|Year : 2010 | Volume
| Issue : 2 | Page : 100-106
Prevention and control of health care-associated infections through improved hand hygiene
E Mathai1, B Allegranzi1, C Kilpatrick1, D Pittet2
1 World Health Organization Patient Safety, World Health Organization, Avenue Appia, 1211 Geneva 27, Switzerland
2 World Health Organization Patient Safety, World Health Organization, Avenue Appia, 1211 Geneva 27; Infection Control Programme University of Geneva Hospitals and Faculty of Medicine, 4 Rue Gabrielle Perret-Gentil, Geneva, Switzerland
|Date of Submission||15-Feb-2010|
|Date of Acceptance||02-Mar-2010|
|Date of Web Publication||16-Apr-2010|
World Health Organization Patient Safety, World Health Organization, Avenue Appia, 1211 Geneva 27; Infection Control Programme University of Geneva Hospitals and Faculty of Medicine, 4 Rue Gabrielle Perret-Gentil, Geneva
Source of Support: None, Conflict of Interest: None
Determined actions are required to address the burden due to health care-associated infections worldwide and improve patient safety. Improving hand hygiene among health care workers is an essential intervention to achieve these goals. The World Health Organization (WHO) First Global Patient Safety Challenge, Clean Care is Safer Care, pledged to tackle the problem of health care-associated infection at its launch in 2005 and has elaborated a comprehensive set of guidelines for use in both developed and developing countries worldwide. The final version of the WHO Guidelines on Hand Hygiene in Health Care was issued in March 2009 and includes recommendations on indications, techniques, and products for hand hygiene. In this review, we discuss the role of hands in the transmission of health care-associated infection, the benefits of improved compliance with hand hygiene, and the recommendations, implementation strategies and tools recommended by WHO. We also stress the need for action to increase the pace with which these recommendations are implemented in facilities across India.
Keywords: Alcohol-based hand rubs, guidelines, hand hygiene, health care-associated infection, international health, intervention, prevention and control of infection
|How to cite this article:|
Mathai E, Allegranzi B, Kilpatrick C, Pittet D. Prevention and control of health care-associated infections through improved hand hygiene. Indian J Med Microbiol 2010;28:100-6
|How to cite this URL:|
Mathai E, Allegranzi B, Kilpatrick C, Pittet D. Prevention and control of health care-associated infections through improved hand hygiene. Indian J Med Microbiol [serial online] 2010 [cited 2015 Dec 1];28:100-6. Available from: http://www.ijmm.org/text.asp?2010/28/2/100/62483
| ~ Introduction|| |
Estimates indicate that hundreds of millions of patients suffer from health care-associated infections (HCAI) each year worldwide.  The most common HCAI are urinary tract, surgical site, lower respiratory tract and bloodstream infections. In addition to increased morbidity and mortality, these infections contribute significantly to the financial burden borne by patients, their families, and the health care system. The increasing incidence of HCAI with antimicrobial-resistant bacteria further complicates the issue. Although the risk of acquiring these infections exists worldwide, the risk and impact are likely to be higher in resource-constrained settings where compliance with standard recommendations for infection prevention and control is generally not optimal. The capacity of existing systems to respond to the increased demand associated with HCAI, such as length of stay, cost, effective antimicrobial therapy and advanced technology is also limited in such settings.
A large proportion of HCAI is preventable. In October 2004, heads of governmental agencies, policy-makers, and patient groups came together for the first time from all corners of the globe to advance the patient safety goal of "First, do no harm" and reduce the adverse health and social consequences of unsafe health care. The World Health Organization (WHO) contributes to this effort through the Patient Safety Programme with its First Global Patient Safety Challenge "Clean Care is Safer Care" (CCiSC), launched in 2005 and dedicated to the prevention of HCAI. One of the important recommendations for reducing HCAI is compliance with hand hygiene practices. Although maintaining hand hygiene is a simple act that should be routine behaviour among health care workers (HCWs), data from studies worldwide show that compliance is universally low. , To achieve sustained improvement in hand hygiene, determined efforts are required at the point of care. For this reason, the core focus of CCiSC is on improving hand hygiene in health care and one of its main outputs, the WHO Guidelines on Hand Hygiene in Health Care,  (available at: http://whqlibdoc.who.int/publications/2009/9789241597906_eng.pdf; accessed 6 November 2009) provides detailed recommendations and tools (available at: http://www.who.int/gpsc/5may/tools/en/index.html; accessed 6 November 2009) to facilitate change.
This review considers the role of hands in transmission of HCAI and examines the recommendations and methods for improving compliance with hand hygiene during routine patient care activities in health-care facilities. It also highlights some of the tools developed by CCiSC to achieve improved compliance. Aspects of surgical hand preparation are not addressed.
| ~ Hands and HCAI|| |
Many studies confirm that pathogens implicated in HCAI can be isolated from the normal intact skin of upper extremities, including hands. ,, The resident flora of the skin consist mostly of bacteria that reside long-term under the superficial cells of the stratum corneum and on the surface of the skin. Staphylococcus epidermidis is the predominant species and oxacillin resistance is very high, especially among those carried by HCWs. , Transient flora include bacteria, viruses and fungi on the skin surfaces that are acquired through direct skin contact or contact with contaminated environmental surfaces. These can be recovered from the skin only for short periods of time and do not usually multiply on skin surfaces. However, they can become temporarily resident and also multiply. , Microorganisms that are part of the transient flora are most commonly associated with HCAI and are readily removed during routine hand hygiene procedures. ,
The rate of hand contamination among HCWs varies. S. aureus, including methicillin-resistant S. aureus (MRSA), is among the most frequent causes of HCAI and often colonizes hands. Different studies show hand contamination rates of 10-78% among HCWs with S. aureus.  Similarly, very high rates of contamination are documented for other Gram-positive bacteria such as vancomycin-resistant enterococci (VRE) and Clostridium difficile, as well as several well-known HCAI causing Gram-negative bacilli. Depending on the species, the duration for which these can persist varies and can be for several hours on the skin, and even for weeks and months on environmental surfaces. 
Five sequential steps can be considered important in the transmission of nosocomial pathogens from one patient to another through HCWs' hands: ,
HCAI caused by bacteria, viruses and fungi transmitted through contaminated hands are well documented in the literature. , There are also reports of infections transmitted to patients from sources outside the hospital through the hands of HCWs. An example is an outbreak of postoperative Serrata marcescens infections traced to a jar of contaminated exfoliant cream in a nurse's home. 
- Microorganisms are present on the patient's skin or shed onto clothing, bed linen and other inanimate objects in the immediate patient surroundings. ,, The bacterial species, counts, and the risk of colonisation can vary. Patients with diabetes, housed in long-term care facilities, undergoing dialysis, or with chronic dermatitis, are more likely to carry S. aureus. ,,
- Organisms are transferred to the hands of HCWs. ,,,, The risk of hand contamination varies and may depend on the type and duration of patient care activity and locations within the facility, such as the intensive care unit (ICU) or general ward. In one study, direct patient contact and respiratory care were most likely to contaminate the fingers of caregivers. Gram-negative bacilli accounted for 15% and S. aureus for 11% of isolates.  Glove contamination rates are similar to hand contamination rates and the use of gloves do not fully protect the hands from contamination.
- Organisms survive for at least several minutes on HCWs' hands. Studies demonstrate that several species can survive for longer periods. 
- Hands remain contaminated because hand hygiene is inadequate or omitted. ,
- The contaminated hands of the HCW come into direct contact with another patient or with an inanimate object that will come into direct contact with the patient. ,, Transmissibility depends on several factors including the type of destination surface, microorganism, size of the inoculum, and moisture level of the surface and hands. ,,
| ~ Preventing Transmission of Nosocomial Pathogens Through Hands|| |
The link between hand hygiene and the prevention of the spread of disease has been established only in the last 200 years. As early as 1847, Ignaz Semmelweis in Vienna, Austria, documented evidence to demonstrate the effect of hand hygiene in preventing nosocomial infections.  Semmelweis was a house officer at one of the two obstetric clinics at the Vienna General Hospital and observed that maternal mortality rates were much higher in the clinic where doctors delivered the women than in the one where midwives were in charge of births. He also noted that doctors and medical students often came directly to the labour room after having performed autopsies and retained a disagreeable odour on their hands, despite hand washing with soap and water. He hypothesised that "cadaverous particles" were transmitted by the hands of doctors and students, thus causing puerperal fever, and he recommended hand antisepsis with chlorinated lime solution, particularly after leaving the autopsy room. Following the implementation of this measure, the mortality rate dropped dramatically in the clinic most affected.
Studies during the past few decades clearly show that a variety of hand hygiene methods reduce bacterial load significantly and prevent cross-transmission and HCAI. ,, An early prospective controlled trial  demonstrated that infants cared for by nurses who did not wash their hands after handling an index infant colonized with S. aureus acquired the organism significantly more often and more rapidly than those cared for by nurses who used hexachlorophene to clean their hands between infant contacts, thus providing compelling evidence for efforts to improve hand hygiene. Other studies have confirmed this finding in a variety of health care settings. ,,,, There is also good evidence to show that hand hygiene reduces the risk of transmission of infections in the community. ,,
A few studies do not show a direct correlation between improved hand hygiene and reduction in HCAI.  Reduction in HCAI without a significant increase in hand hygiene compliance is also documented.  Some of these findings are related to differences in measurements,  given that there was no universally accepted method of measuring compliance or HCAI until recently.  This greatly affected comparability of data. Most studies neither address the quality of products used for hand hygiene nor compliance with recommended procedures for performing hand hygiene, but simply observe whether hand hygiene was performed for certain indications. There are also differences in the indications for hand hygiene in different studies.  Another factor to be considered while evaluating reports is that hand hygiene may not be implemented as a single intervention to reduce HCAI. In this scenario, models using available data demonstrate that interventions aimed at hand hygiene improvement can significantly contribute to reducing HCAI. ,
Most guidelines for infection prevention and control include appropriate hand hygiene as a key recommendation. The methods used for hand hygiene during routine patient care include hand washing with plain or antimicrobial soap (the latter referred to as hygienic hand wash) and hand rubbing with alcohol-based or other antiseptic-based hand rubs.  Different terms such as hand disinfection, hand antisepsis, hygienic hand antisepsis, or hygienic hand rubbing, among others, are used in the literature to name these procedures.
The recommendations in the WHO Guidelines on Hand Hygiene in Health Care are as follows:  "wash hands with soap and water when visibly dirty or visibly soiled with blood or other body fluids or after using the toilet; if exposure to potential spore-forming pathogens is strongly suspected or proven, including outbreaks of Clostridium difficile, hand washing with soap and water is the preferred means; use an alcohol-based hand rub as the preferred means for routine hand antisepsis if hands are not visibly soiled; if alcohol-based hand rub is not obtainable, wash hands with soap and water".
| ~ Products for Hand Hygiene|| |
With the exception of non-medicated soap, every new formulation for hand antisepsis, should be tested to demonstrate that it has superior antimicrobial efficacy over plain soap or meets an agreed performance standard. , In Europe, the most commonly used methods are those of the European Committee for Standardisation (Comité Européen de Normalisation, CEN). In the USA and Canada, these formulations are regulated by the Food and Drug Administration (FDA) and Health Canada, respectively, which refer to the standards of ASTM International, originally known as the American Society for Testing and Materials (ASTM). All these tests have limitations. Using a well-designed protocol that closely simulates the recommended field use of the formulation is most likely to yield useful data on its potential to interrupt transmission of pathogens by hands in healthcare settings.
Hand hygiene has been performed traditionally by hand washing and is effective for the mechanical removal of extraneous matter. Plain soaps that are detergent-based have minimal microbicidal activity and may fail to fully remove pathogens from hands. , Soaps may also be associated with skin irritation and dryness and can occasionally become contaminated with bacteria. , Detergent formulations with additional antiseptics, such as chlorhexidine gluconate and triclosan (medicated soaps), are also widely available for hand washing with the former formulations being most common. These may be more effective than plain soap, but the activity depends on the chemical, concentrations used, duration of exposure, temperature, or the presence of organic matter. , Most of these are relatively safe for use in hand hygiene products, but there is variability in the rapidity with which they act and in residual action. There are also growing concerns on resistance development and cross-resistance to antibiotics. 
Alcohol-based formulations containing ethanol, isopropanol, n-propanol or a combination of these, are used for handrubbing. Alcohols have germicidal activity against vegetative bacteria, Mycobacterium tuberculosis, a variety of fungi, and several enveloped viruses, and are most effective at concentrations of 75-85%. , However, they are ineffective against spores, protozoan cysts, and less effective against some viruses. Although there is evidence to show that alcohol has action against rotavirus, adenovirus, and polio virus, the activity depends on the alcohol, concentration, time of exposure, viral load and presence of proteinaceous materials.  A study using influenza A virus H1N1 showed alcohol-based handrubs and handwashing to be highly effective in eliminating the virus.  Compliance is much higher with alcohol-based hand rubs  and the risk of acquired resistance is insignificant.  The action of alcohol is rapid, but there is little residual activity.  For routine patient care, rapid action is critical, persisting action being significantly more important for surgical hand preparation.  Alcohols are not cleansing agents and, therefore, they are not recommended when hands are visibly soiled. Whether adding antiseptics such as chlorhexidine gluconate to alcohol has additional benefit in terms of clinical effectiveness remains to be further determined. , Recent reports suggest than hand rubs other than alcohol can also be effective in eliminating microorganisms.  More data are required before conclusions can be drawn.
Comparing different products available for hand hygiene is not easy for several reasons. These include the plethora of products available in different countries, variations in efficacy depending on test conditions, such as concentration, temperature, presence of organic matter, inherent problems associated with all current testing methods, and lack of universally-applied test methodologies. Although there is evidence that some medicated soaps have better activity as compared to plain soap, their superiority for routine hand hygiene has yet to be proved. Evidence is steadily accumulating to establish that alcohol-based hand rubbing is more effective in reducing bacterial load on hands, cross-transmission and HCAI, than hand washing with either plain or antimicrobial-containing soap. ,, However, as mentioned above, there are specific situations where hand washing is more effective and therefore recommended.
While selecting a product,  one needs to consider efficacy, cost, aesthetic preferences, such as colour, texture, and fragrance, and practical issues such as availability, ease of dispensing, or preventing contamination. Skin tolerance by HCWs is a critical consideration since these products will have to be used multiple times each day and several formulations have the potential to cause skin irritation and allergy. For hand rubs, drying time is also an important factor that affects compliance. Although some reports suggest that alcohol-based rinses may be more effective than gels,  compliance should receive high consideration while choosing a product. WHO recommends two alcohol-based hand rub formulations that can be produced locally [Table 1] .  Involving HCWs in the choice of the product and pilot testing for acceptability is recommended since it can increase compliance.
| ~ Hand Hygiene: How and When?|| |
The purpose of hand hygiene is to prevent colonisation and infection in the patient, colonisation and infection in the HCW, and contamination of the environment. Therefore, an opportunity for hand hygiene arises every time that there is a possibility of microorganism transfer from one skin or inanimate surface to another surface.  To facilitate easy identification of opportunities for hand hygiene by HCWs and to meet the needs for training, compliance measurements, and comparable performance reporting, CCiSC recommends a "five moments" approach.  This is a simple concept which encompasses the different activities in the complex sequence of care and can be summarized as follows: 1) Before touching a patient; 2) Before a clean/aseptic procedure; 3) After body fluid exposure risk; 4) After touching a patient; and 5) After touching patient surroundings [Figure 1]. The detailed recommendations can be found in the WHO Guidelines on Hand Hygiene in Health Care as well as in the original publication. 
Adherence to recommended techniques, such as the volume of product to be used, hand surfaces to clean, and duration for hand washing and hand rubbing, are important for effectiveness.  [Figure 2] illustrates the recommended technique for hand rubbing using an alcohol-based formulation that requires 20 to 30 seconds. Hand washing with soap and water requires additional steps (rinsing and drying) and usually takes between 40 and 60 to 90 seconds for completion. Because wet hands can readily acquire and spread microorganisms, proper drying of hands  and single-use towels are necessary. Care must be taken to avoid recontamination of hands while drying and turning off the tap. Soap and alcohol-based rubs are not recommended for concomitant use.
| ~ Implementation Strategies|| |
Improving hand hygiene depends on system and behavioural changes. Taking into account interventions required for a change in behaviour, CCiSC recommends a multimodal strategy and has developed a Guide to Implementation and a range of tools to facilitate (available at: http://www.who.int/gpsc/5may/tools/en/index.html; none accessed 6 November 2009) improvement in hand hygiene in health care facilities worldwide. The five essential elements of the strategy are: a) system change, including availability of alcohol-based hand rub at the point of patient care and access to a continuous safe water supply, soap and towels; b) training and education of HCWs; c) monitoring of hand hygiene practices and performance feedback; d) reminders in the workplace; and e) the creation of a safety culture with the participation of both individual HCWs and senior hospital managers. Five sequential steps are recommended for implementation of these strategies. (Available at: http://www.who.int/gpsc/5may/Guide_to_Implementation.pdf;none ; accessed 6 November 2009). These are facility preparedness - readiness for action; baseline evaluation - establishing the current situation regarding hand hygiene compliance; implementation - introducing the improvement activities; follow-up evaluation - evaluating the implementation impact; and an action planning and review cycle - developing a plan for a minimum of the following five years. These recommendations can be modified and adapted to suit requirements and resources at each facility.
Measuring compliance with hand hygiene is essential to understand the current situation, to facilitate change, and to measure the impact of interventions.  There are different methods recommended and these include direct observation, automated monitoring systems, product consumption, and self reporting by HCWs. Monitoring HCAI rates is necessary to understand the impact of hand hygiene improvement. Uniformity in the methods used for these measurements is essential for comparability. The method recommended by WHO for measuring compliance (Sax H, Allegranzi B, Chraiti M-N, Boyce J, Larson E, Pittet D. The World Health Organization hand hygiene observation method. Am J Infect Control 2009; 37:827-34: now published) and the related tools can be obtained from the web site. Available at: : http://www.who.int/gpsc/5may/tools/evaluation_feedback/en/index.htmlnone . Accessed 6 November 2009.
| ~ Need for Action|| |
HCAI rates remain high despite an increase in awareness and actions to reduce these infections, partially due to increasingly complex health care interventions. The momentum created by CCiSC is significant and reports from around the world show an upward trend in compliance with hand hygiene. [Allegranzi B, Sax H, Bengaly L, Richet H, Minta DK, Chraiti M-N, et al. Successful implementation of the WHO hand hygiene improvement strategy in a referral hospital in Mali, Africa. Infect Control Hosp Epidemiol 2010; 31:133-41. - now published] Health care facilities in different parts of the world have already adopted hand hygiene as an essential intervention for reducing HCAI. Several countries have initiated nationally coordinated activities (available at: http://www.who.int/gpsc/national_campaigns/en/; none accessed 6 November 2009) to promote hand hygiene in health care, but the question of sustainability remains.
Although coordinated efforts exist in India to promote hand hygiene in communities and schools to reduce the burden of diarrhoea and other infections, there is a paucity of information on activities to promote hand hygiene in health-care facilities. There is also a lack of satisfactory information from India on HCAI in general. Sporadic reports document the role of hands in spreading infection and isolated efforts at improving hand hygiene across the country. ,,,
It is necessary to increase the pace of activities to reduce HCAI and to effectively engage millions of HCWs in different types of health-care facilities in this effort. The Director General of Health Services of India confirmed his resolve to promote activities at a national level to reduce HCAI by signing a commitment with CCiSC on July 14 2006. (Available at: http://www.who.int/patientsafety/events/06/statements/India_pledge.pdf.none Accessed 6 November 2009). "Developing or enhancing ongoing campaigns at national or sub-national levels to promote and improve hand hygiene among health care providers" is among the activities committed to through this pledge. Professional societies have an important role to play in bringing this commitment into practice through advocacy and contributions to the required technical expertise.
| ~ Conclusion|| |
Although considerable progress is being made in health care facilities worldwide to reduce HCAI by adherence to hand hygiene recommendations, the need to further scale up and ensure that it becomes an essential element of quality of care is evident. Lack of comparable and good quality data is one concern to be addressed. There are also several questions to be answered, especially in areas related to interventions, implementation strategies in different parts of the world, and measurements to evaluate impact. National, facility and individual level commitment, co-operation, and actions are required to address these deficiencies and to make sustainable improvements. Promoting the application of the "5 moments" at the point of care [Figure 1] is one simple step that each HCW and health-care facility can act on now [Table 2].
| ~ Acknowledgments|| |
The authors thank all members of the Infection Control Programme, University of Geneva Hospitals, and team members of the WHO First Global Patient Safety Challenge "Clean Care is Safer Care", and Rosemary Sudan for expert editorial assistance.
| ~ References|| |
|1.||WHO Guidelines on Hand Hygiene in Health Care. (World Health Organization, Geneva) 2009. Available from: http://whqlibdoc.who.int/publications/2009/9789241597906_eng.pdf . [last accessed on 2009 Nov 9]. |
|2.||Consensus Measurement in Hand Hygiene Project Expert Advisory Panel. Measuring hand hygiene adherence: overcoming the challenges. Oakbrook Terrace, IL: The Joint Commission; 2009. |
|3.||Kampf G, Kramer A. Epidemiologic background of hand hygiene and evaluation of the most important agents for scrubs and rubs. Clin Microbiol Rev 2004;17:863-93. |
|4.||Larson E. Skin hygiene and infection prevention: more of the same or different approaches? Clin Infect Dis 1999;29:1287-94. |
|5.||Coello R, Jiménez J, García M, Arroyo P, Minguez D, Fernández C, et al. Prospective study of infection, colonization and carriage of methicillin-resistant Staphylococcus aureus in an outbreak affecting 990 patients. Eur J Clin Microbiol Infect Dis 1994;13:74-81. |
|6.||Pittet D, Allegranzi B, Sax H, Dharan S, Pessoa-Silva C, Donaldson L, et al. Evidence-based model for hand transmission during patient care and the role of improved practices. Lancet Infect Dis 2006;6:641-52. |
|7.||Duckro AN, Blom DW, Lyle EA, Weinstein RA, Hayden MK. Transfer of vancomycin-resistant enterococci via health care worker hands. Arch Intern Med 2005;165:302-7. |
|8.||Lin YT, Wang CT, Chiang BL. Role of bacterial pathogens in atopic dermatitis. Clin Rev Allergy Immunol 2007;33:167-77. |
|9.||Johnson LB, Jose J, Yousif F, Pawlak J, Saravolatz LD. Prevalence of colonization with community-associated methicillin-resistant Staphylococcus aureus among end-stage renal disease patients and healthcare workers. Infect Control Hosp Epidemiol 2009;30:4-8. |
|10.||Reighard A, Diekema D, Wibbenmeyer L, Ward M, Herwaldt L. Staphylococcus aureus nasal colonization and colonization or infection at other body sites in patients on a burn trauma unit. Infect Control Hosp Epidemiol 2009;30:721-6. |
|11.||Pessoa-Silva CL, Dharan S, Hugonnet S, Touveneau S, Posfay-Barbe K, Pfister R, et al. Dynamics of bacterial hand contamination during routine neonatal care. Infect Control Hosp Epidemiol 2004;25:192-7. |
|12.||Pittet D, Dharan S, Touveneau S, Sauvan V, Perneger T. Bacterial contamination of the hands of hospital staff during routine patient care. Arch Intern Med 1999;159:821-6. |
|13.||Larson EL, Eke PI, Wilder MP, Laughon BE. Quantity of soap as a variable in handwashing. Infect Control 1987;8:371-5. |
|14.||McNeil SA, Foster CL, Hedderwick SA, Kauffman CA. Effect of hand cleansing with antimicrobial soap or alcohol-based gel on microbial colonization of artificial fingernails worn by health care workers. Clin Infect Dis 2001;32:367-72. |
|15.||Thompson ND, Novak RT, Datta D, Cotter S, Arduino MJ, Patel PR, et al. Hepatitis C virus transmission in hemodialysis units: importance of infection control practices and aseptic technique. Infect Control Hosp Epidemiol 2009;30:900-3. |
|16.||Harrison WA, Griffith CJ, Ayers T, Michaels B. Bacterial transfer and cross-contamination potential associated with paper-towel dispensing. Am J Infect Control 2003;31:387-91. |
|17.||Nicas M, Sun G. An integrated model of infection risk in a health-care environment. Risk Anal 2006;26:1085-96. |
|18.||Sattar S, Springthorpe S, Mani S, Gallant M, Nair R, Scott E, et al. Transfer of bacteria from fabrics to hands and other fabrics: development and application of a quantitative method using Staphylococcus aureus as a model. J Appl Microbiol 2001;90:962-70. |
|19.||Passaro DJ, Waring L, Armstrong R, Bolding F, Bouvier B, Rosenberg J, et al. Postoperative Serratia marcescens wound infections traced to an out-of-hospital source. J Infect Dis 1997;175:992-5. |
|20.||Allegranzi B, Pittet D. Role of hand hygiene in healthcare-associated infection prevention. J Hosp Infect 2009;73:305-15. |
|21.||Mortimer EA Jr, Lipsitz PJ, Wolinsky E, Gonzaga AJ, Rammelkamp CH Jr. Transmission of staphylococci between newborns. Importance of the hands to personnel. Am J Dis Child 1962;104:289-95. |
|22.||Grayson ML, Jarvie LJ, Martin R, Johnson PD, Jodoin ME, McMullan C, 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;188:633-40. |
|23.||Le TA, Dibley MJ, Vo VN, 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;28:583-8. |
|24.||Pessoa-Silva CL, Hugonnet S, Pfister R, Touveneau S, Dharan S, Posfay-Barbe K, et al. Reduction of health care associated infection risk in neonates by successful hand hygiene promotion. Pediatrics 2007;120:e382-90. |
|25.||Rodríguez-Baño J, García L, Ramírez E, Martínez-Martínez L, Muniain M, Fernández-Cuenca F, et al. Long-term control of hospital-wide, endemic multidrug-resistant Acinetobacter baumannii through a comprehensive "bundle" approach. Am J Infect Control 2009;37:715-22. |
|26.||Luby SP, Agboatwalla M, Feikin DR, Painter J, Billhimer W, Altaf A, et al. Effect of handwashing on child health: a randomised controlled trial. Lancet 2005;366:225-33. |
|27.||Hammond B, Ali Y, Fendler E, Dolan M, Donovan S. Effect of hand sanitizer use on elementary school absenteeism. Am J Infect Control 2000;28:340-6. |
|28.||Meadows E, Le Saux N. A systematic review of the effectiveness of antimicrobial rinse-free hand sanitizers for prevention of illness-related absenteeism in elementary school children. BMC Public Health 2004;4:50. |
|29.||Rupp ME, Fitzgerald T, Puumala S, Anderson JR, Craig R, Iwen PC, et al. Prospective, controlled, cross-over trial of alcohol-based hand gel in critical care units. Infect Control Hosp Epidemiol 2008;29:8-15. |
|30.||Aboelela S, Stone P, Larson E. Effectiveness of bundled behavioural interventions to control healthcare-associated infections: a systematic review of the literature. J Hosp Infect 2007;66:101-8. |
|31.||Hagtvedt R, Griffin P, Keskinocak P, Roberts R. A simulation model to compare strategies for the reduction of health-care-associated infections. Interfaces 2009;39:256-69. |
|32.||McBryde E, Pettitt A, McElwain D. A stochastic mathematical model of methicillin resistant Staphylococcus aureus transmission in an intensive care unit: predicting the impact of interventions. J Theor Biol 2007;245:470-81. |
|33.||Rotter M, Sattar S, Dharan S, Allegranzi B, Mathai E, Pittet D. Methods to evaluate the microbicidal activities of hand-rub and hand-wash agents. J Hosp Infect 2009;73:191-9. |
|34.||Bottone EJ, Cheng M, Hymes S. Ineffectiveness of handwashing with lotion soap to remove nosocomial bacterial pathogens persisting on fingertips: a major link in their intrahospital spread. Infect Control Hosp Epidemiol 2004;25:262-4. |
|35.||Buffet-Bataillon S, Rabier V, Bétrémieux P, Beuchée A, Bauer M, Pladys P, et al. Outbreak of Serratia marcescens in a neonatal intensive care unit: contaminated unmedicated liquid soap and risk factors. J Hosp Infect 2009;72:17-22. |
|36.||Rabier V, Bataillon S, Jolivet-Gougeon A, Chapplain J, Beuchée A, Bétrémieux P. Hand washing soap as a source of neonatal Serratia marcescens outbreak. Acta Paediatr 2008;97:1381-5. |
|37.||Weber DJ, Rutala WA. Use of germicides in the home and the healthcare setting: is there a relationship between germicide use and antibiotic resistance? Infect Control Hosp Epidemiol 2006;27:1107-19. |
|38.||Grayson ML, Melvani S, Druce J, Barr IG, Ballard SA, Johnson PD, et al. Efficacy of soap and water and alcohol-based hand-rub preparations against live H1N1 influenza virus on the hands of human volunteers. Clin Infect Dis 2009;48:285-91. |
|39.||Souweine B, Lautrette A, Aumeran C, Bénédit M, Constantin JM, Bonnard M, et al. Comparison of acceptability, skin tolerance, and compliance between handwashing and alcohol-based handrub in ICUs: results of a multicentric study. Intensive Care Med 2009;35:1216-24. |
|40.||Rotter ML, Kampf G, Suchomel M, Kundi M. Population kinetics of the skin flora on gloved hands following surgical hand disinfection with 3 propanol-based hand rubs: a prospective, randomized, double-blind trial. Infect Control Hosp Epidemiol 2007;28:346-50. |
|41.||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 |
|42.||Nhung DT, Freydiere AM, Constant H, Falson F, Pirot F. Sustained antibacterial effect of a hand rub gel incorporating chlorhexdine-loaded nanocapsules (Nanochlorex). Int J Pharm 2007;334:166-72. |
|43.||Picheansathian W. A systematic review on the effectiveness of alcohol-based solutions for hand hygiene. Int J Nurs Pract 2004;10:3-9. |
|44.||Dharan S, Hugonnet S, Sax H, Pittet D. Comparison of waterless hand antisepsis agents at short application times: raising the flag of concern. Infect Control Hosp Epidemiol 2003;24:160-4. |
|45.||Sax H, Allegranzi B, Uçkay I, Larson E, Boyce J, Pittet D. My five moments for hand hygiene: a user-centred design approach to understand, train, monitor and report hand hygiene. J Hosp Infect 2007;67:9-21. |
|46.||Patrick DR, Findon G, Miller TE. Residual moisture determines the level of touch-contact-associated bacterial transfer following hand washing. Epidemiol Infect 1997;119:319-25. |
|47.||Chandra P, Milind K. Lapses in measures recommended for preventing hospital-acquired infection. J Hosp Infect 2001;47:218-22. |
|48.||Krishna BV, Patil AB, Chandrasekhar MR. Extended Spectrum beta Lactamase producing Klebsiella pneumoniae in neonatal intensive care unit. Indian J Pediatr 2007;74:627-30. |
|49.||Suchitra JB, Lakshmi Devi N. Impact of education on knowledge, attitudes and practices among various categories of health care workers on nosocomial infections. Indian J Med Microbiol 2007;25:181-7. [PUBMED] |
|50.||Taneja N, Das A, Raman Rao DS, Jain N, Singh M, Sharma M. Nosocomial outbreak of diarrhoea by enterotoxigenic Escherichia coli among preterm neonates in a tertiary care hospital in India: pitfalls in healthcare. J Hosp Infect 2003;53:193-7. |
[Figure 1], [Figure 2]
[Table 1], [Table 2]
|This article has been cited by|
||Hand hygiene compliance and associated factors among health care providers in Gondar University Hospital, Gondar, North West Ethiopia
| ||Nura Abdella,Mekuriaw A Tefera,Abebaw E Eredie,Timothy F Landers,Yewunetu D Malefia,Kefyalew Alene |
| ||BMC Public Health. 2014; 14(1): 96 |
||Do wheelchairs spread pathogenic bacteria within hospital walls?
| ||Avi Peretz,Anna Koiefman,Eleonora Dinisman,Diana Brodsky,Kozitta Labay |
| ||World Journal of Microbiology and Biotechnology. 2013; |
||Qualitative study on perceptions of hand hygiene among hospital staff in a rural teaching hospital in India
| ||S.C. Joshi,V. Diwan,A.J. Tamhankar,R. Joshi,H. Shah,M. Sharma,A. Pathak,R. Macaden,C. Stålsby Lundborg |
| ||Journal of Hospital Infection. 2012; 80(4): 340 |
||Delivering the infection control message: a communication challenge
| ||C. Farrugia,M.A. Borg |
| ||Journal of Hospital Infection. 2012; 80(3): 224 |
||Point-of-care hand hygiene: Preventing infection behind the curtain
| ||Anson Kendall,Timothy Landers,Jane Kirk,Elizabeth Young |
| ||American Journal of Infection Control. 2012; 40(4): S3 |
||Qualitative study on perceptions of hand hygiene among hospital staff in a rural teaching hospital in India
| || Joshi, S.C., Diwan, V., Tamhankar, A.J., Joshi, R., Shah, H., Sharma, M., Pathak, A., (...), Stålsby Lundborg, C. |
| ||Journal of Hospital Infection. 2012; 80(4): 340-344 |
||Delivering the infection control message: A communication challenge
| ||Farrugia, C., Borg, M.A. |
| ||Journal of Hospital Infection. 2012; 80(3): 224-228 |
||Hand hygiene: Back to the basics of infection control
| ||Mathur, P. |
| ||Indian Journal of Medical Research. 2011; 134(11): 611-620 |
||Heightening Residentsæ Awareness of Hand Hygiene Guidelines
| ||Sarah J. Middlemas,Monica L. Lypson |
| ||Journal of Graduate Medical Education. 2010; 2(4): 498 |