Infection Control Program, Department of Internal Medicine, University of Geneva Hospitals, Geneva, Switzerland

REVIEW Hand hygieneðbeliefs or science? S. Hugonnet and D. Pittet Infection Control Program, Department of Internal Medicine, University of Geneva Hospitals, Geneva, Switzerland SUMMARY Over a century has passed since Ignaz P. Semmelweis demonstrated the association between hand hygiene and nosocomial infections, but this simple procedure is still not recognized by many healthcare workers as one of the most important measures to prevent cross-transmission of microorganisms. A relatively large amount of research has been done, in particular to try to understand why compliance remains so low, in order to implement successful promotion campaigns.this research has generated a fair amount of strong scienti c data which are sometimes misunderstood and misused because of myths or certain beliefs. Observational or intervention studies have consistently shown a number of risk factors associated with noncompliance, such as high workload, professional category, or type of ward. Others are thought to be barriers to adequate compliance but have not yet been properly assessed.these include skin irritation due to hand hygiene agents, lack of knowledge of hand hygiene recommendations, or lack of institutional policy. Future interventions to promote hand hygiene will need to address these risk factors, and target the individual healthcare worker, as well as the group or institution if a signi cant degree of success is to be achieved. Keywords Hand hygiene, hand disinfection, handwashing, nosocomial infection, compliance Clin Microbiol Infect 2000: 6: 348^354 In 1847, Ignaz P. Semmelweis, a Hungarian-born obstetrician, performed the rst experimental study which clearly demonstrated that appropriate hand hygiene does prevent puerperal infections and maternal deaths [1]. Since then, hand hygiene has been considered by most healthcare professionals to be the simplest and most cost-e ective measure to prevent crosstransmission of microorganisms and nosocomial infections [2,3]. Despite this, healthcare workers (HCWs) show a certain reluctance to translate Semmelweis' message into their daily clinical practice. Indeed, hand hygiene and adherence to recommended practices have been extensively studied, and the vast majority of the observational studies report compliance rates that are unacceptably low, usually below 50% [4^15] (Table 1). As a logical consequence, the issue of hand hygiene became apriorityamong infectioncontrolpractitioners, and a great deal of research has been done to better understand the process of hand contamination, cross-transmission, the factors explaining non-compliance, and the interventions needed to Corresponding author and reprint requests: D. Pittet, Infection Control Program, Department of Internal Medicine, University of Geneva Hospitals, 1211 Geneva 14, Switzerland Tel. 41 22 372 98 28 Fax: 41 22 372 39 87 E-mail: pittet.didier@hcuge.ch improve adherence to hand hygiene recommendations. Tremendous progress has been made, new research questions have arisen, but some gaps in our knowledge remain and controversy is ongoing. Interestingly, the debate surrounding hand hygiene has a tendency to become intermingled with myths, personal beliefs and facts.the aim of this review is to attempt to clarify the state of our present knowledge and to separate what is science from simple beliefs or opinions. IMPORTANCE OF HAND HYGIENE IN THE PREVENTION OF NOSOCOMIAL INFECTIONS This is the central concept underlying the whole discussion around hand hygiene and the e orts employed to increase awareness of its importance. However, it is still argued that there is nocompellingevidence to support the need for rigorous hand hygiene procedures to prevent nosocomial infections [16]. From our point of view, this issue is no longer a subject of debate. As recently reviewed by Larson [17], seven quasiexperimental hospital-based studies of the e ect of hand hygiene on the risk of nosocomial infection were published between 1977 and 1995 [12,18^23]. In one of these, endemic MRSAwas eliminated in 7 months in a neonatal intensive care unit following the introduction of a new hand disinfectant = 2000 Copyright by the European Society of Clinical Microbiology and Infectious Diseases

Hugonnet and Pittet Hand hygieneðbeliefs or science? âãñ Table 1 Compliance with hand hygiene in different hospital settings Year Setting Compliance Author 1981 Open ward ICU 1981 ICUs ICUs 16% 30% 41% 28% Preston et al [4] Albert and Condie [5] 1983 All wards 45% Larson [6] 1987 PICU 30% Donowitz [7] 1990 ICU 32% Graham [8] 1990 ICU 81% Dubbert et al [9] 1991 SICU 51% Pettinger and Nettleman [10] 1992 NICU/others 29% Larson et al [11] 1992 ICUs 40% Doebbeling et al [12] 1992 ICUs 40% Zimakoff et al [13] 1994 Emergency room 32% Meengs et al [14] 1999 All wards ICUs 48% 36% Pittet et al [15] ICUs, intensive care units; PICU, pediatric ICU; NICU, neonatal ICU. capacity of the unit, resulting in an available space per child well below standard recommendations [36]. In parallel, the number of sta on duty was signi cantly below the number required by the workload, and this conjunction resulted in relaxed basic infection control measures. Compliance with hand hygiene before device contact was only 25% during the workload peak but increased to 70% after the end of the understa ng and overcrowding period. Continuous surveillance showed that being hospitalized during this period carried a 4 -fold increased risk of acquiring a nosocomial infection. This study not only shows the association between workload and infection but also highlights the intermediate step: low compliance with hand hygiene procedures. Do these data provide su cient evidence to state that there is a causal link between hand hygiene and nosocomial infections? It would seem to be the case, as several of the Bradford^ Hill criteria for causality are met: consistency of the association, temporal sequence of the association, and plausibility and coherence of the association. HANDWASHING OR HAND DISINFECTION? [19]. Another study reported an MRSA outbreak involving 22 infants in a neonatal unit, which could not be controlled despite intensive and comprehensive measures until another disinfectant was widely introduced [20]. Other studies to examine the e ects of hand hygiene promotion on the risk of infection were conducted in schools or daycare centers [24^ 27], as well as in the community [28^30]. Despite the limitations of these studies in terms of study design, lack of control for confounding factors or power, most reports showed a temporal relation between improved hand hygiene practices and reduced infection rates. In addition to these above-mentioned studies, outbreak investigations have suggested an association between infections and understa ng or overcrowding that was consistently linked with poor compliance to hand hygiene [31^33]. During an outbreak, Fridkin et al investigated risk factors for central venous catheter-associated bloodstream infections [33]. After adjustment for confounding factors, the patient-to-nurse ratio remained an independent risk factor for bloodstream infection, suggesting that nursing sta reduction below a critical threshold may have contributed to this outbreak by jeopardizing adequate catheter care. More recently, Vicca studied and demonstrated the relationship between understa ng and the spread of MRSA in an intensive care unit [34]. These ndings tend to show indirectly that an imbalance between workload and sta ng leads to relaxed basic control measures, such as hand hygiene, and the spread of microorganisms. We recently investigated an outbreak of Enterobacter cloacae in our neonatal intensive care unit [35] which showed that the daily number of hospitalized children exceeded the maximal The skin harbors mainly two types of microorganisms, the resident and the transient or contaminant ora [37]. The resident ora (coagulase-negative staphylococci, Corynebacterium species, Micrococcus species) has a low pathogenic potential unless introduced into the body by invasive devices, and is dif- cult to remove by mechanical means. On the other hand, the transient ora (typically Escherichia coli, Pseudomonas aeruginosa) has a short-term survival rate on the skin, but with a high pathogenic potential, and is responsible for most nosocomially acquired infections resulting from cross-transmission. The aim of hand hygiene is to decrease hand colonization with transient ora. The ideal technique should be quick to perform, reduce hand contamination to the lowest possible level, and be free from signi cant side-e ects on the skin. Hand hygiene can be achieved either through handwashing, or hand disinfection. Handwashing refers to the action of washing hands with an unmedicated detergent and water, or water alone to remove dirt and loose transient ora to prevent cross transmission [2,37]. Hygienic handwash refers to the same procedure when an antiseptic agent is added to the detergent. Hand disinfection refers to any action where an antiseptic solution is used to clean hands, either medicated soap or alcohol. Some experts may refer to the action of degerming with detergent-based antiseptics or alcohol [17]. Hygienic handrub consists of rubbing hands with a small quantity (2^3 ml) of a highly e ective and fast-acting antiseptic agent. Because alcohols have excellent activity and the most rapid bactericidal action of all antiseptics, they are the preferred agents for hygienic handrub. The other main antiseptics include iodophors, chlorhexidine gluconate, triclosan, phenol

âäò Clinical Microbiology and Infection, Volume 6 Number 7, July 2000 derivatives and quaternary ammonium compounds, and have been recently reviewed by Rotter [37]. Plain soap with water can physically decrease the load of microorganisms to a certain level, but antiseptic agents are necessary to obtain a signi cantly stronger reduction or elimination [2,38^40]. To be e ective, time spent washing hands is crucial, since the mean log 10 reduction of hand contamination reaches 0.6^1.1 after 15 s, 1.8^2.8 after 30 s, up to 3 after 1min, and up to 3.3 after 2 min. In contrast, a solution containing at least 50% of n-propanol achieves a 3.7 log 10 reduction in bacterial count after 30 s of exposure. Rotter showed that hand hygiene with unmedicated soap and water removed, at best, some of the transient ora mechanically, whereas preparations containing antiseptic or antimicrobial agents not only removed transient ora mechanically, but also chemically killed contaminating and colonizing ora with long-term residual activity. It is important to recall that hand disinfection is signi cantly more e cient than standard handwashing with soap and water or water alone [37,41], particularly when contamination is heavy [42^44]. However, as standard handwashing was the preferred technique for a long time, there appears to be a certain reluctance to adopt alternative methods of achieving hand hygiene. Alcohol-based handrubs are well suited for hygienic hand disinfection for the following reasons: (1) optimal antimicrobial spectrum (active against all bacteria, and most clinically important viruses, yeast and fungi); (2) no wash basin necessary for their use and easy availability at the bedside; (3) application does not cause microbial contamination of the HCW's uniform; (4) fast-acting. After extensive reduction following hand disinfection with an alcohol preparation, it takes the resident skin ora several hours to become completely restored [37]. Since alcohol alone does not have any lasting e ect, another compound with antiseptic activity, such as chlorhexidine gluconate, is sometimes added to the hand disinfection solution to obtain a prolonged e ect.we recently investigated the colonization of HCWs' hands during routine patient care under various clinical situations, and the e ect of hand hygiene on decolonization [45]. In the multivariate analysis, we found that HCWs who washed their hands with unmedicated soap had an excess of 52 colony-forming units (CFUs) on their ngertips when compared to those who had used a hand disinfectant solution. BARRIERS AND RISK FACTORS FOR NON- COMPLIANCE Although it appears to be an extremely simple action to perform, compliance with hand hygiene recommendations has been repeatedly documented as being low (Table 1). Identi cation of the associated risk factors is of utmost importance to the design of appropriate targeted promotion campaigns, and numerous studies have been undertaken to clarify this issue. The list of potential barriers to hand hygiene is extremely long and heterogeneous; some are related to personal beliefs or behavior, others to institutional policies and constraints; some have been assessed in observational or even intervention studies, while others are simply reported by HCWs. For clarity, we will use the term `risk factors' for independent factors of non-compliance, and`barriers' for opinions or beliefs. Risk factors Risk factors for non-compliance with hand hygiene have been determined objectively in several observational studies or interventions to improve compliance (Table 2) [9,46^52]. Among these, being a physician or a nursing assistant, rather than a nurse, was almost consistently associated with reduced compliance. Similarly, the use of automated sinks also predicted non-compliance [53]. We conducted a hospital-wide observational study to estimate compliance with hand hygiene and assess risk factors for non-compliance [15]. We observed 2834 opportunities for hand hygiene. Overall compliance was 48%. Factors that independently predicted non-compliance were: 1. Professional category: non-compliance was lowest among nurses as compared with other HCWs, and especially physicians. 2. Hospital ward: non-compliance was higher in intensive care units, as compared with internal medicine (OR 2.0, CI 95 1.3^3.1). 3. Time of the day/week: non-compliance was lower during weekends (OR 0.6, CI 95 0.4^0.8). 4. Type of patient care: non-compliance was higher during procedures carrying a high risk of bacterial contamination (OR1.8, CI 95 1.4^2.4). Table 2 Observed risk factors for non-compliance with hand hygiene Risk factors Physician status (rather than a nurse) Nursing assistant status (rather than a nurse) Male gender Working in an intensive care unit Working during the week (rather than during the weekend) Wearing gowns/gloves Automated sink Activities with high risk of cross-transmission High number of opportunities for hand hygiene per hour of patient care

Hugonnet and Pittet Hand hygieneðbeliefs or science? âä" 5. Heavy workload: compliance decreased when the demand for hand cleansing was high; on average, compliance decreased by 5% (þ 2%) per 10 opportunities per hour when the intensity of patient care exceeded this gure. Similarly, the lowest compliance (36%) was found in intensive care units, where opportunities for hand hygiene are typically more frequent (on average, 20 opportunities per hour of care). The highest compliance rate (59%) was observed in pediatric units, where the average activity index was lower than elsewhere (on average, eight opportunities per patient-hour). This study con rmed low compliance with hand hygiene in a teaching institution, and suggested that targeted educational programs may be useful. The results also suggested that full compliance with current guidelines may be unrealistic [15,52,54]. Table 3 Self-reported factors for poor adherence to hand hygiene recommendations Barriers Hand hygiene agents cause irritations and dryness Sinks are inconveniently located/shortage of sinks Lack of soap, paper, towels Often too busy/insuf cient time Understaf ng/overcrowding Patient needs take priority Hand hygiene interferes with HCW±patient relationship Low risk of acquiring infection from patients Wearing of gloves/belief that glove use makes hand hygiene unnecessary Lack of knowledge of guidelines/protocols Not thinking about it/forgetfulness No role model from colleagues or superior(s) Scepticism Disagreement with the recommendations Lack of awareness of de nitive impact of improved hand hygiene on nosocomial infection rates Perceived barriers Apart from these well-documented risk factors, a large number of factors potentially jeopardizing adequate compliance with hand hygiene have been cited in the literature [9,15,46,48^51]. The main reasons reported by HCWs for the lack of adherence with hand hygiene recommendations include: skin irritation by hand hygiene agents, inaccessible hand hygiene supplies, interference with HCW^patient relation, patient needs perceived as a priority, wearing of gloves, forgetfulness, lack of knowledge of guidelines, insu cient time for hand hygiene, high workload and understa ng, and the perceived lack of scienti c evidence showing a de nitive impact of improved hand hygiene on nosocomial infection rates (Table 3). Finally, a trend towards lower compliance among males as compared to females was reported several times, but did not remain an independent risk factor. Skin irritation by hand hygiene agents probably constitutes an important barrier to appropriate compliance [55], and this issue has been recently reviewed by Larson [17].The super cial skin layers contain water to keep the skin soft and pliable, and lipids to prevent dehydration of the corneocytes. Hand cleansing can increase skin ph, reduce lipid content, increase transepidermal water loss, and even increase microbial shedding. However, the relative importance of skin irritation as a risk factor for non-compliance has not been assessed, even though it is regularly incriminated by HCWs as such. Consequently, several actions need to be taken to improve the acceptability of the agent and reduce its side-e ects. HCWs need to be better informed about the possible e ects of hand hygiene agents: a free service should be made available for those who present side-e ects; emollients should be added to the solution since, in addition, they may protect against cross-infection as well as keeping the resident skin ora intact; and the use of hand lotions should be encouraged to help protect skin and reduce microbial shedding. Possible interactions between hand protection and antimicrobial agents should, however, be evaluated in appropriately designed studies. Finally, it is important to recall that alcohol-based formulations for hand disinfection are less irritant on skin than any antiseptic or non-antiseptic detergents. Indeed, to our knowledge, Boyce et al [56] performed the rst clinical trial to compare side-e ects on skin when using an alcoholic hand gel regimen with soap and water. The study was prospective and randomized with a cross-over design, and the skin was assessed by three methods: self-assessment, visual assessment by a study nurse, and estimation of the epidermal water content by measurement of the electrical capacitance of the skin. The three measurement methods were consistent and showed no signi cant changes of the skin when using the alcohol-based gel, whereas dryness and irritation of the skin increased when using soap and water. Poor access to hand hygiene supplies, whether sink, soap, medicated detergent, or waterless alcohol-based handrub solution, is certainly an important barrier to adequate adherence. The most agrant example is the inconveniently located sink that obliges the HCW to leave the patient's bedside. This puts a time-burden on HCWs that renders adequate adherence with hand hygiene recommendations simply impossible [15,54]. System modi cations might solve this problem by providing, for example, individual bottles of alcohol-based handrub solution for pocket carriage, and dispensers available in the immediate vicinity of each patient care location. The observational study performed by Bischo et al [57] illustrates this point. Despite some methodological limitations, they

âäá Clinical Microbiology and Infection, Volume 6 Number 7, July 2000 showed that compliance with hand hygiene increased after alcohol-based waterless dispensers were made available, initially at a ratio of 1 dispenser per 4 beds. Interestingly, compliance was even higher when this ratio was 1: 1, stressing the importance of the ease of access. Wearing gloves might represent a barrier for compliance with hand hygiene. Indeed, HCWs might wear gloves with the primary intention of protecting themselves and not the patient, and may be unaware that contamination on gloves is just the same as on hands. Furthermore, it has been shown that contamination on the skin of gloved hands occurs, implying that hand hygiene is vital after glove removal [58]. Failure to remove gloves after patient contact or between care on dirty and clean body sites on the same patient has to be considered as non-compliance with hand hygiene recommendations [15]. Non-compliance has been identi ed among glove users in at least two studies [59,60]. Lack of knowledge of hand hygiene guidelines, recognition of hand hygiene opportunities during patient care and awareness of the risk of cross-transmission of microbial pathogens constitute barriers to hand hygiene compliance. Furthermore, some HCWs believed that they washed their hands when necessary even when observations indicated that they did not [9,18,61^63]. Guidelines delineating indications for hand hygiene exist, but do not rely on evidence-based studies of contamination of hands [39,64]. However, it is of utmost importance to identify patient care activities associated with colonization of the hands, in order to elaborate meaningful recommendations. In the study we mentioned earlier [45], we observed 417 episodes of care; each observation period started after the initial hand hygiene procedure and ended at the end of a coherent episode of care or when the HCW proceeded to clean his/her hands, and hand contamination was quantitated. Colonization of the hands was constant over time and almost linear, with an acquisition on average of 16 CFUs per minute of care on ungloved hands. The rate of colonization was dependent on the type of activity, as high as 21 CFUs/min for respiratory care, whereas no signi cant colonization occurred during simple skin contact or housekeeping activities. Activities that were most strongly associated with contamination were respiratory care and direct patient contact (both 20 CFUs/min). Not surprisingly, handling body uid or secretions, or rupture in the sequence of patient care, were also associated with high bacterial hand contamination, even after adjustment for confounding factors. Hand hygiene guidelines need to be revisited, taking into account such information, so as to help HCWs recognize at least those opportunities that carry the highest risk of cross-contamination during the sequence of patient care. The lack of scienti c information on the de nitive impact of improved hand hygiene on nosocomial infection rates is repeatedly reported as a barrier to appropriate adherence to hand hygiene recommendations. As discussed previously, and although there are scienti c data to refute this statement, it de nitely needs to be taken into account and calls for more education and lobbying. Some other reported reasons for non-compliance include the lack of hand hygiene promotion, active participation at individual and institutional level, the frequent absence of a role model provided by senior sta, the lack of institutional priority, and the lack of an institutional safety climate. This shows that parameters associated with non-compliance with hand hygiene recommendations are not uniquely related to the individual HCW, but also to the group and institution he/ she belongs to. We therefore agree with Kretzer and Larson [49] that interventions targeted at individuals are insu cient to induce sustained change, and that other factors such as environmental constraints and the institutional climate need to be taken into account. These authors have extensively reviewed and proposed a theoretical model to promote hand hygiene, but the successful implementation of these concepts has not been published so far. CONCLUSIONS The issue of hand hygiene as an important measure to prevent nosocomial infection is among the top priorities of any infection control practitioner, but the understanding of this topic is often distorted by many long-standing beliefs, misunderstandings, or unproven statements. However, a great deal of research has been accomplished that provides convincing data on the association between hand hygiene and nosocomial infections, hand colonization during patient care, advantages and disadvantages of various hand hygiene techniques or agents, and risk factors for non-compliance. These data need to be used to convince care-givers, design interventions, and trigger behavioral modi cations so to improve adherence to recommendations for hand hygiene. Obviously, some gaps in our knowledge remain and need to be addressed through appropriate research. One of these, and not the least, is to determine the most e ective components of a campaign to promote hand hygiene so as to achieve a full recognition among healthcare workers of the importance of this seemingly simple gesture. ACKNOWLEDGMENTS We thank R. Sudan for providing editorial assistance. REFERENCES 1. Semmelweis I. The etiology, concept and prophylaxis of childbed fever. In: Buck C, Llopis A, Najera E,Terris M, eds.the challenge of

Hugonnet and Pittet Hand hygieneðbeliefs or science? âäâ epidemiologyöissues and selected readings. Washington, DC: PAHO Scienti c Publication, 1988: 46^59. 2. Larson EL. CIC 1992^1993 and 1994 APIC Guidelines Committee. APIC guideline for handwashing and hand antisepsis in health care settings. AmJInfect Control 1995; 23: 251^69. 3. BauerTM, Ofner E, Just HM, Just H, Daschner F. An epidemiological study assessing the relative importance of airborne and direct contact transmission of microorganisms in a medical intensive care unit. J Hosp Infect 1990;15: 301^9. 4. Preston GA, Larson EL, Stamm W. The e ect of private isolation rooms on patient care practices, colonization and infection in an intensive care unit. AmJ Med 1981; 70: 641^5. 5. Albert RK, Condie F. Hand-washing patterns in medical intensive-care units. N EnglJ Med1981; 304: 1465^66. 6. Larson E. Compliance with isolation technique. AmJ Infect Control 1983; 11: 221^5. 7. Donowitz L. Handwashing technique in a pediatric intensive care unit. AmJ Dis Child 1987; 141: 683^5. 8. Graham M. Frequency and duration of handwashing in an intensive care unit. AmJInfect Control 1990; 18: 77^81. 9. Dubbert PM, Dolce J, Richter W, Miller M, Chapman S. Increasing ICU sta handwashing: e ects of education and group feedback. Infect Control Hosp Epidemiol 1990; 11: 191^3. 10. Pettinger A, Nettleman M. Epidemiology of isolation precautions. Infect Control Hosp Epidemiol 1991; 12: 303^7. 11. Larson EL, McGinley KJ, Foglia A et al. Handwashing practices and resistance and density of bacterial hand ora on two pediatric units in Lima, Peru. AmJInfect Control 1992; 20: 65^72. 12. Doebbeling BN, Stanley GL, Sheetz CT, Pfaller MA, Houston AK, Annis L. Comparative e cacy of alternative hand-washing agents in reducing nosocomial infections in intensive care units. N EnglJ Med 1992; 327: 88^93. 13. Zimako J, Kjelsberg AB, Larsen SO, Holstein B. A multicenter questionnaire investigation of attitudes toward hand hygiene, assessed by the sta in fteen hospitals in Denmark and Norway. AmJInfect Control 1992; 20: 58^64. 14. Meengs MR, Giles BK, Chisholm CD, Cordell WH, Nelson DR. Hand washing frequency in an emergency department. J Emerg Nurs1994; 20: 183^8. 15. Pittet D, Mourouga P, Perneger TV, the members of the Infection Control Program. Compliance with handwashing in a teaching hospital. Ann Intern Med 1999;130: 126^30. 16. Weeks A. Why I don't wash my hands between each patient contact. Br MedJ1999; 319: 518. 17. Larson E. Skin hygiene and infection prevention: more of the same or di erent approaches? Clin Infect Dis1999; 29: 1287^94. 18. Simmons B, Bryant J, Neiman K, Spencer L, Arheart K. The role of handwashing in prevention of endemic intensive care unit infections. Infect Control Hosp Epidemiol 1990; 11: 589^94. 19. Webster J, Faoagali JL, Cartwright D. Elimination of methicillinresistant Staphylococcus aureus from a neonatal intensive care unit after hand washing with triclosan. J Paediatr Child Health 1994; 30: 59^64. 20. Zafar AB, Butler RC, Reese DJ, Gaydos LA, Mennonna PA. Use of 0.3% triclosan (Bacti-Stat*) to eradicate an outbreak of methicillin-resistant Staphylococcus aureus in a neonatal nursery. Am J Infect Control 1995; 23: 200^208. 21. Casewell M, Phillips I. Hands as a route of transmission of Klebsiella species. Br Med J 1977; 2: 1315^17. 22. Maki DG.The use of antiseptics for handwashing by medical personnel. J Chemother 1989;1: 3^11. 23. Massanari RM, Hierholzer WJJ. A crossover comparison of antiseptic soaps on nosocomial infection rates in intensive care units. AmJInfect Control 1984; 12: 247^8. 24. Butz AM, Larson E, Fosarelli P, Yolken R. Occurrence of infectious symptoms in children in day care homes. Am J Infect Control 1990; 6: 347^53. 25. Early E, Battle K, Cantwell E, English J, Lavin JE, Larson E. E ect of several interventions on the frequency of handwashing among elementary public school children. Am J Infect Control 1998; 26: 263^9. 26. Kimel LS. Handwashing education can decrease illness absenteeism. JSch Nurs1996; 12: 14^16. 27. Master D, Hess Longe SH, Dickson H. Scheduled hand washing in an elementary school population. Fam Med 1997; 29: 336^9. 28. Khan MU. Interruption of shigellosis by handwashing and hospital environmental control.trans R SocTrop Med Hyg 1982; 76: 164^ 8. 29. Shahid NS, Greenough WB, Samadi AR, Huq MI, Rahman N. Hand washing with soap reduces diarrhoea and spread of bacterial pathogens in a Bangladesh village. J Diarrhoeal Dis Res 1996; 14: 85^89. 30. Stanton BF, Clemens JD. An educational intervention for altering water-sanitation behaviors to reduce childhood diarrhea in urban Bangladesh. AmJ Epidemiol 1987; 125: 292^301. 31. Haley RW, Bregman D. The role of understa ng and overcrowding in recurrent outbreaks of staphylococcal infection in a neonatal special-care unit. JInfect Dis 1982; 145: 875^85. 32. Haley RW, Cushion NB,Tenover FC et al. Eradication of endemic methicillin-resistant Staphylococcus aureus infections from a neonatal intensive care unit. JInfect Dis1995; 171: 614^24. 33. Fridkin SK, Pear SM, Williamson T, Galgiani JN, Jarvis WR. The role of understa ng in central venous catheter-associated bloodstream infections. Infect Control Hosp Epidemiol 1996; 17: 150^ 8. 34. Vicca AF. Nursing sta workload as a determinant of methicillin-resistant Staphylococcus aureus spread in an adult intensive therapy unit. J Hosp Infect 1999; 43: 109^13. 35 Harbarth S, Sudre P, Dharan S, Cadenas M, Pittet D. Outbreak of Enterobacter cloacae related to understa ng, overcrowding and poor hygiene practices. Infect Control Hosp Epidemiol 1999; 20: 598^603. 36. Moore DL. Newborn nursery and neonatal intensive care unit. APIC: Infect Control Appl Epidemiol 1996; 94: 1^14. 37. Rotter ML. Hand washing and hand disinfection. In: Mayall CG, ed. Hospital epidemiologyand infection control, 2nd edn. Philadelphia: Lippincott,Williams & Wilkins, 1999: 1339^55. 38. Lilly HA, Lowbury EJL. Transient skin ora. J Clin Pathol 1978; 31: 919^22. 39. Garner JS, Favero MS. CDC guideline for handwashing and hospital environmental control, 1985. Infect Control 1986; 7: 231. 40 Ehrenkranz J. Bland soap handwash or hand antisepsis? The pressing need for clarity. Infect Control Hosp Epidemiol 1992; 13: 299^ 301. 41. Rotter ML. 150 years of hand disinfectionösemmelweis' heritage. Hyg Med1997; 22: 332^9. 42. Graham DR, Anderson RL, Ariel FE et al. Epidemic nosocomial meningitis due to Citrobacter diversus in neonates. J Infect Dis 1981; 144: 203^9. 43. Eckert DG, Ehrenkranz NJ, Alfonso BC. Indications for alcohol or bland soap in removal of aerobic gram-negative skin bacteria: assessment by a novel method. Infect Control Hosp Epidemiol 1989; 10: 306^11.

âäã Clinical Microbiology and Infection, Volume 6 Number 7, July 2000 44. Ehrenkranz NJ, Alfonso BC. Failure of bland soap handwash to prevent hand transfer of patient bacteria to urethral catheters. Infect Control Hosp Epidemiol1991; 12: 654^62. 45. Pittet D, Dharan S,Touveneau S, SauvanV, Perneger TV. Bacterial contamination of the hands of hospital sta during routine patient care. Arch Intern Med 1999;159: 821^6. 46. Conly JM, Hill S, Ross J, Lertzman J, LouieT. Handwashing practices in an intensive care unit: the e ects of an educational program and its relationship to infection rates. AmJ Infect Control1989; 17: 330^9. 47. Jarvis WR. Handwashingöthe Semmelweis lesson forgotten? Lancet1994; 344: 1311^12. 48. Sproat LJ, InglisTJ. A multicentre survey of hand hygiene practice in intensive care units. J Hosp Infect1994; 26: 137^48. 49. Kretzer EK, Larson EL. Behavioral interventions to improve infection control practices. AmJInfect Control1998; 26: 245^53. 50. Larson E, Killien M. Factors in uencing handwashing behavior of patient care personnel. AmJInfect Control1982; 10: 93^9. 51. Larson E, Kretzer EK. Compliance with handwashing and barrier precautions. J Hosp Infect1995; 30: 88^106. 52. Boyce JM. It is time for action: improving hand hygiene in hospitals. Ann Intern Med1999;130: 153^5. 53. Larson E, McGeer A, Quraishi ZA et al. E ects of an automated sink on handwashing practices and attitudes in high-risk units. Infect Control Hosp Epidemiol1991; 12: 422^8. 54. Voss A, Widmer AF. No time for handwashing!? Handwashing versus alcoholic rub: can we a ord 100% compliance? Infect Control Hosp Epidemiol1997; 18: 205^8. 55. Larson E. Handwashing and skin: physiologic and bacteriologic aspects. Infect Control1985; 6: 14^23. 56. Boyce JM, Kelliher S, Vallande N. Skin irritation and dryness associated with two hand hygiene regimen: soap and water handwashing versus hand antisepsis with an alcoholic hand gel. Infect Control Hosp Epidemiol 2000; 21: in press. 57. Bischo 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: 1017^21. 58. Doebbeling BN, Pfaller MA, Houston AK,Wenzel RP. Removal of nosocomial pathogens from the contaminated glove. Ann Intern Med 1988; 109: 394^8. 59. Thompson BL, Dwyer DM, Ussery XT, Denman S, Vacek P, Schwartz B. Handwashing and glove use in a long-term care facility. Infect Control Hosp Epidemiol1997; 18: 97^103. 60. Khatib M, Jamaleddine G, Abdallah A, IbrahimY. Hand washing and use of gloves while managing patients receiving mechanical ventilation in the ICU. Chest1999;116: 172^5. 61. Broughall JM, Marshman C, Jackson B, Bird P. An automatic monitoring system for measuring handwashing frequency in hospital wards. J Hosp Infect1984; 5: 447^53. 62. McLane C, Chenelly S, Sylwestrak ML, Kirchho KT. A nursing practice problem: failure to observe aseptic technique. Am J Infect Control1983; 11: 178^82. 63. Larson E, McGinley KJ, Grove GL. Physiologic, microbiologic, and seasonal e ects of handwashing on the skin of health care personnel. AmJInfect Control1986; 14: 51^9. 64. Larson E. APIC guideline for use of topical antimicrobial agents. AmJInfect Control1988; 16: 253^66.