CSIRO PUBLISHING

Healthcare Infection, 2013, 18, 23–30

http://dx.doi.org/10.1071/HI12047

Methods to evaluate environmental cleanliness

in healthcare facilities

Brett G. Mitchell1,2,3,6 MAdvP, DTN, BN, CICP

Fiona Wilson2 RN, MAdvPrac IC&P, CICP
Stephanie J. Dancer4 MSc, BSc, MBBS
Alistair McGregor2,5 FRACP, FRCPA
1
Australian Catholic University, School of Nursing Midwifery and Paramedicine, PO Box 256,
Canberra, ACT, Australia.
2
Tasmanian Infection Prevention and Control Unit, GPO Box 125, Hobart, Tasmania, Australia.
3
University of Tasmania, School of Nursing and Midwifery, Hobart, Tasmania, Australia.
4
Department of Microbiology, Hairmyres Hospital, East Kilbride, United Kingdom.
5
Department of Microbiology and Infectious Diseases, Royal Hobart Hospital, Hobart, Tasmania, Australia.
6
Corresponding author. Email: bgmitc001@myacu.edu.au

Abstract. Background: The role of environment in infection prevention and control is being increasingly
acknowledged. However, gaps remain between what is promoted as best practice in the literature and what is occurring
in healthcare settings. In part, this is due to a lack of generally accepted scientific standards, further confounding the
ability to demonstrate an undisputed role for the healthcare environment in healthcare-acquired infections (HAIs).
Evaluating environmental cleanliness in a standardised format is required, in order to enable a framework for
performance management and provide a method by which interventions can be evaluated. Standardised assessment
would provide reliable data to support quality-improvement activities and to ensure that healthcare staff have relevant
and useful information to inform and adapt practice.
Methods: This integrative literature review describes approaches to assessing environmental cleanliness. A search
of the published literature was undertaken, in combination with a targeted review of the grey literature.
Results: Four methods for assessing environmental cleanliness were identified: visual inspection, fluorescent gel
marker, adenosine triphosphate (ATP) and microbial cultures. Advantages and disadvantages for each are explored.
Conclusion: Methods that evaluate cleaning performance are useful in assessing adherence to cleaning protocols,
whereas methods that sample bio-burden provide a more relevant indication of infection risk. Fast, reproducible, cost-
effective and reliable methods are needed for routine environmental cleaning evaluation in order to predict timely
clinical risk.

Received 26 October 2012, accepted 19 December 2012, published online 27 February 2013

Background Microorganisms acquired from these sites may then be

There is currently no single solution for controlling transferred to other patients. In the past, the role of the
healthcare-associated infections (HAIs). Key elements inanimate hospital environment in the spread of HAIs has
for preventing infection in healthcare environments been controversial but there is increasing evidence to support
include hand hygiene, environmental cleanliness, isolation the environment as a reservoir for hospital pathogens and
and barrier precautions, surveillance and antimicrobial transmission risk.1
stewardship. To understand how the environment may play The potential for contaminated environmental surfaces to
a part in the acquisition of infections, it is important to facilitate HAIs depends on several factors, including:
consider the role of the patient. For example, individuals *
ability of pathogens to remain viable on environmental
colonised with microorganisms can contaminate their surfaces
environment, whereupon these microorganisms can be *
frequency by which organisms contaminate surfaces
transferred to other sites, most commonly by peoples’ hands. *
location of reservoirs

Journal compilation Ó Australasian College for Infection Prevention and Control 2013 www.publish.csiro.au/journals/hi
24 Healthcare Infection B. G. Mitchell et al.

Published studies demonstrating the importance of

Implications cleaning in outbreaks underscore the role that environmental
*
Environmental contamination plays a role in the contamination plays in the transmission of HAIs.20,21
transmission of HAIs Multiple studies have shown that enhanced cleaning
*
Four methods are commonly used to evaluate significantly decreases environmental contamination by a
standards of cleanliness range of pathogens associated with HAIs.18,22–25 Despite
this, considerable international debate exists regarding the
*
Fast, reproducible, cost-effective and reliable
role of the environment and HAIs, including methods to
methods are needed for routine environmental
evaluate environmental cleanliness. The public has linked
cleaning evaluation
the visual appearance of a hospital with the risk of HAI but
*
A definition for ‘clean’ which relates to clinical risk
more evidence is required to support this view.26,27
for patients is required
The role of environmental cleaning has been
acknowledged and promoted in national guidelines, with
*
hand-touch frequency of surfaces many government-sponsored documents prescribing some
*
adequate contamination levels to present a transmission form of quality-assurance audit or assessment. However, gaps
risk2 remain between what is outlined as best practice and what
*
pathogen infectivity index actually takes place in hospitals. In part, this is due to a lack
Survival time for pathogens in the environment varies of generally-accepted scientific standards,28 which further
considerably and depends upon the particular characteristics confounds the ability to demonstrate an undisputed role for
the healthcare environment in HAIs.29–32
of the organism. Staphylococcus aureus remains capable of
causing infection for at least 10 days after inoculation onto Methods
a dry surface.3 Evidence for longevity of microorganisms
in the environment is supported by numerous studies.4–7 Aim
Unless adequate cleaning is undertaken, microorganisms in The aim of this review is to describe the approaches used to
the healthcare environment may contaminate hands or be assess environmental cleanliness.
deposited onto a patient or surfaces near a patient by air
currents.8–12 Frequently handled sites are of particular Study design
importance. Microorganisms do not discriminate between An integrative review design was used.
environmental sites and when they persist on sites that are
likely to be touched, there is increased risk of onward Search methods
transmission to patients via healthcare workers’ hands. Identifying information on methods to evaluate
Several studies have shown that persistence of environmental cleanliness involved two strategies. First,
microorganisms in the environment leads to an increased risk searches of online databases Medline, Cinahl and PubMed,
of infection in patients subsequently admitted to a room examining articles published in English, using keywords
previously occupied by a patient colonised or infected with were performed. The keywords used in the search strategy
that particular organism.13 Environmental contamination in were ‘healthcare associated infection’, ‘healthcare-acquired
conjunction with colonisation pressure (i.e. proportion of infection’, ‘hospital-acquired infection’, ‘infection control’,
patients colonised or infected with an organism in a ward or ‘cleaning’, ‘environmental cleanliness’ and ‘environment’.
unit) is thought to encourage transmission of microorganisms. The second strategy was to identify information located in
This explains the transmission of organisms such as the grey literature. This involved searching infection-control
methicillin-resistant Staphylococcus aureus (MRSA), professional organisations’ websites and Australian state
Clostridium difficile and vancomycin-resistant enterococcus government and territory infection control unit websites. In
(VRE) in the healthcare environment, and represents the best the case of Australian state-based infection-control units, we
evidence for an environmental role in HAI.14–17 also conducted interviews by phone. To identify further
Microorganisms are found on a large number of surfaces information in the grey literature a specific search of national
in the healthcare environment. Items in close proximity to the guidelines in Australia (National Health and Medical
patient tend to be more heavily contaminated than more Research Council) the United Kingdom (Department of
remote sites.18 It has been suggested that the greatest risk of Health) and the Centers for Disease Control and Prevention
acquiring pathogens arise from near-patient items such as (CDC) was conducted.
bedrails and bedside tables, as contamination of these sites
provides frequent opportunity for hands to touch and transfer Data abstraction and synthesis
organisms. Paradoxically, the thoroughness of cleaning The abstracts of all published articles identified in the
sometimes appears to be oriented towards sites that are literature search were analysed chronologically. In articles
traditionally or aesthetically important, or physically easier to that obtained information in evaluating environmental
clean, such as walls and floors, rather than these high-risk cleanliness, a review of the article was conducted and notes
sites.19 made on the key findings and themes. Information obtained
Methods to evaluate environmental cleanliness Healthcare Infection 25

through this process was reviewed by two researchers. typically passing between 17–93% more surfaces as ‘clean’
Information obtained via the grey literature search and from than other assessment methods.
phone interviews was summarised. Where information was
obtained via a phone interview, the researchers provided the Fluorescent gel marker
interviewee with a summary of the extracted key points to This method employs an invisible transparent gel that
ensure their views were accurately reported. dries on surfaces and resists dry abrasion, but is easily
removed with light abrasion after wetting. The gel is visible
Results only under ultraviolet (UV) light so thoroughness of cleaning
A total of 124 published articles were reviewed. These can be determined by using UV illumination for sites where
described methods for assessing both the efficacy of cleaning the gel was applied before cleaning (Fig. 1). We identified
and the extent of environmental contamination in the studies that used this method to assess the thoroughness of
hospital environment. Methods for assessing environmental routine hospital cleaning and the subsequent effect of cleaning
cleanliness were assessed as one of two main types: process interventions.19,29,38–42
evaluation, where the cleaning process is monitored by visual The fluorescent gel method demonstrates frequent lack of
inspection or by using a fluorescent gel marker; and outcome attention to high-risk surfaces in the near-patient zone.
evaluation, where cleanliness is evaluated with the use of Targeting objects and their subsequent evaluation following
adenosine triphosphate (ATP) or microbial cultures.13 We cleaning has been shown to take less than two minutes per
present the findings within these two categories in conjunction room for each activity, permitting cleaning evaluation to be
with a summary of current Australian and international undertaken on a large scale.38
practices.
Outcome evaluation
Process evaluation Adenosine triphosphate bioluminescence
Visual inspection The measurement of ATP is the first of two methods
The primary method for assessing the cleanliness of commonly employed for sampling bio-burden in the hospital
healthcare environments is visual inspection.33 Visual environment. Sampling a surface for ATP measures the
inspection detects visible dirt, dust, rubbish, stains, soiling amount of organic soil present. This method uses a specialised
and moisture. Environmental cleanliness audits reliant upon swab to sample a standardised area. The swabs are placed in a
visual inspection are generally undertaken by environmental detection device that uses the firefly enzyme and substrate
cleaning staff, and the effectiveness of these is intermittently luciferase and luciferan, respectively, to catalyse a reaction
assessed by healthcare professionals such as infection control with ATP. Light output from the reaction is proportional to
staff or trained monitoring consultants.30,31 the amount of ATP present, and can be measured with a
We identified quantitative studies that compared the luminometer (measured in relative light units or RLUs)
performance of visual assessments with results from (Fig. 2). While considerable variation can occur among
microbial swabbing or ATP assays in the healthcare readouts34,43 and in the sensitivity of commercially available
environment.23,33–37 In these six studies, visual assessment systems,44 very low readings are typically associated with low
was reported to perform poorly at identifying microbial load, aerobic colony counts (ACC) on surfaces.45

Fig. 1. Examples of a fluorescent marker. Note: Pictures of the DAZO Fluorescent Marking Gel and UV Light pen
are used with permission from Ecolab.
26 Healthcare Infection B. G. Mitchell et al.

Fig. 2. Example of an ATP bioluminescence system. Note: Pictures of the 3M Clean-Trace system are used with permission
from FOSS.

Adenosine triphosphate measurement has been used to sample surfaces, and the choice of sampling method will
evaluate cleanliness of food preparation surfaces for over affect microbial colony counts. Dipslides have been evaluated
30 years.13,33 It is increasingly used in studies of hospital as having superior sensitivity and consistency, particularly
surface contamination where ATP data is gathered in for dry surfaces, while swabs will not always accurately
addition to microbial swabbing, either to evaluate cleaning detect surface bio-burden and may retain bacteria within the
performance or to test the success of a cleaning swab bud itself52–54 Finally, there is an airborne component
intervention.23–25,33–36,43,45,46 of infection risk in a ward and this can often be overlooked
Adenosine triphosphate measurements provide in environmental sampling studies. Settle plates and air
quantification of organic material collected from a swab, samplers have been used to measure airborne contamination
including viable bacteria, but also including non-viable caused by floor mopping and bed making, as well as routine
bacteria and organic debris such as food and liquids such cleaning.55–57
as milk, blood or urine.34 Thus, an ATP result represents a In today’s hospitals, environmental sampling typically
quantitative indicator of all of these. However, it is possible targets a range of surfaces within wards or work stations as
to distinguish the ratio of microbial to non-microbial well as equipment. It involves the use of swabs or dipslides to
components of an ATP measurement by enzymatic removal culture organisms in order to gain a quantitative colony count
of non-bacterial ATP before the assay. Studies that have and/or to detect the presence of specific bacteria. This type of
done this calculated that 33% of the ATP load was attributable investigation is generally only recommended as part of an
to microbial organisms.33,47 ongoing outbreak investigation, as a research study, or as
For this reason, ATP measurements illustrate low part of policy or process evaluation because the time taken to
sensitivity and specificity in detecting bacteria, with one study enumerate microbial counts or identify pathogens may be at
finding that one ATP measurement system had a sensitivity least two days, and requires specific expertise as well as
and specificity of just 57%.43 ATP measurements can also access to a microbiology laboratory.31,58
be compromised by factors such as residual detergents or
disinfectants including sodium hypochlorite,48,49 eroded Costs
surfaces,33 plasticisers found in microfibre cloths or
ammonium compounds found in laundry products.50 These We estimated costs of three of the assessment methods –
factors may all impact on ATP readings.34 fluorescent gel marker, ATP and microbiological sampling.
The costs were based on a 350 bed hospital with an
assumption that 10% of hospital beds would be sampled per
Microbial methods quarter, with 6 high-touch areas screened around individual
Microbial methods for evaluating environmental cleaning beds. This equates to 140 bed areas assessed per annum with
have long been used to evaluate surface contamination 840 high-touch areas sampled. Costs were sought from the
and have been employed in hospitals to assess surface manufacturers of the fluorescent gel marker and ATP as
cleanliness.51 Through the late 1950s and 1960s, well as via an Australian microbiology laboratory which
microbiological sampling was common practice as part of is National Association of Testing Authorities (NATA)
on-going hospital monitoring programs and accordingly, accredited to assess environmental surface swabs.
colony counts, Rodac plate counts, and quantitative air The complete fluorescent gel marker system included
sampling were all routinely used in the hospital environment, initial set-up costs, direct data-entry devices, reporting
including screening of inanimate objects13,51 Swabs, software with the gel markers and UV lights. The kit cost
dipslides, sampling sponges and settle plates may all be used to approximately A$9500 for the first year, with costs decreasing
Methods to evaluate environmental cleanliness Healthcare Infection 27

by approximately A$1300 to $A8200 per annum for A review of the literature demonstrates that benefits and
subsequent years. This cost could be reduced to approximately limitations exist for all methods of environmental cleaning
A$900 per annum if gel markers and UV lights only are evaluation. These are summarised in Table 1.
purchased and the training and development of a reporting
matrix was done in-house with costs absorbed by the Discussion
organisation. The initial set-up costs of the ATP system were
Increasing focus on methods for quantitative assessment of
calculated to be approximately A$10 000 with a per annum
cleanliness in hospital environments has highlighted many of
running cost of around $A5000. Again these costs do not
the shortcomings of visual assessment. These studies reiterate
include any software and are only calculated using the costs
that a visual appraisal of cleanliness is not a proxy for adequate
of ATP swabs and luminometer. Microbiological methods
decontamination. While visual assessment of the cleanliness
had a range of costs depending on whether non-selective or
of a hospital ward, surface or item may satisfy aesthetic
selective plates were used, and/or settle plates and/or diluent
obligations, it cannot reliably assess the infection risk posed
methods were used. Estimated costs of A$6300–A$11 620 per
to patients.28 It is the cheapest and quickest of all methods
annum also includes the reporting fee.
described in this report however, requiring less training and
fewer personnel than other methods. As a means of measuring
Australian practices the efficacy of hospital cleaning and personnel performance,
The most commonly used method for assessing visual inspection has its merits as it is the only method that
environmental cleaning within Australian healthcare can quickly assess a large number of surfaces for gross
facilities is visual assessment with a variety of methods deficiencies in a hospital ward that may harbour pathogens.
and programs in use. No jurisdictions routinely use any As with visual assessment, the fluorescent gel method
alternative methodologies such as fluorescent markers, evaluates cleaning performance rather than environmental
ATP bioluminescence or microbial counts for assessing contamination per se and relies upon the assumption that
environmental cleanliness. improved cleaning procedures can reduce environmental
sources of pathogens and thus risk of microbial
transmission.22,61 Furthermore the fluorescent gel method
Local and international guidelines can provide a more standardised approach to process
Routine environmental sampling is not recommended as evaluation compared with visual inspection. Addressing
part of the Australia National Health and Medical Research cleaning performance remains a vital step in the evaluation of
Council guidelines owing to the limitations of the methods environmental cleaning and the use of a fluorescent marking
available. Thus, cleaning audits are mainly carried out via system to monitor cleaning can provide an effective method
visual assessment. A role for environmental sampling may be to accomplish this.
considered in the management of a specific situation.31 The benefits of using ATP measurements to evaluate
In the United Kingdom, a self-assessment framework hospital cleanliness are speed of data collection,35 ease of
known as the Patient Environment Action Team (PEAT) was use36 and the facility to benchmark.
used in all hospitals with more than 10 beds. One component Limitations of ATP measurement systems are found in
of this benchmarking tool enabled hospitals to perform both the propensity of systems to produce false positives, and
an annual assessment of environmental cleanliness. The in the ability of the system to produce consistent results for
cleanliness of both the hospital environment and clinical and all sampling assessments and surfaces. In addition, the low
non-clinical equipment was visually assessed. The results of sensitivity and specificity along with the wide range of
the annual audit could then be benchmarked with the aim factors that can compromise ATP measurements could be
of improving non-clinical services. Each year, a proportion considered to be too unreliable to justify stringent monitoring
of PEAT assessments were validated by an independent using this method alone.
member.59 In January 2012, a replacement for the PEAT Microbiological evaluation of hospital surfaces provides
program was proposed. The development of a patient- lead the most accurate indication of infection risk of all the methods
inspection program is currently underway to replace the discussed because it can detect and quantify viable bacteria
PEAT program. The National Institute for Health and Clinical and fungi. Reasons for not advocating microbiological
Excellence also has a quality-improvement statement for evaluations in all situations centre on the time and resources
environmental cleanliness.60 required to process conventional microbiological cultures.
In the United States of America, the Healthcare Infection While microbiological methods can produce results with
Control Practices Advisory Committee (HICPAC) Guidelines high specificity, sampling techniques have varied sensitivity
for Environmental Infection Control in Health-Care Facilities and often underestimate bio-burden on a surface, thereby
do not outline any specific methodology for assessing hindering accurate assessments of surface contamination
environmental cleanliness, but they do recommend limiting and study comparability.34
microbiological sampling for use in quality assurance A limiting factor for all of the assessment methods studied
purposes, epidemiological investigations or for research is the cost. None of the methods are particularly cheap but
purposes.58 savings could be made if the testing protocol and reporting
28 Healthcare Infection B. G. Mitchell et al.

Table 1. Summary of methodologies

Advantages DisadvantagesA
Assessing performance
Visual inspection Ease of use for large areas (wards, rooms) Subjective
Can be done with minimal training Does not assess bio-burden
Benchmarking possible Does not correlate with bio-burden
Simple and inexpensive Can be confounded by clutter, fabric deficits and odours
Fluorescent gel Quick Does not assess bio-burden
Provides immediate feedback on performance Could be labour intensive as surfaces must be marked
before cleaning and checked post cleaning
Minimal training required Potentially costly
Objective Emphasis on easily visible non-high-touch
surfaces (walls, floors)
Benchmarking possible
Assessing outcome
Adenosine Quick Expensive
triphosphate
bioluminescence
Provides immediate feedback Low sensitivity and specificity
Minimal training required No current standardisation of tests
Objective Variable benchmarks
Technology constantly changing
Microbial cultures High sensitivity and specificity Expensive
Objective Prolonged time for results
Can identify screened pathogen Requires accessible laboratory resources and trained
personnel for interpreting results
Provides quantitative data Not supported for routine use by local
and international guidelines
May suggest or confirm environmental Few laboratories NATA accredited to perform
reservoir(s) and/or source of outbreak these tests
Relies on standardised benchmark to assess infection risk
A
Disadvantages of all of these methods include requiring feedback to cleaners, the fact that they may lose impact over time and that they need to be linked
with formal performance indicators.

matrix are done in-house. This was particularly noticeable in standardised format is required, to enable a framework for
the fluorescent gel system where a substantial sum of money performance management and provide a method by which
could be saved by using in-house devised reporting systems. interventions can be evaluated.
Evaluating environmental cleanliness in a standardised
format is required, in order to enable a framework for Conflict of interest
performance management and provide a method by which
interventions can be evaluated. Standardised assessment One of the authors has an editorial affiliation with the journal.
would provide reliable data to support quality improvement This author play no part whatsoever in the review process.
activities and to ensure that healthcare staff have relevant
and useful information to inform and adapt practice. We need Funding
a definition for ‘clean’ which relates to clinical risk for patients No funding was received in relation to this article.
in healthcare facilities.

Acknowledgements
Conclusion
The authors would like to acknowledge the following personnel for their input
There are four main methods used to evaluate environmental and assistance in this obtaining data for this paper: Executive Directors of
cleanliness in healthcare facilities – ATP bioluminescence, Nursing and infection control units in Tasmania; Fiona Kimber, Infection
microbiological methods, visual inspection and gel markers. Control Department, Canberra Hospital; Ronald Govers, Project Officer,
Each of these methods has advantages and limitations. Healthcare Associated Infections, Clinical Excellence Commission, NSW
Methods that evaluate cleaning performance are useful in Ministry of Health; Tain Gardiner, Infection Control Unit, Darwin Hospital;
assessing adherence to cleaning protocols, whereas methods Irene Wilkinson, Infection Control Service Manager, SA Health; Fiona
Fullerton, Nursing Director, Infection Prevention and Control, CHRISP,
that sample bio-burden provide a more relevant indication of Queensland Health; Rebecca McCann, Infection Control HISWA; Mary-
infection risk. Fast, reproducible, cost-effective and reliable Rose Godsell, Nurse Consultant, Infection Prevention, WACHS; Allison
methods are needed for routine environmental cleaning Peterson, Infection Control Nurse, HISWA, Healthcare Associated Infection
evaluation in order to predict timely clinical risk. Further, a Unit.
Methods to evaluate environmental cleanliness Healthcare Infection 29

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