Measuring handwashing performance in health service audits and research studies

Journal of Hospital Infection (2007) 66, 109e115

www.elsevierhealth.com/journals/jhin

REVIEW

Measuring handwashing performance in health service audits and research studies D.J. Gould a,*, J. Chudleigh a, N.S. Drey a, D. Moralejo b a b

City University, London, UK Memorial University, St John’s N.L., Canada

Available online 11 April 2007

KEYWORDS Handwashing; Hospital-acquired infection; Observation

Summary Handwashing is regarded as the most effective way of controlling healthcare-associated infection. A search of the literature identified 42 intervention studies seeking to increase compliance in which the data were collected by directly observing practice. The methods used to undertake observation were so poorly described in most studies that it is difficult to accept the findings as reliable or as valid indicators of health worker behaviour. Most studies were limited in scope, assessing the frequency of handwashing in critical care units. The ethical implications of watching health workers during close patient contact were not considered, especially when observation was covert or health workers were misinformed about the purpose of the study. Future studies should take place in a range of clinical settings to increase the generalizability of findings. Observation should be timed to capture a complete picture of 24 h activity and should include all health workers in contact with patients because all have the potential to contribute to cross-infection. Reported details of observation should include: vantage of data collectors; inter-rater reliability when more than one individual is involved; and attempts to overcome the impact of observation on usual health worker behaviour. Ideally an additional data collection method should be used to corroborate or refute the findings of observation, but no well-validated method is presently available. ª 2007 The Hospital Infection Society. Published by Elsevier Ltd. All rights reserved.

Introduction

* Corresponding author. Address: City University, School of Nursing and Midwifery, 24 Chiswell Street, London EC1 4TY, UK. Tel.: þ44 0207 0405449; fax: þ44 0207 0405866. E-mail address: [email protected]

Hospital-acquired infection (HAI) is a major problem in modern health care and a source of concern to health workers and the public.1 Handwashing is considered the single most effective and costeffective means of reducing HAI.2 However, health

0195-6701/$ - see front matter ª 2007 The Hospital Infection Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.jhin.2007.02.009

110 workers wash hands too seldom, not always at the most appropriate times and technique is suboptimal.3e7 Numerous approaches have been used to increase hand hygiene compliance. Intervention studies have been systematically reviewed by Naikoba and Hayward.8 Critique was offered about study design and there was detailed comparison between the different types of interventions and their success. In all but two of the 21 studies reviewed, direct observation was the main method of data collection. However, the rigour of observation as a method of data collection was not discussed. This omission is surprising as the validity and reliability of the findings obtained in behavioural studies depend on the appropriateness of the method used to collect data.9 The extent to which participants were aware they were being watched and the impact on their usual behaviour is a key issue, especially in studies where handwashing is the activity of interest.6,9e12

Methods A literature review was conducted to describe and evaluate direct observation used as the main method of obtaining data in studies seeking to increase hand hygiene compliance. Papers were identified from the following computerized databases: MEDLINE, CINAHL, EMBASE, and the Cochrane Library. Additional search strategies included: searching the internet with a general browser; screening the reference lists of papers already retrieved; and handsearching key journals (British Medical Journal; Journal of Hospital Infection; American Journal of Infection Control ). Attempts were made to locate material in the ‘grey’ literature. Key words used were: handwashing and hand hygiene. To meet the inclusion criteria for review, papers had to be empirical studies undertaken to increase compliance with handwashing for health workers using aqueous solutions and/or alcohol-based products. Studies designed to increase compliance by individuals other than health workers were excluded. Also excluded were opinion pieces and general reviews. Data collection had to include direct observation of handwashing, although it was permissible for additional methods to be employed (consumption of soap/alcohol handrubs, monitoring devices attached to taps). All abstracts were inspected to ensure that they met the inclusion criteria. Eligible papers were downloaded, read and scrutinized by at least two readers. The data were extracted onto a template developed especially for the review.

D.J. Gould et al.

Results The searches identified 41 300 papers. Forty-two met the inclusion criteria. Eighteen of the 21 studies reviewed by Naikoba and Hayward were eligible.8 Two were discounted because handwashing compliance had not been assessed by direct observation.13,14 A third paper8 was dismissed because, on careful reading, it proved not to report an intervention.15 Twenty-four new intervention studies using observation as a method of data collection were identified in addition to a report by Pittet et al. which had been discussed in an annex attached to the review by Naikoba and Hayward.8,16 One paper appeared to be a follow-up of the original work in Geneva and was not included.17

What was observed All the studies examined frequency of handwashing and/or use of alcohol products. The hand hygiene event was clearly defined in half the papers, usually with reference to the Association for Professionals in Infection Control and Epidemiology (APIC) or other published guidelines.18 In 13 papers handwashing was considered to be essential before and after patient contacts and/or when moving from one patient to another.19e31 In nine papers compliance was considered in relation to the number of opportunities for handwashing.16,32e39 The others did not offer clearly defined criteria for when hands should be washed. Nine studies assessed handwashing technique each using a different method of evaluation.33,34,39e45

Who was observed In seven studies, data were collected for all personnel visiting a ward or unit.16,23,35,36,46,47 In others, observation was restricted to particular occupational groups: doctors28,29; nurses24,30,34,37,38,41,45,48e50; occupational therapists51; technicians52; and preclinical medical students.53 The remaining studies appeared to include professionally qualified staff (doctors, nurses, therapists) but not ancillary staff. Six studies involved an entire hospital.16,19,26,28,40,49 Of those studies not performed on a hospital-wide basis, only five took place outside critical care units.23,34,47,50,54

How observation was conducted Non-participant observation was employed in 41 studies. In six studies, a supporting method of data

Measurement of handwashing performance collection was also employed (consumption of soap/alcohol, monitoring devices attached to taps).16,33,41,46,47,49 Rates of HAI were included as an outcome measure in six studies.16,39,47,49,55,56 In one study the method of observation was unclear.45 In another study, health workers collected data on each other and it was not clear whether this took place while they were undertaking their usual clinical duties.38 One research team employed participant observation in which the data collector was a member of the usual nursing team.50 Detailed information about the data-collecting instrument was provided in two studies.32,34 Failure of the data collector to document episodes of handwashing through lapses in observation (‘missing observations’) was considered in only one study.34

Who collected data Data collection was undertaken by a range of staff with varying levels of expertise in infection control and skill as observers: graduate nursing students; research assistants; infection control nurses; and in one case by a commercial team.31 Ten studies described the training they received.21,28,31,34,40, 48e50,54,56 Where more than one individual collected data, inter-rater agreement (inter-rater reliability) was an issue and was assessed in nine studies; acceptable levels of concordance were reported in each.16,31,33,35,43,46,48,50,54 In other studies, discussion of inter-rater reliability suggested that data collectors had received training, although this was not mentioned explicitly.

Duration and timing of observation Observation generally took place for short periods (30 mine2 h) usually during early shifts on weekdays. Only a few research teams conducted observation at night.16,32,33,57 The rationale for the time and length of observation was provided in 14 studies.16,19,22,24,31,33e36,40,46,49,50,51 The decision to restrict observation to day shifts was usually justified on the grounds that most patient contacts take place at these times because clinical areas are at their busiest.

111 collectors at any one time. Often observation appeared to take place in relation to all heath workers belonging to the occupational group of interest present on a ward or unit over the period of data collection. In one study, health workers were ‘shadowed’ individually to avoid loss of data.34

The impact of observation on usual handwashing practice The effects of observation on the activity being investigated were first documented during a series of productivity experiments at the Hawthorne Electrical Plant in the USA in the 1930s.59 Researchers found that productivity increased regardless of the variable being manipulated. They concluded that the increase was a direct result of employees being watched. This finding, now described as the ‘Hawthorne effect’ has clear implications for observation studies in which handwashing is being documented, especially in the present climate where health workers know that handwashing is being promoted. In half the studies the authors considered the possible effect of direct observation on handwashing compliance,20,22,24,27e31,33e37,40,41,43,45,46,49,58 but detailed discussion of its impact on healthworker behaviour was offered only by Pittet et al.16 During follow-up data collection, these authors deliberately fostered the ‘Hawthorne effect’ to promote increased compliance. In four studies the purpose of research was known to staff from the outset.24,33,34,45 In five studies health workers were deliberately misinformed about the real purpose of the research throughout.31,37,58 In the remainder, observation was covert at least during baseline data collection or the authors did not state whether staff were informed. In one study, the data collector spent time in the clinical area before documenting handwashing to acclimatize staff to her presence.32

Ethical issues Six authors mentioned obtaining ethical clearance, but none considered the ethical implications associated with intervention studies involving health workers or conducting close observation involving patients.30e32,34,43,51

Vantage

Discussion Seven studies revealed the vantage of data collectors.16,22,31,33,40,46,58 They were generally positioned to monitor health workers entering the unit and entering and leaving single rooms. Very little information was provided about the number of health workers observed by a given number of data

Most studies were narrow in scope. Few contained enough information about the method of observation to permit satisfactory evaluation of the validity and reliability of findings. Overall, inadequate consideration was given to ethical issues.

112

Scope Less than a quarter of the studies evaluated handwashing technique, presumably because frequency is much easier to document.60 Technique was assessed according to different criteria in each of the studies in which it was considered, reflecting the inadequacy of current standards to measure it.60,61 Drying hands is important because bacteria are transferred more readily between damp surfaces than dry ones but none of the studies addressed this issue.62,63 Many studies were restricted to a single clinical setting. This was usually a critical care unit. These were also the studies in which HAI rates were most likely to be included as outcome measures. However, the critical care setting may not be the best location to examine the effectiveness of hand hygiene compliance in reducing rates of HAI because many nosocomial infections are endogenous rather than exogenous in such units.64 A number of studies involved a single occupational group or restricted observation to clinical staff, although all health workers, including ancillary staff, handle objects in the nearpatient environment and thus have the potential to contribute to cross-infection.65

Validity and reliability From the limited information about the process of data collection included in the studies, problems were apparent in relation to the accuracy of data collection, the reliability of findings and the extent to which they are generalizable to other clinical settings and occupational groups. Observation is a skilled activity which cannot be maintained for any length of time without fatigue and data loss.66 However, information about the preparation received by data collectors was scant, and in many papers no mention of training was included. Particular care to observe accurately is needed in busy clinical areas when vantage is poor (e.g. restricted by bedside curtains), especially when several people are watched simultaneously.6,12 When observing a highly specific activity such as handwashing compliance, the very accurate, detailed information required demands a highly structured method of observing and documenting data, but this issue was poorly addressed in the majority of studies.66 The possibility of failing to document episodes of handwashing was not mentioned except for one account, where health workers were ‘shadowed’ individually.34 Limited information was offered concerning the numbers of health workers observed simultaneously, although watching several people closely at the same time is likely to reduce the accuracy

D.J. Gould et al. of what is seen and therefore documented. Interrater reliability was discussed in relatively few studies where it was an issue and glossed over in every case except for the initiative in Geneva.16 The rationale used to justify the timing and length of the observation period was generally inadequate. Morning shifts during weekdays were held as the busiest times, when greatest opportunity for patient handling and cross-infection would occur. However, the majority of studies took place in critical care units, where nursing care (pressure area care, changing position) should be performed regularly over 24 h. In half the studies researchers acknowledged that obvious documentation of handwashing can result in a Hawthorne effect.59 Some authors argued that handwashing is such an ingrained activity that it would not be possible for health workers to maintain any changes in usual practice throughout the period of observation.5,67 This may have been true in early studies, but is no longer likely to be the case. Today health workers know that handwashing forms an important element in quality of care and are likely to become aware when it is being monitored, whether or not the attempt is intended to be unobtrusive. The most frequently used method of trying to avoid the Hawthorne effect was to undertake observation covertly. However, it is difficult to accept that secrecy was effectively maintained once intervention had taken place, especially when it involved feedback on performance or poster campaigns.8 Even attempts to mislead health workers may have had limited success in avoiding the Hawthorne effect as the mere presence of an outsider in the research setting can influence usual activity.68 Threats to the validity of direct observation can be overcome by employing additional methods of data collection to corroborate or refute findings.69 In the case of handwashing there are three possibilities: unobtrusive methods (monitoring devices, consumption of soap and/or alcohol products); rates of HAI; and transmission rates of nosocomial pathogens.70 The value of unobtrusive methods is open to debate. Monitoring devices assess only frequency of handwashing: other important aspects such as technique and appropriateness of the hand hygiene event cannot be assessed. Monitoring devices need to be fitted especially for the study with resource implications when research budgets are tight and they sometimes break down.4,49 Van de Mortel and Murgo compared the results of alcohol uptake with direct observation of hand-cleansing activity.12 Throughout the period of observation, use of alcohol products doubled, but direct observation indicated marked decline in the frequency of hand cleansing. These authors suggest that

Measurement of handwashing performance consumption of alcohol products is a better indicator of compliance than direct observation. However, spillage, use of some products for purposes other than hand hygiene and ‘borrowing’ between wards has been noted during observation studies.71 Eckmanns et al. identified a positive correlation between consumption of hand hygiene products and hand hygiene compliance.70 However, neither of these measures correlated with the incidence of transmission for ten of the most frequently reported nosocomial pathogens on abraded skin.70 Few of the studies reviewed incorporated additional methods of data collection to corroborate direct observation. Most authors appeared to assume that increasing compliance with handwashing is a desirable outcome in its own right without taking into account resource implications such as the cost of consumables, the time-consuming nature of traditional washing72; the deleterious effect of repeated washing on skin already in poor condition73,74; or the increased carriage of potentially nosocomial pathogens.75

Ethical issues Where participants in a research study have not been accurately informed, have been misled or have not given consent, potentially serious ethical questions are raised.76,77 There were numerous examples of poor practice in which researchers deliberately provided false information to health workers or provided incomplete or inaccurate information, especially during baseline data collection. Many infection control teams now regularly document handwashing as part of routine infection control audits,78 promoting the Hawthorne effect to increase compliance.79 If the accuracy and hence the validity of the methods used to evaluate handwashing activity in these initiatives are open to criticism, ethical issues are raised, because health workers are being encouraged to change practice on the basis of faulty and incomplete information. None of the studies considered the possible invasion of privacy for patients during observation, even when non-nursing and medical personnel collected data.

Recommendations for future research Handwashing is receiving considerable emphasis as a straightforward and cost-effective way of reducing HAI.2 The number of studies designed to enhance compliance has doubled since the publication of the last systematic review.8 Pittet’s work in Geneva has yielded the most promising

113 results and is described in the greatest detail.16 It includes some discussion of methodological issues used to obtain observational information. Other accounts suffer from potentially serious flaws in relation to observation as the method of data collection and fail to address ethical issues, reducing the value of the data obtained and the faith that can be placed in their findings. Future studies evaluating the effectiveness of approaches to increase handwashing compliance should take place in a range of settings to increase external validity. Observation in inpatient settings should be timed to capture a complete picture of 24 h activity and should include all health workers having close contact with the immediate patient environment (bedside, objects frequently handled by patients or touching them) because all contribute to cross-infection.65 Reported details of data collection should include: vantage; who collected data; training received; inter-rater reliability where more than one person was involved; an indication of how the data were documented; and mechanisms for coping with lost data. Well-conducted studies will involve more than one method of data collection in order to corroborate findings. This is not possible at present: more research is needed to establish the most effective approaches. However, the greatest challenge will be to design intervention studies which eradicate the Hawthorne effect, yet avoid violating the rights of health workers and patients: they should be fully informed about the purpose of the research.

References 1. Masterton RG, Teare EL. Clinical governance and infection control in the United Kingdom. J Hosp Infect 2001;47:25e31. 2. Reybrouck G. The role of hands in the spread of nosocomial infections. J Hosp Infect 1983;4:103e111. 3. Albert R, Condie F. Handwashing patterns in medical intensive care units. N Engl J Med 1981;304:1465e1466. 4. Broughall J, Marshman C, Jackson B, Bird P. An automatic monitoring system for measuring handwashing frequency in hospital wards. J Hosp Infect 1984;5:447e453. 5. Sedgewick J. Hand-washing in hospital wards. Nurs Times 1984;80(20):64e66. 6. Gould DJ. Nurses’ hand decontamination practice: results of a local study. J Hosp Infect 1994;28:15e30. 7. Taylor LJ. An evaluation of handwashing techniques. Nurs Times 1978. Part 1 74(2);54e55. Part 2 74(3):108e109. 8. Naikoba S, Hayward A. The effectiveness of interventions aimed at increasing handwashing in healthcare workers e a systematic review. J Hosp Infect 2001;47:173e180. 9. Schatzman L, Strauss A. Fieldwork Research. Englewood Cliffs, NJ: Prentice-Hall; 2001. 10. Bogdan R, Taylor S. Introduction to Qualitative Research Methods. 2nd edn. New York: Wiley; 2001. 11. Hammersley M, Atkinson P. Ethnography: Principles in Practice. London: Routledge; 1983.

114 12. Van de Mortel T, Murgo M. An examination of covert observation and solution audit as tools to measure the success of hand hygiene interventions. Am J Infect Control 2006;34:95e99. 13. Hughes WT, Williams B, Pearson T. The nosocomial colonisation of T-Bear. Infect Control 1986;7:495e500. 14. McGuckin M, Waterman R, Porten L, et al. Patient education model for increasing hand washing compliance. Am J Infect Control 1999;27:309e314. 15. Kaplan LM, McGuckin M. Increasing handwashing compliance with more accessible sinks. Infect Control 1986;7: 408e410. 16. Pittet D, Hugonnet S, Mourouga P, et al. Effectiveness of a hospital-wide programme to improve compliance with hand hygiene. Lancet 2000;356:1307e1312. 17. Hugonnet S, Pernager TV, Pittet D. Alcohol-based handrub improves compliance with hand hygiene in intensive care units. Arch Intern Med 2002;162:1037e1043. 18. Larson E. APIC Guidelines for hand hygiene and hand antisepsis in health care settings. Am J Infect Control 1995; 23:251e269. 19. Avila-Aguero M, Umalha MA, Jiminez AL. Handwashing practices in tertiary-care, pediatric hospital and the effect on an educational program. Clin Perform Qua in Health Care 1998;6:70e72. 20. Bischoff WE, Reynolds TM, Curtis N, Sessler CN, Edward MB, Wenzel RP. Handwashing compliance by health care workers: the impact of introducing accessible alcohol-based hand antiseptic. Arch Intern Med 2000;160:1017e1021. 21. Brown SM, Lubimova AV, Khrustalyeva NM, et al. Use of an alcohol-based hand rub and quality improvement interventions to improve hand hygiene in a Russian intensive care unit. Infect Control Hosp Epidemiol 2003;24:172e179. 22. Conly JM, Hills S, Ross J, Lertzman J, Thomas LJ. Hand washing practices in an ICU: the effects of an educational program and its relationship to infection rates. Am J Infect Control 1989;17:330e339. 23. Dorsey ST, Cydulka RK, Emerman CL. Is hand washing teachable? Failure to improve hand washing behaviour in an urban emergency department. Acad Emerg Med 1996;3:360e365. 24. Dubbert PM, Dolce J, Richter W, Miller M, Chapman SW. Increasing ICU staff hand washing: effects of education and group feedback. Infect Control Hosp Epidemiol 1990;11: 191e193. 25. Huang J, Jiang D, Wang X. Changing knowledge, behavior and practice related to universal precautions among hospital nurses in China. J Contin Educ Nurs 2002;35:217e224. 26. Muto CA, Sistrom MG, Farr BM. Hand hygiene rates unchanged by installation of dispensers of a rapidly acting hand antiseptic. Am J Infect Control 2000;28:273e276. 27. Raju NK, Kobler C. Improving hand hygiene habits in the newborn nurseries. Am J Med Sci 1991;302:355e358. 28. Rosenthal VD, McCormick RD, Guzman S, Villamayor C, Orellano PW. Effect of education and performance feedback on handwashing: the benefit of administrative support in Argentinean hospitals. Am J Infect Control 2003;31: 85e92. 29. Salemi C, Canola T, Eck E. Hand washing and physicians: how to get them to together. Infect Control Hosp Epidemiol 2002;23:32e35. 30. Tibbals J. Teaching hospital medical staff to hand wash. Med J Aust 1996;164:395e398. 31. Whitby M, McLaws ML. Handwashing in healthcare workers: accessibility of sink location does not improve compliance. J Hosp Infect 2004;58:247e253. 32. Creedon SA. Health care workers’ hand decontamination practices: compliance with recommended guidelines. J Adv Nurs 2005;51:208e216.

D.J. Gould et al. 33. Earl ML, Jackson M, Rickman LS. Improved rates of compliance with hand antisepsis guidelines: a three-phase observational study. Am J Nurs 2001;101:26e33. 34. Gould DJ, Chamberlain A. The use of a ward-based educational package to enhance nurses’ compliance with infection control procedures. J Clin Nurs 1997;6:55e67. 35. Harbarth S, Pittet D, Grady L, et al. Interventional study to evaluate the impact of an alcohol based hand gel in improving hand hygiene compliance. Pediatr Infect Dis J 2002;21: 496e497. 36. Maury E, Alzieu M, Baudel JL, et al. Availability of an alcohol solution can improve hand disinfection compliance in an intensive care unit. Am J Respir Crit Care Med 2000;162: 324e332. 37. Mayer JA, Dubbert PM, Miller M, Burkett P, Chapman S. Increasing handwashing in an ICU. Infect Control 1986;7: 259e262. 38. Moongtui W, Gauthier D, Turner J. Using peer feedback to improve handwashing and glove usage among Thai health care workers. Am J Infect Control 2000;28:365e369. 39. Won SP, Chou HC, Hsiah WS, et al. Hand washing program for the prevention of nosocomial infections in a neonatal intensive care unit. Infect Control Hosp Epidemiol 2004; 25:742e746. 40. Coignard B, Grandbastien B, Berrouane Y, et al. Handwashing quality impact of a special program. Infect Control Hosp Epidemiol 1998;19:510e513. 41. Colombo C, Giger H, Grote C, et al. Impact of teaching interventions on nurse compliance with hand disinfection. J Hosp Infect 2002;51:69e72. 42. Lam BC, Lee J, Lau YL. Hand hygiene in a neonatal intensive care unit: a multimodal intervention and impact on nosocomial infection. Pediatrics 2004;114:565e571. 43. Larson E, McGeer A, Quaraishi ZA, et al. Effect of an automated sink on hand washing practices and attitudes in high risk units. Infect Control Hosp Epidemiol 1991;12:422e428. 44. Panhotra BR, Saxena AK, Al-Arabi AM. The effect of a continuous educational program on handwashing compliance among healthcare workers in an intensive care unit. Br J Infect Control 2004;5:15e18. 45. Shaw S, Tanner J. Hand washing practices on a neonatal unit: the influence of teaching sessions. J Neo Nurs 2003;9:162e166. 46. Bittner MJ, Rich EC, Turner PD, Arnold WH. Limited impact of sustained simple feedback based on soap and paper towel consumption on the frequency of hand washing in an adult intensive care unit. Infect Control Hosp Epidemiol 2002;23:120e126. 47. Swaboda SM, Earsing K, Strauss K, Lane S, Lipsett PA. Electronic monitoring and voice prompts to improve hand hygiene and decrease nosocomial infections in critical care. Crit Care Med 2004;32:358e363. 48. Larson E, Bryan JL, Adler LM, Lee M, Blane C. Multifaceted approach to changing hand washing behavior. Am J Infect Control 1997;25:3e10. 49. Larson EL, Early E, Cloonan P, Surgue S, Parides M. An organizational climate intervention associated with handwashing and decreased nosocomial infections. Behav Med 2000; 26:14e22. 50. Prieto J, Macleod-Clark J. Contact precautions for Clostridium difficile and methicillin-resistant Staphylococcus aureus (MRSA). J Res Nurs 2005;10:511e526. 51. Van de Mortel T, Heyman L. Performance feedback increases the incidence of hand washing by staff following patient contact in an ICU. Aust Crit Care 1995;8:8e13. 52. Khatib M, Jamaladdine G, Abdullah A, Ibrahim Y. Handwashing and use of gloves while managing patients receiving mechanical ventilation in the ICU. Chest 1999;116:172e175.

Measurement of handwashing performance 53. Diekema DJ, Schult S, Albanese MA, Doebbeling BN. Universal precautions training of preclinical students: impact on knowledge, attitudes and compliance. Prev Med 1995;24: 580e585. 54. Baker DJ. Effects of a video based staff training with manager led exercises in residential support. Ment Retard 1998; 36:198e204. 55. Berg DE, Hershaw RC, Claudia AR, Ramirez CA, Weinstein RA. Control of nosocomial infections in an ICU in Guatemala City. Clin Infect Dis 1995;21:588e593. 56. Simmons B, Bryant J, Neiman R, Spencer L, Arheart K. The role of hand washing in preventing endemic ICU infections. Infect Control Hosp Epidemiol 1990;11:589e594. 57. Graham M. Frequency and duration of hand washing in an intensive care unit. Am J Infect Control 1990;18:77e81. 58. Donowitz LG. Failure of the overgown to prevent nosocomial infection in paediatric ICU. Pediatrics 1986;77:35e38. 59. Roethlisberger FJ, Dickson WJ. Management and the Worker. Cambridge, MA: Harvard University Press; 1939. 60. Gould DJ. Hand washing as the basis for infection control. In: Progressing Antiseptic Development to Reduce Transmission of Antibiotic-resistant Pathogens. Round Table Series, 84. London: J Royal Soc Med Press; 2006. p. 12e20. 61. Jeanes A. Using alcohol products. Nurs Times 2005;101(28): 28e29. 62. Macintosh C, Hoffman P. An extended model for transfer of micro-organisms and the effect of alcohol disinfection. J Hyg 1994;92:345e355. 63. Marples RR, Towers A. A laboratory model for the contact transfer of micro-organisms. J Hyg 1979;82:237e248. 64. Silvestri L, Petros AJ, Sarginson RE, de la Cal ME, Murray AE, van Saene HKF. Hand washing in the intensive care unit: a big measure with modest effects. J Hosp Infect 2005;59:172e179. 65. Lucet JC, Rigaud MP, Mentre F, et al. Hand contamination before and after different hand hygiene techniques: a randomised clinical trial. J Hosp Infect 2002;50:276e280.

115 66. Swanwick M. Observation as a research method. Nurs Res 1994;2:4e12. 67. Gould DJ. Systematic observation of hand decontamination. Nurs Stand 2004;18(47):39e44. 68. Homan R. The Ethics of Social Research. London: Longman; 1991. 69. Adler PA, Adler PA. Observational techniques. In: Denzin NK, Lincoln YS, editors. Handbook of Qualitative Research. London: Sage; 1994. p. 377e391. 70. Eckmanns T, Scwab F, Bessert J, et al. Hand rub consumption and hand hygiene compliance are not indicators of pathogen transmission in intensive care units. J Hosp Infect 2006;63:406e411. 71. Gould DJ, Ream E. Assessing nurses’ hand decontamination practice. Nurs Times Occasional Paper 1993;89(25):47e51. 72. Voss A, Widmer AF. No time for handwashing? Handwashing versus alcoholic rub: can we afford 100% compliance? Infect Control Hosp Epidemiol 1997;18:203e208. 73. Larson E, Killien M. Factors influencing handwashing behavior of patient care personnel. Am J Infect Control 1982;10: 93e99. 74. Kownatzki E. Hand hygiene and skin health. J Hosp Infect 2003;55:239e245. 75. Larson EL, Norton Hughes C, Pyrek JD, Sparks SM, Cagstay EU, Bartkus JM. Changes in bacterial flora associated with skin damage on hands of health care personnel. Am J Infect Control 1998;26:513e521. 76. Humphreys L. Tearoom trade: impersonal sex in public places. Chicago: Aldine; 1975. 77. Knight M, Field D. A silent conspiracy: coping with dying cancer patients on an acute surgical ward. J Adv Nurs 1981;6:221e229. 78. Jeanes A. Establishing a system to improve hand hygiene compliance. Nurs Times Infect Control Suppl 2004;100(5):49e50. 79. Storr J. The effectiveness of the national cleanyourhandscampaign. Nurs Times 2005;101(8):50e51.