Improving Adherence To Hand Hygiene Practice: A Multidisciplinary Approach
Improving Adherence To Hand Hygiene Practice: A Multidisciplinary Approach
Hand hygiene prevents cross-infection in hospitals, but health-care workers adherence to guidelines is poor. Easy, timely access to both hand hygiene and skin protection is necessary for satisfactory hand hygiene behavior. Alcohol-based hand rubs may be better than traditional handwashing as they require less time, act faster, are less irritating, and contribute to sustained improvement in compliance associated with decreased infection rates. This article reviews barriers to appropriate hand hygiene and risk factors for noncompliance and proposes strategies for promoting hand hygiene.
Hand hygiene is the simplest, most effective measure for preventing nosocomial infections (1,2). Despite advances in infection control and hospital epidemiology, Semmelweis message is not consistently translated into clinical practice (3,4), and health-care workers adherence to recommended hand hygiene practices is unacceptably low (3,5-10). Average compliance with hand hygiene recommendations varies between hospital wards, among professional categories of health-care workers, and according to working conditions, as well as according to the definitions used in different studies. Compliance is usually estimated as <50% (Table 1). Promotion of hand hygiene is a major challenge for infection control experts (3,19-21). In-service education, distribution of information leaflets, workshops and lectures, and performance feedback on compliance rates have been associated with transient improvement (3,6,13,22,23). No single intervention has consistently improved compliance with hand hygiene practices (24). This review summarizes factors influencing lack of adherence by health-care personnel to hand hygiene procedures and suggests strategies for improvement.
Table 1. Compliance with hand hygiene in different hospital settings Average Year Setting compliance Author Ref. 1981 Open ward 16% Preston 11 ICU 30% 1981 ICUs 41% Albert 5 ICUs 28% 1983 All wards 45% Larson 12 1987 PICU 30% Donowitz 13 1990 ICU 32% Graham 6 1990 ICU 81% Dubbert 14 1991 SICU 51% Pettinger 15 1992 NICU/others 29% Larson 16 1992 ICUs 40% Doebbeling 7 1992 ICUs 40% Zimakoff 17 1994 Emergency room 32% Meengs 18 1999 All wards 48% Pittet 9 ICUs 36% ICUs = intensive care units; PICU = pediatric ICU; NICU = neonatal ICU.
Definitions
Two major groups of microorganisms are found on the skin: organisms that normally reside on it (resident flora) and contaminants (transient flora) (25). Unless introduced into body tissues by trauma or medical devices such as intravenous catheters, the pathogenic potential of the resident flora is low (26). Transient flora, which are easily removed by handwashing, cause most hospital infections resulting from cross-transmission (27-29). The term hand hygiene includes several actions intended to decrease colonization with transient flora. This objective can be achieved through handwashing or hand disinfection. Handwashing refers to washing hands with an unmedicated detergent and water or water alone. Its objective is to prevent cross-transmission by removing dirt and loose transient flora (10,30). Hygienic handwash refers to the same procedure
Address for correspondence: Didier Pittet, Infection Control Program, Department of Internal Medicine, University of Geneva Hospitals, 24, Rue Micheli-du-Crest, 1211 Geneva 14, Switzerland; fax: 41-22-3723987; e-mail: [email protected]
when an antiseptic agent is added to the detergent. Hand disinfection refers to use of an antiseptic solution to clean hands, either medicated soap or alcohol. Some experts refer to the action of degerming as the use of detergent-based antiseptics or alcohol (21). Hygienic hand rub is rubbing hands with a small quantity (2 mL to 3 mL) of a highly effective, fast-acting antiseptic agent.
234
Special Issue
Rotter showed that hand hygiene with unmedicated soap and water removed some transient flora mechanically; preparations containing antiseptic or antimicrobial agents not only removed flora mechanically but also chemically killed contaminating and colonizing flora, with long-term residual activity (30,34). Alcohol-based preparations have more rapid action than products containing other antiseptics (e.g., chlorhexidine gluconate or povidone iodine) (30,31,35). Semmelweis observed that normal handwashing did not always prevent the spread of fatal infection (1) and recommended hand disinfection in a solution of chlorinated water before each vaginal examination. Hand disinfection is substantially more efficient than standard handwashing with soap and water or water alone (2,30), particularly when contamination is heavy (14,36-40). Frequent handwashing may result in minimal reduction or even an increase in bacterial yield over baseline counts of clean hands (21,41). Because alcohols have excellent activity and the most rapid bactericidal action of all antiseptics, they are the preferred agents for hygienic hand rubs, so-called waterless hand disinfection. In addition, alcohols are more convenient than aqueous solutions for hygienic hand rubs because of their excellent spreading quality and rapid evaporation. At equal concentrations, n-propanol is the most effective alcohol and ethanol the least (30). Alcohol-based hand rubs are well suited for hygienic hand disinfection for the following reasons: optimal antimicrobial spectrum (active against all bacteria and most clinically important viruses, yeasts, and fungi); no wash basin necessary for use and easy availability at bedside; no microbial contamination of health-care workers clothing; and rapidity of action. After extensive reduction following hand disinfection with an alcohol preparation, it takes the resident skin flora several hours to become completely restored (30). Since alcohol alone has no lasting effect, another compound with antiseptic activity may be added to the disinfection solution to prolong the effect. These antiseptics have recently been extensively reviewed by Rotter (30). Prevention of bacterial contamination and subsequent infection requires timely hand cleansing. Guidelines have delineated indications for hand cleansing (10,32,42) but without reliance on evidence-based studies of microbiologic contamination acquired during routine patient care. To provide such evidence, we studied the dynamics of bacterial contamination of health-care workers hands in daily hospital practice (43). Our findings should help identify patient-care situations associated with high contamination levels and improve hand cleansing practices. Structured observations of patient care were conducted by trained external observers, who took an imprint of the fingertips of the health-care workers dominant hand to quantify bacterial colony counts at the end of a defined period of patient care (43). Bacterial contamination on ungloved hands increased linearly during patient care (mean 16 CFU per minute, 95% confidence interval [CI] 11-21). Activities independently associated with higher contamination levels were direct patient contact, respiratory care, handling body fluids, and disruption in the sequence of patient care (all p<0.05). Contamination levels varied according to hospital location, with the medical rehabilitation ward having the highest levels (>49 CFU, p = 0.03). Both the duration and type of patient care influenced hand contamination. Furthermore, simple handwashing before patient care, without hand disinfection, was also associated with higher colony counts
(>52 CFU, p = 0.03), which suggests that hand antisepsis is better than standard handwashing. These findings suggested that intervention trials should explore the role of systematic hand disinfection as a cornerstone of infection control to reduce cross-transmission in hospitals.
235
Special Issue
lack of scientific information demonstrating impact of improved hand hygiene on hospital infection rates.
organisms were cultured from 4% to 100% of the gloves and observed counts were up to 4.7 log on hands after glove removal (53). Additional barriers to hand hygiene compliance include lack of active participation in promotion at the individual or institutional level, of a role model for hand hygiene, of institutional priority assigned to hand hygiene, of administrative sanctions for noncompliance; and of an institutional climate encouraging safety (14,22,41,54,55). A system change may be necessary for improvement in hand hygiene practices by health-care workers.
Table 2. Improved adherence with hand hygiene practice compared with hospital infection rates Year Authors Hospital setting Results 1977 Casewell and Philips Adult ICU Reduction in HIa due to endemic Klebsiella spp 1982 Maki and Hecht Adult ICU Reduction in HI rates 1984 Massanari and Heirholzer Adult ICU Reduction in NI rates 1990 Simmons et al. Adult ICU No effect 1992 Doebbeling et al. Adult ICU Significant difference in rates of HI between two different hand hygiene agents 1994 Webster et al. NICU Elimination of MRSA 1995 Zafar et al. Newborn nursery Elimination of MRSA 1999 Pittet et al. Hospital-wide Significant reduction in HI and MRSA cross-transmission rates aHI = hospital infection; ICU = intensive care unit; NICU = neonatal ICU; MRSA = methicillin-resistant Staphylococcus aureus.
Ref. 58 59 60 22 7 61 62 63
236
Special Issue
proposed a hypothetical framework to enhance hand hygiene practices and stressed the importance of considering the complexity of individual and institutional factors in designing behavioral interventions. Behavioral theories and secondary interventions have primarily focused on the individual, which is insufficient to effect sustained change (46,72,73). Interventions aimed at improving compliance with hand hygiene must be based on the various levels of behavior interaction (20,46,74). Thus, the interdependence of individual factors, environmental constraints, and institutional climate should be considered in strategic planning and development of hand hygiene promotion campaigns. Factors associated with noncompliance with recommendations are related not only to the individual worker but also to the group to which he or she belongs and, by extension, to the parent institution. Factors influencing compliance at the group level include lack of education and performance feedback; working in critical care (high workload); downsizing and understaffing; and lack of encouragement or role models from key staff. Factors operating at the institutional level include lack of written guidelines; lack of appropriate hand hygiene agents; lack of skin care promotion and agents; lack of hand hygiene facilities; lack of atmosphere of compliance; and lack of administrative leadership, sanctions, rewards, and support. Interventions to promote hand hygiene in hospitals should take into account variables at all these levels. The complex dynamic of behavioral change involves a combination of education, motivation, and system change. Various psychosocial parameters influencing hand hygiene behavior include intention, attitude toward the behavior, perceived social norms, perceived behavioral control, perceived risk of infection, habits of hand hygiene practices, perceived model roles, perceived knowledge, and motivation (46). Factors necessary for change include dissatisfaction with the current situation, perception of alternatives, and recognition, both at the individual and institutional level, of the ability and potential to change. While the last factor implies education and motivation, the former two necessitate primarily a system change. Among reasons reported for poor adherence with hand hygiene recommendations, some that are clearly related to the institution (i.e., the system) include lack of institutional priority for hand hygiene, need for administrative sanctions for noncompliance or rewards for compliance, and lack of an institutional climate that encourages safety. Whereas all three reasons would require a system change in most institutions, the last would also involve management commitment, visible safety programs, an acceptable level of work stress, a tolerant and supportive attitude toward reported problems, and belief in the efficacy of preventive strategies (20,46,73,75).
motivation, or system (Table 3). Some parameters are based on epidemiologic evidence and others on the authors and other investigators experience and review of current knowledge. Some parameters may be unnecessary in certain circumstances and helpful in others. In particular, changing the hand hygiene agent could be beneficial in institutions or hospital wards with a high workload and a high demand for hand hygiene when waterless hand rub is not available (9,61,62,76). However, a change in the recommended hand hygiene agent could be deleterious if introduced during winter, when skin is more easily irritated. Several parameters that could potentially be associated with successful promotion of hand hygiene would require a system change (Table 3). Enhancing individual and institutional self-efficacy (the judgment of ones capacity to organize and execute actions to reach the objective), obtaining active participation at both levels, and promoting an institutional safety climate represent major challenges that exceed the current perception of the infection control practitioners role. More research is needed to determine whether education, individual reinforcement technique, appropriate rewarding, administrative sanction, enhanced self-participation, active involvement of a larger number of organizational leaders,
Table 3. Strategies for successful promotion of hand hygiene in hospitals Parameter Tool for change Selected ref.a Education Ea (M, S) 14,23,63,74,76 Routine observation and S (E, M) 6,14,23,63,74,76 feedback Engineering controls S 63 Make hand hygiene easy, S 63,74,77,78 convenient Make available alcoholS 63 based hand rub Alcohol-based hand rub S 63,78 available in highdemand situations Patient education S (M) 79 Reminders in the workplace S 52,63 Administrative sanctions, S 3,20 rewards Change in hand hygiene S (E) 21,80 agent Promote, facilitate skin S (E) 17,21,47,63 care for HCW hands Obtain active participation E, M, S 46,63 at individual and institutional levels Ensure institutional safety S (M) 46,63 climate Enhance individual and S (E, M) 46,63 institutional self-efficacy Avoid overcrowding, S 9,15,63,81,82 understaffing, excessive workload Combination of above E, M, S 14,23,46,63,74 strategies aE = education; M = motivation; S = system; HCW = health-care worker bOnly selected references are listed; refer to more extensive reviews (10,30,46) for exhaustive reference lists.
237
Special Issue
enhanced perception of health threat, self-efficacy, and perceived social pressure (20,46,83,84), or combinations of these factors would improve health-care workers adherence to recommendations. Ultimately, compliance with hand hygiene could become part of a culture of patient safety in which a set of interdependent elements interact to achieve a shared objective (85). More readily achievable than major system change, easy and timely access to hand hygiene in a timely fashion and the availability, free of charge, of skin care lotion both appear to be necessary prerequisites for appropriate hand hygiene behavior. In particular, in high-demand situations, such as in critical care units, in high-stress working conditions, and at times of overcrowding or understaffing, having health-care workers use a hand rub with an alcohol-based solution appears as the best method for achieving and maintaining a higher level of compliance with hand hygiene. Alcohol-based hand rub, compared with traditional handwashing with unmedicated soap and water or medicated hand antiseptic agents, may be better because it requires less time (48), acts faster (30), and irritates hands less often (21,30). This method was used in the only program that reported a sustained improvement in hand hygiene compliance associated with decreased infection rates (63). Finally, strategies to improve compliance with hand hygiene practices should be multimodal and multidisciplinary (Table 3). It is important to note, however, that the proposed framework for such strategies needs further research before implementation.
institutions and need to be tested in others. Infection control professionals should promote and conduct outstanding research and provide solutions to improve health-care worker adherence with hand hygiene and enhance patient safety. Acknowledgments
The author thanks members of the Infection Control Program at the University of Geneva Hospitals, who have been involved in research and institutional projects related to hand hygiene compliance and promotion since 1993, and Rosemary Sudan for editorial assistance. Dr. Pittet is professor of medicine and director, Infection Control Program, the University of Geneva Hospitals, Switzerland. He is a member of the Board of Directors of the Society for Healthcare Epidemiology of America, and recipient of the first Ignaz P. Semmelweis award (1999), the Hygiene-Preis des Rudolf Schlke Stiftung, 1999, and the Pfizer Award for Clinical Research 2001.
References
1. Semmelweis I. The etiology, concept and prophylaxis of childbed fever [excerpts]. In: Buck C, Llopis A, Najera E, Terris M, editors. The challenge of epidemiologyissues and selected readings. Washington: PAHO Scientific Publication; 1988. p. 46-59. 2. Rotter ML. 150 years of hand disinfectionSemmelweis heritage. Hyg Med 1997;22:332-9. 3. Jarvis WR. Handwashingthe Semmelweis lesson forgotten? Lancet 1994;344:1311-2. 4. Rotter ML. Semmelweis sesquicentennial: a little-noted anniversary of handwashing. Current Opinion in Infectious Diseases 1998;11:457-60. 5. Albert RK, Condie F. Hand-washing patterns in medical intensivecare units. N Engl J Med 1981;304:1465. 6. Graham M. Frequency and duration of handwashing in an intensive care unit. Am J Infect Control 1990;18:77-81. 7. Doebbeling BN, Stanley GL, Sheetz CT, Pfaller MA, Houston AK, Annis L, et al. Comparative efficacy of alternative hand-washing agents in reducing nosocomial infections in intensive care units. N Engl J Med 1992;327:88-93. 8. 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 Epidemiol 1997;18:97-103. 9. Pittet D, Mourouga P, Perneger TV, members of the Infection Control Program. Compliance with handwashing in a teaching hospital. Ann Intern Med 1999;130:126-30. 10. Larson EL, CIC 1992-1993, 1994 APIC Guidelines Committee. APIC guideline for handwashing and hand antisepsis in health care settings. Am J Infect Control 1995;23:251-69. 11. Preston GA, Larson EL, Stamm W. The effect of private isolation rooms on patient care practices, colonization and infection in an intensive care unit. Am J Med 1981;70:641-5. 12. Larson E. Compliance with isolation technique. Am J Infect Control 1983;11:221-5. 13. Donowitz L. Handwashing technique in a pediatric intensive care unit. Am J Dis Child 1987;141:683-5. 14. Dubbert PM, Dolce J, Richter W, Miller M, Chapman S. Increasing ICU staff handwashing: effects of education and group feedback. Infect Control Hosp Epidemiol 1990;11:191-3. 15. Pettinger A, Nettleman M. Epidemiology of isolation precautions. Infect Control Hosp Epidemiol 1991;12:303-7. 16. Larson EL, McGinley KJ, Foglia A, Leyden JJ, Boland N, Larson J, et al. Handwashing practices and resistance and density of bacterial hand flora on two pediatric units in Lima, Peru. Am J Infect Control 1992;20:65-72.
Future Research
Among key questions regarding the practices of hand hygiene in the health-care setting today, the following need to be addressed in controlled studies: What are the key determinants of hand hygiene behavior and promotion? Should hand disinfection replace conventional handwashing? What are the best hand hygiene agents? Should hand hygiene solution include a long-lasting compound? What are the most suitable skin emollients to include in hand hygiene solution? How can skin irritation and dryness from hand hygiene agents be reduced? How does skin care protection with hand cream affect the microbiologic efficacy of hand hygiene agents? and What are the key components of hand hygiene agent acceptability by health-care workers? Additional research questions include How can researchers generate more definitive scientific evidence for the impact of improved compliance with hand hygiene on infection rates? What is the acceptable level of compliance with hand hygiene (i.e., What percentage increase in hand hygiene results in a predictable risk reduction in infection rates?) and To what extent should the use of gloves be encouraged or discouraged? Finally, recognizing that individual and institutional factors are interdependent in terms of behavioral changes in health-care settings, what is the best way to obtain top management support for hand hygiene promotion? These questions are addressed to infection control practitioners, laboratory research scientists, and behavioral epidemiologists. The challenge of hand hygiene promotion could be summarized in one question: How can health-care workers behavior be changed? Tools for change are known; some have been tested, and others need to be tested. Some may prove irrelevant in the future; others have worked in some
238
Special Issue
17. Zimakoff J, Kjelsberg AB, Larsen SO, Holstein B. A multicenter questionnaire investigation of attitudes toward hand hygiene, assessed by the staff in fifteen hospitals in Denmark and Norway. Am J Infect Control 1992;20:58-64. 18. Meengs MR, Giles BK, Chisholm CD, Cordell WH, Nelson DR. Hand washing frequency in an emergency department. Journal of Emergency Nursing 1994;20:183-8. 19. Goldmann D, Larson E. Hand-washing and nosocomial infections. N Engl J Med 1992;327:120-2. 20. Boyce JM. It is time for action: improving hand hygiene in hospitals. Ann Intern Med 1999;130:153-5. 21. Larson E. Skin hygiene and infection prevention: more of the same or different approaches? Clin Infect Dis 1999;29:1287-94. 22. 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. 23. Tibballs J. Teaching hospital medical staff to handwash. Medical Journal of Australia 1996;164:395-8. 24. Larson E, Kretzer EK. Compliance with handwashing and barrier precautions. J Hosp Infect 1995;30:88-106. 25. Rotter ML. Hand washing and hand disinfection. In: Mayhall G, editor. Hospital epidemiology and infection control. Baltimore: Williams & Wilkins; 1996. p. 1052-68. 26. Selwyn S, Ellis H. Skin bacteria and skin disinfection reconsidered. BMJ 1972;1:136-40. 27. Lowbury EJL, Lilly HA, Bull JP. Disinfection of hands: removal of transient organisms. BMJ 1964;2:230-3. 28. Ayliffe GAJ, Babb JR, Quoraishi AH. A test for hygienic hand disinfection. J Clin Pathol 1978;31:923-8. 29. Rotter ML, Koller W. European test for the evaluation of the efficacy of procedures for the antiseptic handwash. Hygiene und Medizin 1991;16:4-12. 30. Rotter ML. Hand washing and hand disinfection. In: Mayall CG, editor. Hospital epidemiology and infection control. 2nd ed. Philadelphia: Lippincott, Williams & Wilkins; 1999. p. 1339-55. 31. Lilly HA, Lowbury EJL. Transient skin flora. J Clin Pathol 1978;31:919-22. 32. Garner JS, Favero MS. CDC guideline for handwashing and hospital environmental control, 1985. Infect Control 1986;7:231. 33. Ehrenkranz J. Bland soap handwash or hand antisepsis? The pressing need for clarity. Infect Control Hosp Epidemiol 1992;13:299-301. 34. Mittermayer H, Rotter M. Vergleich der Wirkung von Wasser, einigen Detergentien und thylakohol auf die transiente flora der hnde. Zentralbl Bakteriol Hyg 1975;160:163-72. 35. Lilly HA, Lowbury EJL, Wilkins MD. Limits to progressive reduction of resident skin bacteria by disinfection. J Clin Pathol 1999;32:382-5. 36. Semmelweis I. The etiology, concept and prophylaxis of childbed fever. Madison: University of Wisconsin Press; 1983. 37. Graham DR, Anderson RL, Ariel FE, Ehrenkranz NJ, Rowe B, Boer HR, et al. Epidemic nosocomial meningitis due to Citrobacter diversus in neonates. J Infect Dis 1981;144:203-9. 38. Kager L, Brismar B, Malmborg AS, Nord C. Imipenem concentrations in colorectal surgery and impact on the colonic microflora. Antimicrob Agents Chemother 1989;33:204-8. 39. 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. 40. Ehrenkranz NJ, Alfonso BC. Failure of bland soap handwash to prevent hand transfer of patient bacteria to urethral catheters. Infect Control Hosp Epidemiol 1991;12:654-62. 41. Larson E, McGinley KJ, Grove GL, Leyden JJ, Talbot GH. Physiologic, microbiologic, and seasonal effects of hanswashing on the skin of health care personnel. Am J Infect Control 1986;14:51-9.
42. Larson E. APIC guideline for use of topical antimicrobial agents. Am J Infect Control 1988;16:253-66. 43. 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;159:821-6. 44. Conly JM, Hill S, Ross J, Lertzman J, Louie T. Handwashing practices in an intensive care unit: the effects of an educational program and its relationship to infection rates. Am J Infect Control 1989;17:330-9. 45. Sproat LJ, Inglis TJ. A multicentre survey of hand hygiene practice in intensive care units. J Hosp Infect 1994;26:137-48. 46. Kretzer EK, Larson EL. Behavioral interventions to improve infection control practices. Am J Infect Control 1998;26:245-53. 47. Larson E, Killien M. Factors influencing handwashing behavior of patient care personnel. Am J Infect Control 1982;10:93-9. 48. Voss A, Widmer AF. No time for handwashing? Handwashing versus alcoholic rub: can we afford 100% compliance? Infect Control Hosp Epidemiol 1997;18:205-8. 49. Larson E. Handwashing and skin: physiologic and bacteriologic aspects. Infect Control 1985;6:14-23. 50. Larson E, McGeer A, Quraishi ZA, Krenzischek D, Parsons BJ, Holdford J, et al. Effects of an automated sink on handwashing practices and attitudes in high-risk units. Infect Control Hosp Epidemiol 1991;12:422-8. 51. Michelson A, Kamp HD, Schuster B. Sinusitis in long-term intubated, intensive care patients: nasal versus oral intubation. Anaesthesist 1991;40:100-4. 52. Khatib M, Jamaleddine G, Abdallah A, Ibrahim Y. Hand washing and use of gloves while managing patients receiving mechanical ventilation in the ICU. Chest 1999;116:172-5. 53. Doebbeling BN, Pfaller MA, Houston AK, Wenzel RP. Removal of nosocomial pathogens from the contaminated glove. Ann Intern Med 1988;109:394-8. 54. Broughall JM, Marshman C, Jackson B, Bird P. An automatic monitoring system for measuring handwashing frequency in hospital wards. J Hosp Infect 1984;5:447-53. 55. McLane C, Chenelly S, Sylwestrak ML, Kirchhoff KT. A nursing practice problem: failure to observe aseptic technique. Am J Infect Control 1983;11:178-82. 56. Haley RW, Culver DH, White JW, Morgan WM, Emori TG, Munn VP, et al. The efficacy of infection surveillance and control programs in preventing nosocomial infections in U.S. hospitals. Am J Epidemiol 1985;121:182-205. 57. Bauer TM, 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. 58. Casewell M, Phillips I. Hands as route of transmission for Klebsiella species. BMJ 1977;2:1315-7. 59. Maki D, Hecht J. Antiseptic containing hand-washing agents reduce nosocomial infections: a prospective study [Abstract #188]. Program and abstracts of the 22nd Interscience Conference of Antimicrobial Agents and Chemotherapy, Miami, Oct 4-6, 1982. Washington, DC: American Society for Microbiology; 1982. 60. Massanari RM, Heirholzer WJJ. A crossover comparison of antiseptic soaps on nosocomial infection rates in intensive care units. Am J Infect Control 1984;12:247-8. 61. 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. 62. Zafar AB, Butler RC, Reese DJ, Gaydos LA, Mennonna PA. Use of 0.3% triclosan (Bacti-Stat*) to eradicate an outbreak of methicillinresistant Staphylococcus aureus in a neonatal nursery. Am J Infect Control 1995;23:200-8.
239
Special Issue
63. Pittet D, Hugonnet S, Harbarth S, Mourouga P, Sauvan V, Touveneau S, et al. Effectiveness of a hospital-wide programme to improve compliance with hand hygiene. Lancet 2000;356:1307-12. 64. Maki DG. The use of antiseptics for handwashing by medical personnel. J Chemother 1989;1:3-11. 65. 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. 66. Early E, Battle K, Cantwell E, English J, Lavin JE, Larson E. Effect of several interventions on the frequency of handwashing among elementary public school children. Am J Infect Control 1998;26:263-9. 67. Kimel LS. Handwashing education can decrease illness absenteeism. J Sch Nurs 1996;12:14-6. 68. Master D, Hess Longe SH, Dickson H. Scheduled hand washing in an elementary school population. Fam Med 1997;29:336-9. 69. Khan MU. Interruption of shigellosis by handwashing. Trans R Soc Trop Med Hyg 1982;76:164-8. 70. 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;14:85-9. 71. Stanton BF, Clemens JD. An educational intervention for altering water-sanitation behaviors to reduce childhood diarrhea in urban Bangladesh. Am J Epidemiol 1987;125:292-301. 72. Teare EL, Cookson B, French G, Gould D, Jenner E, McCulloch J, et al. Hand washingA modest measure-with big effects. BMJ 1999;318:686. 73. Teare EL, Cookson B, French GL, Jenner EA, Scott G, Pallett A, et al. U.K. handwashing initiative. J Hosp Infect 1999;43:1-3. 74. Larson EL, Bryan JL, Adler LM, Blane CB. A multifaceted approach to changing handwashing behavior. Am J Infect Control 1997;25:3-10.
75. Weeks A. Why I dont wash my hands between each patient contact. BMJ 1999;319:518. 76. Aspck C, Koller W. A simple hand hygiene exercise. Am J Infect Control 1999;27:370-2. 77. Kaplan LM, McGuckin M. Increasing handwashing compliance with more accessible sinks. Infect Control 1986;7:408-10. 78. Raad I, Darouiche RO, Dupuis J, Abi-Said D, Gabrielli A, Hachem R, et al. Central venous catheter coated with minocycline and rifampine for the prevention of catheter-related colonization and bloodstream infections. A randomized, double-blind trial. Ann Intern Med 1997;127:267-74. 79. McGuckin M, Waterman R, Porten L, Bello S, Caruso M, Juzaitis B, et al. Patient education model for increasing handwashing compliance. Am J Infect Control 1999;27:309-14. 80. Veenstra DL, Saint S, Saha S, Lumley L, Sullivan SD. Efficacy of antiseptic-impregnated central venous catheters in preventing catheter-related bloodstream infection. A meta-analysis. JAMA 1999;281:261-7. 81. Harbarth S, Sudre P, Dharan S, Cadenas M, Pittet D. Outbreak of Enterobacter cloacae related to understaffing, overcrowding and poor hygiene practices. Infect Control Hosp Epidemiol 1999;20:598603. 82. Haley RW, Bregman D. The role of understaffing and overcrowding in recurrent outbreaks of staphylococcal infection in a neonatal special-care unit. J Infect Dis 1982;145:875-85. 83. Kelen GD, Green GB, Hexter DA, Fortenberry DC, Taylor E, Fleetwood DH, et al. Substantial improvement in compliance with universal precautions in an emergency department following institution of policy. Arch Intern Med 1991;151:2051-6. 84. Lundberg GD. Changing physician behavior in ordering diagnostic tests. JAMA 1998;280:2036. 85. Phillips DF. New look reflects changing style of patient safety enhancement. JAMA 1999;281:217-9.
240