashing to be overcome. The microbiological efficiency of alcohol-based hand disinfectants has been demonstrated in vitro 5 in reducing the bacterial count on artificially contaminated hands. In a clinical situation, several studies have shown that handrubbing with alcoholbased hand disinfectants is more efficient than with unmedicated soap. 6±8 Experimental conditions, however, especially the duration of handwashing, have not always been described in these studies. Furthermore, there are no 0195±6701/02/ $35.00/0 & 2002 The Hospital Infection Society
2 Hand hygiene and hand contamination 277 comparative data on the efficiency of handrubbing with an alcohol-based compound and handwashing with antiseptic agents in clinical environments. We conducted a randomized clinical trial to compare the bacterial efficiency of various hand hygiene techniques, including handrubbing with an alcohol-based compound, and handwashing with antiseptic agents and with unmedicated soap. Factors predisposing to hand contamination before hand hygiene were also assessed. Methods The study was conducted in seven wards of the Bichat-Claude Bernard hospital over a two-month period (May and June 2000): the two medical ICUs, the surgical ICU, the cardiac surgery ICU, the surgical recovery unit, and two medical units (infectious diseases unit and internal medicine unit). Five to seven volunteers from each unit, all healthcare workers (HCWs), were asked to participate. The volunteers were chosen so as to have at least one doctor, one nurse assistant and two nurses in each service. Each volunteer performed six hand hygiene techniques in random order immediately after a healthcare procedure: handwashing with unmedicated soap for 10 and 30 s, handwashing with antiseptic soap for 10, 30 or 60 s, or handrubbing with an alcohol-based disinfectant. The duration of handwashing was selected because it was the criterion recommended in France (30 s for handwashing with unmedicated soap, 60 s for antiseptic handwashing), or because it was the criterion usually observed in clinical environments (10 s). The unmedicated soap in use was available in 1 L disposable bags. The antiseptic soap used in the study was either Hibiscrub 1 (containing 4% chlorhexidine gluconate, Zeneca Astra, Rueil Malmaison, France) or Betadine 1 (containing 10% polividone iodine, Asta Medica, MeÂrignac, France). The alcoholbased solution was Sterillium 1 (Bode Chemie, Hamburg, Germany), containing 1-propanol, 30%; 2-propanol, 45%; mecetronium ethyl-sulphate, 0.2%, and emollients. The hand hygiene technique was standardized in terms of volume of product used, duration of application, method for drying hands with a towel and absence of hand recontamination after drying. The six hand hygiene techniques were typically performed over one week by each volunteer. In the event of two hand hygiene techniques being performed on the same day by a volunteer, at least 6 h separated each experiment. For each volunteer, a record was made of age, sex and job. The following information was recorded for each hand hygiene technique: hospital ward in which the procedure was performed, presence of hand irritation, type of healthcare procedure before hand hygiene, and whether gloves were worn during this procedure. Hand irritation was visually assessed using a simplified score with four categories: absence of hand irritation, moderate lesions, severe lesions without hand cracking, presence of hand cracking or skin breaks. The same infection control observer (MPR) observed the state of hands, and collected microbiological specimens. Microbiological techniques After a procedure, all five fingertips on the dominant hand of the volunteer were pressed on a trypticasesoy agar (BioMeÂrieux, Marcy l'etoile, France) for 15 s. In order to obtain identical conditions for each sample, the agar was applied on to the fingers by the observer with identical pressure. The hand hygiene technique was then performed, and a second imprint of the fingertips was obtained 1 min later. Plates were incubated at 37 C under aerobic conditions, and colony-forming units (CFUs) were counted after 48 h. The maximum count was 300 CFUs; beyond this figure, it was considered that there was a confluence, and a bacterial count of 350 CFUs was arbitrarily assigned to the specimen. Potential pathogenic bacteria from transient flora (i.e. Staphylococcus aureus, enterobacteriaceae, aerobic Gram-negative bacteria, enterococci and fungi) were identified using standard microbiological techniques. Residual antiseptic activity was not inactivated in the culture media. Statistical analysis Bacterial counts on hands were compared using the log 10 -transformed bacterial count. In order to take into consideration the log 10 -transformed bacterial count in specimens without bacterial growth, each bacterial count was increased by one bacterium. Firstly, predictors of hand contamination before the hand hygiene techniques were estimated using a linear mixed-effects model, in order to take into account dependency among repeated observations from a given volunteer (SAS PROC MIXED). A univariate analysis was performed to test the
3 278 J.-C. Lucet et al. influence of several variables. A multivariate analysis was then performed, including variables found to be associated with hand contamination at the level of P ˆ 0.1. A similar procedure was used to compare hand contamination in each group of hand hygiene techniques Secondly, a linear model was used to compare the differences in log 10 bacterial counts after hand hygiene techniques. The model was adjusted for the volunteer effect because of the crossover design of the study (SAS PROC GLM). A global test was performed, and comparisons between groups were done using Tukey's method to adjust for multiple comparisons. Several other covariates were also tested. Statistical analysis was conducted using SAS software (version 6.12), with a type I error (P value) set at Results A total of 43 healthcare workers took part in the study: 26 nurses, nine nurse assistants and eight physicians. There were 29 women and 14 men, with a mean age of Thirty-three HCWs were from ICUs and 10 from medical wards. All the HCWs performed each of the six hand hygiene procedures. Therefore, a total of 516 specimens was obtained, 258 before and 258 after hand hygiene. The mean SD number of CFUs (median) before hand hygiene techniques was (38). Hand contamination before hand hygiene Factors significantly associated with marked hand contamination before hand hygiene are presented in Table I. Hand contamination was highest in HCWs working in a medical ward and in physicians. Hand contamination was not significantly different after contact with patients, after contact with patients' environments, or after contact with body fluid secretions or waste. It was significantly higher in HCWs without direct patient contact (mainly undertaking housekeeping activities or rest breaks). Wearing gloves during the procedure (N ˆ 81) significantly reduced hand contamination. Hand contamination was no different in HCWs with hand irritation. In the multivariate analysis, factors associated with marked bacterial hand contamination before hand hygiene were (Table I): working in a medical ward (P ˆ ), physician (P ˆ 0.02), and not wearing gloves during the procedure (P ˆ 0.002). Hand contamination after hand hygiene Bacterial counts before hand hygiene procedures were not significantly different (Table II), with an Table I Factors associated with bacterial contamination of the hands of 43 healthcare workers before hand hygiene Variables Log 10 CFU (mean SD) P* P y Type of unit ± ICU (N ˆ 198) ± Not an ICU (N ˆ 60) Sex ± Male (N ˆ 84) NS ± Female N ˆ 174) Job title ± Nurse (N ˆ 156) ± Nurse assistant N ˆ 54) ± Physician (N ˆ 48) Type of care ± Contact with patient (N ˆ 85) NS ± Contact with patient's environment (N ˆ 135) ± Contact with bodily fluid secretions or waste (N ˆ 10) ± No care (N ˆ 28) Gloves worn during procedure ± Yes (N ˆ 81) ± No (N ˆ 177) Skin irritation ± None (N ˆ 161) NS ± Moderate (N ˆ 86) ± Severe (N ˆ 11) *Univariate analysis; y multivariate analysis.
4 Hand hygiene and hand contamination 279 Table II Bacterial contamination of the hands before and after various hand hygiene techniques in 43 healthcare workers Bacterial contamination Before hand hygiene (Log 10 CFU, mean SD) After hand hygiene (Log 10 CFU, mean SD) Handwashing with unmedicated soap, 10 s Handwashing with unmedicated soap, 30 s Handwashing with antiseptic soap, 10 s Handwashing with antiseptic soap, 30 s Handwashing with antiseptic soap, 60 s Alcohol-based handrub average (median) of between 60 (27) and 101 (64) CFUs among the six groups. There was a significant effect of the hand hygiene techniques on the reduction in bacterial counts (P < 10 4 ). For the pairwise comparisons, the following results were found (Table II). Bacterial reduction after handwashing with antiseptic soap (either 10, 30 or 60 s) or handrubbing with the alcohol-based disinfectant was significantly greater than that obtained after handwashing with unmedicated soap (either 10 or 30 s). There was no significant difference between handwashing with antiseptic soap (either 10, 30 or 60 s) and handrubbing with the alcohol-based disinfectant. No statistically significant difference was found between handwashing with unmedicated soap for 10 or 30 s, although there was a trend towards greater reduction after handwashing with unmedicated soap for 10 s, compared with handwashing with unmedicated soap for 30 s. A slight increase in bacterial reduction was observed after longer handwashing with antiseptic soap (10, 30 and 60 s), but the trend was not statistically significant. Each HCW used the same antiseptic soap in all instances for the three antiseptic handwashing procedures: Hibiscrub in 27 HCWs, and Betadine in 16 HCWs. Bacterial reduction was similar in the two groups (data not shown). Three-hundred and eighty-eight specimens were culture-positive; 241 (94%) before and 147 (57%) after hand hygiene. The predominant bacteria were skin commensals: Corynebacterium sp., coagulasenegative staphylococci, Micrococcus sp. or Bacillus sp. Bacteria from transient flora grew from 11 (4.6%) culture-positive specimens before hand hygiene: Staphylococcus aureus (N ˆ 3), Acinetobacter baumannii (N ˆ 2), Pseudomonas aeruginosa (N ˆ 2), fungi (N ˆ 2) and enterococci (N ˆ 2). The specimens obtained after hand hygiene were still culture-positive in two of these 11 cases, both after handwashing with unmedicated soap (10 s in one instance, 30 s in the other). Discussion This study had two aims: to assess the factors associated with hand contamination after care, and to measure the microbiological efficiency of different hand hygiene techniques. In our study, the average and median levels of hand contamination before hand hygiene were 81 and 39 CFUs, respectively. These figures are comparable with those of another study using the same hand culture method, where hand contamination was assessed after care to determine the predictive factors of hand contamination. 8 Several factors were found to be associated with marked hand contamination. Contamination was higher in the medical than the intensive care units. This result is surprising since it was suggested that compliance with handwashing was greater in the medical unit than in intensive care. 3 However, the greater number of interventions warranting handwashing in intensive care probably increases handwashing in these wards, and explains this. Hand contamination was similar for nurses and nurse assistants, and was greater for doctors after adjusting for other variables. These results have been found elsewhere 9, and may be explained by undertaking fewer procedures requiring handwashings and being less compliant with the requirement. Hand contamination was similar after contact with the patient, after contact with the patient environment and after contact with body fluids or treatment waste. It was significantly higher if there had been no direct patient contact, probably because in this case the hands had not been washed. As observed in other studies, wearing gloves reduced hand contamination. 8,10
5 280 J.-C. Lucet et al. The other aim of the study was to assess the efficiency of different forms of hand hygiene. A nonsignificant tendency was observed towards greater efficiency of handwashing with an unmedicated soap for 10 s than for 30 s. It has been shown that a prolonged duration of handwashing with nonantiseptic soap leads to greater reduction of bacterial counts. 5 Our unusual result may be explained by the mobilization of bacteria from the deeper layers of the epidermis after prolonged handwashing. 11 Handwashing with an antiseptic soap for 10, 30 or 60 s produced similar reductions in the bacterial count on hands. In an attempt to mimic clinical conditions of use in our study, antiseptics were not inactivated on agar for the culture of fingertips. It was hoped this would reproduce any carry-over effect due to the persistence of the antibacterial activity of antiseptic soap on hands. Several clinical studies have compared the efficiency of handwashing with an unmedicated soap with use of an alcohol-based solution. 6±8 Our results confirm the greater efficiency of the alcohol-based product over handwashing with an unmedicated soap. However, to our knowledge, no clinical study has assessed the efficiency of antiseptic handwashing and that of alcoholic hand disinfection. The latter was at least as efficient as antiseptic handwashing. It is possible that a study on a larger population, and using a more sensitive hand bacteria collection method (e.g. the `glove juice' method) would demonstrate a significant difference between the two groups. Our results suggest that alcohol-based handrubbing could replace handwashing with either unmedicated or antiseptic soap for hand hygiene. The qualitative assessment of bacteria on fingertips showed that only 4.6% of hands were contaminated with bacteria from transient flora before hand hygiene. After hand hygiene, bacteria from the transient flora were cultured in two instances, both after handwashing with unmedicated soap. This confirms that handwashing with unmedicated soap does not reliably remove pathogenic bacteria from hands. 8,12,13 In conclusion, this prospective randomized study in a clinical environment shows that alcohol-based hand rubbing and handwashing with antiseptic soap are more effective than handwashing with unmedicated soap, in reducing the bacterial count on hands. The need to reduce carriage of pathogenic bacteria to a minimum suggests that the use of alcohol-based hand disinfectants should be preferred to unmedicated soaps, and possibly to antiseptic soaps. Acknowledgements We thank the staff of the Bichat-Claude Bernard who volunteered to participate in the study. This study was supported by a grant from Rivadis (Thouars, France) and Bode Chemie (Hamburg, Germany). References 1. Larson E. Skin hygiene and infection prevention: more of the same or different approaches? Clin Infect Dis 1999; 29: 1287± Pittet D. Improving compliance with hand hygiene in hospitals. Infect Control Hosp Epidemiol 2000; 21: 381± Pittet D, Mourouga P, Perneger TV. Compliance with handwashing in a teaching hospital. Infection Control Program. Ann Intern Med 1999; 130: 126± Pittet D, Hugonnet S, Harbarth S et al. Effectiveness of a hospital-wide programme to improve compliance with hand hygiene. Lancet 2000; 356: 1307± Rotter ML. Hand washing and hand disinfection. In: Mayhall CG, ed. Hospital Epidemiology and Infection Control. Baltimore: Williams & Wilkins; 1996: 1052± Larson EL, Eke PI, Laughon BE. Efficacy of alcoholbased hand rinses under frequent-use conditions. Antimicrob Agents Chemother 1986; 30: 542± Zaragoza M, Salles M, Gomez J, Bayas JM, Trilla A. Handwashing with soap or alcoholic solutions? A randomized clinical trial of its effectiveness. Am J Infect Control 1999; 27: 258± Pittet D, Dharan S, Touveneau S, Sauvan V, Perneger TV. Bacterial contamination of the hands of hospital staff during routine patient care. Arch Intern Med 1999; 159: 821± Daschner FD. The transmission of infections in hospitals by staff carriers, methods of prevention and control. Infect Control 1985; 6: 97± 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± Meers PD, Yeo GA. Shedding of bacteria and skin squames after handwashing. J Hyg (Cambr.) 1978; 81: 99± Ayliffe GA, Bridges K, Lilly HA, Lowbury EJ, Varney J, Wilkins MD. Comparison of two methods for assessing the removal of total organisms and pathogens from the skin. J Hyg (Cambr.) 1975; 75: 259± Ehrenkranz NJ, Alfonso BC. Failure of bland soap handwash to prevent hand transfer of patient bacteria to urethral catheters. Infect Control Hosp Epidemiol 1991; 12: 654±662.
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