I’ve been asked to write a chapter on the role of the environment in transmission in an Springer book (on the potential role for antimicrobial surfaces in healthcare). So, I’ve been busy updating my 2011 ICHE literature review on a similar topic, drawing on an excellent recent AJIC review by Dr Donskey.
There are some epidemiological associations that suggest an important role for contaminated surfaces in transmission. Most compelling are the studies showing that admission to a room previously occupied by a patient with certain environmentally-associated pathogens increases the risk of acquisition for incoming patients, presumably due to residual contamination. However, in order to really nail a scientific association, an intervention is required. Hence, the environmental intervention studies provide the highest quality evidence evaluating the role of the environment in transmission (see the Table below).
These studies have shown that switching to more effective agents, improving the cleaning / disinfection process or turning to automated “no-touch” room disinfection systems (NTD) can reduce transmission in endemic settings. It’s important to note that some studies report an ineffective environmental intervention. These are important to publish to avoid publication bias. Looking under the bonnet of these studies usually offers an explanation as to why they did not show a significant reduction in transmission. For example:
- Wilcox 2003. There was virtually no impact on the frequency of C. difficile environmental contamination on the wards using bleach, so it’s surprising that they saw any reduction in CDI!
- Valiquette 2007. The bundle of interventions, some of which were environmental, was only given a few months to be effective.
- Wilson 2011. This one is more difficult to explain. Perhaps it was underpowered to detect a clinical impact in the declining prevalence of MRSA in the UK?
- Dharan 1999. The intervention was focused mainly on improving the cleaning and disinfection floors, which are not exactly a high-touch, high-risk sites.
Believe it or not, I still occasionally meet people who tell me that contaminated surfaces do not contribute to transmission. That rather dated viewpoint is becoming increasingly untenable as the volume and quality of data evaluating the role of the environment in transmission continues to increase. For me, the question has now moved on to how much contaminated surfaces contribute to transmission, and how best to address contamination of the hospital environment.
Table. Intervention studies evaluating the role of contaminated surfaces in the endemic transmission of nosocomial pathogens.
| Reference | Setting, location | Organism | Study design | Key findings |
| Mayfield 2000 1 | Three units, USA | C. difficile | 18-month before-after study of a switch from QAC to bleach disinfection. | Significant reduction in CDI incidence on the highest risk unit from 8.6 to 3.3 cases per 1000 patient-days. |
| Wilcox 2003 2 | Two units, UK | C. difficile | 2-year ward cross-over study of a switch from detergent to bleach disinfection. | Significant reduction in CDI incidence on one of the units (from 8.9 to 5.3 cases per 100 admissions), but not on the other. |
| McMullen 2007 3 | MICU and SICU, USA | C. difficile | 2-month before-after evaluation of bleach disinfection of CDI rooms on SICU and 4-month evaluation of bleach disinfection of all rooms on MICU in a hyper-endemic setting. | Significant reduction in CDI incidence on both units (10.4 to 3.9 cases per 1000 patient days on SICU; 16.6 to 3.7 cases per 1000 patient days on MICU). |
| Valiquette 2007 4 | Hospital-wide, Canada | C. difficile | 5-month evaluation of enhanced infection control and disinfection, including a switch to bleach, and a subsequent switch to ‘accelerated’ hydrogen peroxide. | Neither environment intervention made a significant impact on the incidence of CDI; a reduction in the use of high-risk antibiotics significantly reduced the incidence of CDI. |
| Boyce 2008 5 | Hospital-wide, USA | C. difficile | 20-month before-after study on the use of HPV disinfection for terminal disinfection of CDI rooms. | Significant reduction in CDI incidence on five high incidence units (from 2.3 to 1.3 cases per 1000 patient-days). Lesser reduction in CDI incidence hospital wide. |
| Hacek 2010 6 | Three hospitals, USA | C. difficile | 3-year before-after study on switching from QAC to bleach for terminal disinfection of CDI rooms. | Significant reduction in the incidence of CDI (from 0.85 to 0.45 per 1000 patient days). |
| Orenstein 2011 7 | Two medical units, USA | C. difficile | 2-year before-after study on switching to bleach wipes for daily and terminal disinfection of all rooms. | Significant reduction in the incidence of CDI (from 24.2 to 3.6 per 1000 patient days). |
| Manian 2013 8 | Hospital-wide, USA | C. difficile | 3-year before-after study on enhanced terminal disinfection of CDI rooms using HPV and bleach. | Significant reduction in the incidence of CDI (from 0.88 to 0.55 cases per 1000 patient days). |
| Hayden 2006 9 | ICU, USA | VRE | 9-month before-after study on educational improvement of cleaning and hand hygiene. | The frequency of environmental contamination and patient acquisition of VRE were reduced from 33 to 17 acquisitions per 1000 patient-days during the improved cleaning phase. |
| Datta 2011 10 | ICU, USA | VRE / MRSA | 3-year before-after study of an intervention (fluorescent markers, “bucket method” and education) to enhance daily and terminal cleaning. | Significant reduction of MRSA (3.0% to 1.5% of admissions) and VRE (3.0% to 2.2% of admissions) acquisitions; intervention significantly reduced the increased risk from the prior occupant for MRSA but not VRE. |
| Perugini 2011 11 | Hospital-wide, Brazil | VRE | 4-year before-after study of an educational and observational intervention for cleaners. | Significant reduction in VRE infection (from 7.7 to 1.9 per 1000 patient days) and environmental contamination. |
| Grabsch 2012 12 | Hospital-wide, Australia | VRE | 18-month before-after study of a multimodal intervention (switch to bleach, improved monitoring of cleaners, modification of VRE contact isolation, periodic ‘super-clean-disinfection’ of high-risk wards). | Significant reduction of VRE colonization (from 10.7% to 8.0% of patients) and VRE environmental contamination. |
| Passaretti 2013 13 | ICU, USA | VRE / all MDROs | 30-month cohort study on the impact of HPV decontamination. | Patient admitted to rooms disinfected using HPV significantly less likely to acquire an MDRO (15.7 to 6.2 per 1000 patient days) and VRE (11.6 to 2.4 per 1000 patient days). |
| Mahamat 2007 14 | Hospital-wide, UK | MRSA | 8-year interrupted time series analysis of multiple infection control interventions. | Introduction of bleach disinfection, environmental sampling, alcohol gels and admission screening all reduced the prevalence of MRSA. |
| Dancer 2009 15 | Two wards, UK | MRSA | 12-month cross over-study on the impact of one extra cleaner. | Enhanced cleaning was associated with significant reductions surface contamination, hygiene fails and MRSA acquisition. |
| Wilson 2011 16 | ICU, UK | MRSA | 12-month randomized crossover study on the impact of additional twice daily cleaning of hand contact surfaces. | Significant reduction in the detection of MRSA on surfaces and hands, but no significant change in MRSA acquisition was detected. |
| Dharan 1999 17 | 5 medical wards, Switzerland | – | 4-month controlled study where 3-wards received an intervention (including an active oxygen based compound) and 2 wards continued current practice. | Intervention associated with reduced contamination but not reduced nosocomial infection or MRSA infection / colonization. |
HPV = hydrogen peroxide vapour.
References
1. Mayfield JL, Leet T, Miller J, Mundy LM. Environmental control to reduce transmission of Clostridium difficile. Clin Infect Dis 2000; 31: 995-1000.
2. Wilcox MH, Fawley WN, Wigglesworth N, Parnell P, Verity P, Freeman J. Comparison of the effect of detergent versus hypochlorite cleaning on environmental contamination and incidence of Clostridium difficile infection. J Hosp Infect 2003; 54: 109-114.
3. McMullen KM, Zack J, Coopersmith CM, Kollef M, Dubberke E, Warren DK. Use of hypochlorite solution to decrease rates of Clostridium difficile-associated diarrhea. Infect Control Hospital Epidemiol 2007; 28: 205-207.
4. Valiquette L, Cossette B, Garant MP, Diab H, Pepin J. Impact of a reduction in the use of high-risk antibiotics on the course of an epidemic of Clostridium difficile-associated disease caused by the hypervirulent NAP1/027 strain. Clin Infect Dis 2007; 45 Suppl 2: S112-121.
5. Boyce JM, Havill NL, Otter JA et al. Impact of hydrogen peroxide vapor room decontamination on Clostridium difficile environmental contamination and transmission in a healthcare setting. Infect Control Hosp Epidemiol 2008; 29: 723-729.
6. Hacek DM, Ogle AM, Fisher A, Robicsek A, Peterson LR. Significant impact of terminal room cleaning with bleach on reducing nosocomial Clostridium difficile. Am J Infect Control 2010; 38: 350-353.
7. Orenstein R, Aronhalt KC, McManus JE, Jr., Fedraw LA. A targeted strategy to wipe out Clostridium difficile. Infect Control Hosp Epidemiol 2011; 32: 1137-1139.
8. Manian FA, Griesnauer S, Bryant A. Implementation of hospital-wide enhanced terminal cleaning of targeted patient rooms and its impact on endemic Clostridium difficile infection rates. Am J Infect Control 2013; 41: 537-541.
9. Hayden MK, Bonten MJ, Blom DW, Lyle EA, van de Vijver DA, Weinstein RA. Reduction in acquisition of vancomycin-resistant enterococcus after enforcement of routine environmental cleaning measures. Clin Infect Dis 2006; 42: 1552-1560.
10. Datta R, Platt R, Yokoe DS, Huang SS. Environmental cleaning intervention and risk of acquiring multidrug-resistant organisms from prior room occupants. Arch Intern Med 2011; 171: 491-494.
11. Perugini MR, Nomi SM, Lopes GK et al. Impact of the reduction of environmental and equipment contamination on vancomycin-resistant enterococcus rates. Infection 2011; 39: 587-593.
12. Grabsch EA, Mahony AA, Cameron DR et al. Significant reduction in vancomycin-resistant enterococcus colonization and bacteraemia after introduction of a bleach-based cleaning-disinfection programme. J Hosp Infect 2012; 82: 234-242.
13. Passaretti CL, Otter JA, Reich NG et al. An evaluation of environmental decontamination with hydrogen peroxide vapor for reducing the risk of patient acquisition of multidrug-resistant organisms. Clin Infect Dis 2013; 56: 27-35.
14. Mahamat A, MacKenzie FM, Brooker K, Monnet DL, Daures JP, Gould IM. Impact of infection control interventions and antibiotic use on hospital MRSA: a multivariate interrupted time-series analysis. Int J Antimicrob Agents 2007; 30: 169-176.
15. Dancer SJ, White LF, Lamb J, Girvan EK, Robertson C. Measuring the effect of enhanced cleaning in a UK hospital: a prospective cross-over study. BMC Med 2009; 7: 28.
16. Wilson AP, Smyth D, Moore G et al. The impact of enhanced cleaning within the intensive care unit on contamination of the near-patient environment with hospital pathogens: a randomized crossover study in critical care units in two hospitals. Crit Care Med 2011; 39: 651-658.
17. Dharan S, Mourouga P, Copin P, Bessmer G, Tschanz B, Pittet D. Routine disinfection of patients’ environmental surfaces. Myth or reality? J Hosp Infect 1999; 42: 113-117.
Reflections on Infection Prevention and Control 
The environment, in my opinion, is unfortunately still being under-appreciated as a reservoir for multiple HAIs and community transmission of many Abx resistant organisms. This is nice update and current review of the complex nature of trying to wrap your arms around the many varied attempts to do that via the literature.
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Great article Jon. It would be interesting to take this research one step further. What kind of surfaces are being used throughout the hospital? What types of surfaces harbor more bacteria than others? Can they be cleaned effectively with the products that need to be used for disinfection in the healthcare environment? It is critical to test these surfaces in a healthcare setting and more interesting if it was a blind study.
Porous, textured surfaces and seams create additional issues, yet these surfaces are a standard in high touch patient care areas. A quick review of the web for care and maintenance information would reveal that many of the surfaces are not able to be cleaned with bleach or harsh chemicals yet soap and water will not be effective against C.Diff, VRE, MRSA and other bacteria.
Questions such as; what should be used to clean this surface? are rarely if ever asked. When surfaces with antimicrobial properties are evaluated, important questions include; How do we activate the antimicrobial properties and what can inhibit them from being effective? Many would be surprised to find that some of them need water to be activated, or they need to be scrubbed. Some are completely ineffective when they are coated with anything, including oil from your hands. It is important to remember that some disinfectants must be applied to the surface and a dwell time is required to be effective.
Laminate, textured plastic, brushed or smooth stainless steel, wood, granite, yes, I have seen a granite nursing station. Can these surfaces actually be cleaned effectively? It is very clear surfaces contribute significantly to the spread of infection. Now let’s look at what surfaces should be used where based on where or not they can actually be cleaned as well as specific surface characteristics.
In 2006 the FGI Guidelines recommended for the first time ideal surface characteristics. That has expanded with the 2010 edition and continues to be refined in the 2014 edition.
Surfaces do contribute to the spread of infection now let’s look at what surface choices we are making and we might find one more way to minimize the spread of HAI’s.
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Thanks Linda, you make some really useful and challenging points.
I think if you were to start from scratch and design a hospital based on our current understand of the importance of the inanimate environment it would look quite different. It would have lots of surfaces that are easy to clean, no seams, may have some copper surfaces, and each room would have a big red button marked “decontaminate” for when the patient is discharged. And there would be no granite nursing stations! The UK government funded a program called “Design Bugs Out”, which has yielded some interesting new products along these lines.
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At last I think there is consensus that high frequency touch surfaces, alongside hands, cleaning utensils etc, are a “critical control point” for preventing infection transmission in any inhabited environment. What we now need to do is adopt a more scientific approach to designing and standardising hygiene interventions (not just products) which are sufficient to break the chain or transmission. The object is to reduce contamination on the surface by a standardised amount either by removal or by inactivation or a combination of both – all of these have equal potential to do this job. At the moment we focus on what is the performance of disinfectant product, but rarely look at the total “in use” performance where a disinfectant is used in combination with detergent cleaning/wiping/ rinsing actions to produce a surface fit for purpose. Why do we not accept that the principles of achieving a FFP surface is exactly the same for hands, surfaces and laundry? Why do we rarely compare the in use efficacy of detergent-based procedures (e.g handwashing with soap, or surface wiping with a cloth with or without rinsing) with disinfectant based procedures (hand rubs or disinfectant application)? Why do we stress the need to clean before disinfecting as a separate action, and ignore the fact that the cleaning step contributes to the log reduction? Why do we not take account of the fact that disinfection of surfaces is different from instruments which have heavy soiling – many/most environmental surface disinfectants are formulated to work in the presence of the sort of levels of soiling found on touch surfaces.
Last but not least, we need some accepted terminology to distinguish between “cleaning” and “cleaning”! I am frequently confused by papers where I am not sure whether the author is using “cleaning” as a generic term for a “hygiene procedure” (which could involve using a disinfectant) or using it as the generic term for a detergent or wiping-based removal procedure. Although questions about what contamination levels are safe/what performance criteria should we agree on/how do we test efficacy etc are equally important, we need to start by agreeing some ground rules
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