Overcoming Barriers To Hand Hygiene Compliance

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Education & TrainingOvercoming Barriers toHand Hygiene ComplianceEffects of hand hygiene on skin integrityPremiseAn important “barrier” to hand hygienecompliance is the damaged caused to the skin“barrier,” the stratum corneum.SignificancePatient SafetyHealthcare-acquired infections occur intwo million people per year in the UnitedStates and result in 80,000 deaths. 1 Theincidence of infection among intensivecare patients is one in four in industrializednations and estimated to be one in two indeveloping regions worldwide.2 Reductionand prevention of hospital-acquired infectionsis a patient safety goal and a major focus ofimprovement efforts in healthcare institutionsworldwide, particularly since about one-thirdmay be preventable3-5. Nosocomial infectionsaffect up to 26 percent of intensive carepatients.6,7 Those in the neonatal ICUs are atincreased risk of complications due to immature host defense mechanisms and infectionfrom exposure to invasive procedures.5,8In 1947, postpartum maternal mortalitywas significantly reduced after hand disinfection46MANAGING INFECTION CONTROLby Marty Visscher, PhDwith a chlorine solution between patients, an intervention thatwas more effective than soap and water washing.9 Beginning in1961, formal guidelines for hand disinfection in healthcareinstitutions have been published by agencies including the U.S.Public Health Service, the Association for Professionals inInfection Control, the Healthcare Control Practices AdvisoryCommittee, and the Centers for Disease Control and the WorldHealth Organization (WHO).10 The guidelines list the specificprocesses, frequencies, and types of products to be used forhealthcare procedures, e.g., before direct patient contact, betweenpatients, prior to catheter insertion, etc. They are based on data onthe composition of skin microbial flora in normal and healthcaresettings, the differentiation of transient and resident flora, themechanisms of contamination and transfer of flora, and thespecific organisms contributing to various infections. The colonization of normal hand skin is more than 1 x 106 colony formingunits (CFU/cm2) and range from 3.9 x 104 to 4.6 x 106 in healthcare workers.11-13 Normal resident flora are on the skin surfaceand within the top layers. They typically include Staphylococcusepidermidis, Staphylococcus hominis, other coagulase-negativestaphylococci, coryneform bacteria (corynebacteria, dermobacteria, propionibacteria, and micrococci), and sometimes fungi(Pityrosporum spp.)2 Transient flora are on the outermost layersand can multiply on the surface. Increases in bacterial counts,including potential pathogens, were found with diaper changes,skin contact and respiratory care among neonates.14Hand HygieneConsistent performance of hand hygiene procedures, e.g.,soap and water washing, use of antimicrobial scrubs, use ofhand sanitizers, is effective for preventing healthcare associatedinfections.15 Standard practice of hand hygiene is the mostimportant measure for preventing healthcare-associated infectionsin critically ill neonates.5,7,8,16-21 Hand hygiene is effective inreducing neonatal mortality.22,23 Matters of compliance are veryrelevant in ICUs because the need for frequent hand hygienecoupled with the high workload create a significant barrier togood compliance.5-7,10,17,20,21 The indications for hand hygienefrom the most recent, comprehensive guideline to assemble theevidence and address the issues on a worldwide basis, i.e.,the WHO Guidelines on Hand Hygiene in Health Care AdvancedDraft of 2006 are listed in Table 1.2May 2009

Education & TrainingHealthcare Worker SafetyA goal of the U.S. Public Health Service for 2010 is toreduce occupational skin disorders to an incidence of 46 per100,000 full-time workers.24 Occupational dermatitis representsa significant health problem with chronic discomfort and lostwork time.25 Contact dermatitis is the most common disorder,accounting for 90 percent to 95 percent of cases and of those, 80percent are the irritant type.26-28The Skin in Infection ControlThe skin serves multiple functions including barrier (towater loss, irritant exposure, light, etc.), immunosurveillance,infection control, sensation, structural support, and thermalregulation. The outermost layer, known as the stratum corneum(SC), provides a physical, mechanical and immunologicalbarrier against environmental insults. The viable epidermiscontinuously builds and replenishes the barrier. The living cellsrelease their contents to create lipid layers that assemble betweenthe cells which have flattened in shape. In this process, the cells“move up” from the lower layers and are released or shed fromthe skin surface via desquamation. The sequence is carefullyprogrammed and orchestrated through signaling mechanisms toform an incredibly thin and strong structure with that resemblesa “brick and mortar” array. Extremely large forces are requiredto destroy its integrity. Langerhans cells (antigen presentingcells) are located in the viable layer (epidermis). They are part ofthe immune system and “defend” the organism if the SC barrieris breached. The SC barrier shields the Langerhans cells fromdirect environmental exposure thereby serving an essentialfunction in infection control. Figure 1 shows the structuralfeatures of the stratum corneum and epidermis. The maintenanceof a normal, healthy intact skin barrier is essential for maximumprotection of both patients and health care workers alike.Table 1. Indications for Handwashing andHand AntisepsisA.Wash hands with soap and water when visibly dirty orcontaminated with proteinaceous material, or visiblysoiled with blood or other body fluids, or if exposureto potential spore-forming organisms is stronglysuspected or proven (IB) or after using the restroom.B.Preferably use an alcohol-based handrub for routinehand antisepsis in all other clinical situations describedin items C (1) to C (6) listed below, if hands are notvisibly soiled. Alternatively, wash hands with soapand water.C.Perform hand hygiene:1. before and after having direct contact with patients;2. after removing gloves;3. before handling an invasive device for patient care,regardless of whether or not gloves are used;4. after contact with body fluids or excretions,mucous membranes, non-intact skin, or wounddressings;5. if moving from a contaminated body site to aclean body site during patient care;6. after contact with inanimate objects (includingmedical equipment) in the immediate vicinity ofthe patient.D.Wash hands with either plain or antimicrobial soapand water or rub hands with an alcohol-based formulation before handling medication or preparing food.E.When alcohol-based handrub is already used, do notuse antimicrobial soap concomitantly.Figure 1. Structure of the EpidermisThe structure of the epidermis is shown here. It consists of twoparts. The outermost layer, known as the stratum corneum (SC),provides a physical, mechanical and immunological barrieragainst environmental insults. The viable epidermis continuouslybuilds and replenishes the barrier. The living cells release theircontents to create lipid layers that assemble between the cellswhich have flattened in shape. In this process, the cells “moveup” from the lower layers and are released or shed from theskin surface via desquamation. The Langerhans cells (antigenpresenting cells) are located in the viable layer (epidermis). Theyare part of the immune system and “defend” the organism. Themelanocytes are in the lower epidermis and produce skin pigment known as melanin. When the skin is exposed to ultravioletlight, the melanocytes release pigment to shield the livingcells of the epidermis and protect their DNA from damage. Theproduction of pigment is responsible for the “tanning” responseto sun exposure. The melanocytes work together with othercells in the epidermis to determine the skin coloration, e.g.,Caucasian, African American.May 2009MANAGING INFECTION CONTROL47

Education & TrainingFigure 2. Skin Barrier Damage: Exposure to Water and CleansersThe effects of exposure to water and cleansers (e.g., bar soaps, liquid cleansers, surfactants)on the structure and function of the skin barrier, the stratum corneum (SC), are profound. Theyinclude disruption of the lipid bilayer architecture. This disruption creates defects or “holes” inthe lipid layers. In turn, the barrier becomes more permeable, allowing irritants to penetrateinto and through the uppermost layers. As a result, irritants can reach the living cells ofthe viable epidermis to cause inflammation. The cells respond by releasing mediators ofinflammation which act on the capillaries and blood vessels of the dermis to produce visibleerythema. In addition to chemical irritants, microorganisms on the skin surface or in theenvironment can also penetrate into the upper layers.Figure 3. Skin Barrier Following DamageUnder normal conditions, the stratum corneum (SC) skin barrier is a regular arrangement offlattened cells with layers of lipid between them. The cells are connected together as shown.If the skin barrier is compromised, processes in the viable epidermis are up-regulatedto repair the damage and generate “new” stratum corneum. As a result, the SC forms tooquickly, resulting in an abnormal structure with defective architecture, compared to the SCthat is formed during the normal course of SC replacement. This SC has poor water bindingproperties leading to insufficient skin moisture. Normally, the SC cells are lost from the surfaceas individual units but when the moisture is too low, they come off as clumps of cells observedas dry scales.48MANAGING INFECTION CONTROLHand Hygiene and the SkinSkin exposure to water andcleansers (e.g., bar soaps, liquidcleansers, surfactants) and water hasprofound effects on the SC structureand function, as shown in Figure 2.They include disruption of the lipidbilayer architecture to create defectsor “holes” in the barrier. As a result,the barrier becomes more permeable,allowing irritants to penetrate into andthrough the uppermost layers (SC).The irritants can reach the livingcells of the viable epidermis to causeinflammation. The cells release mediators of inflammation which act on thecapillaries and blood vessels of thedermis to produce visible erythema. Incases of severe hand irritation, cracksor fissures (with or without bleeding)may develop indicating damage tothe dermis. In addition to chemicalirritants, microorganisms on the skinsurface or in the environment can alsopenetrate into the upper layers.The skin’s response to thesedamaging effects is immediate sincerestoration of the barrier is criticalfor survival. Processes in the viableepidermis are up-regulated to repairthe damage and generate “new” stratumcorneum. As a result, the SC formstoo quickly, i.e., hyperproliferates,resulting in a structure with defectivearchitecture, compared to the SC thatis formed during the normal courseof SC replacement. This SC has poorwater binding properties leading toinsufficient skin moisture and inadequate desquamation29-42 Normally,the SC cells are lost from the surfaceas individual units but when themoisture is too low, they come offas clumps of cells observed as dryscales, as shown in Figure 3. Undernormal conditions, the cells movefrom the bottom of the SC to berelease over 14 days.43 However, thetime is shorter when there is chronicexposure to irritants such as cleansersand surfactants.44May 2009

Education & TrainingCompliance and Healthcare Worker SkinDespite the importance, compliance rates are only 30percent to 57 percent10 and some improvement programs havebeen unsuccessful.45-47 The primary reason for compliancefailure is skin irritation and the deleterious effects of repeatedexposure to products and procedures.19 Up to 85 percent ofnurses described histories of skin problems and 25 percentreported symptoms of dermatitis.10 Fifty-five percent ofinpatient nurses and 65 percent in ICU had observable handdermatitis.48 ICD may predispose development of allergiccontact dermatitis.49 Overall, the rate of occupational dermatitisis unchanged from the 28 percent reported in 1980.50Healthcare workers (HCWs) often work 12-hour shifts fortwo to three consecutive days followed by three to four days oftime off. Others may work consecutive eight hour shifts. Thenumber of hand hygiene procedures per shift depends uponthe patient load, the severity of illness, the complexity ofcare-giving procedures, etc. In an ICU setting, the requiredhand hygiene can occur four to five times per hour or 50 per 12hour shift, leading to 150 events over three consecutive shifts.These levels of exposure to water, cleansers, and alcohol-basedhand rubs are substantially higher than those used in humanstudies to evaluate formulation effects on skin. Skin assessmentmethods often use repetitive exposure under an occlusive patchon the forearm, rather than the hand. Commonly, the studies areon people with healthy, undamaged skin, a context that isdifferent from the actual HCW setting. It is difficult to conducta clinically realistic study without disrupting normal practice inthe clinical area. As a result, there are relatively few publishedaccounts about various aspects of hand skin condition amongHCWs under typical clinical conditions.17,51-58Effects of Hand Hygiene Procedures on Skin Integrity inHealthcare WorkersThe deleterious effects of repetitive hand cleansing/disinfection procedures on skin condition are well known.37,59-63We studied the effects of hand hygiene procedures on the handskin condition of HCWs in an intensive care setting beginning in2004.64,65 To get a complete picture, we measured the skindryness and erythema under several conditions: a) at thebeginning and end of two to three consecutive work shifts to seethe effects of high frequency exposure to products and procedures, b) at the end of the shifts and after three to four days off tosee what happened after the high frequency of hand hygiene wasstopped for a period, c) during spring time conditions (warmertemperatures, higher humidity), d) during winter conditions,e) with various hand hygiene products, and f) after treatmentwith skin lotion. Hand hygiene products included liquidproducts for soap and water washing and alcohol-based handrubs. We compared HCWs to a similar age group of people whodid not work in a wet environment. Here are the key findings:50MANAGING INFECTION CONTROL1.2.3.4.5.6.Compared to a group of non-HCW control subjects,HCW hand skin was appreciably more compromised.Skin dryness and erythema were higher for the knucklesthan the back of the hands.Dryness grades were significantly higher during thewinter for the knuckles and dorsum regions, indicatinggreater skin barrier damage during winter. The HCWsthemselves reported poorer condition during winter thanin spring.The changes in skin irritation during work were greaterin winter than in spring.Knuckle erythema increased over the cycle in bothseasons (Figure 4).Knuckle erythema decreased during time off in spring,but continued to increase during time away in winter.The skin was dry and erythematous at the start of a workcycle, after several days away from work. The apparentworsening of the skin condition during the time away fromwork most likely is due to continuing effects of exposure.Importantly, the skin barrier does not recover from thedamage during the time off period. HCWs come back to workwith a compromised skin barrier.Figure 4. Effect of High Frequency HandHygiene ExposureThis figure shows the average change in knuckle erythemascore among HCWs who took part in the spring (54 subjects) andwinter (60 subjects) trials. Knuckle erythema increased duringthe work cycle of two to three consecutive 12 hour shifts duringboth seasons (blue bars). During the time away from work, theerythema decreased slightly during spring, indicating improvementin skin condition. In winter, however, skin erythema increased(worsened) during the time off work (red bars).May 2009

Education & TrainingA striking feature of irritant hand dermatitis has beenthe high levels of erythema/inflammation, particularly atthe knuckles. Visual scores were not different for springand winter conditions. Clear determination of the extent(i.e., degrees of severity) is difficult. To quantify theerythema component of skin condition, we used highresolution digital photography with controlled lighting.Next, the image red channel is separated for analysis. Theexcess erythema is the quantity of red that is above (orgreater than) the value of the mean plus one standarddeviation. Figure 5 shows an example. The clinical image(digital photograph) is on the left (A) and the processedimage showing excess erythema (in red) is on the right(B). In essence, excess erythema is the amount of theimage that is much higher than normal. The process allowsus to assign a number to this amount. The images in Figure6 show additional examples to the locations of excesserythema on actual HCW hands. Excess erythema valueswere substantially higher in winter than in spring for thesame HCWs.Regardless of season, high frequency hand hygienelead to chronic, unresolved skin irritation in nearly allhealthcare workers. Levels of inflammation are particularlyhigh in winter conditions.Regardless of season,high frequencyhand hygiene leadto chronic, unresolvedskin irritationin nearly allhealthcare workers.Figure 6. Examples of Excess Erythema in HealthcareWorkersSubject 2 Excess ErythemaASubject 3 Excess ErythemaBFigure 5. High Resolution Digital Photography andImage AnalysisSubject 1 Normal imageshowing clinical conditionASubject 1 Processed imageshowing excess erythemaBSubject 4 Excess ErythemaCThe figure shows a clinical digital photograph (A) of asubject. The regions of erythema and dryness are clearlyvisible in the original image. Figure B shows the processedred channel image with the areas of excess erythema inred. Excess erythema is anything greater than the meanplus one standard deviation of pixels in the red channelimage. This provides a way to quantify the highest levels ofhand erythema.52MANAGING INFECTION CONTROLThe figure shows threeexamples of the redchannel from clinicaldigital photographs withthe excess erythema shownin red. The locations ofthe excess erythema ofteninvolve the knuckle regionsas shown in A, B and C.Figures A and B haveinvolvement on the dorsalregions. Figures B and Cshow areas on the fingers.May 2009

Education & TrainingImplications for Infection ControlChronic hand skin compromise has significantimplications for infection control. A damaged barrieris more susceptible to penetration by environmentalinsults, including microorganisms. As skin damageincreased, the total bacteria counts on the hand werehigher.66 Irritated hands had significantly more colonyforming units (CFUs) than non-irritated hands.67The frequency of colonization with Staphylococcushominis, Staphylococcus aureus, gram-negativebacteria, enterococci, and Candida was higher onnurses with damaged hands.12 Damaged hand skin inHCWs was associated with higher frequencies ofStaphylococcus aureus, gram-negative bacteria andyeast.68 Soap and water washing was ineffective forreducing microorganism contamination of damagedhands.67 The findings suggest that compliance withrequired procedures for hand hygiene results indamaged skin and an increased bacterial load (Figure7). What are the implications for the management ofnosocomial infections?Figure 7. Effects of Hand HygieneThe goal of hand hygiene practice is to reduce the incidenceof nosocomial infections and strong evidence supportsthe efficacy. One of the effects of compliance is skinbarrier compromise, e.g., inflammation, fissuring, dryness, etc. Damaged skin has higher levels of microflorawhich may increase the risk of infection for patients andhealthcare workers.Impact of Alcohol Hand RubsOne of the most important interventions fornosocomial infections has been the addition of alcoholbased hand rubs. Their use leads to improved skincondition compared to soap and water washing17,52,56,60,62In a study among nurses, an alcohol hand rinseproduced significantly better decontamination than54MANAGING INFECTION CONTROLFigure 8. Effect of Hand Rubs on Hand Hygiene Compliancesoap and water, which caused an increase in skin dryness anderythema.66 Protective effects have been reported.69,70 Some HCWsreport stinging or adverse reactions from alcohol rubs, perhaps indicatingthe presence of skin damage.53,71 A change back to soap and waterwashing is likely to worsen skin condition. Inclusion of hydratingingredients, e.g., emollients, improves the effects of hand rubs on skin.7274 Compliance improvement programs emphasize using alcohol rubswhenever indicated.5-7,10,75,76 The significant increase in hand hygienecompliance from 48 percent in 1994 to 66 percent in 1997 (teachinghospital, Geneva) was attributed to the use of hand rubs.77 Figure 8 showsthe total percent compliance and the contributions from soap and waterwashing and use of hand rubs. The percent of hand hygiene events fromhand rubs increased over the period while the proportion from soap andwater was relatively constant. Net, the use of alcohol-based hand rubshas had a positive effect on compliance and on skin condition (i.e.,improvements). However, our HCW research was conducted after theimplementation of alcohol-based hand rubs and clearly demonstratedsignificant, chronic skin barrier compromise.Impact of Hand Lotions/CreamsHealthcare institutions are to provide HCWs with lotions or creamsto minimize the skin damage due to hand hygiene procedures. Thepositive effects of lotion on skin condition have been described.78 Lotionapplication resulted in more rapid SC barrier repair following damagewith surfactant compared to an untreated control.79 An oil-based lotion(mineral oil, petrolatum, lanolin, etc) led to signficantly better skinscores than one based on glycerin (glycerin, isopropyl myristate, stearicacid, etc.) over four weeks in workers with severe hand irritation.18 Apetrolatum-based lotion (Locobase: mineral oil, petrolatum, etc) reducedirritation versus the untreated control (crossover design).78 Decreaseddryness and increased hydration versus no treatment were seen for acream (Baktolan: water, liquid paraffinum, petrolatum, liquid paraffin,wax, etc.) (4x daily, 2 weeks).80 However, lotions containing petrolatumand/or mineral oil are not compatible with gloves since their integrityMay 2009

Education & Trainingcan be compromised. Therefore, they are not a viable choice for usein healthcare institutions. At the present time, the literature onthe effects of glove-compatible lotion/cream treatments for irritant handdermatitis in the HCW clinical settings is limited.Table 2. Strategies to Manage Skin Barrier Compromise Use Use alcohol hand rubs whenever possible: Reduce water and cleanser exposure. Use hand rubs containing emollients to help keep the skinhydrated. Provide a skin lotion or cream that will: To hydrate the stratum corneum and provide moisture tohelp the skin recovery from damage (dryness, erythema); Be compatible with gloves, i.e., free of petrolatum andmineral oil; Have an acceptable feel on the skin; Not interfere with HCW dexterity for bedside procedures,i.e., not slippery, greasy, tacky, etc., to avoid having to“wash it off.” Skin creams and lotions may: Create a “protective” layer on the surface; Reduce water loss from the damaged skin; Protect the skin during the next cleanser and water exposure.cleansers containing surfactants:With low irritation potential, i.e., “minimally damage”;That are easily rinsed from the skin surface;With low protein binding ability;That are present in the “minimum” amounts for cleaning.Figure 9. Hand Hygiene Compliance: Future PotentialLooking to the future, this figure portrays an increase in total hand hygienecompliance that is a step change above the current highest reported levels.It postulates that the addition of an intensive lotion treatment as part of thenormal HCW regimen of hand skin care may be the way to achieve “cleanhands without compromise.”56MANAGING INFECTION CONTROLFuture PerspectiveChronic exposure to irritants, e.g., repetitive handhygiene procedures, has profound effects on the skinbarrier, in some cases for weeks to months aftertreatment has stopped.81 Recovery to the normal,healthy state depends on multiple factors includingthe inherent irritancy of the ingredients. In total,the research results emphasize the importance ofproviding hand hygiene products to minimize irritantdermatitis and maintain an effective skin barrier.Equally important are the use of protective skin carepractices (mild cleansers, lotions, avoidance of harshchemicals) both at work and during time away.There is a substantial need for practices andproducts that disinfect the skin surface withoutcompromising the integrity of the skin barrier. Thecurrent understanding of the causes of skin barrierdamage among healthcare workers and the factorsgoverning severity suggests strategies for minimizingthe compromise and maximizing recovery when itoccurs, as shown in Table 2.Treatments can vary substantially in their effectson irritation and skin barrier integrity and, therefore,in the utility for chronic irritant dermatitis. Anexamination of long term moisturizer applicationand found differing effects on skin, some positiveand some negative.82 Specific moisturizers may notbe effective against all irritants and formulationsshould be targeted at the causes of irritation andbarrier compromise.83Currently, there are few studies of the effects ofintensive use of skin lotions or creams (glovecompatible, CHG compatible) to protect the skin andto aid in the repair of barrier damage in HCWs.However, such a practice is expected to substantiallyimpact and improve hand hygiene compliance.Looking to the future, the graph in Figure 9 portraysan increase in total hand hygiene compliance that is astep change above the current highest reportedlevels. It postulates that the addition of an intensivelotion treatment as part of the normal HCW regimenof hand skin care may be the way to achieve “cleanhands without compromise.”Finally, the research agenda outlined in theWHO guideline states the following as prioritiespertaining to HCW skin condition:2 Determine the most suitable hand hygiene agents; Study the systematic replacement of conventionalhandwashing by handrubbing; Develop hand hygiene agents with low skinirritancy potential;May 2009

Education & Training Study the possible advantages and eventual interactionof hand care lotions, creams, and other barriers to helpminimize the potential irritation associated with handhygiene agents.19.20.21.Progress against this important agenda will requirecollaborations among people and institutions with expertise ininfection control, public policy, healthcare quality and processimprovement science, skin researchers, and representatives ofthe skin care industry. 7.18.58Improving hand hygiene: A guide for improving practices among healthcare workers. Accessed 03/22/09.Who Guidelines on Hand Hygiene in Health Care (Advanced Draft).Accessed March 23, 2009.Aiello AE, Larson EL. Causal inference: the case of hygiene and health.Am J Infect Control. Dec 2002;30(8):503-511.Hilburn J, Hammond BS, Fendler EJ, Groziak PA. Use of alcohol handsanitizer as an infection control strategy in an acute care facility. Am JInfect Control. Apr 2003;31(2):109-116.Lam BC, Lee J, Lau YL. Hand hygiene practices in a neonatal intensivecare unit: a multimodal intervention and impact on nosocomial infection. Pediatrics. Nov 2004;114(5):e565-571.Creedon SA. Healthcare Workers’ Hand Decontamination Practices:Compliance with Recommended Guidelines. Journal of AdvancedNursing. 2005;51(3):208-216.Hugonnet S, Perneger, T.V., & Pittet, D. Alcohol-Based HandrubImproves Compliance with Hand Hygiene in Intensive Care Units.Archives of Internal Medicine. 2002;162(9):1037-1043.Won SP, Chou, H.C., Hsieh, W.S., Chen, C.Y., Huang, S.M., Tsou, K.I.,& Tsao, P.N. Handwashing Program for the Prevention of NosocomialInfections in a Neonatal Intensive Care Unit. Infection Control andHospital Epidemiology. 2004;25(9):742-746.Rotter M. Hand washing and hand disinfection [Chapter 87]. In:Mayhall CG, ed. Hospital epidemiology and infection control. 2nd ed.Philadelphia: Lippincott Williams & Wilkins; 1999.Boyce JM, Pittet D. Guideline for Hand Hygiene in Health-CareSettings. Recommendations of the Healthcare Infection ControlPractices Advisory Committee and the HIPAC/SHEA/APIC/IDSAHand Hygiene Task Force. Am J Infect Control. Dec 2002;30(8):S1-46.Larson E. Effects of handwashing agent, handwashing frequency, andclinical area on hand flora. Am J Infect Control. Apr 1984;12(2):76-82.Larson EL, Hughes CA, Pyrek JD, Sparks SM, Cagatay EU, BartkusJM. Changes in bacterial flora associated with skin damage on hands ofhealth care personnel. Am J Infect Control. Oct 1998;26(5):513-521.Maki DG. Control of colonization and transmission of pathogenicbacteria in the hospital. Ann Intern Med. Nov 1978;89(5 Pt 2Suppl):777-780.Pessoa-Silva CL, Dharan S, Hugonnet S, et al. Dynamics of bacterialhand contamination during routine neonatal care. Infect Control HospEpidemiol. Mar 2004;25(3):192-197.Aiello AE, Larson EL. What is the evidence for a causal link betweenhygiene and infections? Lancet Infect Dis. Feb 2002;2(2):103-110.Karabey S, Ay P, Derbentli S, Nakipoglu Y, Esen F. Handwashing frequencies in an intensive care unit. J Hosp Infect. Jan 2002;50(1):36-41.Larson EL, Aiello AE, Bastyr J, et al. Assessment of two hand hygieneregimens for intensive care unit personnel. Crit Care Med. May2001;29(5):944-951.McCormick RD, Buchman TL, Maki DG. Double-blind, randomizedtrial of scheduled use of a novel barrier cream and an oil-containinglotion for protecting the hands of health care workers. Am J InfectControl. Aug 2000;

the composition of skin microbial flora in normal and healthcare settings, the differentiation of transient and resident flora, the mechanisms of contamination and transfer of flora, and the specific organisms contributing to various infections. The colo-nization of normal hand skin is more than 1 x 106 colony forming

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