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New frontiers in healthcare environmental hygiene: thoughts from the 2022 healthcare cleaning forum

New frontiers in healthcare environmental hygiene: thoughts from the 2022 healthcare cleaning forum Healthcare environmental hygiene (HEH) has become recognized as being increasingly important for patient safety and the prevention of healthcare-associated infections. At the 2022 Healthcare Cleaning Forum at Interclean in Amsterdam, the academic lectures focused on a series of main areas of interest. These areas are indicative of some of the main trends and avenues for research in the coming years. Both industry and academia need to take steps to continue the momentum of HEH as we transition out of the acute phase of the Covid-19 pandemic. There is a need for new ways to facilitate collaboration between the academic and private sectors. The Clean Hospitals network was presented in the context of the need for both cross-disciplinarity and evidence-based interventions in HEH. Govern- mental bodies have also become more involved in the field, and both the German DIN 13603 standard and the UK NHS Cleaning Standards were analyzed and compared. The challenge of environmental pathogens was explored through the example of how P. aeruginosa persists in the healthcare environment. New innovations in HEH were pre- sented, from digitalization to tracking, and automated disinfection to antimicrobial surfaces. The need for sustainabil- ity in HEH was also explored, focusing on the burden of waste, the need for a circular economy, and trends towards increasingly local provision of goods and services. The continued focus on and expansion of these areas of HEH will result in safer patient care and contribute to better health systems. Keywords Infection prevention and control, Environmental hygiene, Cleaning, Sustainability HEH includes surface cleaning and disinfection, air con- Introduction trol, water control, waste management, sterilization and The last few years have been monumental for health - device processing and laundry. Since 2015, there has care environmental hygiene (HEH), partly due to the been an exponential growth in good quality studies that Covid-19 pandemic, but not exclusively. The scope of tie improvements in HEH to a reduction in healthcare- associated infections [1]. The 2022 Healthcare Cleaning *Correspondence: Forum at Interclean in Amsterdam had a very different Didier Pittet Didier.pittet@hcuge.ch atmosphere than the last edition in 2018. There was no Infection Control Programme and WHO Collaborating Center On more need to convince anyone about the importance of Infection Prevention and Control and Antimicrobial Resistance, Hospitals environmental cleaning in healthcare- the last few years and Faculty of Medicine, University of Geneva, Geneva, Switzerland Nouvelle Aquitaine Health Care-Associated Infection Control Centre, of the pandemic had thrust HEH into the spotlight. This Bordeaux University Hospital, Bordeaux, France trend was reflected in the show participation; around 25% Richard Wells Research Centre, University of West London, London, UK 4 of the visitors to Interclean had come to see the Health- Department of Medical Microbiology and Infectious Diseases, Erasmus MC University Medical Centre Rotterdam, Rotterdam, The Netherlands care Cleaning Forum which was organized in coopera- Hywel Dda University Health Board, NHS Wales, Carmarthen, UK tion with Clean Hospitals. © The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Peters et al. Antimicrobial Resistance & Infection Control (2023) 12:7 Page 2 of 7 The field of HEH is beginning to come into its own, facilities became increasingly aware of the role of the and the content of the lectures and presentations at the environment in the transmission of HAIs. In 2021, two Healthcare Cleaning Forum reflected this. They looked new sets of national guidance for cleaning were launched at the impact of Covid-19, and how to keep momen- in and around Europe. In Germany, the German Stand- tum in the field moving forward, development of new ards Institute (DIN) 13603 standard was the first national international guidance in HEH, the need for and role of guidance produced; it applies to all healthcare provid- evidence-based interventions, case studies for the role ers [4]. In England, the National Health Service (NHS) of design and the built environment in combatting envi- Cleaning Standards launched a second and revised ver- ronmental pathogens, and urgent calls for innovation and sion that did not apply to the NHS in Wales, Scotland or sustainability in the field. Northern Ireland or to independent healthcare provid- Covid-19 sensitized the whole world to contact trans- ers [5]. Although independently produced, there were mission. In the early stages of the pandemic, facilities some similarities and some differences in the approaches operated in a setting of knowledge gaps, uncertainty, fear, (Table  1). Both sets had multiple inputs from stakehold- and a lack of supplies. Later, a fatigued workforce and a ers’ groups. However in England, professional societies market flooded with products of varying efficacy would like the Infection Prevention Society and the Healthcare prove to be new challenges for HEH. The disease also Infection Society did not endorse the guidance, whereas spread in unexpected ways; although it was expected that in Germany, the Robert Koch Institute was instrumental patients would be the cause of nosocomial spread, Covid- in the creation process. 19 was often spread through the population of healthcare The NHS standards provide clear advice and guidance workers sharing lunch or carpooling to their patients [2]. on what cleaning is required, and how organizations can demonstrate cleaning services meet these standards. The Clean Hospitals approach Although they state that recommendations are based on The Clean Hospitals initiative, launched at the 2018 sound evidence and accepted good practices, no litera- Healthcare Cleaning Forum, has grown into a collabora- ture review was ever conducted and there is no evidence tive public private partnership with the common goals for of a systematic process. increased communication, improved products and prac- One positive development is that when addressing rec- tices and better patient safety. The network proved useful ommendations for cleaning, the NHS standards make during the pandemic, as industry and academic partners clear statements about the role of clinical staff in envi - were kept abreast of the newest challenges in the field. ronmental decontamination. The DIN standard however The Clean Hospitals academic taskforce worked on two does not define clear responsibilities for staff groups, main pieces of research. The first was a systematic review instead leaving this for individual organizations to define. to assess the impact of interventions in the healthcare It does however describe clear methodologies for clean- environment on patient outcomes, wither healthcare- ing and disinfecting a variety of surfaces. Both standards associated infections (HAIs) or patient colonization [1]. mention the need for training, however the DIN is far Eighty-eight percent of included studies showed some more prescriptive in describing necessary content and kind of reduction in colonization or HAI for at least one levels of attainment. Audit is also covered in both stand- of the microorganisms tested, and 58% showed a signifi - ards however methodologies differ: where the NHS sys - cant reduction in all of the microorganisms tested. The tem is a subjective qualitative visual assessment, whilst studies identified make up the growing body of work the DIN gives great detail on quantitative assessment of that demonstrates the key importance of environmental effectiveness of cleaning. hygiene to patient safety. The largest change in the second version of the NHS The second project, which is still ongoing, is the devel - Standard is the adoption of a collaborative approach for opment of a tool for facilities to assess how well their the responsibility for cleaning, and so combined work- HEH programs work, and give indications of how to ing is necessary to achieve the stated audit standards, improve them. The Healthcare Environmental Hygiene which are then displayed as a ‘star’ rating. The effect of Self-Assessment Framework was first tested as an inter - this on public confidence has not been measured to date. national pilot survey [3], and is currently undergoing the There is no such approach in the DIN standard, which final stage of development before its projected dissemi - adopts an accepted approach to the determination of nation in 2023. quality, using the three interdependent aspects of struc- ture, process and outcome. Interestingly, although both New guidance sets of standards describe cleaning and decontamination During Covid-19, new guidelines and expert reviews processes in varying degrees of detail, neither has taken were developed around the world, and healthcare the opportunity to include accepted and well-established P eters et al. Antimicrobial Resistance & Infection Control (2023) 12:7 Page 3 of 7 Table 1 Comparison of key aspects of England’s NHS and Germany’s DIN guidelines NHS (England) cleaning standards Germany DIN 13063 Audit and inspection method Visual only; subjective. Equipment and items cleaned by the clinical staff Comprehensive description of methods including visual, ATP, Fluorescent are part of audit marking, microbiological. Clinical items not explicitly included Audit results delivery Star rating visually displayed in each area. Star ratings vary by a complex Results need to be communicated to the employees at execution level in functional risk system an understandable and practical form and left to local delivery method Evidence base No literature review; recommendations not supported by evidence in the No literature review; recommendations supported by evidence in the scientific literature scientific literature Guidance applicable to NHS in England only, not Wales, Scotland or independent healthcare All healthcare providers in Germany providers Involvement of specialists Professional cleaning organisations and public institutions; not endorsed Collaborative between professional infection prevention-related societies, by nursing or infection prevention-related professional societies public institutions, companies in the cleaning industry, their suppliers and associations Outline of responsibilities Role of professional cleaners is described. Clear statements about the role Comprehensive; client/service recipient defines interfaces for defining a of clinical staff in decontamination of clinical equipment separation of devices Training needs Mentioned but little detail provided Comprehensive; outlines detail on training, requirement for expertise and stating that the content of training should be monitored Colour coding used to separate different areas Yes Yes Use of ‘novel’ technologies such as UV, Gase- Not mentioned Not mentioned ous decontamination Peters et al. Antimicrobial Resistance & Infection Control (2023) 12:7 Page 4 of 7 evidence-bases automated technologies such as gaseous analyses of the hospital environment have provided some hydrogen peroxide and ultraviolet light technologies. insights into the hospital microbiota, they did not pro- Both sets of standards are a step forward for their vide support for the development of new interventions countries, the NHS including the clinical staff in respon - such as probiotic-based treatments [16–18]. An analysis sibilities for cleaning and the DIN for being the first using a culture-based approach based on MALDI-TOF national guidance. Both however would benefit from a mass spectrometry of sink biofilms did provide some more transparent description of the evidence base and modest leads, but additional experiments are needed to strength of evidence from which the recommendations draw more firm conclusions on which microorganisms have been derived. enable or inhibit P. aeruginosa persistence [8]. Enzymatic, probiotic [18] or phage-based approaches should also be Case study of an environmental pathogen: Pseudomonas explored. Innovative approaches are needed to address aeruginosa persistent environmental reservoirs of bacteria and help A safe hospital is a clean hospital, but what exactly “clean” create microbiologically safe hospitals. The question means can vary. In the context of preventing HAIs, it is how to best foster these types of approaches. could be interpreted as a microbiologically safe hospital without pathogenic microorganisms in its environment. Innovation in environmental hygiene P. aeruginosa is especially capable of surviving in the Innovation is everywhere in our daily-life including the hospital environment, with sinks as the most frequently healthcare system. Infection control and environmental reported reservoir [6–9]. P. aeruginosa bacteria form hygiene have been expected to take advantage of these biofilms in the lumen of pipelines, from which cells may progresses on the condition that we are able to assess be released during sink use and spread outside of drains the efficacy and the impact of new available technologies within droplets or as aerosols. Surfaces in the patient [19]. environment may become contaminated, and ultimately Electronic health records in hospitals and the software reach the patient. A recent analysis showed that the vast to instantaneously aggregate them, provide important majority of P. aeruginosa infections (86.3%) were trans- data that should be available to infection control teams. mitted through the environment as opposed to cross- If collected and analyzed appropriately, this data can transmission from other individuals or patients. Bacterial provide practitioners knowledge which can, in turn, be drain reservoirs are notoriously difficult to eradicate, as transformed into action, and potentially improve infec- commonly-used hospital disinfectants do not remove tion control [20]. biofilms, and recolonization may occur after exposure Other types of digitalization and tracking are now to contaminated materials or retrograde growth from becoming more common in environmental cleaning and p-traps. disinfection. Modern technology can provide autonomy When it is not feasible to remove such pathogenic bac- to the professional, while performing continuous moni- teria, elimination of the complete reservoir can be con- toring, enable early detection of hygiene failures, and sidered; an intervention which several hospitals have facilitate quick interventions. This can ultimately prevent implemented [10–12]. The removal of sinks was per - outbreaks and mitigate both the human and financial formed in the framework of a bundle focused on water- costs associated with HAIs. Managers should encour- free patient care. Though this intervention had an effect age these innovations and their use in a fair manner, by in all three studies, the removal of sinks is not feasible focusing on quality improvement and not on individuals outside of intensive care units, and shower drains may be blame for failures. reservoirs for P. aeruginosa as well [13]. It is desirable to technology to automatize important If neither elimination of the pathogen, nor the com- tasks that are difficult for humans to perform consist - plete removal of the reservoir is possible, elimination or ently. This is especially the case for robots that are quickly control of the transmission route of pathogenic micro- becoming ubiquitous in the field of cleaning and disinfec - organisms from or via the environment is a pragmatic tion. Ultra violet-C (UVC) disinfection, for example, is a approach. A range of such interventions have been pub- promising technology with demonstrated efficacy. How - lished, often focused on an improved sink design [6, ever, international quality standards are lacking, and are 14, 15]. Most of these interventions showed significant important in order for consumers to fully rely on such reductions in transmission, though control was not fully technology where appropriate. Such technologies have achieved. additional effects beyond their efficacy- implementing To identify alternative solutions, a better understanding visible technologies has been shown to improve safety of the hospital’s microbiota and the environmental bio- climates in hospitals by increasing the confidence of both films is key. Though recent studies using (meta)genomic patients and healthcare workers [21]. P eters et al. Antimicrobial Resistance & Infection Control (2023) 12:7 Page 5 of 7 Antimicrobial surfaces are based on technologies that ways healthcare facilities need to go “back to the future” either repel or kill microorganisms when applied to a sur- by having locally, decentralized infrastructure in order to face [22]. The field of possible applications of such tech - support reuse and reprocessing where appropriate. nologies is wide and still growing [23]. A French national Developing a circular economy is central to making organization for standardization/ Association Française it sustainable. In 2020, 100 billion tons of new materi- de Normalisation (AFNOR) efficacy standard (NF S als entered the world economy, and only 8.6 was circu- 90-700) has been published in 2019 and is the basis for lar [31]. The World Economic Forum estimates that 70% what will become the ISO standard. Discussions are still more virgin materials were extracted from the Earth than underway concerning the appropriate efficacy require - what it can safely replenish [31]. Not only do we need ments and the differentiation between similar technolo - to use less, but we need to make things last longer, uti- gies, such as for opaque versus transparent surfaces. The lize renewable energy and regenerative materials, and expected goal of antimicrobial surfaces is to help reduce plan how to reuse and recycle from the very beginning, the transmission burden, especially on high-touch sur- instead of as an afterthought. Recycling should be the faces [24]. end point of a circular economy, not the first thing tried. Innovation in environmental hygiene should not be The cost structure of materials is a major issue, as new seen as an endpoint nor a magic bullet but as compo- materials are often much cheaper than recycled ones nents of an infection control strategy that can be added [32]. This creates frequent incompatibility between sus - in intervention bundles. Industry should focus on dem- tainability and affordability. onstrating the immediate efficacy of such technology and It is also increasingly clear that infection preventionists the infection control experts should decide when, where need to participate in the decision making around sus- and how to use it to maximize its impact. tainability in healthcare in order to prevent new meas- ures from having a negative effect on efficacy. If infection Sustainability control experts do not get involved in this agenda, some- The entirety of this research and projects and new tech - one who is not an expert will set it. Further challenges nologies and trends need to share a common trait; they include a lack of accountability, and social equity. It is must all be sustainable to implement. Sustainability also important to talk about responsibility, both individu- means meeting the needs of the present without com- ally and collectively at the institutional and governmental promising the needs of future generations. For healthcare levels. facilities, there is often a tradeoff (sometimes perceived, Institutions can begin to take steps in a number of sometimes real) of sustainability versus efficacy. ways. First, they can reduce the use of chlorine-based The World Meteorological Organization predicts products [33] and adapt policies to infection preven- 50/50 odds that temps will increase between 1.5 and 2C tion needs as new information evolves. It is important over pre-industrial levels, for one year over the next five to reduce reliance on single use equipment unless abso- [25]. This means that there will be irreversible and per - lutely necessary. Healthcare facilities used to reuse more, haps catastrophic changes to our climate. Globally, the but fear during AIDS pandemic pushed facilities towards healthcare sector is responsible for almost 5% of emis- single use, even for surgical caps and gowns that could be sions [26]. A global analysis of health care waste in the laundered. High-cost, low-volume medical devices are context of Covid-19 showed hundreds of thousands tons often discarded simply on the advice of the manufacturer. of additional waste from Covid-19 test kits, personal pro- Healthcare facilities need to work with manufacturers tective equipment (PPE), vaccine production etc. [27, 28] to change this, and to maximize the safe reusability of Beyond the quantity of waste, the WHO estimates that 1 equipment. in 3 healthcare facilities does not safely manage its waste [27]. Conclusion Countries are beginning to take steps to try to reach The future of HEH is clear as the field becomes more net zero, which means cutting emissions as close to zero recognized as being key component of successful infec- as possible and reabsorb all remaining emissions into tion prevention strategy. Still, more research is needed healthy oceans and forests. The UK’s target is to reach to prove the efficacy of standard interventions and of net zero by 2050 [29]. The UK’s NHS is aiming to reach recently developed technologies. New ways of managing net zero by 2040 [30]. While some aspects are in con- the built environment need to be explored and innova- trol of institutions, others are not. IPC is often still not tion needs to be evidence-based and adopted in a context wholly evidence-based, and this needs to improve so that that is helpful to and respectful of the environmental ser- resources are not used when it is not necessary to do so. vices staff and our planet. PPE needs to be used better and more precisely. In many Peters et al. Antimicrobial Resistance & Infection Control (2023) 12:7 Page 6 of 7 facility level. Am J Infect Control. 2022. https:// doi. org/ 10. 1016/j. ajic. 2022. Networks such as Clean Hospitals need to continue 02. 029. to work on defining the research agenda globally as well 4. DIN 13063, Krankenhausreinigung—Anforderungen an die Reini- as creating awareness for the field. Healthcare facilities gung und desinfizierende Reinigung in Krankenhäusern und anderen medizinischen Einrichtungen (Unpublished manuscript). (2021). around the world need to be able to analyze their own 5. National Health Service (UK). National Standards of Healthcare Cleanli- programs in the context of best practices, and tools must ness 2021. (2021). be developed to help facilitate improvement. Sustainable 6. Parkes LO, Hota SS. Sink-related outbreaks and mitigation strategies in healthcare facilities. Curr Infect Dis Rep. 2018;20:42. international norms and guidelines should be developed 7. Pelegrin AC, et al. High-risk international clones of carbapenem-nonsus- in order for institutions to implement universal mini- ceptible pseudomonas aeruginosa endemic to indonesian intensive care mum standards for quality while ensuring that future units: impact of a multifaceted infection control intervention analyzed at the genomic level. MBio. 2019;10:e02384-e2419. generations can enjoy the same level of access as ours. 8. Pirzadian J, et al. Novel use of culturomics to identify the microbiota in hospital sink drains with and without persistent VIM-positive Pseu- domonas aeruginosa. Sci Rep. 2020;10:17052. Abbreviations 9. Voor In’t Holt AF, Severin JA, Lesaffre EMEH, Vos MC. A systematic review AFNOR A ssociation Française de Normalisation/French national organiza- and meta-analyses show that carbapenem use and medical devices are tion for standardization the leading risk factors for carbapenem-resistant Pseudomonas aerugi- DIN Deutsches Institut für Normung/German Standards Institute nosa. Antimicrob Agents Chemother. 2014;58:2626–37. HAI Healthcare-associated infection 10. Catho G, et al. Outbreak of Pseudomonas aeruginosa producing VIM car- HEH Healthcare environmental hygiene bapenemase in an intensive care unit and its termination by implemen- NHS National health service tation of waterless patient care. Crit Care. 2021;25:301. PPE Personal protective equipment 11. Hopman J, et al. Reduced rate of intensive care unit acquired gram-neg- UVC Ultra violet-C ative bacilli after removal of sinks and introduction of ‘water-free’ patient care. Antimicrob Resist Infect Control. 2017;6:59. Acknowledgements 12. Shaw E, et al. Control of endemic multidrug-resistant Gram-negative Not applicable. bacteria after removal of sinks and implementing a new water-safe policy in an intensive care unit. J Hosp Infect. 2018;98:275–81. Author contributions 13. Hopman J, et al. Risk assessment after a severe hospital-acquired infec- PP, MK, JS, DP wrote and submitted summaries of their respective talks to AP. tion associated with carbapenemase-producing pseudomonas aerugi- TG contributed her slides and materials for summary by AP, and then edited nosa. JAMA Netw Open. 2019;2:e187665. and approved that summary. AP compiled the summaries and wrote the 14. de Jonge E, de Boer MGJ, van Essen EHR, Dogterom-Ballering HCM, paper. MK wrote the table. All authors reviewed, edited and approved the Veldkamp KE. Eec ff ts of a disinfection device on colonization of sink paper. drains and patients during a prolonged outbreak of multidrug-resistant Pseudomonas aeruginosa in an intensive care unit. J Hosp Infect. Funding 2019;102:70–4. There was no specific funding for this paper, the Healthcare Cleaning Forum 15. Pirzadian J, et al. Impact of sink design on bacterial transmission from was funded by Interclean and supported by Clean Hospitals. hospital sink drains to the surrounding sink environment tested using a fluorescent marker. J Hosp Infect. 2022;127:39–43. Availability of data and materials 16. Ashokan A, et al. Environmental dynamics of hospital microbiome upon There was no data generated, but we will gladly share whatever information transfer from a major hospital to a new facility. J Infect. 2021;83:637–43. may be requested. 17. Chng KR, et al. Cartography of opportunistic pathogens and anti- biotic resistance genes in a tertiary hospital environment. Nat Med. 2020;26:941–51. Declarations 18. Klassert TE, et al. Bacterial colonization dynamics and antibiotic resistance gene dissemination in the hospital environment after first patient occu- Ethics approval and consent to participate pancy: a longitudinal metagenetic study. Microbiome. 2021;9:169. Not applicable. 19. Gray J. Infection control: beyond the horizon. J Hosp Infect. 2015;89:237–40. Consent for publication 20. Lin MY, Trick WE. Computer informatics for infection control. Infect Dis Not applicable. Clin North Am. 2021;35:755–69. 21. Rock C, et al. Patient and health care worker perceptions of daily use of Competing interests ultraviolet-C technology as an adjunct to daily cleaning in an academic All authors declare no competing interests. hospital: secondary study of ultra violet-C light evaluation as an adjunct to removing multi-drug resistant organisms. Am J Infect Control. 2018;46:348–9. Received: 9 September 2022 Accepted: 11 November 2022 22. Sheridan M, Winters C, Zamboni F, Collins MN. Biomaterials: Antimicrobial surfaces in biomedical engineering and healthcare. Curr Opin Biomed Eng. 2022;22:100373. 23. Feuillolay C, et al. Antimicrobial activity of metal oxide microspheres: an innovative process for homogeneous incorporation into materials. J Appl References Microbiol. 2018;125:45–55. 1. Peters A, et al. Impact of environmental hygiene interventions on 24. Bäumler W, Eckl D, Holzmann T, Schneider-Brachert W. Antimicrobial healthcare-associated infections and patient colonization: a systematic coatings for environmental surfaces in hospitals: a potential new pillar for review. Antimicrob Resist Infect Control. 2022;11:38. prevention strategies in hygiene. Crit Rev Microbiol. 2021;48(5):531–64. 2. Abbas M, et al. Reconstruction of transmission chains of SARS-CoV-2 https:// doi. org/ 10. 1080/ 10408 41X. 2021. 19912 71. amidst multiple outbreaks in a geriatric acute-care hospital: a combined 25. WMO update: 50:50 chance of global temperature temporarily retrospective epidemiological and genomic study. Elife. 2022;11:e76854. reaching 1.5°C threshold in next five years|World Meteorologi- 3. Peters A, Schmid MN, de Kraker MEA, Parneix P, Pittet D. Results of an cal Organization. https:// public. wmo. int/ en/ media/ press- relea se/ international pilot survey on health care environmental hygiene at the P eters et al. Antimicrobial Resistance & Infection Control (2023) 12:7 Page 7 of 7 wmo- update- 5050- chance- of- global- tempe rature- tempo rarily- reach ing- 15% C2% B0c- thres hold. 26. Watts N, et al. The 2020 report of The Lancet countdown on health and climate change: responding to converging crises. Lancet. 2021;397:129–70. 27. Global analysis of health care waste in the context of COVID-19. https:// www. who. int/ publi catio ns- detail- redir ect/ 97892 40039 612. 28. Mahmoudnia A, Mehrdadi N, Golbabaei Kootenaei F, Rahmati Deiranloei M, Al-e-Ahmad E. Increased personal protective equipment consump- tion during the COVID-19 pandemic: an emerging concern on the urban waste management and strategies to reduce the environmental impact. J Hazard Mater Adv. 2022;7:100109. 29. Net Zero Strategy: Build Back Greener. GOV.UK https:// www. gov. uk/ gover nment/ publi catio ns/ net- zero- strat egy. 30. Greener NHS » Delivering a net zero NHS. https:// www. engla nd. nhs. uk/ green ernhs/a- net- zero- nhs/. 31. World Economic Forum. Circulatity Gap Report. https:// www. circu larity- gap. world/ 2022 (2022). 32. OECD. Improving markets for recycled plastics: trends, prospects and policy responses. OECD;2018. https:// doi. org/ 10. 1787/ 97892 64301 016- en. 33. Parveen N, Chowdhury S, Goel S. Environmental impacts of the widespread use of chlorine-based disinfectants during the COVID-19 pandemic. Environ Sci Pollut Res Int. 2022. https:// doi. org/ 10. 1007/ s11356- 021- 18316-2. 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New frontiers in healthcare environmental hygiene: thoughts from the 2022 healthcare cleaning forum

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Abstract

Healthcare environmental hygiene (HEH) has become recognized as being increasingly important for patient safety and the prevention of healthcare-associated infections. At the 2022 Healthcare Cleaning Forum at Interclean in Amsterdam, the academic lectures focused on a series of main areas of interest. These areas are indicative of some of the main trends and avenues for research in the coming years. Both industry and academia need to take steps to continue the momentum of HEH as we transition out of the acute phase of the Covid-19 pandemic. There is a need for new ways to facilitate collaboration between the academic and private sectors. The Clean Hospitals network was presented in the context of the need for both cross-disciplinarity and evidence-based interventions in HEH. Govern- mental bodies have also become more involved in the field, and both the German DIN 13603 standard and the UK NHS Cleaning Standards were analyzed and compared. The challenge of environmental pathogens was explored through the example of how P. aeruginosa persists in the healthcare environment. New innovations in HEH were pre- sented, from digitalization to tracking, and automated disinfection to antimicrobial surfaces. The need for sustainabil- ity in HEH was also explored, focusing on the burden of waste, the need for a circular economy, and trends towards increasingly local provision of goods and services. The continued focus on and expansion of these areas of HEH will result in safer patient care and contribute to better health systems. Keywords Infection prevention and control, Environmental hygiene, Cleaning, Sustainability HEH includes surface cleaning and disinfection, air con- Introduction trol, water control, waste management, sterilization and The last few years have been monumental for health - device processing and laundry. Since 2015, there has care environmental hygiene (HEH), partly due to the been an exponential growth in good quality studies that Covid-19 pandemic, but not exclusively. The scope of tie improvements in HEH to a reduction in healthcare- associated infections [1]. The 2022 Healthcare Cleaning *Correspondence: Forum at Interclean in Amsterdam had a very different Didier Pittet Didier.pittet@hcuge.ch atmosphere than the last edition in 2018. There was no Infection Control Programme and WHO Collaborating Center On more need to convince anyone about the importance of Infection Prevention and Control and Antimicrobial Resistance, Hospitals environmental cleaning in healthcare- the last few years and Faculty of Medicine, University of Geneva, Geneva, Switzerland Nouvelle Aquitaine Health Care-Associated Infection Control Centre, of the pandemic had thrust HEH into the spotlight. This Bordeaux University Hospital, Bordeaux, France trend was reflected in the show participation; around 25% Richard Wells Research Centre, University of West London, London, UK 4 of the visitors to Interclean had come to see the Health- Department of Medical Microbiology and Infectious Diseases, Erasmus MC University Medical Centre Rotterdam, Rotterdam, The Netherlands care Cleaning Forum which was organized in coopera- Hywel Dda University Health Board, NHS Wales, Carmarthen, UK tion with Clean Hospitals. © The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Peters et al. Antimicrobial Resistance & Infection Control (2023) 12:7 Page 2 of 7 The field of HEH is beginning to come into its own, facilities became increasingly aware of the role of the and the content of the lectures and presentations at the environment in the transmission of HAIs. In 2021, two Healthcare Cleaning Forum reflected this. They looked new sets of national guidance for cleaning were launched at the impact of Covid-19, and how to keep momen- in and around Europe. In Germany, the German Stand- tum in the field moving forward, development of new ards Institute (DIN) 13603 standard was the first national international guidance in HEH, the need for and role of guidance produced; it applies to all healthcare provid- evidence-based interventions, case studies for the role ers [4]. In England, the National Health Service (NHS) of design and the built environment in combatting envi- Cleaning Standards launched a second and revised ver- ronmental pathogens, and urgent calls for innovation and sion that did not apply to the NHS in Wales, Scotland or sustainability in the field. Northern Ireland or to independent healthcare provid- Covid-19 sensitized the whole world to contact trans- ers [5]. Although independently produced, there were mission. In the early stages of the pandemic, facilities some similarities and some differences in the approaches operated in a setting of knowledge gaps, uncertainty, fear, (Table  1). Both sets had multiple inputs from stakehold- and a lack of supplies. Later, a fatigued workforce and a ers’ groups. However in England, professional societies market flooded with products of varying efficacy would like the Infection Prevention Society and the Healthcare prove to be new challenges for HEH. The disease also Infection Society did not endorse the guidance, whereas spread in unexpected ways; although it was expected that in Germany, the Robert Koch Institute was instrumental patients would be the cause of nosocomial spread, Covid- in the creation process. 19 was often spread through the population of healthcare The NHS standards provide clear advice and guidance workers sharing lunch or carpooling to their patients [2]. on what cleaning is required, and how organizations can demonstrate cleaning services meet these standards. The Clean Hospitals approach Although they state that recommendations are based on The Clean Hospitals initiative, launched at the 2018 sound evidence and accepted good practices, no litera- Healthcare Cleaning Forum, has grown into a collabora- ture review was ever conducted and there is no evidence tive public private partnership with the common goals for of a systematic process. increased communication, improved products and prac- One positive development is that when addressing rec- tices and better patient safety. The network proved useful ommendations for cleaning, the NHS standards make during the pandemic, as industry and academic partners clear statements about the role of clinical staff in envi - were kept abreast of the newest challenges in the field. ronmental decontamination. The DIN standard however The Clean Hospitals academic taskforce worked on two does not define clear responsibilities for staff groups, main pieces of research. The first was a systematic review instead leaving this for individual organizations to define. to assess the impact of interventions in the healthcare It does however describe clear methodologies for clean- environment on patient outcomes, wither healthcare- ing and disinfecting a variety of surfaces. Both standards associated infections (HAIs) or patient colonization [1]. mention the need for training, however the DIN is far Eighty-eight percent of included studies showed some more prescriptive in describing necessary content and kind of reduction in colonization or HAI for at least one levels of attainment. Audit is also covered in both stand- of the microorganisms tested, and 58% showed a signifi - ards however methodologies differ: where the NHS sys - cant reduction in all of the microorganisms tested. The tem is a subjective qualitative visual assessment, whilst studies identified make up the growing body of work the DIN gives great detail on quantitative assessment of that demonstrates the key importance of environmental effectiveness of cleaning. hygiene to patient safety. The largest change in the second version of the NHS The second project, which is still ongoing, is the devel - Standard is the adoption of a collaborative approach for opment of a tool for facilities to assess how well their the responsibility for cleaning, and so combined work- HEH programs work, and give indications of how to ing is necessary to achieve the stated audit standards, improve them. The Healthcare Environmental Hygiene which are then displayed as a ‘star’ rating. The effect of Self-Assessment Framework was first tested as an inter - this on public confidence has not been measured to date. national pilot survey [3], and is currently undergoing the There is no such approach in the DIN standard, which final stage of development before its projected dissemi - adopts an accepted approach to the determination of nation in 2023. quality, using the three interdependent aspects of struc- ture, process and outcome. Interestingly, although both New guidance sets of standards describe cleaning and decontamination During Covid-19, new guidelines and expert reviews processes in varying degrees of detail, neither has taken were developed around the world, and healthcare the opportunity to include accepted and well-established P eters et al. Antimicrobial Resistance & Infection Control (2023) 12:7 Page 3 of 7 Table 1 Comparison of key aspects of England’s NHS and Germany’s DIN guidelines NHS (England) cleaning standards Germany DIN 13063 Audit and inspection method Visual only; subjective. Equipment and items cleaned by the clinical staff Comprehensive description of methods including visual, ATP, Fluorescent are part of audit marking, microbiological. Clinical items not explicitly included Audit results delivery Star rating visually displayed in each area. Star ratings vary by a complex Results need to be communicated to the employees at execution level in functional risk system an understandable and practical form and left to local delivery method Evidence base No literature review; recommendations not supported by evidence in the No literature review; recommendations supported by evidence in the scientific literature scientific literature Guidance applicable to NHS in England only, not Wales, Scotland or independent healthcare All healthcare providers in Germany providers Involvement of specialists Professional cleaning organisations and public institutions; not endorsed Collaborative between professional infection prevention-related societies, by nursing or infection prevention-related professional societies public institutions, companies in the cleaning industry, their suppliers and associations Outline of responsibilities Role of professional cleaners is described. Clear statements about the role Comprehensive; client/service recipient defines interfaces for defining a of clinical staff in decontamination of clinical equipment separation of devices Training needs Mentioned but little detail provided Comprehensive; outlines detail on training, requirement for expertise and stating that the content of training should be monitored Colour coding used to separate different areas Yes Yes Use of ‘novel’ technologies such as UV, Gase- Not mentioned Not mentioned ous decontamination Peters et al. Antimicrobial Resistance & Infection Control (2023) 12:7 Page 4 of 7 evidence-bases automated technologies such as gaseous analyses of the hospital environment have provided some hydrogen peroxide and ultraviolet light technologies. insights into the hospital microbiota, they did not pro- Both sets of standards are a step forward for their vide support for the development of new interventions countries, the NHS including the clinical staff in respon - such as probiotic-based treatments [16–18]. An analysis sibilities for cleaning and the DIN for being the first using a culture-based approach based on MALDI-TOF national guidance. Both however would benefit from a mass spectrometry of sink biofilms did provide some more transparent description of the evidence base and modest leads, but additional experiments are needed to strength of evidence from which the recommendations draw more firm conclusions on which microorganisms have been derived. enable or inhibit P. aeruginosa persistence [8]. Enzymatic, probiotic [18] or phage-based approaches should also be Case study of an environmental pathogen: Pseudomonas explored. Innovative approaches are needed to address aeruginosa persistent environmental reservoirs of bacteria and help A safe hospital is a clean hospital, but what exactly “clean” create microbiologically safe hospitals. The question means can vary. In the context of preventing HAIs, it is how to best foster these types of approaches. could be interpreted as a microbiologically safe hospital without pathogenic microorganisms in its environment. Innovation in environmental hygiene P. aeruginosa is especially capable of surviving in the Innovation is everywhere in our daily-life including the hospital environment, with sinks as the most frequently healthcare system. Infection control and environmental reported reservoir [6–9]. P. aeruginosa bacteria form hygiene have been expected to take advantage of these biofilms in the lumen of pipelines, from which cells may progresses on the condition that we are able to assess be released during sink use and spread outside of drains the efficacy and the impact of new available technologies within droplets or as aerosols. Surfaces in the patient [19]. environment may become contaminated, and ultimately Electronic health records in hospitals and the software reach the patient. A recent analysis showed that the vast to instantaneously aggregate them, provide important majority of P. aeruginosa infections (86.3%) were trans- data that should be available to infection control teams. mitted through the environment as opposed to cross- If collected and analyzed appropriately, this data can transmission from other individuals or patients. Bacterial provide practitioners knowledge which can, in turn, be drain reservoirs are notoriously difficult to eradicate, as transformed into action, and potentially improve infec- commonly-used hospital disinfectants do not remove tion control [20]. biofilms, and recolonization may occur after exposure Other types of digitalization and tracking are now to contaminated materials or retrograde growth from becoming more common in environmental cleaning and p-traps. disinfection. Modern technology can provide autonomy When it is not feasible to remove such pathogenic bac- to the professional, while performing continuous moni- teria, elimination of the complete reservoir can be con- toring, enable early detection of hygiene failures, and sidered; an intervention which several hospitals have facilitate quick interventions. This can ultimately prevent implemented [10–12]. The removal of sinks was per - outbreaks and mitigate both the human and financial formed in the framework of a bundle focused on water- costs associated with HAIs. Managers should encour- free patient care. Though this intervention had an effect age these innovations and their use in a fair manner, by in all three studies, the removal of sinks is not feasible focusing on quality improvement and not on individuals outside of intensive care units, and shower drains may be blame for failures. reservoirs for P. aeruginosa as well [13]. It is desirable to technology to automatize important If neither elimination of the pathogen, nor the com- tasks that are difficult for humans to perform consist - plete removal of the reservoir is possible, elimination or ently. This is especially the case for robots that are quickly control of the transmission route of pathogenic micro- becoming ubiquitous in the field of cleaning and disinfec - organisms from or via the environment is a pragmatic tion. Ultra violet-C (UVC) disinfection, for example, is a approach. A range of such interventions have been pub- promising technology with demonstrated efficacy. How - lished, often focused on an improved sink design [6, ever, international quality standards are lacking, and are 14, 15]. Most of these interventions showed significant important in order for consumers to fully rely on such reductions in transmission, though control was not fully technology where appropriate. Such technologies have achieved. additional effects beyond their efficacy- implementing To identify alternative solutions, a better understanding visible technologies has been shown to improve safety of the hospital’s microbiota and the environmental bio- climates in hospitals by increasing the confidence of both films is key. Though recent studies using (meta)genomic patients and healthcare workers [21]. P eters et al. Antimicrobial Resistance & Infection Control (2023) 12:7 Page 5 of 7 Antimicrobial surfaces are based on technologies that ways healthcare facilities need to go “back to the future” either repel or kill microorganisms when applied to a sur- by having locally, decentralized infrastructure in order to face [22]. The field of possible applications of such tech - support reuse and reprocessing where appropriate. nologies is wide and still growing [23]. A French national Developing a circular economy is central to making organization for standardization/ Association Française it sustainable. In 2020, 100 billion tons of new materi- de Normalisation (AFNOR) efficacy standard (NF S als entered the world economy, and only 8.6 was circu- 90-700) has been published in 2019 and is the basis for lar [31]. The World Economic Forum estimates that 70% what will become the ISO standard. Discussions are still more virgin materials were extracted from the Earth than underway concerning the appropriate efficacy require - what it can safely replenish [31]. Not only do we need ments and the differentiation between similar technolo - to use less, but we need to make things last longer, uti- gies, such as for opaque versus transparent surfaces. The lize renewable energy and regenerative materials, and expected goal of antimicrobial surfaces is to help reduce plan how to reuse and recycle from the very beginning, the transmission burden, especially on high-touch sur- instead of as an afterthought. Recycling should be the faces [24]. end point of a circular economy, not the first thing tried. Innovation in environmental hygiene should not be The cost structure of materials is a major issue, as new seen as an endpoint nor a magic bullet but as compo- materials are often much cheaper than recycled ones nents of an infection control strategy that can be added [32]. This creates frequent incompatibility between sus - in intervention bundles. Industry should focus on dem- tainability and affordability. onstrating the immediate efficacy of such technology and It is also increasingly clear that infection preventionists the infection control experts should decide when, where need to participate in the decision making around sus- and how to use it to maximize its impact. tainability in healthcare in order to prevent new meas- ures from having a negative effect on efficacy. If infection Sustainability control experts do not get involved in this agenda, some- The entirety of this research and projects and new tech - one who is not an expert will set it. Further challenges nologies and trends need to share a common trait; they include a lack of accountability, and social equity. It is must all be sustainable to implement. Sustainability also important to talk about responsibility, both individu- means meeting the needs of the present without com- ally and collectively at the institutional and governmental promising the needs of future generations. For healthcare levels. facilities, there is often a tradeoff (sometimes perceived, Institutions can begin to take steps in a number of sometimes real) of sustainability versus efficacy. ways. First, they can reduce the use of chlorine-based The World Meteorological Organization predicts products [33] and adapt policies to infection preven- 50/50 odds that temps will increase between 1.5 and 2C tion needs as new information evolves. It is important over pre-industrial levels, for one year over the next five to reduce reliance on single use equipment unless abso- [25]. This means that there will be irreversible and per - lutely necessary. Healthcare facilities used to reuse more, haps catastrophic changes to our climate. Globally, the but fear during AIDS pandemic pushed facilities towards healthcare sector is responsible for almost 5% of emis- single use, even for surgical caps and gowns that could be sions [26]. A global analysis of health care waste in the laundered. High-cost, low-volume medical devices are context of Covid-19 showed hundreds of thousands tons often discarded simply on the advice of the manufacturer. of additional waste from Covid-19 test kits, personal pro- Healthcare facilities need to work with manufacturers tective equipment (PPE), vaccine production etc. [27, 28] to change this, and to maximize the safe reusability of Beyond the quantity of waste, the WHO estimates that 1 equipment. in 3 healthcare facilities does not safely manage its waste [27]. Conclusion Countries are beginning to take steps to try to reach The future of HEH is clear as the field becomes more net zero, which means cutting emissions as close to zero recognized as being key component of successful infec- as possible and reabsorb all remaining emissions into tion prevention strategy. Still, more research is needed healthy oceans and forests. The UK’s target is to reach to prove the efficacy of standard interventions and of net zero by 2050 [29]. The UK’s NHS is aiming to reach recently developed technologies. New ways of managing net zero by 2040 [30]. While some aspects are in con- the built environment need to be explored and innova- trol of institutions, others are not. IPC is often still not tion needs to be evidence-based and adopted in a context wholly evidence-based, and this needs to improve so that that is helpful to and respectful of the environmental ser- resources are not used when it is not necessary to do so. vices staff and our planet. PPE needs to be used better and more precisely. In many Peters et al. Antimicrobial Resistance & Infection Control (2023) 12:7 Page 6 of 7 facility level. Am J Infect Control. 2022. https:// doi. org/ 10. 1016/j. ajic. 2022. Networks such as Clean Hospitals need to continue 02. 029. to work on defining the research agenda globally as well 4. DIN 13063, Krankenhausreinigung—Anforderungen an die Reini- as creating awareness for the field. Healthcare facilities gung und desinfizierende Reinigung in Krankenhäusern und anderen medizinischen Einrichtungen (Unpublished manuscript). (2021). around the world need to be able to analyze their own 5. National Health Service (UK). National Standards of Healthcare Cleanli- programs in the context of best practices, and tools must ness 2021. (2021). be developed to help facilitate improvement. Sustainable 6. Parkes LO, Hota SS. Sink-related outbreaks and mitigation strategies in healthcare facilities. Curr Infect Dis Rep. 2018;20:42. international norms and guidelines should be developed 7. Pelegrin AC, et al. High-risk international clones of carbapenem-nonsus- in order for institutions to implement universal mini- ceptible pseudomonas aeruginosa endemic to indonesian intensive care mum standards for quality while ensuring that future units: impact of a multifaceted infection control intervention analyzed at the genomic level. MBio. 2019;10:e02384-e2419. generations can enjoy the same level of access as ours. 8. Pirzadian J, et al. Novel use of culturomics to identify the microbiota in hospital sink drains with and without persistent VIM-positive Pseu- domonas aeruginosa. Sci Rep. 2020;10:17052. Abbreviations 9. Voor In’t Holt AF, Severin JA, Lesaffre EMEH, Vos MC. A systematic review AFNOR A ssociation Française de Normalisation/French national organiza- and meta-analyses show that carbapenem use and medical devices are tion for standardization the leading risk factors for carbapenem-resistant Pseudomonas aerugi- DIN Deutsches Institut für Normung/German Standards Institute nosa. Antimicrob Agents Chemother. 2014;58:2626–37. HAI Healthcare-associated infection 10. Catho G, et al. Outbreak of Pseudomonas aeruginosa producing VIM car- HEH Healthcare environmental hygiene bapenemase in an intensive care unit and its termination by implemen- NHS National health service tation of waterless patient care. Crit Care. 2021;25:301. PPE Personal protective equipment 11. Hopman J, et al. Reduced rate of intensive care unit acquired gram-neg- UVC Ultra violet-C ative bacilli after removal of sinks and introduction of ‘water-free’ patient care. Antimicrob Resist Infect Control. 2017;6:59. Acknowledgements 12. Shaw E, et al. Control of endemic multidrug-resistant Gram-negative Not applicable. bacteria after removal of sinks and implementing a new water-safe policy in an intensive care unit. J Hosp Infect. 2018;98:275–81. Author contributions 13. Hopman J, et al. Risk assessment after a severe hospital-acquired infec- PP, MK, JS, DP wrote and submitted summaries of their respective talks to AP. tion associated with carbapenemase-producing pseudomonas aerugi- TG contributed her slides and materials for summary by AP, and then edited nosa. JAMA Netw Open. 2019;2:e187665. and approved that summary. AP compiled the summaries and wrote the 14. de Jonge E, de Boer MGJ, van Essen EHR, Dogterom-Ballering HCM, paper. MK wrote the table. All authors reviewed, edited and approved the Veldkamp KE. Eec ff ts of a disinfection device on colonization of sink paper. drains and patients during a prolonged outbreak of multidrug-resistant Pseudomonas aeruginosa in an intensive care unit. J Hosp Infect. Funding 2019;102:70–4. There was no specific funding for this paper, the Healthcare Cleaning Forum 15. Pirzadian J, et al. Impact of sink design on bacterial transmission from was funded by Interclean and supported by Clean Hospitals. hospital sink drains to the surrounding sink environment tested using a fluorescent marker. J Hosp Infect. 2022;127:39–43. Availability of data and materials 16. Ashokan A, et al. Environmental dynamics of hospital microbiome upon There was no data generated, but we will gladly share whatever information transfer from a major hospital to a new facility. J Infect. 2021;83:637–43. may be requested. 17. Chng KR, et al. Cartography of opportunistic pathogens and anti- biotic resistance genes in a tertiary hospital environment. Nat Med. 2020;26:941–51. Declarations 18. Klassert TE, et al. Bacterial colonization dynamics and antibiotic resistance gene dissemination in the hospital environment after first patient occu- Ethics approval and consent to participate pancy: a longitudinal metagenetic study. Microbiome. 2021;9:169. Not applicable. 19. Gray J. Infection control: beyond the horizon. J Hosp Infect. 2015;89:237–40. Consent for publication 20. Lin MY, Trick WE. Computer informatics for infection control. Infect Dis Not applicable. Clin North Am. 2021;35:755–69. 21. Rock C, et al. Patient and health care worker perceptions of daily use of Competing interests ultraviolet-C technology as an adjunct to daily cleaning in an academic All authors declare no competing interests. hospital: secondary study of ultra violet-C light evaluation as an adjunct to removing multi-drug resistant organisms. Am J Infect Control. 2018;46:348–9. Received: 9 September 2022 Accepted: 11 November 2022 22. Sheridan M, Winters C, Zamboni F, Collins MN. 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Journal

Antimicrobial Resistance and Infection ControlSpringer Journals

Published: Feb 7, 2023

Keywords: Infection prevention and control; Environmental hygiene; Cleaning; Sustainability

References