Hygienic handrub.

Treatment of hands with an antiseptic

handrub to reduce the transient flora without necessarily
affecting the resident skin flora. These preparations are
broad spectrum and fast-acting, and persistent activity is not
necessary.
Hygienic handwash. Treatment of hands with an antiseptic
handwash and water to reduce the transient flora without
necessarily affecting the resident skin flora. It is broad
spectrum, but is usually less efficacious and acts more slowly
than the hygienic handrub.

Historical perspective
on hand hygiene in health care
Handwashing with soap and water has been considered a measure of personal
hygiene for centuries48,49 and has
been generally embedded in religious and cultural habits (see Part I, Section 17).
Nevertheless, the link between
handwashing and the spread of disease was established only two centuries ago,
although this can be considered
as relatively early with respect to the discoveries of Pasteur and Lister that
occurred decades later.
In the mid-1800s, studies by Ignaz Semmelweis in Vienna,
Austria, and Oliver Wendell Holmes in Boston, USA, established
that hospital-acquired diseases were transmitted via the hands
of HCWs. In 1847, Semmelweiss was appointed as a house
officer in one of the two obstetric clinics at the University
of Vienna Allgemeine Krankenhaus (General Hospital). He
observed that maternal mortality rates, mostly attributable to
puerperal fever, were substantially higher in one clinic compared
with the other (16% versus 7%).50 He also noted that doctors
and medical students often went directly to the delivery suite
after performing autopsies and had a disagreeable odour on
their hands despite handwashing with soap and water before
entering the clinic. He hypothesized therefore that cadaverous
particles were transmitted via the hands of doctors and
students from the autopsy room to the delivery theatre and

caused the puerperal fever. As a consequence, Semmelweis

recommended that hands be scrubbed in a chlorinated lime
solution before every patient contact and particularly after
leaving the autopsy room. Following the implementation of this
measure, the mortality rate fell dramatically to 3% in the clinic
most affected and remained low thereafter.
Apart from providing the first evidence that cleansing heavily
contaminated hands with an antiseptic agent can reduce
nosocomial transmission of germs more effectively than
handwashing with plain soap and water, this approach includes
all the essential elements for a successful infection control
intervention: recognize-explain-act.51 Unfortunately, both
Holmes and Semmelweis failed to observe a sustained change
in their colleagues behaviour. In particular, Semmelweis
experienced great difficulties in convincing his colleagues and
administrators of the benefits of this procedure. In the light of
the principles of social marketing today, his major error was that
he imposed a system change (the use of the chlorinated lime
solution) without consulting the opinion of his collaborators.
Despite these drawbacks, many lessons have been learnt
from the Semmelweis intervention; the recognize-explainact
approach has driven many investigators and practitioners
since then and has also been replicated in different fields and
settings. Semmelweis is considered not only the father of hand
hygiene, but his intervention is also a model of epidemiologically
driven strategies to prevent infection.
A prospective controlled trial conducted in a hospital nursery52
and many other investigations conducted over the past 40
years have confirmed the important role that contaminated
HCWs hands play in the transmission of health care-associated
pathogens (see Part I, Sections 79)

The 1980s represented a landmark in the evolution of concepts

of hand hygiene in health care. The first national hand hygiene
guidelines were published in the 1980s,53-55 followed by several
others in more recent years in different countries. In 1995 and
1996, the CDC/Healthcare Infection Control Practices Advisory
Committee (HICPAC) in the USA recommended that either
antimicrobial soap or a waterless antiseptic agent be used 56,57
for cleansing hands upon leaving the rooms of patients with
multidrug-resistant pathogens. More recently, the HICPAC
guidelines issued in 200258 defined alcohol-based handrubbing,

where available, as the standard of care for hand hygiene

practices in health-care settings, whereas handwashing is
reserved for particular situations only.59 The present guidelines
are based on this previous document and represent the most
extensive review of the evidence related to hand hygiene in the
literature. They aim to expand the scope of recommendations to
a global perspective, foster discussion and expert consultation
on controversial issues related to hand hygiene in health
care, and to propose a practical approach for successful
implementation (see also Part VI).
As far as the implementation of recommendations on hand
hygiene improvement is concerned, very significant progress
has been achieved since the introduction and validation of the
concept that promotional strategies must be multimodal to
achieve any degree of success. In 2000, Pittet et al. reported
the experience of the Genevas University Hospitals with
the implementation of a strategy based on several essential
components and not only the introduction of an alcohol-based
handrub. The study showed remarkable results in terms of
an improvement in hand hygiene compliance improvement
and HCAI reduction.60 Taking inspiration from this innovative
approach, the results of which were also demonstrated to be
long-lasting,61 many other studies including further original
aspects have enriched the scientific literature (see Table I.22.1).
Given its very solid evidence base, this model has been adopted
by the First Global Patient Safety Challenge to develop the
WHO Hand Hygiene Improvement Strategy aimed at translating
into practice the recommendations included in the present
guidelines. In this final version of the guidelines, evidence
generated from the pilot testing of the strategy during 2007
2008 is included (see also Part I, Section 21.5). 62

Normal bacterial flora on hands

In 1938, Price63 established that bacteria recovered from the hands could be divided into two
categories, namely
resident or transient. The resident flora (resident microbiota) consists of microorganisms
residing under the
superficial cells of the stratum corneum and can also be found on the surface of the skin.64,65
Staphylococcus
epidermidis is the dominant species,66 and oxacillin resistance is extraordinarily high,
particularly among HCWs.67
Other resident bacteria include S. hominis and other coagulase-negative staphylococci,
followed by coryneform
bacteria (propionibacteria, corynebacteria, dermobacteria, and micrococci).68 Among fungi,
the most common
genus of the resident skin flora, when present, is Pityrosporum (Malassezia) spp.69. Resident
flora has two main
protective functions: microbial antagonism and the competition for nutrients in the
ecosystem.70 In general,
resident flora is less likely to be associated with infections, but may cause infections in
sterile body cavities, the
eyes, or on non-intact skin.71
Transient flora (transient microbiota), which colonizes the
superficial layers of the skin, is more amenable to removal by
routine hand hygiene. Transient microorganisms do not usually

multiply on the skin, but they survive and sporadically multiply

on skin surface.70 They are often acquired by HCWs during
direct contact with patients or contaminated environmental
surfaces adjacent to the patient and are the organisms most
frequently associated with HCAIs. Some types of contact during
routine neonatal care are more frequently associated with higher
levels of bacterial contamination of HCWs hands: respiratory
secretions, nappy/diaper change, and direct skin contact. 72,73
The transmissibility of transient flora depends on the species
present, the number of microorganisms on the surface, and
the skin moisture.74,75 The hands of some HCWs may become
persistently colonized by pathogenic flora such as S. aureus,
Gram-negative bacilli, or yeast.76
Normal human skin is colonized by bacteria, with total aerobic
bacterial counts ranging from more than 1 x 106 colony forming
units (CFU)/cm2 on the scalp, 5 x 105 CFUs/cm2 in the axilla,
and 4 x 104 CFU/cm2 on the abdomen to 1 x 104 CFU/cm2 on
the forearm.77 Total bacterial counts on the hands of HCWs have
ranged from 3.9 x 104 to 4.6 x 106 CFU/cm2. 63,78-80 Fingertip
contamination ranged from 0 to 300 CFU when sampled by
agar contact methods.72 Price and subsequent investigators
documented that although the count of transient and resident
flora varies considerably among individuals, it is often relatively
constant for any given individual. 63,81

Physiology of normal skin

The skin is composed of three layers, the epidermis (50100 m), dermis (12 mm) and
hypodermis (12 mm)
(Figure I.6.1). The barrier to percutaneous absorption lies within the stratum corneum, the
most superficial layer of
the epidermis. The function of the stratum corneum is to reduce water loss, provide
protection against abrasive
action and microorganisms, and generally act as a permeability barrier to the environment.
The stratum corneum is a 1020 m thick, multilayer stratum
of flat, polyhedral-shaped, 2 to 3 m thick, non-nucleated cells
named corneocytes. Corneocytes are composed primarily
of insoluble bundled keratins surrounded by a cell envelope
stabilized by cross-linked proteins and covalently bound lipids.
Corneodesmosomes are membrane junctions interconnecting
corneocytes and contributing to stratum corneum cohesion.
The intercellular space between corneocytes is composed of
lipids primarily generated from the exocytosis of lamellar bodies
during the terminal differentiation of the keratinocytes. These
lipids are required for a competent skin barrier function
The epidermis is composed of 1020 layers of cells. This
pluristratified epithelium also contains melanocytes involved in
skin pigmentation, and Langerhans cells, involved in antigen
presentation and immune responses. The epidermis, as for
any epithelium, obtains its nutrients from the dermal vascular
network.
The epidermis is a dynamic structure and the renewal of
the stratum corneum is controlled by complex regulatory
systems of cellular differentiation. Current knowledge of the
function of the stratum corneum has come from studies of

the epidermal responses to perturbation of the skin barrier

such as: (i) extraction of skin lipids with apolar solvents; (ii)
physical stripping of the stratum corneum using adhesive tape;
and (iii) chemically-induced irritation. All such experimental
manipulations lead to a transient decrease of the skin barrier
efficacy as determined by transepidermal water loss. These
alterations of the stratum corneum generate an increase of
keratinocyte proliferation and differentiation in response to this
aggression in order to restore the skin barrier. This increase
in the keratinocyte proliferation rate could directly influence
the integrity of the skin barrier by perturbing: (i) the uptake
of nutrients, such as essential fatty acids; (ii) the synthesis of
proteins and lipids; or (iii) the processing of precursor molecules
required for skin barrier function.

7.
Transmission of pathogens by hands
Transmission of health care-associated pathogens from one patient to another via HCWs
hands requires

five sequential steps (Figures I.7.16): (i) organisms are present on the patients skin, or
have been shed onto
inanimate objects immediately surrounding the patient; (ii) organisms must be transferred to
the hands of HCWs;
(iii) organisms must be capable of surviving for at least several minutes on HCWs hands;
(iv) handwashing
or hand antisepsis by the HCW must be inadequate or entirely omitted, or the agent used for
hand hygiene
inappropriate; and (v) the contaminated hand or hands of the caregiver must come into
direct contact with
another patient or with an inanimate object that will come into direct contact with the
patient. Evidence
supporting each of these elements is given below
7.1 Organisms present on patient skin or in the
inanimate environment

Health care-associated pathogens can be recovered not only

from infected or draining wounds, but also from frequently
colonized areas of normal, intact patient skin.82-96 The perineal or
inguinal areas tend to be most heavily colonized, but the axillae,
trunk, and upper extremities (including the hands) are also
frequently colonized.85,86,88,89,91,93,97 The number of organisms
such as S. aureus, Proteus mirabilis, Klebsiella spp. and
Acinetobacter spp. present on intact areas of the skin of some
patients can vary from 100 to 106 CFU/cm2.86,88,92,98 Diabetics,
patients undergoing dialysis for chronic renal failure, and those
with chronic dermatitis are particularly likely to have skin areas
colonized with S. aureus.99-106. Because nearly 106 skin squames
containing viable microorganisms are shed daily from normal
skin,107 it is not surprising that patient gowns, bed linen, bedside
furniture and other objects in the immediate environment of
the patient become contaminated with patient flora.93-96,108-114
Such contamination is most likely to be due to staphylococci,
enterococci or Clostridium difficile which are more resistant to
desiccation. Contamination of the inanimate environment has
also been detected on ward handwash station surfaces and
many of the organisms isolated were staphylococci. 115 Tap/
faucet handles were more likely to be contaminated and to be in
excess of benchmark values than other parts of the station. This
study emphasizes the potential importance of environmental
contamination on microbial cross contamination and pathogen
spread.115 Certain Gram-negative rods, such as Acinetobacter
baumannii, can also play an important role in environmental
contamination due to their long-time survival capacities. 116-119

7.2 Organism transfer to health-care workers hands

Relatively few data are available regarding the types of

patient-care activities that result in transmission of patient
flora to HCWs hands.72,89,110,111,120-123 In the past, attempts have
been made to stratify patient-care activities into those most
likely to cause hand contamination,124 but such stratification
schemes were never validated by quantifying the level of
bacterial contamination that occurred. Casewell & Phillips 121
demonstrated that nurses could contaminate their hands with
1001000 CFU of Klebsiella spp. during clean activities such
as lifting patients; taking the patients pulse, blood pressure
or oral temperature; or touching the patients hand, shoulder
or groin. Similarly, Ehrenkranz and colleagues88 cultured the
hands of nurses who touched the groin of patients heavily colonized with P. mirabilis and found 10600
CFU/ml in glove

juice samples. Pittet and colleagues 72 studied contamination of

HCWs hands before and after direct patient contact, wound
care, intravascular catheter care, respiratory tract care or
handling patient secretions. Using agar fingertip impression
plates, they found that the number of bacteria recovered from
fingertips ranged from 0 to 300 CFU. Direct patient contact
and respiratory tract care were most likely to contaminate
the fingers of caregivers. Gram-negative bacilli accounted for
15% of isolates and S. aureus for 11%. Importantly, duration of
patient-care activity was strongly associated with the intensity
of bacterial contamination of HCWs hands in this study. A
similar study of hand contamination during routine neonatal care
defined skin contact, nappy/diaper change, and respiratory care
as independent predictors of hand contamination.73 In the latter
study, the use of gloves did not fully protect HCWs hands from
bacterial contamination, and glove contamination was almost as
high as ungloved hand contamination following patient contact.
In contrast, the use of gloves during procedures such as nappy/
diaper change and respiratory care almost halved the average
increase of bacteria CFU/min on HCWs hands.73
Several other studies have documented that HCWs can
contaminate their hands or gloves with Gram-negative bacilli,
S. aureus, enterococci or C. difficile by performing clean
procedures or touching intact areas of skin of hospitalized
patients.89,95,110,111,125,126 A recent study that involved culturing
HCWs hands after various activities showed that hands were
contaminated following patient contact and after contact with
body fluids or waste.127 McBryde and colleagues128 estimated
the frequency of HCWs glove contamination with methicillinresistant
S. aureus (MRSA) after contact with a colonized
patient. HCWs were intercepted after a patient-care episode
and cultures were taken from their gloved hands before
handwashing had occurred; 17% (confidence interval (CI)
95% 925%) of contacts with patients, a patients clothing or a
patients bed resulted in transmission of MRSA from a patient
to the HCWs gloves. In another study involving HCWs caring
for patients with vancomycin-resistant enterococci (VRE),
70% of HCWs contaminated their hands or gloves by touching
the patient and the patients environment.114 Furthermore,
HCWs caring for infants with respiratory syncytial virus (RSV)
infections have acquired infection by performing activities such
as feeding infants, nappy/diaper change, and playing with
the infant.122 Caregivers who had contact only with surfaces
contaminated with the infants secretions also acquired RSV.
In the above studies, HCWs contaminated their hands with
RSV and inoculated their oral or conjunctival mucosa. Other studies have also documented that the
hands (or gloves) of
HCWs may be contaminated after touching inanimate objects
in patients rooms.73,111,112,125-130 Furthermore, a recent two-part
study conducted in a non-health-care setting found in the
initial phase that patients with natural rhinovirus infections often
contaminated multiple environmental sites in their rooms. In
the second part of the study, contaminated nasal secretions
from the same individuals were used to contaminate surfaces
in rooms, and touching contaminated sites 1178 hours later
frequently resulted in the transfer of the virus to the fingertips of
the individuals.131

Bhalla and colleagues studied patients with skin colonization

by S. aureus (including MRSA) and found that the organism

was frequently transferred to the hands of HCWs who touched

both the skin of patients and surrounding environmental
surfaces.96Hayden and colleagues found that HCWs seldom
enter patient rooms without touching the environment, and
that 52% of HCWs whose hands were free of VRE upon
entering rooms contaminated their hands or gloves with
VRE after touching the environment without touching the
patient.114 Laboratory-based studies have shown that touching
contaminated surfaces can transfer S. aureus or Gram-negative
bacilli to the fingers.132 Unfortunately, none of the studies dealing
with HCW hand contamination was designed to determine if
the contamination resulted in the transmission of pathogens to
susceptible patients.
Many other studies have reported contamination of HCWs
hands with potential pathogens, but did not relate their findings
to the specific type of preceding patient contact.78,79,94,132-142 For
example, in studies conducted before glove use was common
among HCWs, Ayliffe and colleagues 137 found that 15% of
nurses working in an isolation unit carried a median of 1x 104
CFU of S. aureus on their hands; 29% of nurses working in a
general hospital had S. aureus on their hands (median count,
3.8 x 103 CFU), while 78% of those working in a hospital for
dermatology patients had the organism on their hands (median
count, 14.3 x 106 CFU). The same survey revealed that 1730%
of nurses carried Gram-negative bacilli on their hands (median
counts ranged from 3.4 x 103 CFU to 38 x 103 CFU). Daschner135
found that S. aureus could be recovered from the hands of
21% of ICU caregivers and that 21% of doctors and 5% of
nurse carriers had >103 CFU of the organism on their hands.
Maki80 found lower levels of colonization on the hands of HCWs
working in a neurosurgery unit, with an average of 3 CFU of
S. aureus and 11 CFU of Gram-negative bacilli. Serial cultures
revealed that 100% of HCWs carried Gram-negative bacilli at
least once, and 64% carried S. aureus at least once. A study
conducted in two neonatal ICUs revealed that Gram-negative
bacilli were recovered from the hands of 38% of nurses. 138

7.3 Organism survival on hands

Several studies have shown the ability of microorganisms to

survive on hands for differing times. Musa and colleagues
demonstrated in a laboratory study that Acinetobacter
calcoaceticus survived better than strains of A. lwoffi at 60
minutes after an inoculum of 104 CFU/finger.143 A similar study
by Fryklund and colleagues using epidemic and non-epidemic
strains of Escherichia coli and Klebsiella spp. showed a 50%
killing to be achieved at 6 minutes and 2 minutes, respectively. 144
Noskin and colleagues studied the survival of VRE on hands
and the environment: both Enterococcus faecalis and E.
faecium survived for at least 60 minutes on gloved and ungloved
fingertips.145 Furthermore, Doring and colleagues showed that
Pseudomonas aeruginosa and Burkholderia cepacia were
transmissible by handshaking for up to 30 minutes when the
organisms were suspended in saline, and up to 180 minutes
when they were suspended in sputum.146 The study by Islam
and colleagues with Shigella dysenteriae type 1 showed its
capacity to survive on hands for up to 1 hour.147 HCWs who
have hand dermatitis may remain colonized for prolonged
time periods. For example, the hands of a HCW with psoriatic
dermatitis remained colonized with Serratia marcescens for
more than three months.148 Ansari and colleagues149,150 studied
rotavirus, human parainfluenza virus 3, and rhinovirus 14 survival

on hands and potential for cross-transfer. Survival percentages

for rotavirus at 20 minutes and 60 minutes after inoculation
were 16.1% and 1.8%, respectively. Viability at 1 hour for human
parainfluenza virus 3 and rhinovirus 14 was <1% and 37.8%,
respectively.
The above-mentioned studies clearly demonstrate that
contaminated hands could be vehicles for the spread of certain
viruses and bacteria. HCWs hands become progressively
colonized with commensal flora as well as with potential
pathogens during patient care.72,73 Bacterial contamination
increases linearly over time.72 In the absence of hand hygiene
action, the longer the duration of care, the higher the degree
of hand contamination. Whether care is provided to adults
or neonates, both the duration and the type of patient care
affect HCWs hand contamination.72,73 The dynamics of hand
contamination are similar on gloved versus ungloved hands;
gloves reduce hand contamination, but do not fully protect from
acquisition of bacteria during patient care. Therefore, the glove
surface is contaminated, making cross-transmission through
contaminated gloved hands likely.

7.4 Defective hand cleansing, resulting in hands

remaining contaminated

Studies showing the adequacy or inadequacy of hand cleansing

by microbiological proof are few. From these few studies, it can
be assumed that hands remain contaminated with the risk of
transmitting organisms via hands. In a laboratory-based study,
Larson and colleagues151 found that using only 1 ml of liquid
soap or alcohol-based handrub yielded lower log reductions
(greater number of bacteria remaining on hands) than using 3 ml
of product to clean hands. The findings have clinical relevance
since some HCWs use as little as 0.4 ml of soap to clean their
hands. Kac and colleagues152 conducted a comparative, crossover
study of microbiological efficacy of handrubbing with an
alcohol-based solution and handwashing with an unmedicated
soap. The study results were: 15% of HCWs hands were
contaminated with transient pathogens before hand hygiene;
no transient pathogens were recovered after handrubbing,
while two cases were found after handwashing. Trick and
colleagues153 did a comparative study of three hand hygiene
agents (62% ethyl alcohol handrub, medicated handwipe, and
handwashing with plain soap and water) in a group of surgical
ICUs. They also studied the impact of ring wearing on hand
contamination. Their results showed that hand contamination
with transient organisms was significantly less likely after the use of an alcohol-based handrub
compared with the medicated
wipe or soap and water. Ring wearing increased the frequency
of hand contamination with potential health care-associated
pathogens. Wearing artificial acrylic fingernails can also result
in hands remaining contaminated with pathogens after use
of either soap or alcohol-based hand gel154 and has been
associated with outbreaks of infection155 (see also Part I, Section
23.4).
Sala and colleagues156 investigated an outbreak of food
poisoning attributed to norovirus genogroup 1 and traced the
index case to a food handler in the hospital cafeteria. Most of
the foodstuffs consumed in the outbreak were handmade, thus
suggesting inadequate hand hygiene. Noskin and colleagues 145
showed that a 5-second handwash with water alone produced
no change in contamination with VRE, and 20% of the initial
inoculum was recovered on unwashed hands. In the same

study, a 5-second wash with two soaps did not remove the
organisms completely with approximately a 1% recovery; a
30-second wash with either soap was necessary to remove the
organisms completely from the hands.
Obviously, when HCWs fail to clean their hands between patient
contact or during the sequence of patient care in particular
when hands move from a microbiologically contaminated body
site to a cleaner site in the same patient microbial transfer is
likely to occur. To avoid prolonged hand contamination, it is not
only important to perform hand hygiene when indicated, but
also to use the appropriate technique and an adequate quantity
of the product to cover all skin surfaces for the recommended
length of time.

7.5 Cross-transmission of organisms by

contaminated hands

Cross-transmission of organisms occurs through contaminated

hands. Factors that influence the transfer of microorganisms
from surface to surface and affect cross-contamination rates
are type of organism, source and destination surfaces, moisture
level, and size of inoculum. Harrison and colleagues157 showed
that contaminated hands could contaminate a clean paper
towel dispenser and vice versa. The transfer rates ranged from
0.01% to 0.64% and 12.4% to 13.1%, respectively.
A study by Barker and colleagues158 showed that fingers
contaminated with norovirus could sequentially transfer
virus to up to seven clean surfaces, and from contaminated
cleaning cloths to clean hands and surfaces. Contaminated
HCWs hands have been associated with endemic HCAIs. 159,160
Sartor and colleagues160 provided evidence that endemic
S. marcescens was transmitted from contaminated soap
to patients via the hands of HCWs. During an outbreak
investigation of S. liquefaciens, BSI, and pyrogenic reactions in a
haemodialysis centre, pathogens were isolated from extrinsically
contaminated vials of medication resulting from multiple dose
usage, antibacterial soap, and hand lotion.161 Duckro and
colleagues126 showed that VRE could be transferred from a
contaminated environment or patients intact skin to clean sites
via the hands of HCWs in 10.6% of contacts.
Several HCAI outbreaks have been associated with
contaminated HCWs hands.162-164 El Shafie and colleagues164
investigated an outbreak of multidrug-resistant A. baumannii
and documented identical strains from patients, hands of staff,
and the environment. The outbreak was terminated when
remedial measures were taken. Contaminated HCWs hands
were clearly related to outbreaks among surgical148,162 and
neonatal163,165,166 patients.
Finally, several studies have shown that pathogens can be
transmitted from out-of-hospital sources to patients via the
hands of HCWs. For example, an outbreak of postoperative S.
marcescens wound infections was traced to a contaminated
jar of exfoliant cream in a nurses home.167 An investigation
suggested that the organism was transmitted to patients via the
hands of the nurse, who wore artificial fingernails. In another
outbreak, Malassezia pachydermatis was probably transmitted
from a nurses pet dogs to infants in an intensive care nursery
via the hands of the nurse