Introduction

Revolutions are often started by ideas whose time have come. Compared to other domains in medicine, revolutions in the field of Infection Prevention and Control (IPC) are generally few and far between. The last one was probably the global shift to using alcohol-based handrub (ABHR) instead of washing hands with soap and water, about 25 years ago- a seemingly small change in practice that continues to save millions of lives [1–3]. Today, looking at the IPC landscape, the one area that has been consistently undervalued and understudied is the role of the hospital 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 enough evidence to demonstrate that cleaning hospitals helps prevent infections. Still, good intervention 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 services departments, this creates lasting issues in regards to patient and healthcare worker safety.

The situation is not helped by the lack of literature concerning the exact impact that a soiled or contaminated environment has on healthcare-associated infections (HAI). In order to begin the initiative to change how hospitals think about their environment, a group of infection control experts teamed up with Interclean, the largest cleaning trade-show in the world, to create the Healthcare Cleaning Forum: a nexus where hospital managers, industry, and healthcare and cleaning experts could meet productively. For the first time, Interclean dedicated an entire hall to cleaning in healthcare, and hosted a conference featuring leaders in healthcare environmental science from across Europe. The speakers summarized the state of the art knowledge in the field, challenged the current dogma and began to shape a research agenda for developing the field of hospital hygiene and environmental control. This article outlines the major issues and points brought up during the conference. It attempts to illustrate the large gap that exists between environmental hygiene and the healthcare industry, as well as bring some much-deserved attention to a concept whose time has come.

Cleaning as a patient safety initiative

We need to change how we think about the hospital environment- if the risks of transmission are known, no one wants to be the next patient in a contaminated room [4]. When the world changed how they thought about hand hygiene 25 years ago [2, 5, 6], it realized how important hands were as the main vectors for spreading diseases from one patient to another in hospital settings. It is estimated that over 50–70% of all HAI are spread through contaminated hands. It is time to focus on the other 30–50%, a part of which might be linked to environmental transmission (Fig. 1). After all, “hands are really just another highly mobile surface in healthcare that are commonly contaminated and rarely disinfected” [7]. Since there is a dynamic interchange between contamination on surfaces and hands [8], some of the transfer in which contaminated hands are the final link include contaminated surfaces as links earlier in the chain of transmission. Ideally, hospital environmental hygiene should follow the World Health Organization (WHO) model of “Clean Care is Safer Care” established for hand hygiene in 2005 [6], which spearheads good practices in more than 180 countries today [1, 9]. There is a need for creating evidence-based guidelines for hospital cleaning, and for using those guidelines to develop the right tools for education and implementation.

Fig. 1
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“No one wants to stay in a contaminated room”

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Although high-quality interventional studies are limited, there are enough to show that cleaning and disinfecting hospitals in order to prevent infection works. Analysis of numerous studies shows a clear correlation between “cleaning hygiene failures” and the number of intensive care unit-acquired infections (Fig. 2). Several studies showed that patients were much more likely to contract certain pathogens if the patient in the room before them was colonized or infected with a pathogen linked to HAI (Fig. 3) [4, 10–12]. There is a wealth of information on what products or chemicals eliminate which pathogens and how to apply them. This includes efficacy and toxicity studies as well as a few clinical studies assessing the effect of specific interventions to control outbreaks [10]. More research is needed to measure the effects that cleaning methods have on HAI. Since improved environmental cleaning and decontamination measures are always bundled with other interventions during outbreaks, it is difficult to measure their precise impact.

Fig. 2
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Relationship between environmental bioburden and hospital-acquired infection [10]

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Fig. 3
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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

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Cleaning in healthcare

Hospital environmental hygiene is complex because it is dependent on the pathogen present and the product used to remove it. There are five main variables to cleaning, whether removing soil or disinfecting and cleaning on a microbiological level (Table 1; the acronym “WASTE” can be used to recall the 5 variables). These elements are: what product or intervention is applied, the technique and equipment used to apply the product, the type of surface, the level of contamination of the environment, and last but not least, the environmental hygiene personnel doing the cleaning [13]. If any one of these elements is lacking, the cleaning will by definition be suboptimal. Because of this, changing cleaning practices in hospitals must be implemented 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 personnel are useless if the product they are using is not effective against the particular pathogen that needs to be removed or killed.

Table 1 Environmental hygiene: How to get there – WASTEa
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But what is “clean”? (Table 2) Maintaining a hygienic hospital environment is not only about removing soil, but also about organizing an environment that is optimal for patient safety. Obviously if an area is visibly dirty, one cannot disinfect it. Visibly soiled surfaces must first be cleaned, and then, when or if appropriate, disinfected. Failure to do so means that the infective organisms cannot be targeted effectively [10]. The 2018 survey from the European network to promote infection prevention for patient safety (EUNETIPS) aimed to analyze how different hospitals evaluated and have created their cleaning strategies [14]. Cleanliness of a hospital also plays a large role in patient perception of the healthcare setting, and consequently of patient satisfaction [15, 16]. Patients are instrumental in convincing administrators to invest in cleaning, and must be sensitized to the issues in order to be allies for creating change.

Table 2 Glossary of terms
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Available products

In addition to a vast array of detergents and cleaning/disinfecting equipment, common chemicals used for disinfection include: alcohol, chlorine and chlorine compounds, formaldehyde, glutaraldehyde, hydrogen peroxide, iodophors, ortho-phthalaldehyde, peracetic acid, phenolics, and quaternary ammonium compounds [17]. This paper will not go into any detail on these products as such a discussion would be too extensive and was not the purpose of the Healthcare Cleaning Forum 2018.

An ideal product would be effective against all bacteria, spores, viruses, and prions while having no impact on the environment and being completely safe as well as easy to use. Currently no such product exists; thus choosing any product will result in some level of tradeoff.

For example, hydrogen peroxide vapor does not leave any residues in the environment, but is expensive, can be corrosive, and is difficult to use compared with liquid disinfectants. Chlorine solutions are effective against spores, but have a strong odor, leave residues, and may damage certain environmental surfaces. UV light leaves no residue but cannot disinfect areas that it cannot shine on directly. This is the case for every single product available today; most only work against certain types of pathogens, and others are toxic or degrade certain materials in the patient environment.

The human component

But cleaning is not only dependent on the chemicals used. The ideal environmental hygiene personnel (Table 2) would remain thorough and meticulous, and always use the right technique, product and materials. Cleaning and disinfecting a hospital is a repetitive task that can quickly become mundane. Environmental hygiene personnel are often not trained sufficiently, and do not feel that they have the agency to make a difference in patient safety. Additionally, the amount of work that they are expected to do is not always in accordance with the time assigned to the task. Within the hospital hierarchy, environmental hygiene personnel are on one of the lowest rungs, and often credit is not given to them, especially considering the importance of their work. There is a major problem with how “cleaners” are often perceived as menial and uneducated by the rest of the hospital staff. In many countries, particularly in high-resources settings, cleaning personnel frequently originate from outside of the country, and do not express themselves in the local language, thus making discussions and interactive exchanges with other categories of health professionals difficult or even impossible.

Additionally, few hospitals have sufficient systems in place to train and certify their cleaning staff. Without certification, advancement is unstructured and can be limited since there is no way to gauge the quality of a staff as a whole. Often there is a high turnover rate among personnel within the cleaning service or a language barrier between the cleaners and the rest of the staff. Cleaning personnel must be trained to understand why their work is important to the hospital, and need to be recognized and certified in order to improve motivation and compliance [18].

Logistics of hospital cleaning

The place of the environmental hygiene services department (Table 2) within a hospital is important, especially with regard to how they work together with the IPC service. Nursing assistants are generally responsible for cleaning one part of the patient environment and the environmental hygiene personnel for another; but often, respective tasks are not clearly defined. For example, if who needs to clean the bedside table is not explicitly stated, then there is a good chance that that table may not be cleaned by anyone. In one survey, one third of environmental hygiene personnel admitted that they were not really clear about what they were responsible for [19]. Absences or shortage of staff on wards, and/or the transfer of responsibilities between colleagues could complicate an already unclear situation and result in crucial maintenance not being performed. This can result in the spreading of disorder: a few minor mistakes, or disregard for a few of the rules, eventually cause increased disregard for rules in general among the whole staff [19].

In addition to the aforementioned issues, environmental hygiene services are often outsourced to external companies. While probably not as much of an issue in a stairwell or an office, it is virtually impossible for a hospital to optimize the cleaning staff and its quality if they have little to no oversight of or influence on the environmental hygiene. Outsourcing is not necessarily bad, but the right conditions must be observed, and crucial areas need to be cleaned by trained and certified professionals, even if costs are bit higher initially.

Education, training and communication

So how can we effectively educate and train hospital personnel for modern environmental hygiene maintenance? While the science of cleaning and disinfecting agents and equipment has evolved immensely in the last few decades, the education of cleaning personnel and their integration into healthcare worker teams has not. Cleaning and disinfecting hospitals is very different from cleaning public spaces such as hotels or offices; hospitals must realize this and adapt to the challenges. There is a range of environments within each hospital, from offices to intensive care units or hospital pharmacy services, some of which require specialized approaches to environmental hygiene maintenance. There are even different requirements for different sectors within the same department. The pathogens present in hospitals can be quite different from those present in the community, and the patient population is more vulnerable. Each type of pathogen has its own specific transmission pattern, host affinity, and microbiological characteristics.

Leaders and trainers must be seen as legitimate by staff, and need to ensure their understanding and motivation. Only if there is a high process understanding in training can quality become routine; an informed person tends to be more compliant, and a compliant person is more motivated. Motivated teams are more efficient and more aware, and individuals need to understand that everyone’s work is important. Personal responsibility and team cohesion require solid collaboration, which in turn requires the equality and realization of rights and duties. Repetition, feedback and team-building help optimize performance in environments that inherently foster human error. Analyzing hospital architecture, workflow, and ergonomics can go a long way to reducing it. It is important to realize that the best product, equipment or intervention is worthless without well-trained, responsible and compliant staff.

Possibilities of automation and self-disinfecting surfaces

Automation can be useful, but currently does not replace the need for thorough manual cleaning. Although manual cleaning and disinfection can be qualitatively as good as machine automated disinfection (or even better in some instances), one has less oversight over humans, and they do not clean at their best all of the time. Environmental hygiene service managers can use a variety of tools including visual inspection, cultures, ATP meters or UV light reactive fluorescent markers to verify how well a given area has been cleaned and disinfected. Though even the best-trained people are prone to error, machines never skip any steps. Automated or semi-automated room disinfection is not to replace personnel, but to raise the bar on the standard of disinfection and, in some instances, prevent work-related musculoskeletal constraints among environmental hygiene personnel. At some point, solely manual approaches are doomed to fail, as hospital environments are intricate and difficult to maintain in an appropriately clean state. In one study, up to 50% of an environment remained uncleaned after manual cleaning. Another study showed that after four rounds of manual cleaning and disinfection with a bleach solution, 25% of rooms were still contaminated with Acinetobacter baumanii [20]. Automated room disinfection with hydrogen peroxide vapor or ultraviolet light have shown promising results in targeting specific microorganisms, although they only work once a room has already been manually cleaned to remove soil [21].

Beyond machines, there is an important need for more research into surfaces that inherently inhibit bacterial contamination or that have self-disinfecting properties. A few that have been studied are the micro-patterning of surfaces or the inclusion of copper in them in order to reduce contamination [11]. The idea of having something permanently in the patient environment that is always working is an attractive one (although perhaps expensive): if one can control the level of contamination at the source, then there is less to remove and less risk for sub-optimal cleaning and disinfection. Further research, including unbiased, high-quality clinical efficacy and effectiveness studies are however still needed before further recommendations can be made regarding these materials [22, 23].

Cost vs. value of hospital cleaning and disinfection

It is imperative to develop a new and efficient model for hospital environmental hygiene maintenance. The return on investment for successful hand hygiene promotion has been shown to up to 23 times the initial amount invested [24–26]. In order to have similar figures for hospital environmental hygiene, we need to first understand what the cost of maintaining a clean hospital environment is, and what its value is. Although many hospitals are quick to spend money on new software, specialized staff and fancy equipment, they often look at maintaining the environment hygiene as an opportunity to save in the budget.

Hospitals often try to cut environmental hygiene maintenance costs as much as possible, both in the products that they use, and in the training and continued education of their workforce. The essential shift in approach needs to happen in how hospitals assess this cost and value. Because the costs of not cleaning can affect numerous budgets within a hospital, it is difficult to accurately account for them. Hospitals need to look beyond actual expenditures to averted expenditures, such as increase in patient-days due to HAI, as well as opportunity costs such as hospital staff time or missed surgical revenue due to increased turnaround time in an operating theater. There are also increases in costs associated with antimicrobial resistance in HAI, which has a cost estimated at over €85 trillion ($100 trillion) globally by 2050 [27]. For example, one relatively small outbreak with approximately 40 cases cost a hospital over €1 million [28]. Prevention is always better and less expensive than a cure, especially when we are running out of antibiotics. So when making a decision about which environmental hygiene maintenance systems to buy, which products to use, or how much to invest in training the cleaning personnel, hospitals would do well to look at the costs of not doing so, or deciding on a cheaper solution. In order to save money in the long-term and improve patient satisfaction, hospitals need to invest in quality across the board whether in materials, disinfectants, technological innovation, or the training, education, and certification of their workforce (Fig. 4).

Fig. 4
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Hospitals should value environmental hygiene cleaning and maintenance

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A time for cooperation

It is imperative to develop public-private partnerships in the field of clean hospitals. Industry and academia both have a role to play in raising standards and providing hospitals with the best possible products and methods. First, currently marketed sub-standards products and methods should be suppressed. Ultimately, the difference will no longer be between good and bad products on the market, but within implementation and training of those products and technologies.

Cleaning and environmental maintenance is a science. Initially, assessing the approach for the hygiene of a toilet seat seems almost redundant. However, many of the questions around this seemingly simple activity require study and scientific assessment. One must decide material to use to clean the toilet seat (e.g. microfiber or cotton cloth), which liquid agent to use (e.g. a detergent or a disinfectant and, if a disinfectant, which one), and the ideal frequency of the cleaning and disinfection (e.g. daily, after each use, or both). Many questions remain unanswered; some are addressed in the Appendix (see Appendix). Hospitals must get out of the vicious circle of cutting costs and instead assess value. They must realize that being a hospital “cleaner” is not a job but a profession, and invest in their workforce. Academics must encourage further studies (see research agenda, Table 3) as well as weave together the data available in order to present hospitals with a convincing business case of why to invest in hospital cleaning.

Table 3 Hospital cleaning: overall research agenda
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Because clean hospitals is an idea whose time is now.

Comment

The authors alone are responsible for the views expressed in this article and they do not necessarily represent the views, decisions or policies of the institutions with which they are affiliated.