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Keeping hospitals clean is a crucial patient safety issue. The importance of the hospital environment in patient care has only recently been recognized widely in infection prevention and control (IPC). In order to create a movement for change, a group of international infection control experts teamed up with Interclean, the largest cleaning trade- show in the world to create the Healthcare Cleaning Forum. This paper is the result of this conference, which featured leaders in healthcare environmental science from across Europe. Although the available literature is limited, there is now enough evidence to demonstrate that maintaining the hygiene of the hospital environment helps prevent infections. Still, good interventional studies are rare, the quality of products and methods available is heterogeneous, and environmental hygiene personnel is often relatively untrained, unmotivated, under-paid, and under-appreciated by other actors in the hospital. Coupled with understaffed environmental hygiene service departments, this creates lasting issues in regards to patient and healthcare worker safety. The Healthcare Cleaning Forum was designed as a platform for healthcare experts, cleaning experts, hospital managers and industry to meet productively. The conference aimed to summarize the state-of-the-art knowledge in the field, create awareness and dialogue, challenge dogma and begin to shape a research agenda for developing the field of hospital hygiene and environmental control. Hospital environmental hygiene is far more complex than other types of cleaning; further evidence-based research in the field is needed. It involves the integration of current and new technologies with human elements that must work together synergistically to achieve optimal results. The education, training and career development, behavior, and work organization of environmental hygiene personnel are at the core of the proposals for the creation of a global initiative. Ultimately, what is needed is a reevaluation of how hospitals view environmental hygiene: not just as an area from which to cut costs, but one that can add value. Hospitals and key stakeholders must work together to change how we maintain the hospital environment in order to better protect patients. Keywords: Infection prevention, Cleaning, Disinfection, Environment, Healthcare-associated infection, Public health, Environmental hygiene, Hand hygiene, Infection control, Antimicrobial resistance Introduction instead of washing hands with soap and water, about 25 Revolutions are often started by ideas whose time have years ago- a seemingly small change in practice that con- come. Compared to other domains in medicine, revolutions tinues to save millions of lives [1–3]. Today, looking at the in the field of Infection Prevention and Control (IPC) are IPC landscape, the one area that has been consistently generally few and far between. The last one was probably undervalued and understudied is the role of the hospital the global shift to using alcohol-based handrub (ABHR) environment in patient care. Keeping hospitals clean is not just an aesthetic, but a patient safety issue. Although the available literature is limited, there is * Correspondence: didier.pittet@hcuge.ch enough evidence to demonstrate that cleaning hospitals Infection Control Programme and WHO Collaborating Centre on Patient helps prevent infections. Still, good intervention studies Safety, University of Geneva Hospitals and Faculty of Medicine, 4 Rue Gabrielle-Perret-Gentil, 1211 Geneva, Switzerland are rare, the quality of products and methods available is Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Peters et al. Antimicrobial Resistance and Infection Control (2018) 7:132 Page 2 of 12 heterogeneous, and environmental hygiene personnel is wants to be the next patient in a contaminated room [4]. often relatively untrained, unmotivated, under-paid, and When the world changed how they thought about hand under-appreciated by other actors in the hospital. Coupled hygiene 25 years ago [2, 5, 6], it realized how important with understaffed environmental hygiene services depart- hands were as the main vectors for spreading diseases ments, this creates lasting issues in regards to patient and from one patient to another in hospital settings. It is esti- healthcare worker safety. mated that over 50–70% of all HAI are spread through The situation is not helped by the lack of literature con- contaminated hands. It is time to focus on the other 30– cerning the exact impact that a soiled or contaminated en- 50%, a part of which might be linked to environmental vironment has on healthcare-associated infections (HAI). transmission (Fig. 1). After all, “hands are really just an- In order to begin the initiative to change how hospitals other highly mobile surface in healthcare that are com- think about their environment, a group of infection con- monly contaminated and rarely disinfected” [7]. Since trol experts teamed up with Interclean, the largest clean- there is a dynamic interchange between contamination on ing trade-show in the world, to create the Healthcare surfaces and hands [8], some of the transfer in which con- Cleaning Forum: a nexus where hospital managers, indus- taminated hands are the final link include contaminated try, and healthcare and cleaning experts could meet pro- surfaces as links earlier in the chain of transmission. ductively. For the first time, Interclean dedicated an entire Ideally, hospital environmental hygiene should follow the hall to cleaning in healthcare, and hosted a conference fea- World Health Organization (WHO) model of “Clean Care turing leaders in healthcare environmental science from is Safer Care” established for hand hygiene in 2005 [6], across Europe. The speakers summarized the state of the which spearheads good practices in more than 180 coun- art knowledge in the field, challenged the current dogma tries today [1, 9]. There is a need for creating and began to shape a research agenda for developing the evidence-based guidelines for hospital cleaning, and for field of hospital hygiene and environmental control. This using those guidelines to develop the right tools for educa- article outlines the major issues and points brought up tion and implementation. during the conference. It attempts to illustrate the large Although high-quality interventional studies are lim- gap that exists between environmental hygiene and the ited, there are enough to show that cleaning and disin- healthcare industry, as well as bring some much-deserved fecting hospitals in order to prevent infection works. attention to a concept whose time has come. Analysis of numerous studies shows a clear correlation between “cleaning hygiene failures” and the number of intensive care unit-acquired infections (Fig. 2). Several Cleaning as a patient safety initiative studies showed that patients were much more likely to We need to change how we think about the hospital en- contract certain pathogens if the patient in the room vironment- if the risks of transmission are known, no one before them was colonized or infected with a pathogen Fig. 1 “No one wants to stay in a contaminated room” Peters et al. Antimicrobial Resistance and Infection Control (2018) 7:132 Page 3 of 12 Fig. 2 Relationship between environmental bioburden and hospital-acquired infection [10] linked to HAI (Fig. 3)[4, 10–12]. There is a wealth of cleaning on a microbiological level (Table 1; the acro- information on what products or chemicals eliminate nym “WASTE” can be used to recall the 5 variables). which pathogens and how to apply them. This includes These elements are: what product or intervention is ap- efficacy and toxicity studies as well as a few clinical plied, the technique and equipment used to apply the studies assessing the effect of specific interventions to product, the type of surface, the level of contamination control outbreaks [10]. More research is needed to of the environment, and last but not least, the environ- measure the effects that cleaning methods have on mental hygiene personnel doing the cleaning [13]. If HAI. Since improved environmental cleaning and de- any one of these elements is lacking, the cleaning will contamination measures are always bundled with other by definition be suboptimal. Because of this, changing interventions during outbreaks, it is difficult to measure cleaning practices in hospitals must be implemented their precise impact. through a multimodal strategy that takes these variables into account. The best cleaning substance in the world is useless if not applied correctly, and the best-trained Cleaning in healthcare personnel are useless if the product they are using is Hospital environmental hygiene is complex because it not effective against the particular pathogen that needs is dependent on the pathogen present and the product to be removed or killed. used to remove it. There are five main variables to But what is “clean”?(Table 2) Maintaining a hygienic cleaning, whether removing soil or disinfecting and hospital environment is not only about removing soil, Fig. 3 Risk of acquisition from prior room occupants by organism [4]. Risk of acquisition from prior room occupants by organism. M-H, Mantel–Haenszel; VRE, vancomycin-resistant enterococci; MRSA, meticillin-resistant Staphylococcus aureus; Ajao et al.’s study involved extended spectrum β-lactamase producing Klebsiella or Escherichia coli organisms. Acinetobacter: Acinetobacter baumannii; Pseudomonas: Pseudomonas aeruginosa. It was not possible to separate Klebsiella sp. and Escherichia coli data in the Ajao et al. study. Reprinted with permission from the Journal of Hospital Infection Peters et al. Antimicrobial Resistance and Infection Control (2018) 7:132 Page 4 of 12 Table 1 Environmental hygiene: How to get there – WASTE but also about organizing an environment that is optimal for patient safety. Obviously if an area is visibly dirty, one Workforce The individuals responsible of organizing, executing and verifying a cleaning activity cannot disinfect it. Visibly soiled surfaces must first be Area The environment to be cleaned. This includes the type of cleaned, and then, when or if appropriate, disinfected. Fail- surface, if it is intact and the level and type of ure to do so means that the infective organisms cannot be contamination. targeted effectively [10]. The 2018 survey from the Euro- Substance The chemical component/product to cleaning, whether pean network to promote infection prevention for patient detergent or disinfectant safety (EUNETIPS) aimed to analyze how different hospi- Technique The method by which the cleaning substance is applied by tals evaluated and have created their cleaning strategies either a person or a machine [14]. Cleanliness of a hospital also plays a large role in pa- Equipment The machines or tools used to effectuate cleaning. This tient perception of the healthcare setting, and conse- includes everything from a microfiber cloth to a hydrogen peroxide vapor machine. quently of patient satisfaction [15, 16]. Patients are instrumental in convincing administrators to invest in WASTE: workforce, area, substance, technique, equipment cleaning, and must be sensitized to the issues in order to be allies for creating change. Table 2 Glossary of terms Term Definition Antisepsis Destruction or inhibition of microorganisms in or on living tissue, e.g., on the skin or mucous membranes [29]. Automated disinfection Disinfection using machines instead of manual application. Examples incl. Hydrogen peroxide vapor and UV light machines. Cleaning General term for the removal of soil. Cleaning & disinfection Removal of soil and killing of microbes. Decontamination The neutralization or removal of dangerous substances, radioactivity, or germs from an object, area or person [29]. Detergents Water-soluble cleansing agents which combine with impurities and dirt to make them more soluble, and differ from soap in not forming a scum with the salts in hard water [30]. Disinfectants/disinfecting Agents capable of destroying pathogenic microorganisms or inhibiting their growth activity [31]. Especially: chemicals agents that destroy vegetative forms of harmful microorganisms (such as bacteria and fungi) especially on inanimate objects but that may be less effective in destroying spores [32]. Disinfecting detergents The combination of a detergent with a disinfecting agent for the simultaneous removal of soil and the killing of microbes. Disinfection The antimicrobial reduction of the number of viable micro-organisms to a level previously specified as appropriate for its intended further handling or use [29]. Environmental hygiene Cleaning and/or disinfection of a specific environment. Environmental hygiene People in charge of cleaning and disinfecting, and maintaining the hospital environment. personnel Environmental hygiene Service within a hospital that takes care of cleaning and hygiene of the environment. services Fumigation To apply smoke, vapor, or gas especially for the purpose of disinfecting or of destroying pests [33]. In the past, this term was often used to mean automatic disinfection. In the context of environmental hygiene, the “pests” part of the definition does not usually apply. Pasteurization Disinfection, usually by heat, of microorganisms that can be harmful or cause product spoilage. Frequently applied for preservation. The prevention of the multiplication of microorganisms in products [29]. Resistance The inability of an anti-infective or biocide to be effective against a target microorganism [29]. Sanitization Disinfection of microorganisms that pose a threat to public health [29]. Sterilization Defined process used to render a surface or product free from viable organisms, including bacterial spores [29]. It also frequently includes the objective of allowing the maintenance of the sterile state. Terminal cleaning Cleaning and disinfection of a room after a patient carrying a dangerous/resistant pathogen leaves the room. Tolerance Decreased effect of an active agent against a target microorganism and requiring increased concentration or other effects to be effective [29]. In General a) Surfaces can be processed by detergent cleaning, disinfection, or a combination of the two (detergent plus disinfectant) b) Medical devices require a pre-disinfection (immediately after use to prevent biofilm) including (or not) mechanical cleaning, followed by disinfection or sterilization Peters et al. Antimicrobial Resistance and Infection Control (2018) 7:132 Page 5 of 12 Available products whole. Often there is a high turnover rate among personnel In addition to a vast array of detergents and cleaning/disin- within the cleaning service or a language barrier between fecting equipment, common chemicals used for disinfection the cleaners and the rest of the staff. Cleaning personnel include: alcohol, chlorine and chlorine compounds, formal- must be trained to understand why their work is important dehyde, glutaraldehyde, hydrogen peroxide, iodophors, to the hospital, and need to be recognized and certified in ortho-phthalaldehyde, peracetic acid, phenolics, and quater- order to improve motivation and compliance [18]. nary ammonium compounds [17]. This paper will not go into any detail on these products as such a discussion Logistics of hospital cleaning would betoo extensiveand was not thepurpose of the The place of the environmental hygiene services depart- Healthcare Cleaning Forum 2018. ment (Table 2) within a hospital is important, especially An ideal product would be effective against all bacteria, with regard to how they work together with the IPC ser- spores, viruses, and prions while having no impact on the vice. Nursing assistants are generally responsible for clean- environment and being completely safe as well as easy to ing one part of the patient environment and the use. Currently no such product exists; thus choosing any environmental hygiene personnel for another; but often, product will result in some level of tradeoff. respective tasks are not clearly defined. For example, if For example, hydrogen peroxide vapor does not leave who needs to clean the bedside table is not explicitly stated, any residues in the environment, but is expensive, can be then there is a good chance that that table may not be corrosive, and is difficult to use compared with liquid dis- cleaned by anyone. In one survey, one third of environ- infectants. Chlorine solutions are effective against spores, mental hygiene personnel admitted that they were not but have a strong odor, leave residues, and may damage really clear about what they were responsible for [19]. Ab- certain environmental surfaces. UV light leaves no residue sences or shortage of staff on wards, and/or the transfer of but cannot disinfect areas that it cannot shine on directly. responsibilities between colleagues could complicate an This is the case for every single product available today; already unclear situation and result in crucial maintenance most only work against certain types of pathogens, and not being performed. This can result in the spreading of others are toxic or degrade certain materials in the patient disorder: a few minor mistakes, or disregard for a few of environment. the rules, eventually cause increased disregard for rules in general among the whole staff [19]. The human component In addition to the aforementioned issues, environmental But cleaning is not only dependent on the chemicals used. hygiene services are often outsourced to external compan- The ideal environmental hygiene personnel (Table 2) ies. While probably not as much of an issue in a stairwell would remain thorough and meticulous, and always use or an office, it is virtually impossible for a hospital to the right technique, product and materials. Cleaning and optimize the cleaning staff and its quality if they have little disinfecting a hospital is a repetitive task that can quickly to no oversight of or influence on the environmental hy- become mundane. Environmental hygiene personnel are giene. Outsourcing is not necessarily bad, but the right often not trained sufficiently, and do not feel that they conditions must be observed, and crucial areas need to be have the agency to make a difference in patient safety. cleaned by trained and certified professionals, even if costs Additionally, the amount of work that they are expected are bit higher initially. to do is not always in accordance with the time assigned to the task. Within the hospital hierarchy, environmental Education, training and communication hygiene personnel are on one of the lowest rungs, and So how can we effectively educate and train hospital often credit is not given to them, especially considering personnel for modern environmental hygiene mainten- the importance of their work. There is a major problem ance? While the science of cleaning and disinfecting with how “cleaners” are often perceived as menial and un- agents and equipment has evolved immensely in the last educated by the rest of the hospital staff. In many coun- few decades, the education of cleaning personnel and their tries, particularly in high-resources settings, cleaning integration into healthcare worker teams has not. Clean- personnel frequently originate from outside of the coun- ing and disinfecting hospitals is very different from clean- try, and do not express themselves in the local language, ing public spaces such as hotels or offices; hospitals must thus making discussions and interactive exchanges with realize this and adapt to the challenges. There is a range other categories of health professionals difficult or even of environments within each hospital, from offices to in- impossible. tensive care units or hospital pharmacy services, some of Additionally, few hospitals have sufficient systems in which require specialized approaches to environmental place to train and certify their cleaning staff. Without certi- hygiene maintenance. There are even different require- fication, advancement is unstructured and can be limited ments for different sectors within the same department. sincethereis no waytogaugethequalityofa staffas a The pathogens present in hospitals can be quite different Peters et al. Antimicrobial Resistance and Infection Control (2018) 7:132 Page 6 of 12 from those present in the community, and the patient or the inclusion of copper in them in order to reduce con- population is more vulnerable. Each type of pathogen has tamination [11]. The idea of having something permanently its own specific transmission pattern, host affinity, and in the patient environment that is always working is an at- microbiological characteristics. tractive one (although perhaps expensive): if one can con- Leaders and trainers must be seen as legitimate by staff, trol the level of contamination at the source, then there is and need to ensure their understanding and motivation. less to remove and less risk for sub-optimal cleaning and Only if there is a high process understanding in training disinfection. Further research, including unbiased, high- can quality become routine; an informed person tends to quality clinical efficacy and effectiveness studies are how- be more compliant, and a compliant person is more moti- ever still needed before further recommendations can be vated. Motivatedteams aremoreefficient andmoreaware, made regarding these materials [22, 23]. and individuals need to understand that everyone’sworkis important. Personal responsibility and team cohesion re- Cost vs. value of hospital cleaning and disinfection quire solid collaboration, which in turn requires the equal- It is imperative to develop a new and efficient model ity and realization of rights and duties. Repetition, feedback for hospital environmental hygiene maintenance. The and team-building help optimize performance in environ- return on investment for successful hand hygiene pro- ments that inherently foster human error. Analyzing hos- motion has been shown to up to 23 times the initial pital architecture, workflow, and ergonomics can go a long amount invested [24–26]. In order to have similar fig- way to reducing it. It is important to realize that the best ures for hospital environmental hygiene, we need to product, equipment or intervention is worthless without first understand what the cost of maintaining a clean well-trained, responsible and compliant staff. hospital environment is, and what its value is. Although many hospitals are quick to spend money on new soft- Possibilities of automation and self-disinfecting surfaces ware, specialized staff and fancy equipment, they often Automation can be useful, but currently does not replace look at maintaining the environment hygiene as an op- the need for thorough manual cleaning. Although manual portunity to save in the budget. cleaning and disinfection can be qualitatively as good as Hospitals often try to cut environmental hygiene machine automated disinfection (or even better in some maintenance costs as much as possible, both in the instances), one has less oversight over humans, and they products that they use, and in the training and contin- do not clean at their best all of the time. Environmental ued education of their workforce. The essential shift in hygiene service managers can use a variety of tools includ- approach needs to happen in how hospitals assess this ing visual inspection, cultures, ATP meters or UV light re- cost and value. Because the costs of not cleaning can active fluorescent markers to verify how well a given area affect numerous budgets within a hospital, it is difficult has been cleaned and disinfected. Though even the to accurately account for them. Hospitals need to look best-trained people are prone to error, machines never beyond actual expenditures to averted expenditures, skip any steps. Automated or semi-automated room disin- such as increase in patient-days due to HAI, as well as fection is not to replace personnel, but to raise the bar on opportunity costs such as hospital staff time or missed the standard of disinfection and, in some instances, pre- surgical revenue due to increased turnaround time in vent work-related musculoskeletal constraints among en- an operating theater. There are also increases in costs vironmental hygiene personnel. At some point, solely associated with antimicrobial resistance in HAI, which manual approaches are doomed to fail, as hospital envi- has a cost estimated at over €85 trillion ($100 trillion) ronments are intricate and difficult to maintain in an ap- globally by 2050 [27]. For example, one relatively small propriately clean state. In one study, up to 50% of an outbreak with approximately 40 cases cost a hospital environment remained uncleaned after manual cleaning. over €1 million [28]. Prevention is always better and Another study showed that after four rounds of manual less expensive than a cure, especially when we are run- cleaning and disinfection with a bleach solution, 25% of ning out of antibiotics. So when making a decision rooms were still contaminated with Acinetobacter bauma- about which environmental hygiene maintenance sys- nii [20]. Automated room disinfection with hydrogen per- tems to buy, which products to use, or how much to in- oxide vapor or ultraviolet light have shown promising vest in training the cleaning personnel, hospitals would results in targeting specific microorganisms, although they do well to look at the costs of not doing so, or deciding only work once a room has already been manually cleaned on a cheaper solution. In order to save money in the to remove soil [21]. long-term and improve patient satisfaction, hospitals Beyond machines, there is an important need for more need to invest in quality across the board whether in research into surfaces that inherently inhibit bacterial con- materials, disinfectants, technological innovation, or tamination or that have self-disinfecting properties. A few the training, education, and certification of their work- that have been studied are the micro-patterning of surfaces force (Fig. 4). Peters et al. Antimicrobial Resistance and Infection Control (2018) 7:132 Page 7 of 12 Fig. 4 Hospitals should value environmental hygiene cleaning and maintenance A time for cooperation cotton cloth), which liquid agent to use (e.g. a detergent It is imperative to develop public-private partnerships in or a disinfectant and, if a disinfectant, which one), and the field of clean hospitals. Industry and academia both the ideal frequency of the cleaning and disinfection (e.g. have a role to play in raising standards and providing daily, after each use, or both). Many questions remain hospitals with the best possible products and methods. unanswered; some are addressed in the Appendix (see First, currently marketed sub-standards products and Appendix). Hospitals must get out of the vicious circle methods should be suppressed. Ultimately, the difference of cutting costs and instead assess value. They must will no longer be between good and bad products on the realize that being a hospital “cleaner” is not a job but a market, but within implementation and training of those profession, and invest in their workforce. Academics products and technologies. must encourage further studies (see research agenda, Cleaning and environmental maintenance is a science. Table 3) as well as weave together the data available in Initially, assessing the approach for the hygiene of a toi- order to present hospitals with a convincing business let seat seems almost redundant. However, many of the case of why to invest in hospital cleaning. questions around this seemingly simple activity require Because clean hospitals is an idea whose time is now. study and scientific assessment. One must decide mater- ial to use to clean the toilet seat (e.g. microfiber or Comment The authors alone are responsible for the views expressed Table 3 Hospital cleaning: overall research agenda in this article and they do not necessarily represent the Mobilize stakeholders views, decisions or policies of the institutions with which Develop standardized guidelines for hospital cleaning they are affiliated. Develop standardized operating procedures (SOP) for assessing quality of the cleaning performed Appendix During the speaker presentations at the Healthcare Clean- Build a solid business case for investing in cleaning services, taking into consideration the cost and value of hospital cleaning and disinfection ing Forum conference in Amsterdam (May 16th, 2018), Encourage increased research in methods, implementation, compliance, audience participants were able to ask questions directly and clinical outcomes of hospital cleaning via their smartphones. A total of 87 questions were sub- Foster cooperation between private enterprise and public institutions mitted. Some of these questions were chosen and then posted on the screen above the speakers, who then ad- Compile existing and publish new literature supporting the best products, technology and practices on the market dressed them directly after each presentation. These ques- Develop a model of a proven way of organizing hospital environmental tions, as well as some that there were not posted during cleaning services. Address the issue of cleaning personnel certification. the conference, have been organized, and in some cases, How to train and educate personnel for modern cleaning tasks? combined or rephrased for clarity. The responses from the Ensure process understanding in training: quality must become routine speakers have been synthesized in the table below. Address hospital perception of hospital environmental cleaning Questions answered directly in the paper are not listed personnel- cleaning is not just a job, but a profession in the Table. Peters et al. Antimicrobial Resistance and Infection Control (2018) 7:132 Page 8 of 12 Table 4: Questions from the Healthcare Cleaning Forum 2018 Questions on the technical process of cleaning: Q: In the process of wiping a surface clean, how many variables are involved? A: Please see Table 1. Q: Is the use of probiotics allowed in the healthcare sector for cleaning and can this be a solution for difficult to reach surfaces? A: Emerging evidence suggests that seeding the hospital environment with Bacillus spp. spores may reduce the level of pathogens that are culturable from surfaces. Whilst this could be as a result of competitive ecological exclusion, it could be possible that the Bacillus spores are merely masking the presence of pathogens. Further evaluations of this approach, including clinical outcome studies, are required. Q: Is a combined disinfection and detergent wipe better? A: It depends on the application. There are instances where it is better, but other instances where a disinfectant may not be required. Please see Table 2. Q: Are bacteriophage-based disinfection technologies (aerosolized for instance) considered as a complementary solution for disinfection? A: Bacteriophage-based disinfection of the environment, whether applicable to surfaces or air, deserves both a literature search (particularly in Russian) and further in vivo and clinical research. Q: Is it worth investing in an airborne disinfection solution? A: There is emerging evidence that contaminated air may be involved in the transmission of pathogens that were traditionally associated with contact transmission, such as C. difficile and Acinetobacter spp. Further research is needed to understand the role of airborne transfer and airborne disinfection in hospital environmental hygiene. Q: Does the cleaning of equipment wheels in ward areas help in reducing infection? A: There is no evidence-based research demonstrating that cleaning of equipment wheels in regular ward areas helps to reduce infection; it is usually recommended at entrance of high-risk areas (ie. operative theatre), but further research is needed for definitive guidelines to be recommended. Q: With no-touch cleaning and disinfecting, how is the soiling contamination removed? If the soil remains behind, is it possible to disinfect? A: The room or area should be cleaned to remove dirt and organic soiling before an automated room disinfection system is applied. Please see also Table 2 for definitions. Q: How do you deal with the issue of shadows in UV (ultraviolet light) systems? A: Whilst the efficacy of UV systems in areas that are out of direct line of site of the UV device receive a lower dose of UV, they do receive a dose of UV due to reflection from other surfaces. The impact of line of sight in UV room disinfection can be mitigated by staging the device in different parts of the room, or using multiple emitters. The only solution is to change the angle of the UV light or to use alternative methods for decontamination. Q: How important is cleaning of ceilings? How important is selection of building materials so that surfaces are less prone to infection? A: Cleaning of ceilings is not that important as patients do not come in contact with ceilings. Surfaces must be chosen that are chemically resistant and easy to clean (non-porous). No surface is “resistant to infection”; some surfaces could be less prone to contamination. Please see also Table 2 for definitions. Q: Have either hydrogen peroxide vapor (HPV) or UV-C devices been proven superior to the other in preventing surgical site infections? A: To the best of the authors’ knowledge, none of the two methods has been associated with a significant reduction in surgical site infection in a controlled study. Q: What are your thoughts about preventive (not corrective) disinfection with UV-C in high-risk areas after standard cleaning procedures? A: Most studies that tested the impact of UV devices in healthcare settings used the devices to treat the rooms of patients known to be infected or colonized with a pathogen. There is a theoretical possibility that using UV more regularly would have an impact, but this requires further evaluation. Q: What is your opinion on the overuse of chlorine and its health impacts in our hospital cleaning personnel? A: On the one hand, we need chlorine, as it is one of the few active substances on spores, easily available and cheap. On the other hand, we can reduce the risk of respiratory and muco-cutaneous toxicity by always wearing appropriate protective equipment, using chlorine in the recommended concentration and only in the required situations. Viable alternative sporicidal agents to chlorine (such as peracetic acid and hydrogen peroxide-based chemistries) are now available, and should be considered. Strategic Questions for Companies: Q: For an experienced cleaning vendor wanting to enter into the healthcare cleaning sector, what advice would you give to the company? A: Get the best training in the field with infection control and hospital cleaning professionals. Q: Is there a guide for presenting a business case for improving cleaning practices to hospital administrators? A: There are a number of published papers that provide help and support with business case writing – the authors are happy to provide further information upon request. Q: Making certified cleaning professionals will cost more money. How to convince finance people from hospital to prioritize quality of cleaning instead of the budget? A: Professionals’ certification should be part of hiring conditions and over the long-term, not be associated with significant cost increases for the institution. Return on investment would be evident as soon as any adverse event linked to misuse of cleaning methods/techniques related to the absence of adequate training/certification would occur. Peters et al. Antimicrobial Resistance and Infection Control (2018) 7:132 Page 9 of 12 Table 4: Questions from the Healthcare Cleaning Forum 2018 (Continued) Q: Do you think the move towards biosurfactants and microorganisms in cleaning chemicals will affect the industry? A: Most probably not. The use of products respectful of the environment will, however, gain momentum. Strategic Questions for Hospitals/Institutions: Q: Can (and should) patients be educated so that they can assess the healthcare facility they are staying? A: Patients’ participation in IPC is advocated and could help institutions to take actions (see paper). Q: How can cleaning be validated without standard methods to measure cleanliness? A: There are different methods to assess cleanliness, but no universal standards. Further research is needed to propose and promote universal standards. Q: What is the best way to measure cleanliness in a hospital room, and is it in real-time? A: Visual inspection, fluorescent markers, and ATP measurements can be used in real-time; bacterial cultures of an area take more time and use more resources. Q: How do cleaning and disinfection affect the rates of urinary tract infections? A: To the best of the authors’ knowledge, there is yet no study that relates a possible relation between surface cleaning and urinary tract infection rates. Q: Soft surfaces like mattresses and stretchers are commonly damaged in healthcare; how important is surface integrity in infection prevention? A: It is virtually impossible to clean a damaged surface. Surface integrity must be preserved if a surface is to be cleaned. Q: What is the recommended practice to suppress Clostridium difficile spores from the hospital environment? A: Most experts recommend the use of a sporicidal disinfectant such as chlorine, chlorine-containing, or peroxygen-based substances to clean rooms or wards hosting patients colonized or infected with C. difficile and to control C. difficile in hospitals. Q: Do you have any good success stories or tips to help engage healthcare workers to work closely with cleaning service providers? A: Yes, there are documented success stories, but there is no universal model yet. Q: Should IPC teams train hospital cleaning personnel? A: IPC team members should be involved in hospital cleaning personnel training, together with the key collaborators/head of the hospital environmental cleaning department. Q: Would a fixed ratio of hospital cleaning personnel per hospital bed be a helpful key performance indicator? A: Yes it could be a very useful (structure-level) performance indicator; however, one would need further research and optimal adjustment to develop and propose such a model. Q: How could HPV and UV be implemented within mixed and open wards or in an ICU? A: Although possible, their application could be quite challenging in conditions with high occupancy bed and rapid turnover rates because areas treated using HPV or UV need to be vacated by patients and staff. Q: Is average patient length of stay aggregated on the basis of underlying morbidity a better measure of infection cost than solely monetary values? A: Yes, indeed. Most estimates of the monetary impact of infections are centered on increased lengths of stay. There are however many additional aspects to include in cost-effectiveness analyses. Q: What is the recommended time for cleaning single patient room, a 4 bed-room and a 6 bed-room? A: There is no standard time. Models need to be developed and validated. Q: What is your perspective of HPV and UV disinfection systems in improving bed turnaround time? A: Both HPV and UV will extend bed turnaround time (HPV more so than UV). But, under defined circumstances, both HPV and UV have been associated with reduced heathcare-associated infections. Therefore, there may be a net improvement in patient throughput. More evidence should however be generated before recommendations could be established at large. Q: How should the person responsible for the environmental services in a hospital be recognized/ should they earn more for becoming excellent at their job? A: Training, permanent position, job recognition, certification, and job progress are essential to maintain motivation, as in other professions. Q: Is there any data on the cost of bed disinfection per bed in any EU member country? A: The cost of cleaning/disinfection will vary widely based on the methods used and the local approach to delivering cleaning and disinfection. Broader Issues: Q: How do you educate people in the developing world about health care hygiene, where the level of literacy and awareness is so low? A: The level of literacy is not the most important parameter in maintaining the hospital environment clean; hospitals in low and middle resources countries can be maintained at a very high level. As mentioned above training, a permanent position, job recognition, certification, and job progress are essential to maintain motivation, as in other professions. Q: What is your key target for the next 12 months with regard to healthcare cleaning? A: See the proposed research agenda (Table 3). Not all points will be addressed over the next 12 months, but this is the direction in which we would like to develop the field. Peters et al. Antimicrobial Resistance and Infection Control (2018) 7:132 Page 10 of 12 Table 4: Questions from the Healthcare Cleaning Forum 2018 (Continued) Q: Would television ads be useful for increasing public awareness? A: This approach certainly deserves to be tested. Q: In the private sector, a person who is persistently non-compliant is disciplined. Why can’t this be done in healthcare settings? A: It has been done, but is certainly rare. Evidence suggests that a “sticks and carrots” approach to improving human behavior works best, with incentivizing the good more effective than penalizing the bad. Q: What are the top factors that lead to lower healthcare-associated infection rates in hospitals? A: Successful hand hygiene promotion is the top priority, and has been associated with significant risk reduction. Prevention of device-associated and surgical site infections are certainly key priorities together with appropriate use of antimicrobials. Hospital cleaning is part of key strategies to reduce the bio-burden from the environment associated with the risk of cross-transmission and spread of multi-resistant organisms, linked to almost all infections in healthcare. Q: Are we ready for new critical outbreaks like Ebola? A: Pandemic preparedness has improved, informed by outbreaks such as the Ebola outbreak in West Africa, as recently demonstrated in the handling of the recent outbreak in RDC. Handling such risks however merits constant attention and adaptation of both patient care and environmental control protocols. Q: Without any standardized and validated cleaning methods how can an infectious diseases specialist approve a cleaning contract? A: There is definitively a need for universal, standardized and validated cleaning protocols, as discussed in the paper. Q: Using ABHR instead of hand washing was a game changing strategy for hygiene. What is the game changer in surface cleaning in terms of chemical, process, materials, equipment, etc.? A: Developing a model for the implementation and culture change of environmental cleaning best practices could constitute the solution. Q: Is there a guide or reference on the scope of the work of healthcare workers and cleaning service providers? A: To the best of the current authors’ knowledge there is no such universal guide; further development is needed. Q: Should national healthcare system reimbursement schemes (such as the NHS) reward/promote prevention in hospital cleaning? A: This tool might be part of a solution; yet one must first develop universal recommendations before one could propose such a tool. Q: Do you think we can improve the human factor without investing more in training and monitoring hospital cleaning personnel? A: No, training and monitoring is key to improving behavior. Q: Can we automate the human factor improvements? A: Understanding human factors is vital to improving human behavior. Automation can help in some situations; it cannot replace optimal behavior. Q: What is your opinion on the report of the Dutch Health Council saying that there is a serious risk of bacteria getting resistant against disinfectants? A: There is no evidence that microbes become resistant to most disinfectants at clinically meaningful levels. However, considering that resistance to antiseptics, as well as to antibiotics, antiviral-, antifunfals, and antiparasitic agents do exist, careful attention should be recommended for specialized research laboratory so that emergence could be traced as soon as possible if it would appear. Q: When there is outbreak, it is often blamed on cleaning service providers not doing a good job. How can we change the perception of “teamwork” among all stakeholders? A: Outbreak investigation and control is a challenge. Cross-transmission risk can be controlled most frequently by multimodal, multi-disciplinary interventions involving all health staff at multiple levels. Environmental control is key and most frequently cleaning services providers and/or personnel are accused of not doing an appropriate job. Although it is most frequently not the case, outbreaks associated with the lack of appropriate environmental control have been clearly identified. Q: When will WHO guidelines be updated to adapt to new technologies? A: There are currently no WHO guidelines on environmental control including recent and new technologies; the authors have no information regarding the possible update of WHO guidelines. Q: Is it possible to get the presentations from today’s event? A: Each of the presentations are available on the website of the Healthcare Cleaning Forum by clicking on the individual speakers [33]. Hand Hygiene References Hand Hygiene: Numerous questions on hand hygiene came up during the forum. Because this paper is not on hand hygiene in particular, there are a number of references below that contain all of the pertinent information. [7, 34–38] Peters et al. Antimicrobial Resistance and Infection Control (2018) 7:132 Page 11 of 12 Abbreviations Author details ABHR: Alcohol-based handrub; HAI: Healthcare-associated infection; Infection Control Programme and WHO Collaborating Centre on Patient IPC: Infection prevention and control; WHO: World Health Organization Safety, University of Geneva Hospitals and Faculty of Medicine, 4 Rue Gabrielle-Perret-Gentil, 1211 Geneva, Switzerland. Imperial College London, London, UK. Infection Prevention and Control Service, St. Constantin Acknowledgements Hospital, Brasov, Romania. Nouvelle Aquitaine Healthcare-Associated The authors would like to thank Interclean, CAP Partners and colleagues and Infection Control Centre, Bordeaux University Hospital, Bordeaux, France. collaborators who made the Healthcare Cleaning Forum possible, especially Radboud Centre for Infections, Radboud UMC, and Department of Medical Marianne Kemmer, Sofie Struve Løgstrup, Henrik J. Nielsen, Paul Riemens, and Microbiology, Canisius-Wilhelmina Hospital, Nijmegen, The Netherlands. Rob den Hertog. They also wish to thank Markus Dettenkofer for his contribution. The authors would also like to address their special thanks to Received: 10 September 2018 Accepted: 11 October 2018 Nasim Lotfinejad from the Department of Research, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran, for her illustrations. Funding Principal funding by the Infection Control Programme & WHO Collaborating References Centre on Patient Safety (SPCI/WCC), University of Geneva Hospitals and Faculty 1. World Health Organization. WHO Guidelines on Hand Hygiene in Health of Medicine, Geneva, Switzerland; hand hygiene research activities at the SPCI/ Care. 2009. WCC are supported by the Swiss National Science Foundation 2. Vermeil T, et al. Hand hygiene in hospitals: anatomy of a revolution. J Hosp (32003B_163262). Infect. 2018. Andreas Voss has received grants by the Framework Programme of the 3. Grayson ML, et al. Effects of the Australian National Hand Hygiene Initiative European Commission, Interreg, ZonMW, and VWS. In addition he received after 8 years on infection control practices, health-care worker education, funding or speakers fees by Ophardt, Deb, Ecolab, Momentum Bioscience, and clinical outcomes: a longitudinal study. Lancet Infect Dis. 2018;0. Brill & Partner, Gama, bioMerieux, UVDI, and 3M. 4. Mitchell BG, Dancer SJ, Anderson M, Dehn E. Risk of organism acquisition Didier Pittet has received funding by the European Commission and the from prior room occupants: a systematic review and meta-analysis. J Hosp Swiss National Science Foundation for several research and clinical studies; Infect. 2015;91:211–7. he also works with the WHO in the context of the WHO initiative Private 5. Pittet D, et al. Effectiveness of a hospital-wide programme to improve Organizations for Patient Safety (POPS) Hand Hygiene. The aim of this WHO compliance with hand hygiene. Infection Control Programme. Lancet Lond initiative is to harness industry strengths to align and improve implementation Engl. 2000;356:1307–12. of WHO recommendations for hand hygiene in healthcare in different parts of 6. Pittet D, Donaldson L. Clean care is safer care: a worldwide priority. Lancet the world, including in least developed countries. In this instance companies/ Lond Engl. 2005;366:1246–7. industry with a focus on hand hygiene and infection control related advancement 7. Otter J. The inaugural healthcare cleaning forum. Reflect Infect Prevent have the specific aims of improving access to affordable hand hygiene products as Contr. 2018. well as supporting education and research. 8. Pittet D, et al. Evidence-based model for hand transmission during patient The 2018 Healthcare Cleaning Forum was logistically supported by Interclean care and the role of improved practices. Lancet Infect Dis. 2006;6:641–52. and benefitted from the coordination efforts of CAP Partners. 9. Kilpatrick C, Storr J, Allegranzi B. ‘A Worldwide WHO Hand Hygiene in Healthcare Campaign’ Ch. 38 in Hand Hygiene: A Handbook for Medical Availability of data and materials Professionals. Hoboken: Wiley-Blackwell; 2017. pp. 275–284. Data sharing not applicable to this article as no datasets were generated or 10. Dancer SJ. Controlling hospital-acquired infection: focus on the role of the analyzed during the current study. environment and new Technologies for Decontamination. Clin Microbiol Rev. 2014;27:665–90. Authors’ contributions 11. Weber DJ, Rutala WA, Miller MB, Huslage K, Sickbert-Bennett E. Role of All authors read and approved the final manuscript. AP drafted the hospital surfaces in the transmission of emerging health care-associated manuscript, all authors edited and approved it. Content was generated from pathogens: norovirus, Clostridium difficile, and Acinetobacter species. Am J the all authors. All authors except for AP spoke at the conference. Infect Control. 2010;38:S25–33. 12. Otter JA, Yezli S, Salkeld JAG, French GL. Evidence that contaminated surfaces contribute to the transmission of hospital pathogens and an Ethics approval and consent to participate overview of strategies to address contaminated surfaces in hospital settings. Please see signed author forms, ethical approval was not needed for this paper. Am J Infect Control. 2013;41:S6–S11. 13. Albrecht, P. HUG Entretien environment du patient. 2018. Consent for publication 14. Parneix, P. Cleaning as a patient safety initiative. 2018. Not applicable 15. Quintana JM, et al. Predictors of patient satisfaction with hospital health care. BMC Health Serv Res. 2006;6:102. Competing interests 16. Schoenfelder T, Klewer J, Kugler J. Determinants of patient satisfaction: a Alexandra Peters and Didier Pittet have no conflicts of interest to study among 39 hospitals in an in-patient setting in Germany. Int J Qual declare and have received funding from the Swiss National Science Health Care. 2011;23:503–9. Foundation for research. 17. Mitchell BG, et al. Changes in knowledge and attitudes of hospital Andreea Moldovan: has no conflicts of interest to declare and has received environmental services staff: the researching effective approaches to funding from St. Constantin Hospital, Brasov, Romania. cleaning in hospitals (REACH) study. Am J Infect Control. 2018;46(9): Jon Otter has, in the last 3 years, received Academic fees from CAP Partner, 980–5. Centre for Clinical Infection and Diagnostics Research, Elsevier, and IDSA; 18. Voss, A. Cleaning in healthcare: the new concept. 2018. consulting fees from Aquarius, Arthur D Little, Fields Consulting, Gama 19. Strassle P, et al. The effect of terminal cleaning on environmental Healthcare Ltd., GK Intelligence Limited, Pfizer Ltd.; and speaker fees from contamination rates of multidrug-resistant Acinetobacter baumannii. Am J 3M, Hospital Da Luz, Portugal, Odense University Hospital (Denmark), Pall Infect Control. 2012;40:1005–7. Medical Ltd., Serosep Ltd., Society for Applied Microbiology, Virox, and 20. Havill NL, Moore BA, Boyce JM. Comparison of the microbiological efficacy Webber Training. of hydrogen peroxide vapor and ultraviolet light processes for room Pierre Parneix French Ministry of Health through the Regional Health Agency decontamination. Infect Control Hosp Epidemiol. 2012;33:507–12. of Nouvelle Aquitaine. 21. Mann EE, et al. Surface micropattern limits bacterial contamination. Antimicrob Resist Infect Control. 2014;3:28. Publisher’sNote 22. Hall L, et al. Researching effective approaches to cleaning in hospitals: Springer Nature remains neutral with regard to jurisdictional claims in published protocol of the REACH study, a multi-site stepped-wedge randomised trial. maps and institutional affiliations. Implement Sci. 2016;11:44. Peters et al. Antimicrobial Resistance and Infection Control (2018) 7:132 Page 12 of 12 23. M Abbas et al. Conflicts of interest in infection prevention and control research: no smoke without fire. A narrative review. Intensive Care Med Press; 2108. 24. Pittet D, Sax H, Hugonnet S, Harbarth S. Cost implications of successful hand hygiene promotion. Infect Control Hosp Epidemiol. 2004;25:264–6. 25. Graves N. The economic impact of improved hand hygiene. In: Hand Hygiene: Wiley-Blackwell; 2017. p. 285–93. https://doi.org/10.1002/ 9781118846810.ch39. 26. Craig, D, et al. Economic evaluations of interventions to prevent healthcare- associated infections literature review. 2017. 27. The Review on Antimicrobial Resistance Chaired by Jim O’Neill. Tackling Drug Resistant Infections Globally: Final Report and Recommendations. 2016. 28. Otter JA, et al. Counting the cost of an outbreak of carbapenemase- producing Enterobacteriaceae: an economic evaluation from a hospital perspective. Clin Microbiol Infect. 2017;23:188–96. 29. Disinfection and Decontamination: Principles, Applications and Related Issues Edited by Gurusamy Manivannan Boca Raton, FL: CRC Press, 2007. 512 pp., Illustrated. 30. Detergent | Definition of detergent in English by Oxford Dictionaries. Available at: https://en.oxforddictionaries.com/definition/detergent. Accessed 16 Aug 2018. 31. Disinfectant | definition of disinfectant by Medical dictionary. Available at: https://medical-dictionary.thefreedictionary.com/disinfectant. Accessed 16 Aug 2018. 32. Disinfectant | Definition of Disinfectant by Merriam-Webster. Available at: https://www.merriam-webster.com/dictionary/disinfectant. Accessed: 16 Aug 2018. 33. Fumigate | Definition of Fumigate by Merriam-Webster. Available at: https://www.merriam-webster.com/dictionary/fumigate. Accessed 16 Aug 2018. 34. Healthcare forum. Available at: https://www.intercleanshow.com/en/ amsterdam/healthcare-cleaning-forum. Accessed 26 June 2018. 35. WHO. WHO guidelines on hand hygiene in health care. WHO. Available at: http://www.who.int/gpsc/5may/tools/9789241597906/en/.Accessed 26 June 2018. 36. Allegranzi B, et al. Burden of endemic health-care-associated infection in developing countries: systematic review and meta-analysis. Lancet Lond Engl. 2011;377:228–41. 37. Allegranzi B, et al. Global implementation of WHO’s multimodal strategy for improvement of hand hygiene: a quasi-experimental study. Lancet Infect Dis. 2013;13:843–51. 38. Pittet D. Hand hygiene: It’s all about when and how. Infect Control Hosp Epidemiol. 2008;29:957–9.
Antimicrobial Resistance and Infection Control – Springer Journals
Published: Nov 8, 2018
Keywords: Infection prevention; Cleaning; Disinfection; Environment; Healthcare-associated infection; Public health; Environmental hygiene; Hand hygiene; Infection control; Antimicrobial resistance
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