Journal of Hospital Infection
Volume 73, Issue 4 , Pages 305-315, December 2009

Role of hand hygiene in healthcare-associated infection prevention

  • B. Allegranzi

      Affiliations

    • World Alliance for Patient Safety, World Health Organization, Geneva, Switzerland
    • Corresponding Author InformationCorresponding author. Address: First Global Patient Safety Challenge, World Alliance for Patient Safety, IER/PSP, Room L319, L Building, World Health Organization, 20 Avenue Appia, 1211 Geneva 27, Switzerland. Tel.: +41 22 791 2689; fax: +41 22 791 1388.
  • ,
  • D. Pittet

      Affiliations

    • World Alliance for Patient Safety, World Health Organization, Geneva, Switzerland
    • Infection Control Programme, University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland

published online 17 May 2010.

Article Outline

Summary 

Healthcare workers' hands are the most common vehicle for the transmission of healthcare-associated pathogens from patient to patient and within the healthcare environment. Hand hygiene is the leading measure for preventing the spread of antimicrobial resistance and reducing healthcare-associated infections (HCAIs), but healthcare worker compliance with optimal practices remains low in most settings. This paper reviews factors influencing hand hygiene compliance, the impact of hand hygiene promotion on healthcare-associated pathogen cross-transmission and infection rates, and challenging issues related to the universal adoption of alcohol-based hand rub as a critical system change for successful promotion. Available evidence highlights the fact that multimodal intervention strategies lead to improved hand hygiene and a reduction in HCAI. However, further research is needed to evaluate the relative efficacy of each strategy component and to identify the most successful interventions, particularly in settings with limited resources. The main objective of the First Global Patient Safety Challenge, launched by the World Health Organization (WHO), is to achieve an improvement in hand hygiene practices worldwide with the ultimate goal of promoting a strong patient safety culture. We also report considerations and solutions resulting from the implementation of the multimodal strategy proposed in the WHO Guidelines on Hand Hygiene in Health Care.

Keywords: Alcohol-based hand rub, Hand hygiene, Healthcare-associated infection, Intervention, Patient safety, Promotion, World Health Organization

 

Back to Article Outline

Introduction 

Numerous studies document the pivotal role of healthcare workers' (HCWs) hands in the propagation of micro-organisms within the healthcare environment and ultimately to patients.1 As recently described, patient-to-patient transmission of pathogens via HCWs' hands involves five sequential steps.2 Patients' skin can be colonised by transient pathogens that are subsequently shed onto surfaces in the immediate patient surroundings, thus leading to environmental contamination.2 As a consequence, HCWs contaminate their hands by touching the environment or patients' skin during routine care activities, sometimes even despite glove use.2 It has been shown that organisms are capable of surviving on HCWs' hands for at least several minutes following contamination.2 Thus, if hand hygiene practices are suboptimal, microbial colonisation is more easily established and/or direct transmission to patients or a fomite in direct contact with the patient may occur.2

Based on this evidence and the demonstration of its effectiveness, optimal hand hygiene behaviour is considered the cornerstone of healthcare-associated infection (HCAI) prevention.2, 3, 4 Furthermore, not only is it a key element of standard and isolation precautions, but its importance is emphasised also in the most modern ‘bundle’ approaches for the prevention of specific site infections such as catheter-related bloodstream infection (CRBSI), catheter-related urinary tract infection (CRUTI), surgical site infection (SSI), and ventilator-associated pneumonia (VAP).5, 6, 7, 8, 9

Together with other specific prevention measures, environmental cleaning is another essential measure to prevent the spread of some pathogens, particularly Clostridium difficile, vancomycin-resistant enterococci (VRE), norovirus, Acinetobacter spp. and meticillin-resistant Staphylococcus aureus (MRSA), and should not be neglected.10, 11, 12

Over the past few years, scientific evidence to support the role of hand hygiene in the improvement of patient safety has increased considerably, but some key controversial issues still challenge care practitioners and researchers. This review summarises the key themes on the role of hand hygiene in preventing HCAI. Interpretations and solutions based on the evidence and experience available through the work of the First Global Patient Safety Challenge of the WHO World Alliance for Patient Safety are suggested.

Back to Article Outline

Factors influencing hand hygiene compliance 

It has been known for many years that HCWs encounter difficulties in complying with hand hygiene indications at different levels.4 Insufficient or very low compliance rates have been reported from both developed and developing countries.1, 4 Reasons which explain suboptimal practices are multiple and may vary according to the setting and the resources available. For example, the lack of appropriate infrastructure and equipment to enable hand hygiene performance, the cultural background, and even religious beliefs can play an important role in hindering good practices.13, 14, 15 The most frequently observed factors determining poor hand hygiene compliance are: (i) belonging to a certain professional category (i.e. doctor, nursing assistant, physiotherapist, technician); (ii) working in specific care areas (i.e. intensive care, surgery, anaesthesiology, emergency medicine); (iii) understaffing and overcrowding; and (iv) wearing gowns and/or gloves.1 Unfortunately, hand hygiene indications at higher risk of being neglected are the ones that prevent pathogen transmission to the patient (i.e. before patient contact and clean/aseptic procedures).1 This is also in concordance with the fact that care activities with a higher risk of cross-transmission lead to a higher risk of poor compliance.1

Individual factors such as social cognitive determinants may provide additional insight into hand hygiene behaviour.3, 16, 17, 18 Many factors play a role in eventually determining either a hand hygiene action or lack of compliance: perception and knowledge of the transmission risk and of the impact of HCAI; social pressure; HCWs' conviction of their self-efficacy; the evaluation of perceived benefits against the existing barriers; the intention to perform the hand hygiene action. For instance, intention to wash hands did not predict observed handwashing behaviour in one study, whereas it did in another.19, 20 Hence, hand hygiene behaviour appears not to be homogeneous and can be classified into at least two types of practice.21 Inherent hand hygiene practice, which drives most community and HCW hand hygiene actions, occurs when hands are visibly soiled, sticky or gritty. On the other hand, elective hand hygiene practice represents those opportunities for hand cleansing not encompassed in the inherent category. Among HCWs, this component of hand hygiene behaviour is similar to many common social interactions, such as shaking hands. During healthcare, it would include touching a patient (e.g. taking a pulse or blood pressure) or having contact with an inanimate object in the patient's surroundings. As they recall a common social behaviour, these contacts do not necessarily trigger an intrinsic need to cleanse hands, although they do involve the risk of cross-transmission. According to behavioural theories, this is the component of hand hygiene most likely to be omitted by busy HCWs and it has been repeatedly confirmed by field observations.

Back to Article Outline

Impact of hand hygiene promotion on HCAI 

Given the complexity of hand hygiene behaviour and the influence of numerous external factors, promotion of good practices is complex and its potential for success depends on the delicate balance between evaluation of benefits and existent barriers. Demonstration of the effectiveness of recommendations and strategies to improve hand hygiene on the ultimate outcome, i.e. the HCAI rate, is crucial in both motivating HCWs' behavioural change and securing an investment in this preventive measure by policy-makers and healthcare managers. However, research in this field represents a very challenging activity since methodological and ethical concerns make it difficult to conduct randomised controlled trials with appropriate sample sizes that could establish the relative importance of hand hygiene in the prevention of HCAI. In addition, HCAI surveillance is a very resource- and time-consuming activity requiring rigorous and standardised methods, and therefore is seldom available on a regular and reliable basis.

Nevertheless, there is convincing evidence that improved hand hygiene can reduce infection rates. More than 20 hospital-based studies of the impact of hand hygiene on the risk of HCAI have been published between 1977 and 2008 (Table I).22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45 Of these, some were conducted hospital-wide and report long-term follow-up to demonstrate sustainability.29, 30, 38, 42 Despite study limitations, almost all reports showed a temporal association between improved hand hygiene practices and reduced infection and cross-transmission rates. Most investigations were conducted in adult or neonatal intensive care units (ICUs) and the large majority introduced the use of alcohol-based hand rubs in association with other promotional components in a multimodal implementation strategy (Table I). Three studies failed to show HCAI reduction following hand hygiene promotion.24, 41, 44 In one study, the intervention did not succeed in significantly increasing hand hygiene compliance.24 In another, the methods and definitions used to detect HCAI were not described and therefore the data reliability cannot be assessed.44 In a prospective, controlled, cross-over trial, Rupp and colleagues observed no substantial change in device-associated infection rates and infections due to multidrug-resistant pathogens, despite a significant and sustained improvement in hand hygiene adherence.41 Nevertheless, although the study was well designed, it was criticised for lack of screening for cross-transmission, lack of statistical power, and use of an alcohol-based hand rub that failed to meet the EN 1500 standards for antimicrobial efficacy.46, 47, 48

Table I. Most relevant studies assessing the impact of hand hygiene promotion on HCAI (1977–2008)
YearHospital settingInterventionImpact on hand hygiene complianceImpact on HCAIDuration of follow-upReference
1977Adult ICUPromotion of hand washing with a chlorhexidine hand cleanserNASignificant reduction (P<0.001) in the percentage of patients colonised/infected by Klebsiella spp.2 years22

1989Adult ICUEducation on hand washing, hand hygiene observation, performance feedbackCompliance increase from 14% to 73% (before patient contact) and from 28% to 81% (after patient contact)Significant reduction (P=0.02) in HCAI rates (from 33% to 12% and from 33% to 10%, respectively, after two intervention periods 4 years apart)6 years23

1990Adult ICUHand-washing promotionCompliance increase from 22% to 29.9%No impact on HCAI rates11 months24

1992Adult ICUsProspective multiple cross-over trial on hand hygiene with either chlorhexidine soap or 60% isopropyl alcohol with optional hand washing with plain soapNASignificant reduction (P<0.02) in HCAI rates using hand washing with chlorhexidine soap8 months25

1994NICUIntroduction of hand washing with triclosan 1% (w/v)NAElimination of MRSA, when combined with multiple other infection control measures.9 months26
Significant reduction (P<0.02) in nosocomial bacteraemia (from 2.6% to 1.1%) using triclosan compared with chlorhexidine for hand washing

1995Newborn nurseryIntroduction of HCWs' hand washing and neonates' bathing with triclosan 0.3% (w/v)NAControl of MRSA outbreak3.5 years27

2000MICU/NICUOrganisational climate interventionNASignificant (85%) relative reduction (P=0.02) in VRE rate in the intervention hospital; statistically not significant (44%) relative reduction in control hospital; no significant change in MRSA8 months28
2000Hospital-wideAlcohol-based hand rub introduction, hand hygiene observation, training, performance feedback, postersSignificant increase in compliance from 48% to 66%Significant reduction (P=0.04 and P<0.001) in the annual overall HCAI prevalence (42%) and MRSA cross-transmission rates (87%). Active surveillance cultures and contact precautions implemented during same period. A follow-up study showed continuous increase in hand rub use, stable HCAI rates and cost savings.8 years29, 30

2003Orthopaedic surgical unitAlcohol-based hand rub introduction, posters, feedback on HCAI rates, patient education and involvementNA36% decrease (P value, NA) in HCAI (mainly urinary tract infection and SSI) rates (from 8.2% to 5.3%)10 months31

2004Hospital-wideAlcohol-based hand rub introduction, hand hygiene observation, posters, performance feedback, informal discussionsNo significant increase in compliance before and after patient contactSignificant reduction (P=0.03) in hospital-acquired MRSA cases (from 1.9% to 0.9%)1 year32

2004Adult intermediate care unitHand hygiene electronic monitoring at exit from patient rooms, direct observation and voice promptsCompliance increase from 19.1% to 27.3% by electronic monitoringReduction in HCAI rates (not statistically significant, P value, NA)2.5 months33

2004NICUAlcohol-based hand rub introduction, hand hygiene observation, training, hand-hygiene protocols, postersCompliance increase from 40% to 53% (before patient contact) and from 39% to 59% (after patient contact)Reduction (P=0.14) in HCAI rates (from 11.3 to 6.2 per 1000 patient-days)6 months34

2004NICUEducation, written instructions, hand hygiene observation, posters, performance feedback, financial incentivesCompliance increase from 43% to 80%Significant reduction (P=0.003) in HCAI rates (from 15.1 to 10.7 per 1000 patient-days), in particular for respiratory infections2 years35
2005Hospital-wideAlcohol-based hand rub introduction, hand hygiene observation, training, postersCompliance increase from 62% to 81%Significant reduction (P=0.01) in hospital-associated rotavirus infections4 years36

2005Adult ICUsHand-washing observation, training, guideline dissemination, posters, performance feedbackCompliance increase from 23.1% to 64.5%Significant reduction (P<0.001) in HCAI rates (from 47.5 to 27.9 per 1000 patient-days)21 months37

2005Hospital-wideAlcohol-based hand rub introduction, hand hygiene observation, training, posters, promotional gadgetsCompliance increase from 21% to 42%Significant reduction (57%, P=0.01) in MRSA bacteraemia36 months38

2007NeurosurgeryAlcohol-based hand rub introduction, training, postersNAReduction (54%, P=0.09) in overall incidence of SSI. Significant reduction (100%, P=0.007) in superficial SSI rates2 years39

2007Neonatal unitPosters, focus groups, hand hygiene observation, HCWs' perception assessment, feedback on performance, perception and HCAI ratesCompliance increase from 42% to 55%Reduction (P value, NA) in overall HCAI rates (from 11 to 8.2 infections per 1000 patient-days) and 60% decrease (P value NA) in risk of HCAI in very low birth weight neonates (from 15.5 to 8.8 episodes per 1000 patient-days)27 months40

2008ICUProspective, controlled, cross-over trial in two units with education, posters and alcohol-based hand rub introductionCompliance increase from 38–37% to 68–69%No impact on device-associated infection and infections due to multidrug-resistant pathogens2 years41
2008(1) Six pilot hospitalsAlcohol-based hand rub introduction, hand hygiene observation, training, posters, promotional gadgets(1) Compliance increase from 21% to 48%(1) Significant reduction (P=0.035) in MRSA bacteraemia (from 0.05 to 0.02 per 100 patient discharges per month) and of clinical MRSA isolates (P=0.003)(1) 2 years42
(2) All public hospitals in Victoria (Australia)(2) Compliance increase from 20% to 53%(2) Reduction in MRSA bacteraemia (from 0.03 to 0.01 per 100 patient discharges per month, P=0.09) and of clinical MRSA isolates (P=0.043)(2) 1 year

2008Urology UnitAlcohol-based hand rub introduction, hand hygiene observation, training, posters, patient educationCompliance increase from 0% (estimation) to 28.2%Significant reduction (P<0.001) in HCAI rates from 13.1% to 2.1%6 months43

2008NICUAlcohol-based hand rub introduction, training, postersNASignificant reduction (P=0.009) in HCAI incidence (4.1 vs 1.2 per 1000 patient-days)18 months44

2008NICUAlcohol-based hand rub introduction, hand hygiene observation, training, posters, performance feedback, focus groupsCompliance increase from 6.3% to 81.2%No impact on HCAI rates (9.7 vs 13.5 per 1000 patient-days) (P-value NA)7 months45

HCAI, healthcare-associated infection; ICU, intensive care unit; NICU, neonatal intensive care unit; MICU, medical intensive care unit; VRE, vancomycin-resistant enterococcus; MRSA, meticillin-resistant Staphylococcus aureus; SSI, surgical site infection; NA, not available.

In many countries, the evidence from studies on hand hygiene effectiveness has been convincing enough to motivate governments to invest resources in hand hygiene national and subnational campaigns.49 However, this evidence mainly reflects findings from interventions implemented in healthcare settings in developed countries. Further research is needed to evaluate the relative efficacy of each key element of multimodal strategies, to assess their implementation feasibility in settings with limited resources, and to gather information on successful solutions allowing adaptation. Among its main objectives, the First Global Patient Safety Challenge, launched by the WHO World Alliance for Patient Safety, intends to make available implementation tools for field use and to assess their validation and adoption in countries at different income levels.49

Another controversial issue is how significant should be the hand hygiene compliance increase following the intervention in order to be considered satisfactory. No data are available yet to answer this question. Among all the above-mentioned studies, increased compliance rates at follow-up did not exceed 81% (Table I). One study with a follow-up of eight years showed a sustained compliance increase of up to a maximum of 66% and succeeded in parallel to maintain the achieved reduction in HCAI rates of <10%.29, 30 To achieve 100% compliance is not strictly necessary to determine improvement of patient safety at the bedside. On the other hand, the goal of sustained 100% compliance appears unlikely to be achieved because of the complex range of factors influencing HCWs' behaviour related to hand hygiene performance. Thus, there is a need for careful consideration before setting a goal of zero tolerance to hand hygiene non-compliance to avoid failure and frustration.

Back to Article Outline

Challenging issues related to the adoption of alcohol-based hand rubs 

The adoption of alcohol-based hand rubs is considered the gold standard for hand hygiene in most clinical situations. This recommendation, promoted by the CDC and WHO and embraced by many national hand hygiene guidelines, is based on the evidence of better microbiological efficacy, less time required to achieve the desired effect, point of patient care accessibility and a better skin tolerance profile.1, 29, 50, 51, 52, 53, 54, 55, 56

The WHO Guidelines on Hand Hygiene in Health Care have been conceived to catalyse hand hygiene improvement in any setting regardless of the resources available and the cultural background.1, 49, 57 Since there is a strong emphasis in the Guidelines and in their implementation tools on the availability of alcohol-based hand rubs as a key factor for hand hygiene improvement, the issue of the procurement and cost of these products, especially in developing countries, challenges the recommendation feasibility. Indeed, global sales of commercially produced, alcohol-based hand rubs in 2007 were as high as US $3 billion, corresponding to 295millionL in volume, with an overall 16.3% increase compared with 2003 (WHO, unpublished data), mostly observed in Europe and North America (27% and 23% increase, respectively). Looking at procurement opportunities, these products are available only in South Africa in the African continent and in China, India, and Japan in the Asia–Pacific region (WHO unpublished data). The most important issue curbing the purchasing power in these regions is the high cost of these products. Market prices vary from US $2.50 to 8.40 per 100mL dispenser and are clearly unaffordable for many developing countries. The WHO multimodal hand hygiene improvement strategy offers a possible solution to this obstacle: the local production of either of two WHO-recommended hand rub formulations.1 The implementation toolkit accompanying the WHO Guidelines on Hand Hygiene in Health Care includes a Guide to Local Production to manufacture alcohol-based hand rubs in hospital pharmacies or other facilities for local use.1 Two formulations are proposed: one based on ethanol 80% v/v, and one based on isopropyl alcohol 75% v/v; both include hydrogen peroxide 0.125% v/v and glycerol 1.45% v/v. Local production has been carried out in many healthcare settings worldwide and was carefully monitored and evaluated by WHO in several sites (WHO unpublished data). No major procurement, production, and storage obstacles were encountered and long-term stability at tropical temperatures was shown (up to 19 months). The final products complied with quality control standards and had good skin tolerability at very low cost (less than US $0.50 per 100mL).

Back to Article Outline

Controversial issues related to the use of alcohol-based hand rubs and Clostridium difficile spread 

Following the widespread use of alcohol-based hand rubs as the gold standard for hand hygiene in healthcare, concern has been raised about their lack of efficacy against spore-forming pathogens. Indeed, apart from iodophors, albeit at a concentration remarkably higher than the one used in antiseptics, no hand hygiene agent (including alcohols, chlorhexidine, hexachlorophene, chloroxylenol, and triclosan) is reliably sporicidal against Clostridium or Bacillus spp.1, 58 Mechanical friction while washing hands with soap and water may help physically remove spores from the surface of contaminated hands.59, 60, 61 As a consequence, contact precautions are highly recommended during C. difficile-associated outbreaks, in particular, glove use and hand washing with a non-antimicrobial or antimicrobial soap and water following glove removal after caring for patients with diarrhoea.5

The widespread use of alcohol-based hand rubs in healthcare settings has been blamed repeatedly for the increase in C. difficile-associated disease rates, although this has not been demonstrated by any study to date.62, 63 On the contrary, the observed increase in C. difficile-associated disease began in the USA long before the wide use of alcohol-based hand rubs.64, 65 Furthermore, one large outbreak with the epidemic strain REA-group B1 (equivalent to ribotype 027) was managed successfully by introducing alcohol-based hand rub for all patients other than those with C. difficile-associated disease.66 In addition, several studies recently demonstrated a lack of association between the consumption of alcohol-based hand rubs and the incidence of clinical isolates of C. difficile.67, 68, 69 In conclusion, discouraging the widespread use of alcohol-based hand rubs for the care of patients other than those with C. difficile-associated disease will only jeopardise overall patient safety in the long term.

Back to Article Outline

Discussion 

From the available evidence it appears that multimodal interventions are the most suitable strategy to determine behavioural change leading to improved hand hygiene compliance and reduction in HCAI rates. Introduction of alcohol-based hand rubs and continuous educational programmes are key factors to overcome infrastructure barriers and to build solid knowledge improvement. Support by healthcare administrators and commitment by national and local governments are essential to make hand hygiene an institutional and national priority for patient safety and to ensure long-term sustainability of promotional programmes. Higher priority should also be given to hand hygiene as a research topic, through good-quality, randomised, controlled trials to determine definitively its impact on HCAI and the relative effectiveness of the different components of multimodal strategies.

Back to Article Outline

Acknowledgements 

We wish to thank all members of the Infection Control Programme, University of Geneva Hospitals and members of the WHO First Global Patient Safety Challenge ‘Clean Care is Safer Care’ core group (lead, D. Pittet): J. Boyce, B. Cookson, N. Damani, D. Goldmann, L. Grayson, E. Larson, G. Mehta, Z. Memish, H. Richet, M. Rotter, S. Sattar, H. Sax, W.H. Seto, A. Voss, A. Widmer.

Back to Article Outline

Conflict of interest statement 

WHO takes no responsibility for the information provided or the views expressed in this paper.

Back to Article Outline

Funding sources 

None.

Back to Article Outline

References 

  1. WHO guidelines for hand hygiene in health care (Advanced draft). Geneva: World Health Organization; 2006;
  2. Pittet D, Allegranzi B, Sax H, et al. Evidence-based model for hand transmission during patient care and the role of improved practices. Lancet Infect Dis. 2006;6:641–652
  3. Kretzer EK, Larson EL. Behavioral interventions to improve infection control practices. Am J Infect Control. 1998;26:245–253
  4. Pittet D, Boyce J. Hand hygiene during patient care: pursuing the Semmelweis legacy. Lancet Infect Dis. 2001; April;9–20
  5. Siegel JD, Rhinehart E, Jackson M, Chiarello L. Guideline for isolation precautions: preventing transmission of infectious agents in health care settings. Am J Infect Control. 2007;35(Suppl. 2):S65–S164
  6. Eggimann P, Harbarth S, Constantin MN, Touveneau S, Chevrolet JC, Pittet D. Impact of a prevention strategy targeted at vascular-access care on incidence of infections acquired in intensive care. Lancet. 2000;355:1864–1868
  7. O'Grady NP, Alexander M, Dellinger EP, et al. Guidelines for the prevention of intravascular catheter-related infections. MMWR Recomm Rep. 2002;51:1–29
  8. Pronovost P, Needham D, Berenholtz S, Sinopoli D, Chu H, Cosgrove S. An intervention to decrease catheter-related bloodstream infections in the ICU. N Engl J Med. 2006;335:2725–2732
  9. Mangram AL, Horan TC, Pearson ML, Silver LC, Jarvis WR, Hospital Infection Control Practices Advisory Committee . Guideline for prevention of surgical site infection, 1999. Infect Control Hosp Epidemiol. 1999;20:247–278
  10. Rampling A, Wiseman S, Davis L, et al. Evidence that hospital hygiene is important in the control of methicillin-resistant Staphylococcus aureus. J Hosp Infect. 2001;49:109–116
  11. Dancer SJ. Importance of the environment in meticillin-resistant Staphylococcus aureus acquisition: the case for hospital cleaning. Lancet Infect Dis. 2008;8:101–113
  12. Goodman ER, Platt R, Bass R, Onderdonk AB, Yokoe DS, Huang SS. Impact of an environmental cleaning intervention on the presence of methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci on surfaces in intensive care unit rooms. Infect Control Hosp Epidemiol. 2008;29:593–599
  13. Ahmed QA, Memish ZA, Allegranzi B, Pittet D. Muslim health-care workers and alcohol-based handrubs. Lancet. 2006;367:1025–1027
  14. Duerink DO, Farida H, Nagelkerke NJD, et al. Preventing nosocomial infections: improving compliance with standard precautions in an Indonesian teaching hospital. J Hosp Infect. 2006;64:36–43
  15. Allegranzi B, Memish ZA, Donaldson L, Pittet D. Religion and culture: potential undercurrents influencing hand hygiene promotion in healthcare. Am J Infect Control. 2009;37:28–34
  16. Whitby M, PessoaSilva CL, McLaws ML, et al. Behavioural considerations for hand hygiene practices: the basic building blocks. J Hosp Infect. 2007;65:1–8
  17. Seto WH. Staff compliance with infection control practices: application of behavioural sciences. J Hosp Infect. 1995;30(Suppl.):107–115
  18. Pittet D. The Lowbury lecture: behaviour in infection control. J Hosp Infect. 2004;58:1–13
  19. O'Boyle CA, Henly SJ, Larson E. Understanding adherence to hand hygiene recommendations: the theory of planned behavior. Am J Infect Control. 2001;29:352–360
  20. Jenner EA, Watson PWB, Miller L, Jones F, Scott GM. Explaining hand hygiene practice: an extended application of the theory of planned behaviour. Psychol Health Med. 2002;7:311–326
  21. Whitby M, McLaws M-L, Ross RW. Why healthcare workers don't wash their hands: a behavioral explanation. Infect Control Hosp Epidemiol. 2006;27:484–492
  22. Casewell M, Phillips I. Hands as route of transmission for Klebsiella species. Br Med J. 1977;2:1315–1317
  23. Conly JM, Hill S, Ross J, et al. Handwashing practices in an intensive care unit: the effects of an educational program and its relationship to infection rates. Am J Infect Control. 1989;17:330–339
  24. Simmons B, Bryand J, Neiman K, Spencer L, Arheart K. The role of handwashing in prevention of endemic intensive care unit infections. Infect Control Hosp Epidemiol. 1990;11:589–594
  25. Doebbeling BN, Stanley GL, Sheetz CT, 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
  26. Webster J, Faoagali JL, Cartwright D. Elimination of methicillin-resistant Staphylococcus aureus from a neonatal intensive care unit after hand washing with triclosan. J Paediatr Child Health. 1994;30:59–64
  27. 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
  28. Larson EL, Early E, Cloonan P, Sugrue S, Parides M. An organizational climate intervention associated with increased handwashing and decreased nosocomial infections. Behav Med. 2000;26:14–22
  29. Pittet D, Hugonnet S, Harbarth S, et al. Effectiveness of a hospital-wide programme to improve compliance with hand hygiene. Lancet. 2000;356:1307–1312
  30. Pittet D, Sax H, Hugonnet S, Harbarth S. Cost implications of successful hand hygiene promotion. Infect Control Hosp Epidemiol. 2004;25:264–266
  31. Hilburn J, Hammond BS, Fendler EJ, Groziak PA. Use of alcohol hand sanitizer as an infection control strategy in an acute care facility. Am J Infect Control. 2003;31:109–116
  32. MacDonald A, Dinah F, MacKenzie D, Wilson A. Performance feedback of hand hygiene, using alcohol gel as the skin decontaminant, reduces the number of inpatients newly affected by MRSA and antibiotic costs. J Hosp Infect. 2004;56:56–63
  33. Swoboda SM, Earsing K, Strauss K, Lane S, Lipsett PA. Electronic monitoring and voice prompts improve hand hygiene and decrease nosocomial infections in an intermediate care unit. Crit Care Med. 2004;32:358–363
  34. Lam BC, Lee J, Lau YL. Hand hygiene practices in a neonatal intensive care unit: a multimodal intervention and impact on nosocomial infection. Pediatrics. 2004;114:e565–e571
  35. Won SP, Chou HC, Hsieh WS, et al. Handwashing program for the prevention of nosocomial infections in a neonatal intensive care unit. Infect Control Hosp Epidemiol. 2004;25:742–746
  36. Zerr DM, Allpress AL, Heath J, et al. Decreasing hospital-associated rotavirus infection: a multidisciplinary hand hygiene campaign in a children's hospital. Pediatr Infect Dis J. 2005;24:397–403
  37. Rosenthal VD, Guzman S, Safdar N. Reduction in nosocomial infection with improved hand hygiene in intensive care units of a tertiary care hospital in Argentina. Am J Infect Control. 2005;33:392–397
  38. Johnson PD, Martin R, Burrell LJ, et al. Efficacy of an alcohol/chlorhexidine hand hygiene program in a hospital with high rates of nosocomial methicillin-resistant Staphylococcus aureus (MRSA) infection. Med J Aust. 2005;183:509–514
  39. Thi Anh Thu L, Dibley MJ, Nho VV, Archibald L, Jarvis WR, Sohn AH. Reduction in surgical site infections in neurosurgical patients associated with a bedside hand hygiene program in Vietnam. Infect Control Hosp Epidemiol. 2007;28:583–588
  40. Pessoa-Silva CL, Hugonnet S, Pfister R, et al. Reduction of health care associated infection risk in neonates by successful hand hygiene promotion. Pediatrics. 2007;120:e382–e390
  41. Rupp ME, Fitzgerald T, Puumala S, et al. Prospective, controlled, cross-over trial of alcohol-based hand gel in critical care units. Infect Control Hosp Epidemiol. 2008;29:8–15
  42. Grayson ML, Jarvie LJ, Martin R, et al. Significant reductions in methicillin-resistant Staphylococcus aureus bacteraemia and clinical isolates associated with a multisite, hand hygiene culture-change program and subsequent successful statewide roll-out. Med J Aust. 2008;188:633–640
  43. Nguyen KV, Nguyen PT, Jones SL. Effectiveness of an alcohol-based hand hygiene programme in reducing nosocomial infections in the urology ward of Binh Dan Hospital, Vietnam. Trop Med Int Health. 2008;13:1297–1302
  44. Capretti MG, Sandri F, Tridapalli E, Galletti S, Petracci E, Faldella G. Impact of a standardized hand hygiene program on the incidence of nosocomial infection in very low birth weight infants. Am J Infect Control. 2008;36:430–435
  45. Picheansathian W, Pearson A, Suchaxaya P. The effectiveness of a promotion programme on hand hygiene compliance and nosocomial infections in a neonatal intensive care unit. Int J Nurs Pract. 2008;14:315–321
  46. Mermel LA, Boyce JM, Voss A, Allegranzi B, Pittet D. Trial of alcohol-based hand gel in critical care units. Infect Control Hosp Epidemiol. 2008;29:577–579author reply 580–582
  47. McGuckin M, Waterman R. “Cannot detect a change” is not the same as “there is not a change”. Infect Control Hosp Epidemiol. 2008;29:576–577author reply 580–582
  48. Widmer AF, Rotter M. Effectiveness of alcohol-based hand hygiene gels in reducing nosocomial infection rates. Infect Control Hosp Epidemiol. 2008;29:576;author reply 580–582
  49. Allegranzi B, Pittet D. Healthcare-associated infection in developing countries: simple solutions to meet complex challenges. Infect Control Hosp Epidemiol. 2007;28:1323–1327
  50. Boyce JM, Pittet D. Guideline for hand hygiene in health-care settings. Recommendations of the Healthcare Infection Control Practices Advisory Committee and the HICPAC/SHEA/APIC/IDSA Hand Hygiene Task Force. MMWR Recomm Rep. 2002;51:1–45
  51. Larson EL, Eke PI, Laughon BE. Efficacy of alcohol-based hand rinses under frequent-use conditions. Antimicrob Agents Chemother. 1986;30:542–544
  52. Larson EL, Aiello AE, Bastyr J, et al. Assessment of two hand hygiene regimens for intensive care unit personnel. Crit Care Med. 2001;29:944–951
  53. Picheansathian W. A systematic review on the effectiveness of alcohol-based solutions for hand hygiene. Int J Nurs Pract. 2004;10:3–9
  54. Widmer AF. Replace hand washing with use of a waterless alcohol hand rub?. Clin Infect Dis. 2000;31:136–143
  55. Boyce JM. Scientific basis for handwashing with alcohol and other waterless antiseptic agents. In:  Rutala WA editors. Disinfection, sterilization and antisepsis: principles and practices in healthcare facilities. Washington, DC: Association for Professionals in Infection Control and Epidemiology; 2001;p. 140–151
  56. Graham M. Frequency and duration of handwashing in an intensive care unit. Am J Infect Control. 1990;18:77–81
  57. Pittet D, Allegranzi B, Storr J, et al. Infection control as a major WHO priority for developing countries. J Hosp Infect. 2008;68:285–292
  58. Rotter ML. Hand washing and hand disinfection. In:  Mayhall G editors. Hospital epidemiology and infection control. Baltimore: Williams & Wilkins; 1996;p. 1052–1068
  59. McFarland LV, Mulligan ME, Kwok RY, Stamm WE. Nosocomial acquisition of Clostridium difficile infection. N Engl J Med. 1989;320:204–210
  60. Bettin K, Clabots C, Mathie P, Willard K, Gerding DN. Effectiveness of liquid soap vs chlorhexidine gluconate for the removal of Clostridium difficile from bare hands and gloved hands. Infect Control Hosp Epidemiol. 1994;15:697–702
  61. Hubner NO, Kampf G, Löffler H, Kramer A. Effect of a 1min hand wash on the bactericidal efficacy of consecutive surgical hand disinfection with standard alcohols and on skin hydration. Int J Hyg Environ Health. 2006;209:285–291
  62. Clabots CR, Gerding SJ, Olson MM, Peterson LR, Gerding DN. Detection of asymptomatic Clostridium difficile carriage by an alcohol shock procedure. J Clin Microbiol. 1989;27:2386–2387
  63. Wullt M, Odenholt I, Walder M. Activity of three disinfectants and acidified nitrite against Clostridium difficile spores. Infect Control Hosp Epidemiol. 2003;24:765–768
  64. McDonald LC, Owings M, Jernigan DB. Clostridium difficile infection in patients discharged from US short-stay hospitals, 1996–2003. Emerg Infect Dis. 2006;12:409–415
  65. Archibald LK, Banerjee SN, Jarvis WR. Secular trends in hospital-acquired Clostridium difficile disease in the United States, 1987–2001. J Infect Dis. 2004;189:1585–1589
  66. Muto CA, Pokrwka M, Shutt K, et al. A large outbreak of Clostridium difficile-associated disease with an unexpected proportion of deaths and colectomies at a teaching hospital following increased fluoroquinolone use. Infect Control Hosp Epidemiol. 2005;26:273–280
  67. Boyce JM, Ligi C, Kohan C, Dumigan D, Havill NL. Lack of association between the increased incidence of Clostridium difficile-associated disease and the increasing use of alcohol-based hand rubs. Infect Control Hosp Epidemiol. 2006;27:479–483
  68. Vernaz N, Sax H, Pittet D, Bonnabry P, Schrenzel J, Harbarth S. Temporal effects of antibiotic use and hand rub consumption on the incidence of MRSA and Clostridium difficile. J Antimicrob Chemother. 2008;62:601–617
  69. Kaier K, Hagist C, Frank U, Conrad A, Meyer E. Two time-series analyses of the impact of antibiotic consumption and alcohol-based hand disinfection on the incidences of nosocomial methicillin-resistant Staphylococcus aureus infection and Clostridium difficile infection. Infect Control Hosp Epidemiol. 2008;29:593–599

PII: S0195-6701(09)00186-8

doi:10.1016/j.jhin.2009.04.019

Journal of Hospital Infection
Volume 73, Issue 4 , Pages 305-315, December 2009