International Journal of Surgery (2006) 4, 53e65

www.int-journal-surgery.com

REVIEW

Hand hygiene: An evidence-based review for

surgeons
C.R. Nicolay

Academic Surgical Unit, 10th Floor QEQM Wing, St Marys Hospital, Praed St, London W2 1NY, UK

KEYWORDS Abstract This review of the literature discusses the scientific evidence behind
Hand hygiene; using different hand hygiene agents on the surgical ward, and in theatre for
Handwashing; preoperative disinfection. It considers the mechanism of action of the agents and
Infection; their effectiveness against different pathogens, as well as possible future agents,
Alcohol; and how they are tested. It addresses problems such as the poor compliance with
Handrub hand hygiene guidelines by healthcare workers (especially doctors) and investigates
what can be done to improve compliance. Finally, it demonstrates the reduction in
hospital acquired infection (HAI) rate that can be achieved by improving hand
hygiene compliance, and shows that the savings associated with this easily
outweigh the cost.
2005 Surgical Associates Ltd. Published by Elsevier Ltd. All rights reserved.

Introduction simply washing their hands between contact with

It has been clear since the 1840s when both Oliver
Holmes1 and Ignaz Semmelweis2 independently
reported the contagious nature of puerperal fever,
that healthcare workers should cleanse their hands
before contact with patients. Semmelweis insisted
that doctors who had performed autopsies must
wash their hands before delivering a baby, and in
one step he reduced mortality from streptococcal
sepsis by nearly 90%. Sixteen decades later, many
studies have confirmed that by healthcare workers
E-mail address: christopher.nicolay@doctors.org.uk
patients, the hospital acquired infection rate can
be reduced.3 However, adherence by doctors to
hand hygiene guidelines is often unacceptably
poor at below 50%,4e9 and is usually poorer than
nurses and other healthcare workers.
Approximately 10% of hospital inpatients are
suffering from an infection acquired following
their admission,10,11 and Department of Health
guidance suggests that approximately 30% of these
HAIs could be avoided by better application of
existing knowledge and realistic infection control
practices.12 The 70% of HAIs that are not prevent-
able demonstrates the scale of endogenous in-
fection compared with cross-infection. Hospital

1743-9191/$ - see front matter 2005 Surgical Associates Ltd. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.ijsu.2005.06.002
54
acquired infections with antibiotic-resistant bac-
teria such as methicillin-resistant Staphylococcus
aureus (MRSA) are not uncommon and can be
difficult and expensive to treat.
According to a study funded by the Department
of Health,13 adult inpatients in common specialties
who develop a hospital acquired infection remain
in hospital 2.5 times longer, incur hospital costs
nearly 3 times higher, and incur higher general
practitioner, district nurse, and hospital costs
after discharge from hospital than uninfected
patients. Even after adjustment for various factors
including age, diagnosis and the number of co-
morbidities, patients with an HAI are 7 times more
likely to die in hospital than uninfected patients. It
has been estimated that 5000 deaths a year in the
UK are primarily attributable to HAI (1% of all
deaths), and in a further 15,000 deaths, HAI may
be a significant contributor. The estimated mean
additional hospital cost of an HAI in a surgical
patient is about 4000. An extrapolation of figures
to NHS hospitals in England suggests a total addi-
tional annual cost of HAI in adult patients of all
specialties to be nearly 1000 million.
A brief summary of part of the National Institute
of Clinical Excellence (NICE) evidence-based clin-
ical guidelines for the prevention of hospital
acquired infection14 is as follows:
1. Hands must be decontaminated immediately
before each and every episode of direct
patient contact or care and after any activity
or contact that potentially results in hands
becoming contaminated.
2. Hands that are visibly soiled or potentially
grossly contaminated with dirt or organic
material, must be washed with liquid soap
and water.
3. Hands must be decontaminated, preferably
with an alcohol-based handrub unless hands
are visibly soiled, between caring for different
patients and between different care activities
for the same patient.
4. An effective handwashing technique involves
three stages: preparation, washing and rinsing,
and drying. Preparation requires wetting hands
under tepid running water before applying
liquid soap or an antimicrobial preparation.
The handwash solution must come into contact
with all of the surfaces of the hand. The hands
must be rubbed together vigorously for a min-
imum of 10e15 s, paying particular attention to
the tips of the fingers, the thumbs and the
areas between the fingers. Hands should be
rinsed thoroughly before drying with good
quality paper towels.
C.R. Nicolay
With hospital hygiene and the superbug MRSA
often in the media, there is a vast amount of
literature published on this broad topic, and much
research forming the basis of hospital hand hy-
giene guidelines worldwide. John Boyce, MD and
Didier Pittet, MD published a comprehensive 48-
page report on the subject15 and this review
summarises the parts of the literature particularly
relevant to the field of surgery, together with more
recent work published.
Normal bacterial skin flora
It is important to appreciate normal bacterial skin
flora, before considering the options for hand
hygiene. Normal human skin is colonised by bac-
teria, but to different extents depending on the
site, for example: 100 ! 104 CFU (colony forming
units) cm2 on the scalp, 50 ! 104 CFU cm2 in the
axillae, 4 ! 104 CFU cm2 on the abdomen, and
1 ! 104 CFU cm2 on the forearm.16 The two major
groups of bacteria on the skin are those that
normally reside on it (resident flora), and contam-
inants (transient flora). Transient flora such as
S. aureus, gram-negative bacteria and yeast in-
habit the superficial layers of the skin and are
those acquired by doctors during patient contact,
or by contact with contaminated surfaces. These
are the bacteria that are most responsible for
hospital acquired infections and are the ones
that are more easily removed by hand hygiene.
Resident flora such as coagulase-negative staphy-
lococci (e.g. Staphylococcus epidermidis) and
Corynebacteria are attached to deeper layers of
the skin and are less easy to remove by hand
hygiene and also less likely to cause HAIs. However,
low virulence resident flora can cause huge
complications for patients, for example in ortho-
paedic wound infections.
Review of hand hygiene agents
Plain soap
The term soap is a class name for the sodium and
potassium salts of stearic acid and other fatty
acids, and they are available in different forms,
commonly bar or liquid. They have little if any
antibacterial activity but may remove loose tran-
sient flora. It has been shown that a 1 min hand-
wash with plain soap reduces the artificial bacterial
contamination of hands by a log10 reduction factor
of only 2.8, compared with a value of 4.6 for the
alcohol propan-2-ol (60% v/v).17 In a small study,
Hand hygiene: An evidence-based review
plain soap handwashing failed to prevent gram-
negative bacterial transfer to a catheter in 11 of 12
experiments,18 and it can even carry the risk of
spreading bacterial contamination.19,42
Over time, soap usage can make the skins pH
more alkaline, and cause significant skin dryness
and irritation, as measured by self-assessment,
external visual assessment and epidermal water
content measurement (skin capacitance).20 This
effect can be reduced by adding emollients to
preparations or by using hand creams. The combi-
nation of dryness and removing the natural de-
fensive acidic pH of the skin can lead to easier
colonisation with potential pathogens.
Alcohols
Alcohol-based hand hygiene products contain ei-
ther ethanol, propan-2-ol (isopropanol, isopropyl
alcohol), propan-1-ol (n-propanol, n-propyl alco-
hol), or combinations thereof (Fig. 1). They have
antimicrobial activity due to their ability to de-
nature proteins,21 and concentrations of 60e95%
are most effective, with higher concentrations
being less potent because water is needed for
the denaturation process.21
In vitro, alcohols have powerful antibacterial
activity against gram-positive and gram-negative
bacteria including antibiotic-resistant organisms
such as MRSA, Mycobacterium tuberculosis and
certain fungi.21e23 Enveloped lipophilic viruses
such as HSV, HIV, RSV and influenza virus are
also susceptible.21,24,25 Hepatitis B and hepatitis
C viruses are less susceptible but destroyed by
60e70% alcohol.26 Alcohols have very poor in vitro
activity against bacterial spores, non-enveloped
viruses and protozoan cysts.
In vivo, alcohols effectively reduce bacterial
counts on hands22 and the log10 reduction factor of
test bacteria from artificially contaminated hands
averages 4.6 after a 1-min application of 60%
Figure 1 From left to right: ethanol, propan-1-ol and propan-2-ol molecular structures.
55
propan-2-ol17 (the European EN 1500 reference
standard for alcohol-based handrub products).
Although rapidly bactericidal when applied to
skin the effect is short-lived and alcohol gels
unfortunately lack the important characteristic
of residual activity,31 but re-growth does occur
more slowly after use.27 Despite very poor in vitro
activity against non-enveloped viruses, in vivo
activity has been shown, with 70% propan-2-ol
and 70% ethanol being more effective than both
soap and other antiseptic agents in reducing
rotavirus titers (a common cause of infantile
gastroenteritis) on fingerpads.28,29
Although alcohol use is not recommended when
hands are visibly soiled or potentially grossly
contaminated with dirt or organic material, when
small amounts of proteinaceous material such as
blood is present, ethanol and propan-2-ol may
reduce bacterial counts more than plain soap or
antiseptic agents.30
Alcohols have been shown to prevent the transfer
of pathogens from healthcare workers. Gram-
negative bacilli were transferred from a colonised
patients skin to a piece of catheter material via the
hands of nurses in only 2 out of 12 occasions after
alcohol handrub, compared with 11 out of 12
occasions after handwashing with soap and water.18
Alcohol-based products are more effective for
standard hand hygiene by healthcare workers than
plain soap or antimicrobial soaps.18,31e42 In nearly
all trials, alcohol reduced antibacterial counts on
hands more than washing with plain soap or
detergents containing povidoneeiodine, 4% chlo-
rhexidine, or triclosan alone. Importantly, looking
at antibiotic-resistant organisms, alcohol-based
products reduced the number of pathogens
recovered from the hands of healthcare workers
more effectively than soap and water.43,44
The efficacy of alcohol-based products is influ-
enced by several factors including the amount of
alcohol used, the concentration, the time contact
56
lasts for, the type of alcohol and whether hands
are wet or not. For example, applying 1 ml of
alcohol is much less effective than using 3 ml.45
Frequent use of alcohol-based formulations can
cause skin drying unless other substances such as
glycerol and emollients, etc. are added. Interest-
ingly, and even more in the favour of alcohol use,
alcohol-based products containing emollients
cause significantly less skin irritation than soaps
or antimicrobial detergents tested.20,42,46
Chlorhexidine
Chlorhexidine gluconate is a cationic bisbiguanide
developed in the UK in the 1950s (Fig. 2) and is
found in antiseptic solutions in different concen-
trations e.g. Hibiscrub
and Hibisol
, as well as
other products such as dental mouthwashes.
It is antibacterial due to its ability to attach to
and disrupt cytoplasmic membranes leading to cell
content precipitation,47 but it has a slower imme-
diate activity than alcohols. It has good activity
against gram-positive bacteria, but less against
gram-negative and fungi. Chlorhexidine in alcohol
has been shown to have better activity against
MRSA in vitro than both aqueous chlorhexidine and
povidoneeiodine.48,49 It has minimal activity
against tubercle bacilli and it is not sporicidal. It
also has in vitro activity against enveloped viruses
such as HSV, HIV, CMV, RSV and influenza, but less
activity against non-enveloped viruses.
As chlorhexidine is a cation, its activity is
reduced by natural soaps, inorganic anions, non-
ionic surfactants and hand creams containing
anionic emulsifying agents.50 Aqueous or detergent
formulations containing 0.5% or 0.75% chlorhexi-
Figure 2 Chlorhexidine (free base) molecular structure.
C.R. Nicolay
dine are more effective than plain soap but less
effective than 4% chlorhexidine gluconate.
Importantly, unlike alcohol, chlorhexidine has
substantial residual activity,31,51,52 and so addition
of low concentrations (0.5e1%) to alcohol-based
preparations gives better residual activity than
alcohol alone.
Chlorhexidine is safe to use53 with minimal skin
absorption. Contact with eyes in concentrations
greater than 1% must be avoided as it can cause
conjunctivitis and severe corneal damage. Its
ototoxicity prevents its use in surgery of the inner
or middle ear, and contact with brain and menin-
ges should also be avoided.
Iodine
Iodine has been used as an antiseptic since the
1800s but because of skin irritation and discolour-
ing, it has been mostly replaced by iodophors
(iodine, iodide or triiodide together with a high
molecular weight polymer carrier) as the active
component in antiseptics. Iodine rapidly pene-
trates the cell wall of bacteria and forms com-
plexes with amino acids and unsaturated fatty
acids leading to disrupted protein synthesis and
cell membranes.
The amount of free molecular iodine present
determines the level of antimicrobial activity,
for example 10% povidoneeiodine formulations
contain 1% available iodine giving a 1 ppm free
iodine concentration.54 The combination with var-
ious polymer carriers increases iodine solubility,
reduces skin irritation and promotes sustained
iodine release. These polymers are often polyvinyl
pyrrolidone (povidone) (Fig. 3) and ethoxylated
nonionic detergents (poloxamers).
Hand hygiene: An evidence-based review
* triclosan binding to the active site of enoylacyl
* carrier protein reductase, an enzyme that is
I I
N type II fatty acid synthase systems.58,59
O Triclosan has a broad range of antimicrobial
n cantly greater activity against gram-positive or-
Figure 3 Povidoneeiodine molecular structure.
Iodine and iodophors have antibacterial action
against gram-positive, gram-negative bacteria and
mycobacteria, viruses and fungi, but at the con-
centrations used, they are usually not sporicidal.
In vivo studies have shown that they reduce the
number of viable organisms recovered from the
hands of personnel.37,41,44 The antibacterial activ-
ity is significantly reduced if organic material is
present such as blood or sputum.55 Future applica-
tions of povidoneeiodine include MRSA eradication
from nasal mucosa and other mucous mem-
branes, and treatment for herpes simplex and
Chlamydia infections.56
Iodophors cause less skin irritation and fewer
allergic reactions than iodine but more irritant con-
tact dermatitis than other antiseptics commonly
used today.19
Triclosan
Triclosan (2,4,4#-trichloro-2#-hydroxydiphenyl ether)
is a nonionic colourless substance developed in the
1960s and introduced into soaps and other prod-
ucts such as washing-up liquid, mouthwash and
toothpaste (Fig. 4). Concentrations of 0.2e2% have
antimicrobial activity by entering bacterial cells
and affecting RNA, fatty acid and protein synthe-
sis.57 More recent research suggests this is due to
Figure 4 Triclosan molecular structure.
57
important for completing cycles of elongation in
activity but is often bacteriostatic. It has signifi-
ganisms, particularly MRSA60 (introducing triclosan
preparations eliminated MRSA outbreaks in two
independent neonatal units61,62) than gram-nega-
tive and has reasonable activity against mycobac-
teria and Candida spp. In several studies, however,
log10 reductions of bacterial counts on hands after
washing with triclosan have been poorer than
after chlorhexidine, iodophors or alcohol-based
products.31,63
Future agents
Clearly, the search for the optimum hand hygiene
agent is still underway. With such factors as skin pH,
skin irritation, allergy, effective concentration,
interaction with other substances, e.g. organic
matter, and human preference such as ease of
rinsing, odour, etc., it is a difficult challenge. A
recent study looking at the effectiveness of rubbing
hands with a 4% w/w hypochlorite solution until the
hands are slippery (about 5 min), as recommended
by Semmelweis showed that it was 30 times more
effective than a 1-min rub with 60% propan-2-ol.64 It
is, however, often irritating to the skin, has a strong
odour, and compliance is already poor without
introducing a 5-min washing regimen.
Future products are likely to be combinations of
existing substances at different concentrations or
the combination of novel compounds with existing
products to optimise their activity, for example
improving the residual antimicrobial activity of
alcohols. A new preparation that has persistent
antimicrobial activity on surfaces and human skin
has been created by adding silver-containing poly-
mers to an ethanol carrier e Surfacine
. Micro-
organisms contacting this intelligent coating
accumulate silver until their toxicity threshold is
exceeded, and they eventually lyse and detach
from the surface.65
Research must still continue because just as
strains of antibiotic-resistant bacteria emerge,
resistance to antiseptic agents could become
a problem in the future. Strains of S. aureus that
demonstrate increased resistance to chlorhexidine
and triclosan have already been isolated. The
future environmental effects of rinsing thousands
of litres of these agents into the water supply also
need to be borne in mind.
58
Testing hand hygiene substances e EN
1499 and EN 1500
EN 1499 is the European standard by which
antiseptic liquid soaps must demonstrate efficacy
under practical conditions compared with the
reference, plain soap, tested on Escherichia coli
K12 (NTCC 10538). The product should be signifi-
cantly more effective than the reference soap. EN
1500 is the standard by which products for hygienic
hand disinfection such as hand rinses or gels must
demonstrate efficacy under practical conditions in
comparison with the reference, propan-2-ol (60%
v/v) tested on E. coli K12 (NTCC 10538). The
product should be significantly more effective than
this reference alcohol.17
These test protocols involve a crossover design
with 12 to 15 volunteers (not doctors or nurses)
using the hand hygiene product for 1 min. This is
despite the fact that numerous observational
studies show that doctors and other healthcare
workers only spend between 7 and 24 s washing
their hands.15 Indeed, the NICE guidelines them-
selves state that hands must be rubbed together
vigorously for a minimum of 10 to 15 s.14 Protocols
fail to use protein contamination of the hands that
can interact with the agents, and also the bacte-
rial skin flora of doctors hands may be very
different to that of volunteers. These shortcom-
ings in testing unfortunately mean that there is
little data on the efficacy of these products under
the conditions in which they will actually be used.
This problem was reported in the Lancet in 2002,
with no alcohol gel tested meeting EN 1500
requirements within 30 s of application.17 In fact,
the 30-s efficacy of most alcohol gels is closer to
a simple handwash with soap than to the reference
hand disinfection, i.e. only a log10 reduction factor
of 2.8, rather than 4.6. Sterillium
gel was the only
alcohol gel that passed EN 1500 within 30 s.
Technique is also an important variable in de-
termining the effectiveness of hand hygiene
products (Fig. 5). A study published in 2004
demonstrated that the mean log10 reduction in
healthcare workers using alcohol-based handrub
was only 2.0, with 25% achieving less than 1.1.66
Years of experience was the single most important
factor predicting antimicrobial activity, demon-
strating the importance of technique and senior
staff leading by example and how training should
be given before switching policies from handwash-
ing to alcohol handrub.
The fact remains though that it is not really
known what log10 reduction in hand bacterial
colonisation is needed to prevent the transmission
C.R. Nicolay
of bacteria responsible for HAIs. The most power-
ful evidence promoting the use of different agents
does not come from laboratory testing and the
counting of colony forming units on agar plates,
but rather from an observed fall in the HAI rate
after their introduction and use on the ward.
Preoperative hand disinfection
Lister recommended the application of carbolic
acid (phenol) to the hands of surgeons in the 1800s
and since then the preoperative ritual of washing
hands and forearms with an antiseptic has been
a common practice, with a presumed 100% com-
pliance (unlike hand hygiene on the ward). No
randomised controlled trials have ever taken place
to show that surgical infection rates are reduced
by using an antiseptic agent rather than plain soap.
However, there is evidence that the bacteria on
the hands of surgeons can cause wound infections
if introduced into the operative field during sur-
gery. A single strain of S. epidermidis caused an
outbreak of postoperative wound infections and
endocarditis during a 6-month period and was
traced back to the hands of a single cardiac
surgeon.67 Also, rapid bacterial growth occurs
under surgical gloves if plain soap is used, but
growth is slower after using an antiseptic68 (per-
haps gloves internally impregnated with an anti-
bacterial coating would be a cost-effective
solution). Reducing the resident skin flora on the
surgeons hands for the duration of the procedure
reduces the risk of contamination if gloves become
punctured during surgery. When vascular surgeons
who normally used an antiseptic began using plain
soap instead, at least one outbreak of surgical site
infection occurred.69
Preoperative antiseptic preparations are selected
for their ability to reduce the number of bacteria
on hands immediately after washing, after wear-
ing gloves for 6 h (persistence) and after multiple
applications over five days (cumulative activity).
They also need to be non-irritating and have
broad-spectrum activity.
The most effective agents for reducing bacterial
counts immediately after hand disinfection are
formulations containing 60e95% alcohol alone or
50e95% when combined with chlorhexidine gluco-
nate. These are followed by, in order of decreasing
activity, chlorhexidine gluconate, iodophors, tri-
closan, and plain soap.70e74
Persistence, however, is a very important virtue
in an antiseptic, and one that alcohols lack,
although bacteria appear to grow more slowly on
Hand hygiene: An evidence-based review
Figure 5 Effective hand hygiene technique. Based on procedure described by Ayliffe GAJ, Babb JR, Quoraishi AH.
J Clin Pathol. 1978;31(10):923e8. Images produced by author.
the hands after alcohol use, and counts after
wearing gloves for between 1 and 3 h rarely
exceed pre-disinfection values. A recent study
showed that a 61% ethanol preparation did not
achieve adequate persistent activity at 6 h after
use.75 The addition of 0.5% or 1% chlorhexidine
gluconate to alcohol preparations, however, pro-
duces an antiseptic with persistence that has
equalled or exceeded that of 2% or 4% chlorhex-
idine gluconate, the agent with best persistence.
The next greatest persistent antibacterial activity
is found with triclosan, then iodophors.52,74,76,77
Hexachlorophene has not been discussed as it is
absorbed into the blood with repeated use, so
seldom used for surgical hand hygiene.
Duration of preoperative hand disinfection
Disinfection for 10 min preoperatively often leads
to skin damage, and 5 min of equivalent activity
reduces bacterial counts as effectively, or even
more effectively.78,79 Studies have shown that a
2 or 3 min regime reduces bacterial counts to
acceptable levels.77,80,81
Based on the characteristics of the antiseptic
substances discussed already, however (immediate
activity, persistence and cumulative activity), it
would seem sensible that perhaps the actual
products used rather than the length of time spent
scrubbing would be a more sensible avenue to
explore. Alcohols have the optimum immediate
59
antibacterial effect, and chlorhexidine gluconate
the optimum persistent effect, so a combination of
the two, or a two-stage disinfection regime would
seem a better option than washing for endless
minutes with povidoneeiodine. Indeed, an initial
1e2 min wash with 4% chlorhexidine gluconate or
povidoneeiodine followed by the application of an
alcohol-based product has been shown to be as
effective as a 5-min regime with an antiseptic.51,82
Sponge and brush?
Some surgical preoperative protocols require sur-
geons to scrub with a brush, but this can lead to
skin damage and result in increased shedding of
bacteria from the hands.83 Several studies indicate
that neither a brush nor a sponge is necessary to
reduce bacterial counts, especially when alcohol-
based products are used.46,75,76,78,84 Indeed, one
study showed that using 1% chlorhexidine with 61%
ethanol without scrubbing or using water produced
significantly greater microbial reduction on the
hands of volunteers than using 4% chlorhexidine
with a scrub brush in 2e3-min surgical scrubs.75
Compliance with hand hygiene
guidelines
Compliance of healthcare workers to recommen-
ded hand hygiene guidelines is notoriously poor,
60
with a baseline ranging from 5% to 81%, mean
40%.15 However, the definitions and criteria used
and the methods of collecting data vary widely
between studies and most of them have been
carried out in intensive care units (ICUs), which
are probably not representative of behaviour else-
where in the hospital. Improved compliance after
different interventions has been reported, but
most studies have short follow-up periods so long-
lasting effects are unknown. This is probably partly
because of the high turnover of staff rotating jobs
and hospitals in the medical profession.
In a large hospital wide survey of hand hygiene
practices, 2834 opportunities for hand hygiene
were observed, with an average compliance of
48%.85 Compliance was greatest with nurses and at
weekends rather than a weekday. Noncompliance
was greatest in intensive care units compared with
medical wards, and when intensity of patient care
was high. There have been several other observa-
tional studies that have determined the risk
factors for noncompliance (Table 1).9,85e87
Improving compliance with hand
hygiene guidelines
Since a substantial proportion of HAIs result from
cross-infection, and transmission of microorgan-
isms by the hands of healthcare workers is recog-
nized as the main route of spread,88 it is essential
to implement changes to improve compliance.
From the list of risk factors above, one common
factor is clear e lack of time for hand hygiene. In
one study in ICU, it took nurses an average of 62 s
to leave a patients bedside, walk to a sink, wash
their hands and return to the patient.89 If alcohol-
Table 1 Risk factors for noncompliance to hand hygiene guidelines
Observed risk factors
 Being a doctor (rather than nurse)
 Being a nursing assistant (rather than a nurse)
 Being male
 Working in ICU
 Working on a weekday
 Activities with high risk of cross-contamination
 Wearing gloves or gowns
 Higher number of hand hygiene
opportunities per hour of patient care
C.R. Nicolay
based handrub dispensers are placed at each
patients bedside or carried on each person as
a small clip-on dispenser, however, a significant
amount of time can be saved. In addition to ease
and quickness of use, alcohol gels, when used
properly, act faster and irritate hands less than
plain soap or antiseptic agents. They were also
used in the only programme that has shown
a sustained improvement in hand hygiene compli-
ance combined with a fall in HAI rate.90
If a hand hygiene agent is introduced in the
future with better residual activity than those
available now, it may no longer become necessary
to disinfect hands as often and compliance may
increase and guidelines may change. Expecting
nurses to disinfect their hands 20 times per day
for example may be more acceptable and achiev-
able than perhaps 60 or 80 times per day.
A small study in the UK91 looked at changing
hand hygiene behaviour by educating patients, and
involving them to ask all healthcare workers who
were going to have direct contact them Did you
wash your hands?, based on the American Partners
in Your Care programme.92 This empowers pa-
tients with responsibility for their care and in-
creased soap usage and handwashings by an
average of 50%. Interestingly, but perhaps not
unpredictably, all patients asked nurses but only
35% asked doctors. Of course, for this to be
effective patients need to be well enough to be
alert and able to understand and speak English.
Considering the breadth of factors, both behav-
ioural and institutional interfering with hand
hygiene compliance, clearly a solution to this
problem will involve intervention at a personal,
and at an institutional level. Regular education
demonstrating correct hand hygiene technique and
Self-reported risk factors
 Skin irritation
 Inaccessible supplies
 Too busy or lack of time
 Inconveniently located sinks
 Insufficient number of sinks
 Low risk of acquiring infection from patient
 High workload and understaffing
 Interference with patienteworker relationship
 Patient needs perceived as priority
 Wearing gloves
 Forgetfulness
 Ignorance of or disagreement with guidelines
 Lack of scientific evidence for the impact
of hand hygiene on HAI rates
Hand hygiene: An evidence-based review 61

the scientific evidence behind the benefits of hand
hygiene is important. Encouragement from seniors,
and senior staff leading by example on ward rounds
would help to promote good hand hygiene behav-
iour. A system of continually published cycles of
audit looking at both hand hygiene compliance and
hospital acquired infection rate with feedback to
individual wards would create an environment
where people are constantly aware of infection
control.
Impact of improved hand hygiene
on HAI rate
The lack of scientific evidence showing that im-
proved hand hygiene leads to a reduction in HAI is
cited as a reason why some healthcare workers are
not compliant with hand hygiene guidelines. Of
seven hospital-based studies, most demonstrated
a temporal relationship between improved hand
hygiene and lower HAI rates (Table 2).
In 1977, an ICU-based study93 showed that
the introduction of routine handwashing by staff
before moving from one patient to the next was
associated with a significant and sustained re-
duction in the number of patients colonised or
infected with Klebsiella spp. A different study in
a neonatal ICU (NICU) showed the elimination of
endemic MRSA after the introduction of 1% triclo-
san w/v for hand hygiene, with all other infection
control measures remaining in place.61 Compared
with the previous 12 months, fewer antibiotics
were prescribed and fewer hospital acquired in-
fections were recorded (p ! 0.05).
In 2000, a study at the University of Geneva
Hospital demonstrated the effectiveness of a hos-
pital wide, longstanding programme to promote
hand hygiene.90 This was achieved with posters,
feedback meetings, and bedside and pocket alco-
hol handrub dispensers, and HAI rates, attack rates
of MRSA cross-transmission and alcoholic handrub
consumption were measured. Hand hygiene com-
pliance improved from 48% in 1994 to 66% in 1997
(p ! 0.001), and although handwashing with soap
and water remained constant, frequency of hand
disinfection increased (p ! 0.001). Hand hygiene
improved significantly among nurses and nursing
assistants but still remained poor amongst doctors.
Alcohol handrub consumption increased from 3.5

Table 2 Association between improved hand hygiene compliance and HAI rate
Year Site Intervention Results Follow-up
1977 ICU93 Introduction of handwashing Reduction in Klebsiella spp. 2 years
between patients HAI rate
1989 ICU94 6-week trial each of 10% 50% reduction in HAI rate with 18 weeks
povidoneeiodine vs 4% 10% povidone & 4% aqueous
aqueous chlorhexidine vs soap chlorhexidine vs soap.
1992 ICU95 Prospective multiple crossover Chlorhexidine use reduced the 8 months
trial comparing chlorhexidine HAI rate more effectively than
with 60% propan-2-ol and soap 60% propan-2-ol and soap, partly
explained by better compliance
with chlorhexidine.
1994 NICU61 Introduction of triclosan 1% w/v MRSA eliminated. A$17,000 saved 1 year
from reduction in vancomycin use.
1995 Newborn After an MRSA skin infection MRSA eliminated. 3.5 years
nursery62 outbreak, aggressive infection
control measures instituted including
changing plain soap to 0.3% triclosan.
2000 ICU96 Intervention with multiple Reduction in VRE infection, 6 months
components designed to increase no change in MRSA incidence.
handwashing with plain soap,
compared with control hospital.
2000 Hospital-wide90 Hand hygiene promotion with Hand hygiene compliance 5 years
posters, feedback meetings, and increased from 48% to 66%, and
bedside and pocket alcohol significant reduction in HAI rate
dispensers. and MRSA incidence.
NICU Z neonatal ICU.
62
to 15.4 l per 1000 patient-days (p ! 0.001), and
during the same period HAI prevalence decreased
41% from 16.9% in 1994 to 9.9% in 1998 (p Z 0.04),
and MRSA rates decreased 57% from 2.16 to 0.93
episodes per 10,000 patient-days, (p Z 0.001).
Even more impressively, annual incidence of MRSA
bacteraemia decreased 68% from 0.74 to 0.24
episodes per 10,000 patient-days (p ! 0.001).
The cost of hand hygiene
The financial cost of hand hygiene products used in
hospitals is an important consideration, and in
a study in 1999 a 450-bed community teaching
hospital in America spent US$22,000 on plain soap,
2% chlorhexidine preparations, and alcohol han-
drub.97 Compared with liquid soap, the equivalent
amount of 2% chlorhexidine gluconate costs about
1.7 times the amount, and alcohol-based handrub
almost double the cost. However, the expenditure
by hospital trusts on hand hygiene products must
be compared against the excess costs arising from
hospital acquired infections, and must not be seen
as a barrier to promoting optimum hand hygiene.
The costs associated with only four or five HAIs
may be the same as the entire annual hand hygiene
product budget. Indeed, just one severe surgical
site infection, lower respiratory tract infection or
septicaemia may cost more than this budget!
Based on current BNF prices, the cost of 10 days
treatment for MRSA is 346.40 with vancomycin
(1 g bd iv) or 391.82 with teicoplanin (400 mg od
iv), without the additional costs of drug level
monitoring, nursing time, cannulae, etc. One study
demonstrated a saving of about A$17,000 over just
7 months from using less vancomycin due to the
reduction in MRSA incidence.61 Of course, less use
of antibiotics also reduces the chance of antibiotic
resistance developing.
In the study at the University of Geneva Hospital
discussed previously,90 the cost of the programme
was estimated at no more than 155,000, including
direct and indirect costs. The authors conserva-
tively assumed that 25% of the observed reduction
in HAI was due to the hand hygiene programme,
thereby preventing 900 infections. At an average
(very conservative) estimate of 1400 per infec-
tion, their estimate of overall savings of 1.25
million far outweighs the costs.
It is clear that the savings made by reducing the
HAI rate by improving hand hygiene compliance far
outweigh the cost to hospital trusts of purchasing
more effective and more acceptable hand hygiene
products, improving hand hygiene education and
increasing HAI surveillance.
C.R. Nicolay
Conclusion
Hospital acquired infection affects approximately
10% of inpatients, leads directly to an estimated
5000 deaths a year in the UK and costs the NHS an
estimated 1000 million a year. Despite nearly
one-third of these infections being caused by
cross-infection by healthcare workers, compliance
with recommended hand hygiene guidelines is
poor, particularly amongst doctors.
This review discusses the effectiveness and the
properties of different hand hygiene agents avail-
able for use on the ward and for preoperative hand
disinfection. There are a vast number of studies
looking at different hand hygiene agents and their
effectiveness, but there is a lack of good research
using adequate numbers, control groups, long-term
follow-up, and using HAI rate as an outcome rather
than hand hygiene frequency or bacterial growth
from hands. Hand hygiene products are needed with
better residual activity, and testing of these agents
is needed using short application times, under the
conditions they are actually used in hospitals rather
than in mock protocols by volunteers in laboratories.
Improved hand hygiene compliance has been
shown to significantly reduce the HAI rate. This
improvement requires a multifactorial approach
including the availability of alcohol handrubs on
every person and bedside, education, peer exam-
ple, and a continually published cycle of audit
looking at hand hygiene compliance and accur-
ately measuring the HAI rate. The financial savings
associated with fewer HAIs and less antibiotic use
easily outweigh the cost of programmes to improve
hand hygiene compliance.
In the 21st century, 16 decades after the reports
of Semmelweis and Holmes, we are facing an ever-
increasing battle against hospital acquired infec-
tion, antibiotic-resistant bacteria and increasing
patient numbers from an ageing population. There
has never been a more simple and cost-effective
intervention to help our patients than hand hygiene.
References
1. Holmes OW. The contagiousness of puerperal fever. N Engl
Q J Med Surg April 1843;1:503e30. Reprinted in Med Class
1936;1:211e43.
2. Semmelweis IP. Die Aetiologie, derBegriff und die Pro-
phylaxis des Kindbettfiebers. Pest-Wien-Leipzig, 1861.
Reprinted with a new introduction by A.F. Guttmacher.
New York/London, 1966. Translated into English by
F.R. Murphy as The Etiology, the Concept and Prophylaxis
of Childbed Fever, in Med Class 1941;5:350e773.
3. Larson EL. APIC Guidelines for handwashing and hand
antisepsis in health care settings. Am J Infect Control
1995;23:251e69.
Hand hygiene: An evidence-based review
4. Steere AC, Mallison GF. Handwashing practices for the
prevention of nosocomial infections. Ann Intern Med 1975;
83:683e90.
5. Albert RK, Condie F. Hand-washing patterns in medical
intensive-care units. N Engl J Med 1981;304:1465e6.
6. Jarvis WR. Handwashingdthe Semmelweis lesson forgot-
ten? Lancet 1994;344:1311e2.
7. Sproat LJ, Inglis TJ. A multicentre survey of hand hygiene
practice in intensive care units. J Hosp Infect 1994;26:
137e48.
8. Thompson BL, Dwyer DM, Ussery XT, Denman S, Vacek P,
Schwartz B. Handwashing and glove use in a long-term-care
facility. Infect Control Hosp Epidemiol 1997;18:97e103.
9. Pittet D. Improving adherence to hand hygiene practice:
a multidisciplinary approach. Emerg Infect Dis 2001;7(2):
234e40.
10. Meers PD, Ayliffe GA, Emmeron AM, Leigh DA, Mayon-
White RT, Mackintosh CA, et al. Report on the national
survey of infection in hospitals 1980. J Hosp Infect (Suppl)
1981;2:1e11.
11. Emmerson AM, Enstone JE, Griffin M, Kelsey MC, Smyth ET.
The second national prevalence survey of infection in
hospitals e an overview of results. J Hosp Infect 1996;32:
175e90.
12. Hospital Infection Working Group of the Department of
Health & Public Health Laboratory Service. Hospital in-
fection control: guidance on the control of infection in
hospitals. London: Department of Health; 1995:84.8.
13. Plowman R, Graves N, Griffin M, Roberts JA, Swan A,
Cookson B, et al. The socio-economic burden of hospital-
acquired infection. London: Public Health Laboratory
Service and The London School of Hygiene and Tropical
Medicine; 2000.
14. Infection control. Prevention of healthcare associated
infection in primary and community care. NICE clinical
guideline 2; June 2003.
15. Centers for Disease Control and Prevention. Guideline for
hand hygiene in health-care settings: recommendations of
the Healthcare Infection Control Practices Advisory Com-
mittee and the HICPAC/SHEA/APIC/IDSA Hand Hygiene Task
Force. MMWR 2002;51(RR-16):1e48.
16. Selwyn S. Microbiology and ecology of human skin.
Practitioner 1980;224:1059e62.
17. Kampf G, Ostermeyer C. Efficacy of alcohol-based gels
compared with simple hand wash and hygienic hand
disinfection. J Hosp Infect 2004;56:S13e5.
18. Ehrenkranz NJ, Alfonso BC. Failure of bland soap handwash
to prevent hand transfer of patient bacteria to urethral
catheters. Infect Control Hosp Epidemiol 1991;12:654e62.
19. Larson E, Leyden JJ, McGinley KJ, Grove GL, Talbot GH.
Physiologic and microbiologic changes in skin related to
frequent handwashing. Infect Control 1986;7:59e63.
20. Boyce JM, Kelliher S, Vallande N. Skin irritation and dryness
associated with two hand-hygiene regimens: soap-
and-water handwashing versus hand antisepsis with an
alcoholic hand gel. Infect Control Hosp Epidemiol 2000;21:
442e8.
21. Larson EL, Morton HE. Alcohols. [chapter 11]. In: Block SS,
editor. Disinfection, sterilization and preservation. 4th ed.
Philadelphia, PA: Lea and Febiger; 1991. p. 642e54.
22. Girou E, Loyeau S, Legrand P, Oppein F, Brun-Buisson C.
Efficacy of handrubbing with alcohol based solution versus
standard handwashing with antiseptic soap: randomised
clinical trial. BMJ 2002;325:362.
23. Kampf G, Ho fer M, Wendt C. Efficacy of hand disinfectants
against vancomycin-resistant enterococci in vitro. J Hosp
Infect 1999;42:143e50.
63
24. Platt J, Bucknall RA. The disinfection of respiratory
syncytial virus by isopropanol and a chlorhexidine-deter-
gent handwash. J Hosp Infect 1985;6:89e94.
25. Krilov LR, Harkness SH. Inactivation of respiratory syncytial
virus by detergents and disinfectants. Pediatr Infect Dis J
1993;12:582e4.
26. Sattar SA, Tetro J, Springthorpe VS, Giulivi A. Preventing
the spread of hepatitis B and C viruses: where are
germicides relevant? Am J Infect Control 2001;29:187e97.
27. Lilly HA, Lowbury EJL, Wilkins MD, Zaggy A. Delayed
antimicrobial effects of skin disinfection by alcohol. J Hyg
(Lond) 1979;82:497e500.
28. Ansari SA, Springthorpe VS, Sattar SA, Tostowaryk W,
Wells GA. Comparison of cloth, paper, and warm air drying
in eliminating viruses and bacteria from washed hands. Am
J Infect Control 1991;19:243e9.
29. Ansari SA, Sattar SA, Springthorpe VS, Wells GA,
Tostowaryk W. In vivo protocol for testing efficacy of
hand-washing agents against viruses and bacteria: experi-
ments with rotavirus and Escherichia coli. Appl Environ
Microbiol 1989;55:3113e8.
30. Larson E, Bobo L. Effective hand degerming in the presence
of blood. J Emerg Med 1992;10:7e11.
31. Ayliffe GAJ, Babb JR, Davies JG, Lilly HA. Hand disinfection:
a comparison of various agents in laboratory and ward
studies. J Hosp Infect 1988;11:226e43.
32. Lilly HA, Lowbury EJL, Wilkins MD. Detergents compared
with each other and with antiseptics as skin degerming
agents. J Hyg (Lond) 1979;82:89e93.
33. Bartzokas CA, Gibson MF, Graham R, Pinder DC. A
comparison of triclosan and chlorhexidine preparations
with 60 per cent isopropyl alcohol for hygienic hand
disinfection. J Hosp Infect 1983;4:245e55.
34. Rotter ML, Koller W, Wewalka G, Werner HP, Ayliffe GAJ,
Babb JR. Evaluation of procedures for hygienic hand-
disinfection: controlled parallel experiments on the Vienna
test model. J Hyg (Lond) 1986;96:27e37.
35. Namura S, Nishijima S, Asada Y. An evaluation of the
residual activity of antiseptic handrub lotions: an in use
setting study. J Dermatol 1994;21:481e5.
36. Ayliffe GA, Bridges K, Lilly HA, Lowbury EJ, Varney J,
Wilkins MD. Comparison of two methods for assessing the
removal of total organisms and pathogens from the skin.
J Hyg (Lond) 1975;75:259e74.
37. Rotter M, Koller W, Wewalka G. Povidoneeiodine and
chlorhexidine gluconate-containing detergents for disinfec-
tion of hands. J Hosp Infect 1980;1:149e58.
38. Rotter ML. Hygienic hand disinfection. Infect Control 1984;
1:18e22.
39. Rotter ML, Koller W. Test models for hygienic handrub and
hygienic handwash: the effects of two different contamina-
tion and sampling techniques. J Hosp Infect 1992;20:163e71.
40. Leyden JJ, McGinley KJ, Kaminer MS, Bakel J, Nishijima S,
Grove MJ, et al. Computerized image analysis of full-hand
touch plates: a method for quantification of surface
bacteria on hands and the effect of antimicrobial agents.
J Hosp Infect 1991;18(Suppl. B):13e22.
41. Cardoso CL, Pereira HH, Zequim JC, Guilhermetti M.
Effectiveness of hand-cleansing agents for removing Acine-
tobacter baumannii strain from contaminated hands. Am J
Infect Control 1999;27:327e31.
42. Winnefeld M, Richard MA, Drancourt M, Grobb JJ. Skin
tolerance and effectiveness of two hand decontamination
procedures in everyday hospital use. Br J Dermatol 2000;
143:546e50.
43. Casewell MW, Law MM, Desai N. A laboratory model for
testing agents for hygienic hand disinfection: handwashing
64
and chlorhexidine for the removal of Klebsiella. J Hosp
Infect 1988;12:163e75.
44. Huang Y, Oie S, Kamiya A. Comparative effectiveness of
hand-cleansing agents for removing methicillin-resistant
Staphylococcus aureus from experimentally contaminated
fingertips. Am J Infect Control 1994;22:224e7.
45. Larson EL, Eke PI, Wilder MP, Laughon BE. Quantity of soap
as a variable in handwashing. Infect Control 1987;8:371e5.
46. Larson EL, Aiello AE, Heilman JM, Lyle CT, Cronquist A,
Stahl JB, et al. Comparison of different regimens for
surgical hand preparation. AORN J 2001;73:412e20.
47. Russell AD. Chlorhexidine: antibacterial action and bacte-
rial resistance. Infection SeptembereOctober 1986;14(5):
212e5.
48. Sakuragi T, Yanagisawa K, Dan K. Bactericidal activity of
skin disinfectants on methicillin-resistant Staphylococcus
aureus. Anesth Analg 1995;81:555e8.
49. Kampf G, Jarosch R, Ru den H. Limited effectiveness of
chlorhexidine based hand disinfectants against methicillin-
resistant Staphylococcus aureus (MRSA). J Hosp Infect 1998;
38:297e303.
50. Walsh B, Blakemore PH, Drabu YJ. The effect of handcream
on the antibacterial activity of chlorhexidine gluconate.
J Hosp Infect 1987;9:30e3.
51. Pereira LJ, Lee GM, Wade KJ. An evaluation of five protocols
for surgical handwashing in relation to skin condition and
microbial counts. J Hosp Infect 1997;36:49e65.
52. Larson EL, Butz AM, Gullette DL, Laughon BA. Alcohol for
surgical scrubbing? Infect Control Hosp Epidemiol 1990;11:
139e43.
53. Rosenberg A, Alatary SD, Peterson AF. Safety and efficacy
of the antiseptic chlorhexidine gluconate. Surg Gynecol
Obstet 1976;143:789e92.
54. Anderson RL. Iodophor antiseptics: intrinsic microbial
contamination with resistant bacteria. Infect Control Hosp
Epidemiol 1989;10:443e6.
55. Larson EL, APIC Guidelines Committee. APIC guideline for
handwashing and hand antisepsis in health care settings.
Am J Infect Control 1995;23:251e69.
56. Reimer K, Wichelhaus TA, Scha fer V, Rudolph P, Kramer A,
Wutzler P, et al. Antimicrobial effectiveness of povidonee
iodine and consequences for new application areas.
Dermatology 2002;204(Suppl. 1):114e20.
57. Jones RD, Jampani HB, Newman JL, Lee AS. Triclosan:
a review of effectiveness and safety in health care settings.
Am J Infect Control 2000;28:184e96.
58. Ward WH, Holdgate GA, Rowsell S, McLean EG, Pauptit RA,
Clayton E, et al. Kinetic and structural characteristics of the
inhibition of enoyl (acyl carrier protein) reductase by
triclosan. Biochemistry 1999;38:12514e25.
59. Heath RJ, Li J, Roland GE. Inhibition of the Staphylococcus
aureus NADPH-dependent enoyl-acyl carrier protein re-
ductase by triclosan and hexachlorophene. J Biol Chem
2000;275:4654e9.
60. Faoagali JL, George N, Fong J, Davy J, Dowser M.
Comparison of the antibacterial efficacy of 4% chlorhex-
idine gluconate and 1% triclosan handwash products in an
acute clinical ward. Am J Infect Control 1999;27:320e6.
61. 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;30:59e64.
62. 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;23:200e8.
C.R. Nicolay
63. Larson E, Mayur K, Laughon BA. Influence of two handwash-
ing frequencies on reduction in colonizing flora with three
handwashing products used by health care personnel.
Am J Infect Control 1988;17:83e8.
64. Rotter ML. Semmelweis sesquicentennial: a little-noted
anniversary of handwashing. Curr Opin Infect Dis 1998;11:
457e60.
65. Rutala WA, Weber DJ. New disinfection and sterilization
methods. Emerg Infect Dis MarcheApril 2001;7(2):348e53.
66. Widmer AE, Dangel M. Alcohol-based handrub: evaluation of
technique and microbiological efficacy with international
infection control professionals. Infect Control Hosp Epide-
miol March 2004;25(3):207e9.
67. Boyce JM, Potter-Bynoe G, Opal SM, Dziobek L,
Medeiros AA. A common-source outbreak of Staphylococcus
epidermidis infections among patients undergoing cardiac
surgery. J Infect Dis 1990;161:493e9.
68. Dewar NE, Gravens DL. Effectiveness of septisol antiseptic
foam as a surgical scrub agent. Appl Microbiol 1973;26:
544e9.
69. Grinbaum RS, de Mendonc a JS, Cardo DM. An outbreak of
handscrubbing-related surgical site infections in vascular
surgical procedures. Infect Control Hosp Epidemiol 1995;
16:198e202.
70. Babb JR, Davies JG, Ayliffe GAJ. A test procedure for
evaluating surgical hand disinfection. J Hosp Infect 1991;
18(Suppl. B):41e9.
71. Aly R, Maibach HI. Comparative antibacterial efficacy of
a 2-minute surgical scrub with chlorhexidine gluconate,
povidoneeiodine, and chloroxylenol sponge-brushes. Am J
Infect Control 1988;16:173e7.
72. Faoagali J, Fong J, George N, Mahoney P, ORourke V.
Comparison of the immediate, residual, and cumulative
antibacterial effects of Novaderm R, Novascrub R, Betadine
Surgical Scrub, Hibiclens, and liquid soap. Am J Infect
Control 1995;23:337e43.
73. Herruzo-Cabrera R, Vizcaino-Alcaide MJ, Fdez-AciZero MJ.
Usefulness of an alcohol solution of N-duopropenide for the
surgical antisepsis of the hands compared with handwashing
with iodineepovidone and chlorhexidine: clinical essay.
J Surg Res 2000;94:6e12.
74. Peterson AF, Rosenberg A. Comparative evaluation of
surgical scrub preparations. Surg Gynecol Obstet 1978;
146:63e5.
75. Mulberry G, Snyder AT, Heilman J, Pyrek J, Stahl J.
Evaluation of a waterless, scrubless chlorhexidine glucona-
te/ethanol surgical scrub for antimicrobial efficacy. Am J
Infect Control 2001;29:377e82.
76. Hobson DW, Woller W, Anderson L, Guthery E. Development
and evaluation of a new alcohol-based surgical hand scrub
formulation with persistent antimicrobial characteristics
and brushless application. Am J Infect Control 1998;26:
507e12.
77. Pereira LJ, Lee GM, Wade KJ. The effect of surgical
handwashing routines on the microbial counts of operating
room nurses. Am J Infect Control 1990;18:354e64.
78. Galle PC, Homesley HD, Rhyne AL. Reassessment of the
surgical scrub. Surg Gynecol Obstet 1978;147:215e8.
79. OFarrell DA, Kenny G, OSullivan M, Nicholson P,
Stephens M, Hone R. Evaluation of the optimal hand-scrub
duration prior to total hip arthroplasty. J Hosp Infect 1994;
26:93e8.
80. Hingst V, Juditzki I, Heeg P, Sonntag HG. Evaluation of the
efficacy of surgical hand disinfection following a reduced
application time of 3 instead of 5 min. J Hosp Infect 1992;
20:79e86.
Hand hygiene: An evidence-based review
81. Wheelock SM, Lookinland S. Effect of surgical hand scrub
time on subsequent bacterial growth. AORN J 1997;65:
1087e98.
82. Deshmukh N, Kjellberg SI, Kramer JW. A comparison of 5-
minute povidoneeiodine scrub and 1-minute povidoneeiodine
scrub followed by alcohol foam. Mil Med 1998;163:145e7.
83. Kikuchi-Numagami K, Saishu T, Fukaya M, Kanazawa E,
Tagami H. Irritancy of scrubbing up for surgery with or
without a brush. Acta Derm Venereol 1999;79:230e2.
84. Loeb MB, Wilcox L, Smaill F, Walter S, Duff Z. A randomized
trial of surgical scrubbing with a brush compared to
antiseptic soap alone. Am J Infect Control 1997;25:11e5.
85. Pittet D, Mourouga P, Perneger TV. Members of the infection
control program. Compliance with handwashing in a teach-
ing hospital. Ann Intern Med 1999;130:126e30.
86. Boyce JM. It is time for action: improving hand hygiene in
hospitals. Ann Intern Med 1999;130:153e5.
87. Larson E, Kretzer EK. Compliance with handwashing and
barrier precautions. J Hosp Infect 1995;30:88e106.
88. Bauer TM, Ofner E, Just HM, Just H, Daschner FD. An
epidemiological study assessing the relative importance of
airborne and direct contact transmission of microorganisms
in a medical intensive care unit. J Hosp Infect 1990;15:
301e9.
89. Voss A, Widmer AF. No time for handwashing!? Handwashing
versus alcoholic rub: can we afford 100% compliance? Infect
Control Hosp Epidemiol 1997;18(3):205e8.
65
90. Pittet D, Hugonnet S, Harbarth S, Mourouga P, Sauvan V,
Touveneau S, et al. Effectiveness of a hospital-wide
programme to improve compliance with hand hygiene.
Lancet 2000;356:1307e12.
91. McGuckin M, Waterman R, Storr J, Bowler CJW, Ashby M,
Topley K, et al. Evaluation of a patient-empowering hand
hygiene programme in the UK. J Hosp Infect 2001;48:
222e7.
92. McGuckin M, Waterman R, Porten L, Bello S, Caruso M,
Juzaitis B, et al. Patient education model for increasing
handwashing compliance. Am J Infect Control 1999;27:
309e14.
93. Casewell M, Phillips I. Hands as route of transmission for
Klebsiella species. Br Med J 1977;2:1315e7.
94. Maki DG. The use of antiseptics for handwashing by medical
personnel. J Chemother 1989;1(Suppl. 1):3e11.
95. Doebbeling BN, Stanley GL, Sheetz CT, Pfaller MA,
Houston AK, Annis L, et al. Comparative efficacy of
alternative hand-washing agents in reducing nosocomial
infections in intensive care units. N Engl J Med 1992;327:
88e93.
96. Larson EL, Early E, Cloonan P, Sugrue S, Parides M. An
organizational climate intervention associated with in-
creased handwashing and decreased nosocomial infections.
Behav Med 2000;26:14e22.
97. Boyce JM. Antiseptic technology: access, affordability, and
acceptance. Emerg Infect Dis 2001;7:231e3.