The Role Played by Contaminated Surfaces in the Transmission of Nosocomial Pathogens

Author(s): Jonathan A. Otter PhD; Saber Yezli PhD; Gary L. French MD, FRCPath
Source: Infection Control and Hospital Epidemiology, Vol. 32, No. 7 (July 2011), pp. 687-699
Published by: The University of Chicago Press on behalf of The Society for Healthcare Epidemiology
of America
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 infection control and hospital epidemiology july 2011, vol. 32, no. 7

review article

The Role Played by Contaminated Surfaces in

the Transmission of Nosocomial Pathogens

Jonathan A. Otter, PhD;1,2 Saber Yezli, PhD;2 Gary L. French, MD, FRCPath1

Studies in the 1970s and 1980s suggested that environmental surface contamination played a negligible role in the endemic transmission
of healthcare-associated infections. However, recent studies have demonstrated that several major nosocomial pathogens are shed by patients
and contaminate hospital surfaces at concentrations sufficient for transmission, survive for extended periods, persist despite attempts to
disinfect or remove them, and can be transferred to the hands of healthcare workers. Evidence is accumulating that contaminated surfaces
make an important contribution to the epidemic and endemic transmission of Clostridium difficile, vancomycin-resistant enterococci,
methicillin-resistant Staphylococcus aureus, Acinetobacter baumannii, Pseudomonas aeruginosa, and norovirus and that improved environ-
mental decontamination contributes to the control of outbreaks. Efforts to improve environmental hygiene should include enhancing the
efficacy of cleaning and disinfection and reducing the shedding of pathogens. Further high-quality studies are needed to clarify the role
played by surfaces in nosocomial transmission and to determine the effectiveness of different interventions in reducing associated infection
rates.
Infect Control Hosp Epidemiol 2011;32(7):687-699

Contamination of hospital equipment, medicines, and water
supplies with hospital pathogens is a well-recognized cause
of common-source outbreaks of infection.1,2 Extensive guid-
ance on the prevention and control of such contamination
is available from manufacturers, specialist societies, and
health departments, and there is often a legal requirement to
comply with associated health and safety regulations. In con-
trast, the degree to which ongoing contamination of the sur-
face environment contributes to the development of health-
care-associated infections is unclear, and approaches to
control are uncertain.
Hospital patients shed pathogens into their surrounding
environments, but there is debate over the importance of the
resulting surface contamination as a source for subsequent
transmission. Since the 1950s, hospital design and hygienic
practices have been largely directed at controlling nosocomial
pathogens contaminating air, hands, equipment, and sur-
faces.3 However, several studies in the 1970s and early 1980s
suggested that the hospital environment contributed negli-
gibly to endemic transmission.4,5 Routine surveillance cultures
of the hospital environment were regarded as unjustified, and
the significance of environmental cultures performed during
outbreaks was questioned.6,7 Consequently, the frequency of
routine environmental sampling declined from three-quarters
of US hospitals in 19756 to virtually none today. Indeed, in
recent Centers for Disease Control and Prevention (CDC)
guidelines environmental sampling is recommended only
during outbreaks.8 Recently, however, there has been a reas-
sessment of the role played by contaminated surfaces in the
transmission of nosocomial pathogens.2,9
Pathogen transfer from an affected patient to a susceptible
host occurs most commonly via the hands of healthcare work-
ers (HCWs), but contaminated objects, surfaces, and air can
be either directly or indirectly involved in the transmission
pathway (Figure 1). Here we review evidence that nosocomial
pathogens are shed by patients and can contaminate hospital
surfaces at concentrations sufficient for transmission, can sur-
vive for extended periods, can persist despite attempts to
disinfect or remove them, and can be transferred to the hands
of HCWs. We also review evidence that improved environ-
mental hygiene can help to bring outbreaks under control
and reduce endemic nosocomial transmission.
pathogens are s hed i nto the
hospital environment
Several important pathogens, including Clostridium difficile,
methicillin-resistant Staphylococcus aureus (MRSA), vanco-
mycin-resistant enterococci (VRE), Acinetobacter baumannii,
Pseudomonas aeruginosa, and norovirus, have the ability to
survive in the dry-surface environment, which may then be-
come a source for transmission. Fungiin particular Asper-
gillus speciescan also contaminate the hospital environment

Affiliations: 1. Directorate of Infection, St. Thomas Hospital and Kings College London, United Kingdom; 2. Bioquell UK Ltd, Andover, Hampshire,
United Kingdom.
Received December 15, 2010; accepted February 21, 2011; electronically published May 25, 2011.
2011 by The Society for Healthcare Epidemiology of America. All rights reserved. 0899-823X/2011/3207-0010$15.00. DOI: 10.1086/660363

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688 infection control and hospital epidemiology july 2011, vol. 32, no. 7
figure 1. Generic transmission routes. MRSA, methicillin-resistant Staphylococcus aureus; VRE, vancomycin-resistant enterococci.
and cause healthcare-associated infection; however, fungi are
a special group with unusual features that have been well
reviewed elsewhere and will not be considered here.10
Bacteria, spores, and viruses are shed from infected and/
or colonized patients (and sometimes staff) into the hospital
environment. Wide variation in the reported frequency of
environmental contamination can be explained by several
factors, including the culturability of the organism, the degree
of shedding by the patient, the sampling methodology, the
ease of contamination (or difficulty of cleaning) of the par-
ticular environment, and whether there is an ongoing out-
break at the time of sampling. Methodological differences in
sample collection and culture make comparisons between
studies difficult, and in some cases the true level of environ-
mental contamination may be underestimated.
Patients are the prime source of contamination, so surfaces
in the vicinity of patients that are touched frequently by
HCWs and patientstermed high-touch surfaceshave a
higher frequency of contamination than other sites.11-14 For
example, a recent study defined high-touch surfaces as the
bed rails, the bed surface, and the supply cart, on the basis
of their observed frequency of contact.12 Developing an un-
derstanding of which sites are more likely to be contaminated
with pathogens can guide infection control practice and direct
new innovations.
Areas around patients are frequently contaminated with
MRSA, VRE, and C. difficile.15-17 The frequency of MRSA and
VRE contamination correlates with the number of culture-
positive body sites.13,18,19 Infected patients shed more patho-
gens than those who are only colonized, and diarrhea results
in widespread contamination.13,20,21
Contamination of rooms of unaffected patients has been
reported for C. difficile, MRSA, and VRE. C. difficile was
identified in 16%17% of samples from the rooms of patients
without known C. difficile infection (CDI),22,23 MRSA was
cultured from 43% of beds used by patients not known to
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be MRSA positive,17 and VRE was cultured from 13% of
surfaces in the rooms of patients with unknown VRE status.24
Contamination of rooms of unaffected patients is most likely
to be due to continued viability of organisms shed by previous
occupants17,25,26 but may also result from importation by
HCWs or visitors or from shedding from asymptomatic
carriers.27,28
Relatively few prospective studies have been conducted of
gram-negative or norovirus surface contamination. The fre-
quency of contamination is approximately 5%10% of sur-
faces for gram-negative bacteria29,30 and was found to be
highly variable but less than 20% of surfaces for norovirus
RNA in one pediatric study.31
Highly variable levels of contamination have been re-
ported during outbreaks. Frequent environmental contam-
ination has been identified and implicated as a contributory
factor during continuing outbreaks of C. difficile, MRSA,
VRE, A. baumannii, and norovirus.21,32-35
Contamination of air has been reported, but the inter-
change between contaminated air and surfaces is not well
defined.36,37
concentration o f c ontamination is
sufficient for transmission
In general, colonized or infected patients have a higher con-
centration of contamination than their surrounding sur-
faces.14,19 The concentration of VRE is approximately 103
colony-forming units (CFUs)/50 cm2 on the skin of patients,38
whereas the concentration of C. difficile, VRE, and MRSA
ranges from 103 to 109 CFUs/g in stool.20,39,40 The concentra-
tion of norovirus can be more than 1012 particles/g in stool,41
and patients can vomit more than 107 norovirus particles
assuming a vomit bolus volume of 2030 mL and the fact
that 106 particles/mL need to be present for detection by
electron microscopy.42 In contrast, the concentration of nos-

ocomial pathogens is generally in the range of less than 1 to
100 CFUs/cm2 on surfaces43,44 and is often detected only by
broth enrichment.13,17 Reports of higher concentrations of
surface contamination do occur and include total aerobic
counts of more than 200 CFUs/cm2 both before and after
cleaning45 and more than 15 to more than 100 MRSA colonies
from 23% of sites positive by direct plating in the rooms of
MRSA-positive patients with diarrhea.20
The presence of a pathogen on a surface does not neces-
sarily represent a transmission risk.8 However, the infectious
dose for most environmentally associated nosocomial path-
ogens appears to be low. For example, less than 15 S. aureus
cells were sufficient to cause infection in experimental le-
sions,46 less than 1 CFU/cm2 was sufficient to cause C. difficile
disease in mice,47 and a single norovirus particle is thought
to have the capacity to cause infection.48 Importantly, despite
the comparatively low concentration of contamination on
surfaces compared with that on the skin of patients, touching
a VRE-contaminated surface carries approximately the same
risk for acquisition of VRE on hands as touching an affected
patient.11,14 Therefore, the presence of a pathogen on a surface
at any concentration may be a risk for transmission, and this
is reflected in proposed guidelines for microbiological hygiene
standards.49
nosocomial pathogens can survive
on surfaces for long periods
Studies investigating the survival of nosocomial pathogens on
surfaces were recently reviewed by Kramer et al.50 Under cer-
tain conditions, C. difficile spores, VRE, MRSA, and Acinet-
obacter species can survive for 45 months or more on dry
surfaces, and norovirus can survive for a week or more. Large
variations in survival times in different reports is partly due
to species and strain variation but is also due to differences
in experimental conditions, including inoculum size, humid-
ity, the suspending medium, and the surface material.50
limitations of cleaning a nd
disinfection
Cleaning is the removal of soil and contaminants from sur-
faces, whereas disinfection relates to the inactivation of path-
ogens by use of a disinfectant.8 Microorganisms vary in their
resistance to disinfectants, so agents must be chosen carefully
for their effectiveness, particularly for C. difficile spores.51 Fur-
thermore, the hospital environment is complex and often
difficult to clean, and use of a cleaning agent that is not
effective against the target organism can spread pathogens to
other surfaces.51,52
Liquid disinfectants may damage equipment, especially
electronics, and chlorine-containing materials may corrode
metals.53 Disinfectants can potentially harm users, and the
discharge of waste biocides into the environment may en-
courage the development of both biocide and antibiotic re-
sistance and have other, more general environmentally dam-
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role played by surface contamination in transmission 689
aging effects.53 For these reasons, some authorities have
questioned the use of routine disinfectant decontamination
of the hospital environment and favor instead the use of
detergents only.53 There has been a tendency for disinfectants
to be used in the United States and detergents in Europe.53,54
Recently, United Kingdom and European workers have
moved more toward the use of disinfectants to control MRSA
and C. difficile, but the debate continues while we await more
evidence for the effective use of particular agents.
Cleaning and disinfection does not always eradicate path-
ogens from surfaces. C. difficile was cultured from 44% of 54
surfaces after bleach disinfection in 9 rooms16 and from 16%
of 243 surfaces after bleach disinfection implemented during
an outbreak.35 VRE was cultured from 71% of 102 samples
after bleach disinfection in 17 rooms,16 and it took an average
of 2.8 bleach treatments to eradicate VRE in another study.55
MRSA was cultured from 66% of 124 surfaces in MRSA pa-
tient rooms after cleaning with a detergent sanitizer,17 was
cultured from 16% of 65 sites after bleach and steam cleaning
during an outbreak in a surgical ward,34 and was found at a
concentration of 0.7 CFUs/plate after phenolic disinfection
during an outbreak in a burn unit.44 Contamination has been
identified on apparently clean surfaces during outbreaks due
to A. baumannii 56 and viruses.32 The frequent finding of con-
tamination in empty rooms and in rooms occupied by pa-
tients unaffected by pathogens suggests residual contamina-
tion from previous occupants.26,57 However, the thoroughness
of cleaning and disinfection was not evaluated in these stud-
ies, meaning that it is difficult to determine whether it is the
products, the procedures, or a combination of the two that
is responsible for the failure to eradicate pathogens from
surfaces.
nosocomial pathogens can b e
transfer red from contaminated
surfaces t o the hands o f hcw s
In vitro studies present a picture of rapid dynamic transfer
from surfaces to hands and vice versa (Table 1). For example,
DNA markers dried onto toys were transferred readily to the
hands of researchers and subsequently onto clean toys, and
the markers spread rapidly when introduced into a child care
center.58,59 Similarly, experimentally contaminated fingers se-
rially contaminated multiple surfaces with norovirus.52 Sim-
ilar findings have been reported using surfaces experimentally
contaminated with bacteria and bacteriophage.60,61 Impor-
tantly, experimentally contaminated fingers have been shown
to transfer more than 30% of inoculated bacteria and bacte-
riophage to the mouths of volunteers, with clear implications
for the fecal-oral transmission of nosocomial pathogens.60
Several studies have shown that various bacterial pathogens
can be acquired on the hands of HCWs through contact with
environmental surfaces in the absence of direct patient con-
tact (Table 1).11,13,62,63 Patients and contaminated surfaces ap-
pear to transfer VRE to the hands of HCWs at similar fre-
 table 1. Transfer of Pathogens and Surrogate Markers from Surfaces to Hands
No. (%)
Reference Setting, location Organism(s) Method No. contaminated Comment
60
Rusin et al (2002) Laboratory, USA Bacteria and phage Fomites were experimentally contami- 1020 ... Transfer efficiency was higher for non-
nated with a mixture of bacteria porous fomites (28%66%); gram-
and phage and touched by positive bacteria had the highest
volunteers transfer efficiency (41%)
Jiang et al59 (1998) Child care center, USA Virus surrogate DNA was dried onto toys, which were 5 5 (100) Subsequent transfer of DNA to clean
passed to researchers to hold toys occurred on 3 of 5 occasions
Rheinbaben et al61 (2000) Laboratory, Germany Phage Volunteers contacted an experimen- 14 14 (100) 30%66% of the inoculated virus was
tally contaminated door handle recovered from the hands of
volunteers
Boyce et al13 (1997) Ward side rooms, USA MRSA Hand cultures were performed after 12 5 (42) All 12 HCWs wore gloves
routine patient care without direct
patient contact
Ray et al62 (2002) Wards side rooms, USA VRE Hand cultures were performed after 13 6 (46) 5 of 6 hand cultures were indistin-
5-second contact with bed rail and guishable from environmental cul-
bedside table in rooms of VRE tures by PFGE
patients
Barker et al52 (2004) Laboratory, UK Norovirus Clean fingertips touched contaminated 30 12 (40) 4 of 10 door handles, 5 of 10 tele-
surfaces and then other objects phones, and 3 of 10 taps became
contaminated
Bhalla et al63 (2004) 8 wards, USA Pathogens Hand cultures were performed after 64 34 (53) Positive hand culture results were ob-
5-second contact with bed rail and tained for 24% of 25 rooms that

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bedside table
Hayden et al11 (2008) ICU, USA VRE Hand cultures were performed for 44
HCWs who had negative hand cul-
ture results at study entry and
touched only environmental sur-
had been cleaned after patient
discharge
44 23 (52) Each contact with patient or environ-
mental surface represented a 10%
risk of acquiring VRE

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faces during routine patient care
note. HCW, healthcare worker; ICU, intensive care unit; MRSA, methicillin-resistant Staphylococcus aureus; PFGE, pulsed-field gel electrophoresis; VRE, vancomycin-resistant
enterococci.

quencies.11,14 In a recent study, however, compliance with
hand hygiene was 80% of 142 opportunities after patient
contact compared with only 50% of 196 opportunities after
contact with a patients environment (P p .01, Fisher exact
test), meaning that contamination acquired from a patients
environment is less likely to be dealt with by hand hygiene.64
evidence that surface
contamination contributes to
nosocomial cross-transmission
A number of studies have identified the previous presence of
a colonized or infected patient in a side room as a risk factor
for the acquisition of the same pathogen by a new occupant,
presumably because of residual room contamination that is
not removed through terminal cleaning and disinfection. This
effect has been shown for VRE,19,26,65,66 MRSA,66 C. difficile,67
multidrug-resistant P. aeruginosa,68 and A. baumannii 68 (Table
2). A further strand of evidence suggesting that the contam-
inated surface environment contributes to the transmission
of nosocomial pathogens is the effect of improved cleaning
and disinfection on infection rates.2
The next sections will review evidence that contaminated
surfaces are important in the transmission of C. difficile, VRE,
MRSA, norovirus, and certain gram-negative rods (Table 3).
C. difficile
C. difficile outbreaks were first linked to contaminated sur-
faces in the 1980s.35 Samore et al69 conducted a detailed 6-
month prospective study of all C. difficile cases in a US hos-
pital. The frequency of positive hand culture results and
clinical cultures that matched the pulsotype of the index case
patient among contacts (either roommates, neighbors, or sub-
sequent room occupants of index case patients) correlated
with the intensity of environmental contamination, suggest-
ing that the transmission risk was related to the intensity of
contamination.
Several studies have investigated the effect of improved
environmental hygiene on the incidence of CDI. Mayfield et
al70 showed that switching from quarternary ammonium
compounds to bleach disinfection reduced the incidence of
CDI for high-risk bone marrow transplant patients. However,
no significant reduction in infection rates occurred for lower-
risk patient groups, and environmental contamination was
not quantified. Wilcox et al71 conducted a crossover study in
elderly care wards to compare the effect of routine cleaning
with detergent versus bleach and demonstrated a significant
reduction in infection rates on one ward. No significant re-
duction was demonstrated on the other ward and the fre-
quency of environmental contamination was not reduced in
any study arm, suggesting that other factors were involved.
More recently, Boyce et al43 found that the use of hydrogen
peroxide vapor (HPV) to decontaminate rooms after the dis-
charge of patients with CDI reduced the incidence of CDI in
5 high-incidence wards. The hospital-wide incidence of CDI
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role played by surface contamination in transmission 691
was also reduced, but this was statistically significant only
when the analysis was limited to the months when the epi-
demic NAP1 C. difficile strain was known to be present. An-
other before-after study of HPV by Manian et al72 also re-
ported a significant hospital-wide reduction in the incidence
of CDI.
Recent evidence from an in vitro model provides proof of
concept that C. difficile spores can be transmitted via envi-
ronmental surfaces.47 Mice exposed to an experimentally con-
taminated enclosure became colonized in a dose-dependent
manner, and oxidizing agents, including a chlorine-contain-
ing liquid disinfectant and HPV, effectively reduced the level
of contamination and blocked transmission. A recent study
found that prior room occupancy by patients with CDI in-
creased the risk of C. difficile acquisition, providing evidence
that the in vitro concept translates into the clinical setting
(Table 2).67
VRE
Evidence from several studies suggests that hospital acqui-
sition of VRE is associated with environmental contamina-
tion. Huang et al66 found that admission to a room previously
occupied by a VRE-infected patient significantly increased the
risk of acquiring VRE (Table 2). In this study, other routes
of transmission (which may involve contaminated surfaces
indirectly) accounted for the majority of nosocomial trans-
mission. More recently, Drees et al26 found that VRE acqui-
sition was associated with a positive room culture result be-
fore admittance to the room, with a prior room occupant
positive for VRE, and with any VRE-positive room occupants
within the 2 weeks before admission (Table 2). A recent co-
hort study of HPV decontamination in 6 intensive care units
found that patients admitted to rooms decontaminated by
HPV were less likely to acquire VRE than were patients ad-
mitted to rooms cleaned using standard methods when the
prior room occupant was positive for VRE (incidence rate
ratio, 0.22).73
In addition to patient-level analysis, several studies have
shown that improved environmental hygiene can reduce the
general incidence of VRE. Hayden et al57 investigated the
effect of environmental and hand hygiene improvements on
VRE infections in an intensive care unit. An educational im-
provement program for environmental cleaning reduced the
frequency of contamination in the rooms of patients with
and without VRE infection, and the incidence of VRE ac-
quisition fell. The reduction in contamination was sustained
through a washout period during which no further inter-
vention occurred and through a subsequent hand hygiene
educational improvement program. The study by Manian et
al72 that demonstrated a reduction in CDI following the use
of HPV environmental decontamination also demonstrated
an association with a significant hospital-wide reduction in
the incidence of VRE.
 table 2. Effect of the Colonization or Infection Status of the Prior Room Occupant on the Acquisition of Pathogens by Subsequent Occupants of the Same Room
Setting Did not Percentage Adjusted ratio
Reference (study design) Findings Variables Acquired acquire difference (95% CI)
Martinez et al65 ICU, USA (9-month Placement within a room from Admitted to room from which VRE had been 13% of 30 2% of 60 87.5 OR: 81.7 (2.23,092)
(2003) retrospective case- which VRE had been cultured cultured
control study) was associated with VRE ac-
quisition in the subsequent
room occupant
Drees et al26 ICU, USA (14-month Positive VRE room culture re- Positive culture before admission or acquisition 8.0% of 50 4.8% of 588 40.5 HR: 4.3 (1.512.5)
(2008) prospective cohort sults or previous VRE-positive Prior room occupant with VRE 38.0% of 50 20.2% of 588 46.7 HR: 3.8 (2.07.3)
study) room occupants were associ- Any room occupant with VRE in past 2 weeks 60.0% of 50 41.8% of 588 30.3 HR: 2.7 (1.45.3)
ated with VRE acquisition
Nseir et al68 ICU, France (12-month Admission to a room previously Prior room occupant with A. baumannii 28.1% of 57 7.9% of 454 71.8 OR: 4.2 (2.08.8)
(2010) prospective cohort occupied by an A. bauman- Prior room occupant with P. aeruginosa 25.6% of 82 14.9% of 429 41.7 OR: 2.3 (1.24.3)
study) nii or P. aeruginosapositive
patient was associated with
acquisition of these pathogens
Prior room occupant status
Positive Negative
(% acquired) (% acquired)
Huang et al66 ICU, USA (20-month Admission to a room previously VRE status of prior room occupant 4.5% of 1,291 2.8% of 9,058 37.1 OR: 1.4 (1.01.9)
(2006) retrospective cohort occupied by a MRSA- or MRSA status of prior room occupant 3.9% of 1,454 2.9% of 8,697 28.8 OR: 1.4 (1.11.8)
study) VRE-positive patient was as-
sociated with acquisition of

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these pathogens
Shaughnessy ICU, USA (18-month Admission to a room previously C. difficile status of prior room occupant 11.0% of 91 4.6% of 1,679 58.3 HR: 2.3 (1.24.5)
et al67 (2008) retrospective cohort occupied by a C. diffi-
study) cilepositive patient was asso-
ciated with C. difficile
acquisition

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note. Martinez et al,65 Drees et al,26 and Nseir et al68 compared associations listed in the Variables column in patients who did acquire the pathogen with patients who did not acquire the pathogen;
Huang et al66 and Shaughnessy et al67 compared the frequency of patients who acquired the pathogen depending on the status of the prior room occupant. CI, confidence interval; HR, hazard ratio;
ICU, intensive care unit; MRSA, methicillin-resistant Staphylococcus aureus; OR, odds ratio; VRE, vancomycin-resistant enterococci.

MRSA
74
Dancer recently reviewed evidence that environmental con-
tamination makes an important contribution to the trans-
mission of MRSA. That review summarized evidence that
staphylococci are carried by people and shed into the envi-
ronment, can survive for extended periods on surfaces, and
can spread between people and the environment and that
improved hygiene reduces staphylococcal infection rates.
Dancer reviewed prospective studies25,75 investigating the role
played by contaminated surfaces in the transmission of MRSA
(Table 3). More recently, Dancer et al76 conducted a ward
crossover study to investigate the effect of an extra cleaner,
focusing on hand-touch sites. The enhanced cleaning was
associated with a significant reduction in the total aerobic
counts on surfaces and in the number of failures to reach a
hygienic standard considered to be acceptable (more than 2.5
CFUs/cm2) and with a significant reduction in MRSA ac-
quisition by patients. However, there was no significant re-
duction in surface contamination with methicillin-susceptible
S. aureus and MRSA admission screening was not universally
applied, so the true MRSA acquisition rate was uncertain.
Nonetheless, the study provides further evidence to support
the view that reducing surface contamination reduces MRSA
nosocomial transmission.
Gram-Negative Rods
A recent prospective cohort study showed that prior room
occupancy by a patient colonized or infected with A. bau-
mannii or P. aeruginosa was a significant risk factor for the
acquisition of these pathogens. This was the first evidence
from an endemic setting that contaminated surfaces contrib-
ute to the transmission of gram-negative rods (Table 2).68
Numerous outbreaks of A. baumannii have been associated
with contaminated inanimate fomites, which resolve once the
common source is identified and removed, replaced, or ad-
equately disinfected.2 Several outbreaks in which environ-
mental surfaces were contaminated but a common source
was not identified offer limited evidence that surface con-
tamination also plays a role in continued transmission.33,77,78
For example, during a A. baumannii outbreak in the United
Kingdom affecting 19 patients in a neurosurgical unit, 53%
of 51 surfaces in the unit were contaminated with the out-
break strain, and monthly screens showed that the frequency
of contamination correlated with the number of affected pa-
tients in the unit.33 Crucially, failure to maintain low levels
of contamination resulted in increases in patient colonization,
suggesting that the contamination was contributing to the
outbreak. However, it was not possible to prove causality
because neither molecular epidemiological analysis nor hand
cultures were performed.
Further evidence for the role played by contaminated sur-
faces in the transmission of A. baumannii comes from an
investigation of a multi-institutional outbreak of A. bauman-
nii among war-wounded US soldiers.79 In this study, outbreak
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role played by surface contamination in transmission 693
strains of A. baumannii were cultured from 21% of 175 sur-
faces in 7 field hospitals, but a very low frequency of con-
tamination was identified in soil samples and on the skin of
healthy soldiers.
The continued emergence of multidrug-resistant gram-
negative rodsin particular those producing carbapenemases
such as Klebsiella pneumoniae carbapenemase and New Delhi
metallo-b-lactamasemeans that there is an urgent need to
understand the epidemiology of these pathogens, including
the extent to which contaminated surfaces contribute to their
transmission.80,81
Norovirus
Compelling evidence for the role played by surface contam-
ination in the transmission of norovirus comes from out-
breaks affecting epidemiologically distinct cohorts of passen-
gers on boat trips.82-84 For example, an outbreak affected 74%
of guests on 3 consecutive houseboat trips.82 An environ-
mental investigation identified norovirus RNA on 71% of
surfaces in bathrooms, kitchens, and door handles, and fomite
contamination appeared to contribute to continuation of the
outbreak over the 3 trips.
Several investigations have identified surface contamina-
tion with norovirus in the absence of other potential reser-
voirs during continuing outbreaks. During one outbreak in
a long-term care facility, norovirus RNA was identified on 5
of 10 environmental sites collected after phenolic disinfection,
suggesting widespread persistent contamination.32 Positive
sites included an elevator call button used only by staff. The
outbreak resolved following a second, more thorough facility-
wide disinfection, suggesting that environmental contami-
nation contributed to transmission. Various community out-
breaks have been linked to shared computer keyboards,85
specific episodes of vomiting (for example, a kitchen assistant
vomited into a sink that was used to prepare vegetables),86,87
contamination of carpets after a hospital outbreak,88 and per-
sistent widespread contamination in a United Kingdom
hotel.89 However, a key limitation of these studies is that the
role played by symptomatic or asymptomatic staff carriage
in transmission often was not investigated. Thus, prospective
studies are required to quantify the role played by surface
contamination in the spread of norovirus.
environmental cleaning,
disinfection, and infection c ontrol
Improving the Efficacy of Cleaning and Disinfection
Several studies have demonstrated that focused efforts can im-
prove the efficacy of cleaning. For example, Eckstein et al16
found that a research team was able to eradicate persistent VRE
and C. difficile from surfaces, whereas a housekeeping team
was not. In addition, improved monitoring of cleaning by
means of markers invisible to the naked eye or routine quan-
titative microbiological culture and educational interventions
 table 3. Studies Investigating the Role Played by Contaminated Surfaces in the Endemic Transmission of Nosocomial Pathogens
Reference Setting, location Organism Study design Key findings
Samore et al69 (1996) Hospital-wide, USA C. difficile 6-month prospective observational study Frequency of transmission correlated with the intensity of envi-
ronmental contamination
Mayfield et al70 (2000) 3 units, USA C. difficile 18-month prospective before-after study of a Significant reduction in CDI incidence in the highest-risk unit
switch from QAC to bleach disinfection (from 8.6 to 3.3 cases per 1,000 patient-days)
Wilcox et al71 (2003) 2 units, UK C. difficile 2-year prospective ward crossover study of a Significant reduction in CDI incidence in one of the units (from
switch from detergent to bleach disinfection 8.9 to 5.3 cases per 100 admissions) but not in the other
Boyce et al43 (2008) Hospital-wide, USA C. difficile 20-month prospective before-after study of rou- Significant reduction in CDI incidence in 5 high-incidence units
tine use of HPV decontamination (from 2.3 to 1.3 cases per 1,000 patient-days); lesser reduc-
tion in CDI incidence hospital-wide
Manian et al72 (2010) Hospital-wide, USA C. difficile/VRE 24-month prospective before-after study of rou- Significant reductions in C. difficile (from 1.0 to 0.5 cases per
tine use of HPV decontamination 1,000 patient-days) and VRE (from 0.3 to 0.15 cases per
1,000 patient-days); substantial but not statistically significant
reductions in MRSA and Acinetobacter species
Bonten et al19 (1996) ICU, USA VRE 2-month prospective observational study 23% of 13 patients admitted to VRE-contaminated rooms ac-
quired VRE
Hayden et al57 (2006) ICU, USA VRE 9-month prospective before-after study of edu- Frequency of environmental contamination was reduced; patient
cational improvement of cleaning and hand acquisition of VRE was reduced from 33 to 17 acquisitions
hygiene per 1,000 patient-days during the improved cleaning phase
Passaretti et al73 (2008) ICU, USA VRE 12-month prospective cohort study investigating HPV was protective against VRE acquisition when the prior
the effect of HPV decontamination room occupant had VRE (IRR for patients admitted to rooms
decontaminated using HPV vs standard methods, 0.22)
Hardy et al25 (2006) ICU, UK MRSA 14-month prospective observational study More than 10% of acquisitions were likely to be have been di-

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rectly from the environment
Mahamat et al75 (2007) Hospital-wide, UK MRSA 8-year prospective interrupted time-series analy- Introduction of bleach disinfection, environmental sampling, al-
sis of multiple infection control interventions cohol gels, and admission screening all reduced the preva-
lence of MRSA
Dancer et al76 (2009) 2 wards, UK MRSA 12-month prospective crossover study of the ef- Enhanced cleaning was associated with significant reductions in
fect of 1 extra cleaner surface contamination, hygiene failures, and MRSA

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acquisition
note. CDI, Clostridium difficile infection; HPV, hydrogen peroxide vapor; ICU, intensive care unit; IRR, incidence rate ratio; MRSA, methicillin-resistant Staphylococcus aureus;
QAC, quarternary ammonium compound; VRE, vancomycin-resistant enterococci.

have been shown to improve cleaning efficacy.49,90-92 However,
the long-term effect of educational cleaning improvements has
not yet been evaluated fully.93
Dancer49 proposed setting standards for environmental hy-
giene audited by routine microbiological culturea process
currently not recommended by the CDC.8 The introduction
of routine environmental sampling was associated with a re-
duction in MRSA prevalence in one study75 and standards
exist for the quality of air in operating theaters,94 so why not
for surfaces in healthcare settings? Regardless of whether we
return to routine microbiological sampling in hospitals, as
was done in the 1970s,6 improved sampling methods to assess
the frequency and concentration of surface contamination
would be useful.
Technological developments to assist with cleaning and
disinfection include the introduction of microfiber cleaning
materials, which may be more effective than standard cloths
for removing pathogens from surfaces.95 The use of aden-
osine triphosphate analysis as a rapid surrogate test for the
assessment of surface hygiene is becoming a popular mon-
itoring method but does not necessarily correlate with mi-
crobial contamination.95 Designers and manufacturers of
hospital equipment can help by producing hospitals that
are easier to clean.96 For example, the Design Bugs Out
initiative (http://www.designcouncil.org.uk/designbugsout)
in the United Kingdom aims to design hospital furniture
and equipment that is easier and quicker to clean.
New liquid disinfectants boast improved efficacy and prac-
ticability, reducing the risk for human error during formu-
lation.53 However, liquid detergents and disinfectants rely on
the operator to ensure adequate distribution and contact time.
Area decontamination methods such as HPV,17 aerosolized
hydrogen peroxide,97 and UV radiation98 do not rely on the
operator to ensure distribution and contact time and are
generally more efficacious than conventional terminal dis-
infection. However, they require areas to be vacated and pre-
cleaning to remove visible soil, and they take longer and are
more expensive than conventional terminal disinfection. Fur-
ther research is required to determine when use of these
methods is cost-effective.99
Reducing and Controlling the Extent of Environmental
Contamination
In addition to improving the efficacy of cleaning and dis-
infection once contamination has occurred, steps can be taken
to prevent or reduce the incidence of recontamination. Rapid
identification and isolation of affected patients could reduce
contamination of bays and open ward areas shared by un-
affected patients.100 Identification and isolation of asymptom-
atic shedders may also play a role. Asymptomatic carriers of
C. difficile were a source of widespread contamination in one
study,28 and asymptomatic fecal carriage of small round virus
(probably norovirus) was common in another study in a long-
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All use subject to JSTOR Terms and Conditions
role played by surface contamination in transmission 695
term care facility.27 Further work is required to determine the
extent and length of time that patients continue to shed path-
ogens into the environment after the resolution of symptoms,
particularly for C. difficile and norovirus.
A novel approach to reducing environmental contamina-
tion is source control by daily washing of the skin of pa-
tients with chlorhexidine.38 This process has been shown to
reduce contamination of patient skin, environmental surfaces,
and the hands of HCWs and to reduce the incidence of VRE
transmission. It is possible that controlling contamination at
the source may be effective in reducing the incidence of trans-
mission of other pathogens as well. Source control could be
used in conjunction with complementary strategies aimed at
improving cleaning and disinfection to further reduce trans-
mission. However, chlorhexidine is not effective against
spores and resistance may emerge, so novel source control
strategies are warranted.
Improvements in hospital design and surface science can
help to reduce the potential for contamination.101 Copper,
silver, and other antimicrobial-impregnated materials reduces
bacterial survival in vitro,102 and numerous antibacterial sur-
face materials or treatments are now available. However, such
treatments do not remove the need for cleaning, and there
is very limited evidence that they have any significant effect
on hospital infection rates. The results of carefully designed
trials are awaited.
Improving the Quality of the Evidence
The quality of evidence supporting the role played by surface
contamination in transmission has improved from outbreak
reports to large, well-designed prospective studies (Tables 2
and 3). Structured reporting of future outbreaksfor ex-
ample, by using the ORION guidance103will help, but large,
prospective controlled trials are needed to properly elucidate
the role played by surface and air contamination (and de-
contamination) in the transmission of nosocomial pathogens.
Most of the evidence investigating the role played by con-
taminated surfaces in transmission comes from acute care
facilities. However, environmental contamination may play
an important role in transmission in long-term care facilities
and other nonacute healthcare facilities.28,32 There is consid-
erable evidence that contaminated environmental surfaces are
involved in the transmission of norovirus in the commu-
nity,86-89 and there is emerging evidence that contamination
with pathogens such as community-associated MRSA may be
involved in transmission in outpatient and community set-
tings.104-106 Environmental interventions that are effective for
the prevention and control of the transmission of pathogens
in acute healthcare facilities may not be effective in com-
munity and nonacute settings. Therefore, further research is
required to investigate the role played by surface contami-
nation in the transmission of pathogens in nonacute and
community settings.
696 infection control and hospital epidemiology
conclusion
The historical perspective that contaminated surfaces con-
tribute negligibly to nosocomial transmission has been re-
evaluated in light of new information. There is now com-
pelling evidence that contaminated surfaces make an
important contribution to the epidemic and endemic trans-
mission of C. difficile, VRE, MRSA, A. baumannii, and P.
aeruginosa (Tables 2 and 3) and to the epidemic transmission
of norovirus. However, few studies have quantified the link
between contaminated surfaces and the risk of transmission.
This is in part due to the difficulties in conducting research
in this area because of the multifaceted nature of nosocomial
transmission (Figure 1). In addition, the widespread view that
contaminated surfaces are relatively unimportant in trans-
mission has meant that fundholders and administrators have
not commissioned research in this area until relatively re-
cently. There is now sufficient evidence to support further
studies in this area to identify the best methods of achieving
and maintaining clean hospitals and to evaluate the cost and
effectiveness of such interventions with respect to reducing
the incidence of hospital-associated infections. In particular,
there is a need to conduct large, high-quality prospective
controlled trials to identify interventions that significantly
reduce surface contamination and transmission.
acknowledgments
Potential conflicts of interest. J.A.O. and S.Y. are employed by Bioquell UK
Ltd. G.L.F. reports no conflicts of interest relevant to this article.
Address correspondence to Gary L. French, MD, FRCPath, Infection and
Immunology Delivery Unit, 5th Floor, North Wing, St. Thomas Hospital,
Lambeth Palace Road, London SE1 7EH, UK (gary.french@kcl.ac.uk).
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