Editorial

How Do Biofilms Affect Surface Cleaning in Hospitals?

Stephanie J. Dancer

Department of Microbiology, NHS Lanarkshire and School of Applied Sciences, Edinburgh Napier University,
Edinburgh EH10 5DT, UK; stephanie.dancer@lanarkshire.scot.nhs.uk

The science of biofilms is progressing rapidly. Now that there is recognition that
microorganisms in dry surface biofilm might contribute towards healthcare-acquired infec-
tion (HAI), work has escalated to define, investigate and identify biofilm components on
accessible surfaces in the healthcare environment. The risk of HAI comes from direct trans-
fer of pathogens released from biofilm to patients, compromised by inadequate cleaning
and decontamination. Staff, patients and visitors acquire pathogens on their hands and
fingertips after touching surfaces and either inoculate a potential infection site themselves
or transfer microbes to other sites including those on vulnerable recipients. This clearly
raises a question over the validity of routine cleaning practices for healthcare surfaces.
What do we mean by biofilm, and how prevalent is it in our hospitals [1]? Dry
surface biofilm coats most, if not all, surfaces in the indoor environment, including floors,
walls, fittings, fixtures, furniture and equipment, although the coatings are not necessarily
uniform [2,3]. It begins with airborne organisms settling on surfaces, along with others
transferred from direct and indirect contact from a range of living things, including people,
animals, birds and insects. These microbial immigrants need to protect themselves to ensure
survival while facilitating their potential transfer to more habitable sites [4,5]. Thus, biofilm
can be thought of as a ‘microbial village’, with an identifiable infrastructure supporting a
disparate mesh of bacteria, viruses, fungi, protozoa and spores embedded in exopolymeric
substances (EPS) [6].
EPS makes up 90% of the biofilm and plays an important role in maintaining its
Citation: Dancer, S.J. How Do mechanical stability [7]. The microscopic community is shielded by this protective cov-
Biofilms Affect Surface Cleaning in ering, while the base elements penetrate tiny surface crevices, or even ‘glue’ themselves
Hospitals?. Hygiene 2022, 2, 132–135. onto underlying surfaces [6]. This level of adherence means that biofilm poses a signifi-
https://doi.org/10.3390/ cant physical challenge to remove, as well as presenting an almost impenetrable barrier
hygiene2030011 to chemical agents such as disinfectants [8,9]. Difficulty in removal is compounded by
Received: 2 August 2022
increased resistance or tolerance of biofilm components, including viable pathogens, to
Accepted: 19 August 2022
disinfectants, antiseptics, heavy metals and a range of antimicrobial agents used for pa-
Published: 2 September 2022
tients [10]. Biofilms typically present gradients of physiology and concentration for any
chosen decontamination agent, which enables the less susceptible species to survive [11].
Publisher’s Note: MDPI stays neutral
Biofilm villages periodically release free-swimming planktonic bacteria onto the sur-
with regard to jurisdictional claims in
face, thus allowing them the opportunity for onward transfer. Wiping surfaces will not
published maps and institutional affil-
substantially disrupt or remove the biofilm structure, although it might dislodge newly
iations.
released superficial microbes. Aggressive cleaning or use of disinfectants damages the
microbial community and its supporting structure, thus releasing a larger proportion of
viable planktonic microorganisms and other material [5,12,13]. These may be detected
Copyright: © 2022 by the author.
by sampling, but the real risk is contact with hands and/or fingertips and subsequent
Licensee MDPI, Basel, Switzerland. transmission to other surfaces or patients. While this risk seems obvious, few studies
This article is an open access article have so far managed to irrevocably link immured biofilm pathogens from dry healthcare
distributed under the terms and surfaces with patient infections. The extensive surface area of the general indoor envi-
conditions of the Creative Commons ronment complicates sampling, making it difficult to locate potential pathogens from dry
Attribution (CC BY) license (https:// surface biofilm.
creativecommons.org/licenses/by/ Studies on outbreaks involving microorganisms from ‘wet’ surface biofilm, as found
4.0/). on contaminated plumbing components and specialist healthcare equipment, serve to

Hygiene 2022, 2, 132–135. https://doi.org/10.3390/hygiene2030011 https://www.mdpi.com/journal/hygiene

Hygiene 2022, 2 133

highlight the potential infection risk from dry surface biofilm [14,15]. There are clear
associations between pathogens originating from sink traps, filters and drains, and invasive
equipment such as endoscopes, with increasing numbers of cross-transmission incidents in
healthcare environments [16]. These organisms often demonstrate tolerance to the agent(s)
used for routine decontamination as well as multi-drug resistance to antimicrobial agents
used for patient treatment [14,17]. The risk from dry surface biofilm can also be surmised
from sampling studies targeting general surfaces. These studies have characterised known
hospital pathogens using genotypic methods, which confirm their identity with the same
species linked to previous cases or outbreaks occurring weeks or months before in the
same hospital [18–20]. Furthermore, genomic material conferring resistance properties in
biofilm components can be transferred to organisms eventually identified from patient
infections [20]. These studies infer that generic dry surfaces could pose an equitable HAI
risk to patients just as much as endoscopes, sinks, plumbing, filters and drains.
Microbes use biofilm to persist in the healthcare environment pending release, should
they survive. Indeed, over half of the organisms immured in biofilm do survive and will be
viable [6,18]. The question is, what should we do about the risk of infection posed by dry
surface biofilm? Is the risk sufficient to change current operating procedures for cleaning
and decontamination, or do we continue with standard practice? It is possible that frequent
application of powerful disinfectants will control or even eventually eradicate surface
biofilm over time, and inhibit its recovery, provided surfaces remain undamaged [13]? The
type (and strength) of disinfectant used is almost certainly important although there is
insufficient evidence to distinguish between multiple products [21]. It is already known
that bleach will not necessarily eradicate biofilm at first application and captured organisms
within the ‘village’ eventually demonstrate tolerance or frank resistance after repeated
exposure [9,21].
Routine detergent cleaning in hospitals is unlikely to remove the biofilm community
from general surfaces although wet wipes should pick up superficial microbes depend-
ing upon cleaning process (‘one wipe; one site; one direction’) [22]. Failure to disrupt
hard surface biofilm does not necessarily have to invalidate this type of manual cleaning,
however we should determine the relative risk from cleaning frequencies required for the
timely removal of newly liberated pathogens while leaving the biofilm structure relatively
intact. At present, optimal cleaning frequencies for all surface types and different areas of
clinical risk in the healthcare environment remain unknown. Perhaps seeking complete
obliteration of hard surface biofilm in our hospitals might be viewed as disproportionate,
let alone time-wasting and expensive. Indeed, excessive use of disinfectants, enzymes and
physical force could create additional risk, since nature abhors a vacuum and will fill it up
if it can [23].
Eradicating all surface microbes, whether part of a biofilm community or not, will
encourage the rapid repopulation of a newly decontaminated surface with environmen-
tal, and other, microbes. Some of these represent a bigger risk to patients than those
originally present. For example, one recent study showed that disrupting wet surface
biofilms following bleach exposure resulted in increased detection of multidrug resistant
organisms including carbapenemase-producing Enterobacteriaceae [17]. These organisms
are becoming increasingly common as healthcare pathogens can be extremely difficult
to treat. It is also known that hospitals using disinfectants are more likely to encourage
multidrug resistant pathogens such as vancomycin-resistant enterococci, Acinetobacter spp.
and Gram-negative organisms such as Stenotrophomonas spp., simply due to the selection
of linked biocidal and antimicrobial resistance characteristics [21,24–26]. Hospitals that
rely upon detergent or probiotic-type products encourage the repopulation of surfaces
with inert environmental organisms such as Methylobacteria, Bacillus spp. and other
non-pathogens [27,28].
It is clear that there are many gaps in our knowledge of dry surface biofilm in the
healthcare environment and we do yet not know how those gaps relate to the infection risk
for patients. Managing biofilm constitutes a challenge due to its tenacious character and
Hygiene 2022, 2 134

the current lack of evidence. It is hoped that this supplement will go some way towards
contributing useful findings from this microbial world at our fingertips.

Funding: None required for the writing of this article.

Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Not applicable.
Conflicts of Interest: The author declares no conflict of interests.

References
1. Ledwoch, K.; Dancer, S.J.; Otter, J.A.; Kerr, K.; Roposte, D.; Rushton, L.; Weiser, R.; Mahenthiralingam, E.; Muir, D.D.; Maillard, J.Y.
Beware biofilm! Dry biofilms containing bacterial pathogens on multiple healthcare surfaces; a multi-centre study. J. Hosp. Infect.
2018, 100, e47–e56. [CrossRef] [PubMed]
2. Vickery, K.; Deva, A.; Jacombs, A.; Allan, J.; Valente, P.; Gosbell, I.B. Presence of biofilm containing viable multiresistant organisms
despite terminal cleaning on clinical surfaces in an intensive care unit. J. Hosp. Infect. 2012, 80, 52–55. [CrossRef] [PubMed]
3. Ledwoch, K.; Dancer, S.J.; Otter, J.A.; Kerr, K.; Roposte, D.; Maillard, J.Y. How dirty is your QWERTY? The risk of healthcare
pathogen transmission from computer keyboards. J. Hosp. Infect. 2021, 112, 31–36. [CrossRef] [PubMed]
4. Tahir, S.; Chowdhury, D.; Legge, M.; Hu, H.; Whiteley, G.; Glasbey, T.; Deva, A.K.; Vickery, K. Transmission of Staphylococcus
aureus from dry surface biofilm (DSB) via different types of gloves. Infect. Control Hosp. Epidemiol. 2019, 40, 60–64. [CrossRef]
5. Chowdhury, D.; Tahir, S.; Legge, M.; Hu, H.; Prvan, T.; Johani, K.; Whiteley, G.S.; Glasbey, T.O.; Deva, A.K.; Vickery, K. Transfer
of dry surface biofilm in the healthcare environment: The role of healthcare workers’ hands as vehicles. J. Hosp. Infect. 2018,
100, e85–e90. [CrossRef]
6. Lindsay, D.; von Holy, A. Bacterial biofilms within the clinical setting: What healthcare professionals should know. J. Hosp. Infect.
2006, 64, 313–325. [CrossRef]
7. Xia, Y.; Jayathilake, P.G.; Li, B.; Zuliani, P.; Deehan, D.; Longyear, J.; Stoodley, P.; Chen, J. Coupled CFD-DEM modeling to
predict how EPS affects bacterial biofilm deformation, recovery and detachment under flow conditions. Biotechnol. Bioeng. 2022,
119, 2551–2563. [CrossRef]
8. Parvin, F.; Hu, H.; Whiteley, G.S.; Glasbey, T.; Vickery, K. Difficulty in removing biofilm from dry surfaces. J. Hosp. Infect. 2019,
103, 465–467. [CrossRef]
9. Almatroudi, A.; Gosbell, I.B.; Hu, H.; Jensen, S.O.; Espedido, B.A.; Tahir, S.; Glasbey, T.O.; Legge, P.; Whiteley, G.; Deva, A.; et al.
Staphylococcus aureus dry-surface biofilms are not killed by sodium hypochlorite: Implications for infection control. J. Hosp. Infect.
2016, 93, 263–270. [CrossRef]
10. Donlan, R.M. Role of biofilms in antimicrobial resistance. ASAIO J. 2000, 46, S47–S52. [CrossRef]
11. Webber, M.A.; Whitehead, R.N.; Mount, M.; Loman, N.J.; Pallen, M.J.; Piddock, L.J. Parallel evolutionary pathways to antibiotic
resistance selected by biocide exposure. J. Antimicrob. Chemother. 2015, 70, 2241–2248. [CrossRef] [PubMed]
12. Bogusz, A.; Stewart, M.; Hunter, J.; Yip, B.; Reid, D.; Robertson, C.; Dancer, S.J. How quickly do hospital surfaces become
contaminated after detergent cleaning? Healthc. Infect. 2013, 18, 3–9. [CrossRef]
13. Stewart, M.; Bogusz, A.; Hunter, J.; Devanny, I.; Yip, B.; Reid, D.; Robertson, C.; Dancer, S.J. Evaluating use of neutral electrolyzed
water for cleaning near-patient surfaces. Infect. Control Hosp. Epidemiol. 2014, 35, 1505–1510. [CrossRef] [PubMed]
14. Betteridge, T.; Merlino, J.; Natoli, J.; Cheong, E.Y.; Gottlieb, T.; Stokes, H.W. Plasmids and bacterial strains mediating multidrug-
resistant hospital-acquired infections are coresidents of the hospital environment. Microb. Drug Resist. 2013, 19, 104–109.
[CrossRef]
15. Brunke, M.S.; Konrat, K.; Schaudinn, C.; Piening, B.; Pfeifer, Y.; Becker, L.; Schwebke, I.; Arvand, M. Tolerance of biofilm
of a carbapenem-resistant Klebsiella pneumoniae involved in a duodenoscopy-associated outbreak to the disinfectant used in
reprocessing. Antimicrob. Resist. Infect. Control 2022, 11, 81. [CrossRef] [PubMed]
16. Dancer, S.J. Controlling hospital-acquired infection: Focus on the role of the environment and new technologies for decontamina-
tion. Clin. Microbiol. Rev. 2014, 27, 665–690. [CrossRef]
17. Fernando, S.A.; Phan, T.; Parker, C.; Cai, T.; Gottlieb, T. Increased detection of carbapenemase-producing Enterobacteriaceae on
post-clean sampling of a burns unit’s wet surfaces. J. Hosp. Infect. 2019, 101, 179–182. [CrossRef]
18. Fux, C.A.; Costerton, J.W.; Stewart, P.S.; Stoodley, P. Survival strategies of infectious biofilms. Trends Microbiol. 2005, 13, e34–e40.
[CrossRef]
19. Dancer, S.J.; White, L.F.; Lamb, J.; Girvan, E.K.; Robertson, C. Measuring the effect of enhanced cleaning in a UK hospital:
A prospective cross-over study. BMC Med. 2009, 7, 28. [CrossRef] [PubMed]
20. Kizny Gordon, A.; Phan, H.T.T.; Lipworth, S.I.; Cheong, E.; Gottlieb, T.; George, S.; Peto, T.E.A.; Mathers, A.J.; Walker, A.S.;
Crook, D.W.; et al. Genomic dynamics of species and mobile genetic elements in a prolonged blaIMP-4-associated carbapenemase
outbreak in an Australian hospital. J. Antimicrob. Chemother. 2020, 75, 873–882. [CrossRef]
Hygiene 2022, 2 135

21. Otter, J.A.; Vickery, K.; Walker, J.T.; Pulcini, E.D.; Stoodley, P.; Goldenberg, S.D.; Salkeld, J.A.; Chewins, J.; Yezli, S.; Edgeworth, J.D.
Surface-attached cells, biofilms and biocide susceptibility: Implications for hospital cleaning and disinfection. J. Hosp. Infect. 2015,
89, 16–27. [CrossRef] [PubMed]
22. Dancer, S.J.; Kramer, A. Four steps to clean hospitals: Look, Plan, Clean and Dry. J. Hosp. Infect. 2019, 103, e1–e8. [CrossRef]
[PubMed]
23. Mora, M.; Mahnert, A.; Koskinen, K.; Pausan, M.R.; Oberauner-Wappis, L.; Krause, R.; Perras, A.K.; Gorkiewicz, G.; Berg, G.;
Moissl-Eichinger, C. Microorganisms in Confined Habitats: Microbial Monitoring and Control of Intensive Care Units, Operating
Rooms, Cleanrooms and the International Space Station. Front. Microbiol. 2016, 7, 1573. [CrossRef] [PubMed]
24. Kampf, G. Challenging biocide tolerance with antiseptic stewardship. J. Hosp. Infect. 2018, 100, e37–e39. [CrossRef]
25. Kampf, G. Biocidal Agents Used for Disinfection Can Enhance Antibiotic Resistance in Gram-Negative Species. Antibiotics 2018,
7, 110. [CrossRef]
26. Mahnert, A.; Moissl-Eichinger, C.; Zojer, M.; Bogumil, D.; Mizrahi, I.; Rattei, T.; Martinez, J.L.; Berg, G. Man-made microbial
resistances in built environments. Nat. Commun. 2019, 10, 968. [CrossRef]
27. Klassert, T.E.; Zubiria-Barrera, C.; Neubert, R.; Stock, M.; Schneegans, A.; López, M.; Driesch, D.; Zakonsky, G.; Gastmeier, P.;
Slevogt, H.; et al. Comparative analysis of surface sanitization protocols on the bacterial community structures in the hospital
environment. Clin. Microbiol. Infect. 2022, 28, 1105–1112. [CrossRef]
28. Vickery, K.; Johani, K.; Hu, H.; Costa, D.; Dancer, S.J.; Melo, D.; Gosbell, I.; Jensen, S.; Lopes, L.K.; Whiteley, G.; et al. The
Microbiome of Dry Surface Biofilm Sampled from Intensive Care Units around the World. In Proceedings of the SHEA Spring
Conference, Portland, OR, USA, 18–20 April 2018.

Short Biography of Authors

Stephanie J. Dancer , BSc, MB.BS, MSc, MD, FRCPath, DTM&H, FRCP(Ed), FESCMID, FISAC.
Stephanie is a medical microbiologist in NHS Lanarkshire and a Professor of Microbiology at Edin-
burgh Napier University in Scotland. She edited the Journal of Hospital Infection for over 20 years, five
of them as editor-in-chief, and now edits for Infection, Disease & Health and International Journal of
Antimicrobial Agents. She trained at St. Bartholomew’s Hospital in London followed by a period of
postgraduate study at Guy’s Hospital, where she gained a thesis on the epidemiology and biochem-
istry of toxin-producing staphylococci. She has worked and travelled all over the world, including the
Canadian High Arctic, where she resuscitated 30,000-year-old organisms from glacial ice. She spent
six years as Infection Control Officer for Argyll before moving to Health Protection Scotland as their
inaugural microbiologist (2002–2005). There, she set up MRSA surveillance for Scotland, evaluated
real-time PCR for MRSA screening and helped establish the Scottish Microbiology Forum. She has
been a member of various working groups on antibiotic prescribing, MRSA and hospital cleaning,
and is a current or recent member of NHS Scotland Decontamination; UK NICE (infection control &
antimicrobial prescribing); UK HTA (screening and diagnostics); ESCMID groups on infection control,
MRSA & multi-resistant Gram-negative bacilli; 2023 ECCMID conference committee. She advised
DEFRA on surface cleaning and hygiene during the COVID-19 pandemic and has been collaborating
with an international group of virologists, physicists, ventilation engineers and aerosol scientists
on airborne spread of SARS-CoV-2. She has published books, book chapters and over 200 papers
in peer-reviewed journals on hospital cleaning, antimicrobial management, infection control and
MRSA. At present, she balances editorial duties with research and teaching, specifically antimicrobial
stewardship and environmental control of hospital pathogens.