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Evaluation of the Effectiveness of Two Automated Room Decontamination Devices Under Real-Life Conditions

Evaluation of the Effectiveness of Two Automated Room Decontamination Devices Under Real-Life... ORIGINAL RESEARCH published: 23 February 2021 doi: 10.3389/fpubh.2021.618263 Evaluation of the Effectiveness of Two Automated Room Decontamination Devices Under Real-Life Conditions Birte Knobling, Gefion Franke, Eva M. Klupp, Cristina Belmar Campos and Johannes K. Knobloch* Institute for Medical Microbiology, Virology and Hygiene, University Medical Center Hamburg-Eppendorf, Hamburg, Germany To evaluate the effectiveness of automated room decontamination devices, a common aerosolized hydrogen peroxide (aHP) as well as a recent gaseous ozone-based device, which produces the disinfectant reagent without the need of consumables, were tested under real-life conditions. Twenty-two contaminated surfaces were positioned in different areas in a patient room with adjacent bathroom and anteroom. Following the decontamination process bacteria were recovered and reduction factors were calculated after performing quantitative culture. Following the manufactures instructions, Edited by: the ozone-based device displayed a bactericidal effect (log > 5), whereas the aHP Ruixue Huang, Central South University, China system failed for a high bacterial burden and achieves only a complete elimination of Reviewed by: a realistic bioburden (log 2). After increasing the exposure time to 30 min, the aHP M. Jahangir Alam, device also reached a bactericidal effect. Nevertheless, our results indicate, that further University of Houston, United States research and development is necessary, to get knowledge about toxicity, efficacy and David Paige Gilkey, Colorado State University, safety by using in complex hospital conditions and achieve meaningful integration in United States cleaning procedures, to reach positive effects on disinfection performance. *Correspondence: Johannes K. Knobloch Keywords: automated room disinfection, hydrogen peroxide, ozone, real-life condition, terminal cleaning and j.knobloch@uke.de disinfection, non-touch room decontamination Specialty section: This article was submitted to INTRODUCTION Environmental health and Exposome, a section of the journal Pathogens associated with common nosocomial infections like methicillin resistant Staphylococcus Frontiers in Public Health aureus, vancomycin-resistant enterococci or Clostridioides difficile can survive on dry surfaces Received: 27 October 2020 for several weeks to month (1). Furthermore, these pathogens are often detected in patient’s Accepted: 02 February 2021 environment, if patients are colonized or infected (2–5). Contaminated surfaces might be an Published: 23 February 2021 important source for transmission and acquisition of healthcare associated pathogens (5–8). This Citation: recognition is supported by recent studies, which pointed out an increased risk of acquiring these Knobling B, Franke G, Klupp EM, pathogens with possible subsequent healthcare associated infections, if prior room occupants had Belmar Campos C and Knobloch JK already been infected (9–12). (2021) Evaluation of the Effectiveness Regular cleaning such as terminal cleaning and disinfection of surfaces, have been implemented of Two Automated Room in hospitals in the past to reduce the risk of transmission by contact to inanimate surfaces (13, 14). Decontamination Devices Under However, various studies have demonstrated that adequate disinfection from routine daily cleaning Real-Life Conditions. Front. Public Health 9:618263. was not achieved. Using a fluorescence method, Carling et al. showed that only an average of doi: 10.3389/fpubh.2021.618263 48% of examined surfaces were cleaned successfully (15). In addition, another study demonstrates Frontiers in Public Health | www.frontiersin.org 1 February 2021 | Volume 9 | Article 618263 Knobling et al. Effectiveness of Automatic Room Decontamination a terminal cleaning thoroughness of average 57% for frequently Mettlach, Germany) to generate high and primary contaminated touched surfaces after patients discharge (16). surfaces (HCS & PCS). The high contaminated surfaces serve Routine disinfection depends on several human factors, such to prove a bactericidal reduction capacity of log10 > 5 (24). as the selection of suitable substances, complete application to all Furthermore, surfaces with low contamination were generated relevant surfaces, compliance with the required exposure time, by a touch transfer assay, to demonstrate efficacy against a and correct implementation of cleaning protocols. Moreover, realistic bioburden (25). In brief, dried E. faecium was picked the complex hospital environment contains areas, which up by touching the PCS with one finger covered with a sterile are unattainable and difficult to clean (17). Furthermore, cotton glove after moistening on Columbia Agar with Sheep unclarified responsibilities for cleaning of special sites such as Blood (COLS+, OXOID Deutschland GmbH, Wesel, Germany) medical equipment negatively affects cleaning and disinfection and bacteria were transferred to another sterile ceramic tile to success (18). produce the secondary contaminated surface (SCS). Only SCS 2 3 To achieve more effective results automated room disinfection that met an initial surface load of 5 × 10 -5 × 10 cfu were systems were developed to address vulnerabilities associated with included in the final analysis. manual cleaning and improve patient safety. In hospital settings The HCS were placed at 22 certain positions locations in the automated room disinfection devices could be an additional complex room structure to represent both vertical and horizontal method of disinfection, to prevent environmental-borne surfaces in different heights and positions [close to patients (n = transmission. Currently, aerosolized and vapored hydrogen 4); distant from patients (n = 10); bathroom (n = 3); anteroom peroxide, chlorine dioxide and ultraviolet germicidal radiation (n = 5)]. Four SCS were placed close to the patient area, while are disinfectants, which were used for room decontamination two were positioned in furnishings within the patient room and (18, 19). Different studies had shown the effectiveness of these bathroom (Figure 1). Also, one HCS and one SCS were placed agents in experimental settings (18–21). The efficacy of hydrogen outside the test room as controls. peroxide has also been demonstrated in hospital settings, e.g., Both systems for automatic room disinfection were during outbreak situations but also in routine use (19–21). In investigated at least in four independent experiments with contrast, gaseous ozone is not a common reagent, because of identical placement of contaminated surfaces. The disinfection the need of permanent moisture to achieve effectiveness (22). devices were employed according to manufactures instructions. Consequently, only a few studies reported using ozone for For the ozone-based device, a normal cycle with 70–80 ppm decontamination but not yet for hospital room decontamination ozone concentration was applied for a holding time of 15 min (21, 23). and 80–90% relative humidity. For the aHP unit a fogging In our study, the disinfection performance of a recently time of 20 min was used in accordance with the manufacturer’s developed, fully automated system for generating ozone from specifications depending on the volume of the test room. atmospheric oxygen in combination with an integrated nebulizer After insufficient decontamination performance according to for controlled increase of room humidity, was compared with manufactures instructions (n = 3), we increased fogging time a commercial nebulizer for generation of aerosolized hydrogen to 30 min (n = 4). Before application, doors and ventilation peroxide (aHP) under realistic conditions. diffusers as well as smoke detectors were sealed. After each decontamination process bacteria were recovered from both, treated and untreated ceramic tiles, by using flocked TM nylon swabs (eSwab Standard, Copan; Brescia, Italien). After MATERIALS AND METHODS moistening the swab with transport medium, the ceramic tiles The efficacy of aHP and ozone-based devices for automated were wiped in horizontal, vertical and diagonal direction while room disinfection were evaluated in a typical patient room the swab was rotated continuously. The bacteria were eluted into (31.89 m²) with adjacent bathroom (6.63 m²) and anteroom (7.11 the transport medium by vortexing for 30 s and subsequently m²) as displayed in Figure 1. Aerosolized hydrogen peroxide quantitative cultures were performed in double determination (aHP) was produced by the Sentinel H O Fogger system (IC (detection limit 5 cfu/25 cm²) by spreading 100 μl of the Amies 2 2 Solutions Leipzig, Germany) and ozone as well as the required Medium on COLS+, using a Drigalski spatula. Agar plates TM ◦ humidity were generated by the STERISAFE Pro system were incubated for 18–24 h at 37 C. The reduction factors were (STERISAFE Pro version 1.0, STERISAFE ApS, Ole Maaløe’s calculated by subtracting the log10 of the control and the log10 TM vej 5, DK – 2200 Copenhagen). The STERISAFE Pro has an after disinfection. Statistical analysis was performed in R (26) by integrated measuring device to monitor and document the ozone using a Bonferroni corrected pairwise t-test. concentration as well as humidity. A successful disinfection cycle is only confirmed, if the permissible limit value is exceeded. In addition, at the end of disinfection procedure an active RESULTS purification phase is included to remove existing ozone by degradation to oxygen and removal of fine dust by filtration. Evaluation of quantitative cultures of untreated high To prepare standardized contaminated surfaces a suspension contaminated surfaces (HCS) showed a mean of 7.4 × 10 7 8 2 of E. faecium ATCC 6057 with 5.0 × 10 -1.2 × 10 colony cfu/25 cm for all tested devices (Figure 2A). This surface load is forming units (cfu)/mL was produced. 20 μL of this suspension suitable for demonstrating a reduction of >5 log10 and was able was dried on ceramic tiles (5 × 5 cm, #3709PN00, Villeroy&Boch, to designate a product as a bactericidal disinfectant. The bacterial Frontiers in Public Health | www.frontiersin.org 2 February 2021 | Volume 9 | Article 618263 Knobling et al. Effectiveness of Automatic Room Decontamination FIGURE 1 | Illustration of test room with depiction of target positions and location of automated room decontamination devices. Both test devices (A: Sentinel TM H O -Fogger; B: STERISAFE Pro Ozone) were positioned at different spots in patient room according to manufactures instructions. The different symbols [O: high 2 2 contaminated surfaces (HCS); X: HCS into furnishings; 1: secondary contaminated surfaces (SCS)] represent the kind of contaminated surface used at particular positions. In addition, superscript numbers display the position heights into the room (1 on the ground; 2 middle level; 3 at the top). load of untreated SCS revealed an average of 2.1 × 10 cfu/25 Furthermore, no bacteria could be recovered from the SCS cm modeling a worst case contamination of frequent touched after automated room disinfection, regardless of the device used surfaces (25, 27). and the amount of nebulized H O . This results in a log10 2 2 The ozone-based STERISAFE Pro achieved a log10 reduction reduction factor of average >3. The reduction factors of the factor of >5 in all parts of test room, regardless of the placement different devices are only varying in dependence of bacterial load of the HCS. The total cycle time needed for one decontamination of untreated SCS (Figure 2C). Therefore, a statistical evaluation process was ∼3 h. The Sentinel H O Fogger needed about of these results was omitted. 2 2 2 h for one cycle, but did not achieve the reduction rate required for disinfectants, taking into account the manufacturer’s instructions. Under these conditions only a mean reduction of DISCUSSION 2 log10 was observed. Strikingly, different reduction rates were Manual cleaning is not standardized and often refuses to remove achieved in the three connected rooms under these conditions. Despite the direction of the device spray into the patient’s bioburden on frequently touched surfaces, because of different personal-related reasons (17, 18, 22). Therefore, automated room room, non-significantly lower reduction rates were observed in the patient’s room with a mean reduction rate of log10 decontamination systems could be a suitable method to enhance the success of cleaning and disinfection processes in hospitals. 1.73 compared to the anteroom (mean = 2.31, p > 0.05) and the bathroom (mean = 1.86, p > 0.05). Because of this, The efficacy of a procedure, the ease and safety of use, rapid availability and ability to be integrated into routine processes after three experiments the exposure time was increased to 30 min for four additional experiments. After this adaption, are important for using new standardized procedures for final the Sentinel H O Fogger achieved a log10 reduction rate of disinfection (18). Therefore, studies characterizing such devices 2 2 are essential to ensure effectivity as well as safe operation >5 at all test positions equally (Figure 2B). The reduction factors determined for the Sentinel H O Fogger at 20 min in hospitals. 2 2 The efficacy of the established aerosolized hydrogen were significantly less effective compared to the reductions TM achieved by Sterisafe Pro and Sentinel H O Fogger at 30 min peroxide (aHP) process was investigated in comparison to 2 2 a recently developed fully automated device for disinfection exposure (p < 0.01). Frontiers in Public Health | www.frontiersin.org 3 February 2021 | Volume 9 | Article 618263 Knobling et al. Effectiveness of Automatic Room Decontamination FIGURE 2 | Initial contamination of HCS and SCS surfaces (A) and reduction factors achieved by two different automated room decontamination devices (B,C). The distribution of contamination used for the experiments (A) are shown separately as boxplot for the HCS and the SCS for the equipment and processes performed. (Continued) Frontiers in Public Health | www.frontiersin.org 4 February 2021 | Volume 9 | Article 618263 Knobling et al. Effectiveness of Automatic Room Decontamination 2 3 FIGURE 2 | Only SCS that met an initial surface load of 5 × 10 -5 ×10 cfu were included (dashed lines). The effectiveness of the disinfection processes was TM determined in several independent experiments with quantification of recoverable bacterial load in duplicate (STERISAFE Pro [n = 4], Sentinel 20 min [n = 3], Sentinel 30 min [n = 4]). The distribution of the calculated reduction factors for the HCS (B) and the SCS (C) is shown separately as a boxplot for the patient room, the TM bathroom and the anteroom. Disinfection using STERISAFE Pro as well as a 30-min nebulization of H O , achieved the mean reduction rate of 5 log10 (B, dashed 2 2 line) required for a process recognized as disinfection. Both disinfection processes were superior to a 20-min nebulization of H O , as confirmed with the HCS 2 2 (p < 0.01 paired t-test with Bonferroni correction). Realistic bacterial contamination was completely eliminated (C) for both processes (for aHP regardless of nebulization time). The differences in the distribution of the reduction rates displayed in the boxplots, results exclusively from the differences in the contamination used (A, right side). using ozone under conditions as close to reality as possible. These data indicate that experimental dose finding for an aHP All decontamination experiments were carried out in a fully system is required before routine use. furnished patient room with two adjacent rooms using highly Both systems require a process time of more than 2 h and contaminated surfaces according to the European Committee of also require time-consuming preparation (e.g., sealing doors, air Standardization (24) as well as surfaces with a realistic bioburden. diffusers, and smoke detectors with adhesive tape) and therefore Both devices were used according to the manufacturer’s cannot be used at all times. Occupational safety aspects are well- TM specifications. The ozone-based device showed the required taken into account with the STERISAFE Pro device, since bactericidal effect with a reduction of >5 log10, while aHP did at the end of the process the active substance is completely not meet the requirement with an average reduction of only 2 degraded and the concentration of ozone prevailing in the log10 for the high contamination. However, a realistic surface room is continuously displayed on a mobile tablet computer contamination, which was modeled with touch transfer, could and recorded in a standardized manner. In contrast, there is be completely eliminated by both devices. By extending the no possibility of monitoring or logging process parameters for fogging time of the aHP device and thus increasing the amount the simple aHP nebulizer. For such devices, it is recommended of hydrogen peroxide applied, the full disinfecting efficacy could to use additional measurement equipment to verify sufficient be achieved. concentration and ensure adherence to safety exposure limits The obtained results show a bactericidal effectiveness of the afterwards (18). Both principles of action are based on reactive ozone device independent of the position in the room. Previous oxygen species that inactivate pathogens, so that sensitive studies demonstrated a reduction of bacteria known to cause materials could be attacked. However, many medical device hospital-acquired infections by only >3 log10 (28, 29). Here, manufacturers allow wipe disinfection with hydrogen peroxide, an ozone concentration of 25 ppm was applied over different so material compatibility data is available for many materials. exposure times and a relative humidity of 75–95%. However, Ozone is a highly reactive and corrosive gas (22, 23) and in the a reduction of >3 log10 does not meet the requirements for future further investigations on material compatibility have to bactericidal disinfection performance (24). Moat et al. assume take place. that an increase in the ozone concentration might led to The following limitations of present study should be noted: the achievement of disinfecting efficacy (29). Zoutman et al. The microbiocidal efficiency has only been tested for one showed that a reduction >6 log10 for MRSA could only be pathogen, which is known to be environmentally-resistant. achieved at 500 ppm ozone concentration (90 min exposure To make a general statement on the effectiveness of such time) at a relative humidity of 80%, which was produced devices in routine use, further investigations with other by a separate humidifier (30). However, enterococci were not healthcare associated pathogens such as S. aureus, C. difficile, or sufficiently reduced under these conditions. Only the addition Acinetobacter baumannii should be performed. Furthermore, the of 1% hydrogen peroxide instead of water nebulized to increase influence of soiling and organic load, which have contributed to the room humidity resulted in a high efficacy with a 30 min the reduction in efficacy of automated room decontamination exposure time (30). It was shown that an increased humidity devices in other studies (17, 32), has not yet been included in level enhances microbiocidal efficiency (31), our results with full our study. Additionally, tests should be carried out on various bactericidal efficacy are consistent with these previous data as surface materials to assess the impact of different surface texture the new system combines a controlled high relative humidity on disinfection performance. with a continuous ozone level above 70 ppm for 60 min. These In conclusion, both ozone-based as well as hydrogen data indicate, that full activity can be reached without the use peroxide automated room decontamination systems can of additional consumables (e.g., HP) if the process is controlled achieve bactericidal effectiveness and might have a high during the whole disinfection cycle. potential to improve disinfection performance in hospitals by The aHP system, only reaches full bactericidal effectiveness standardization of the process. The fact that no consumables after extending the fogging time to 30 min. This is in agreement are needed to generate ozone, could be a decisive advantage with observations that aHP shows varying antimicrobial activity especially in pandemic situations like current Covid-19, depending on the location of contaminated surfaces in the which, was in part characterized by supply bottlenecks also of room (17, 32–34). Consistent with Fu et al. (17), we did not disinfectants (35). However, currently unknown aspects of safety observe full efficacy for aHP at all positions when following the and material compatibility as well as long decontamination cycles manufacturer’s instructions, while full efficacy was observed at might restrain a routine use in terminal cleaning procedures. all positions with an increased amount of nebulized disinfectant. Therefore, additional research under real-life conditions is Frontiers in Public Health | www.frontiersin.org 5 February 2021 | Volume 9 | Article 618263 Knobling et al. Effectiveness of Automatic Room Decontamination needed to confirm effectiveness against a wide variety of AUTHOR CONTRIBUTIONS pathogens as well as for various environmental conditions BK and JK conceived and planned the experiments. BK and GF and surfaces. carried out the experiments. BK, GF, EK, CB, and JK contributed to the experiments and the interpretation of the results. BK DATA AVAILABILITY STATEMENT and JK performed the statistical analyses. BK, GF, and JK wrote the manuscript in consultation with EK and CB. All authors The original contributions presented in the study are included in the article/supplementary material, further inquiries can be discussed the results and critically revised and approved the final version of manuscript. directed to the corresponding author. REFERENCES 15. Carling PC, Parry MM, Rupp ME, Po JL, Dick B, von Beheren S. Improving cleaning of the environment surrounding patients in 36 acute care hospitals. 1. Kramer A, Schwebke I, Kampf G. 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Surface germicidal effects of ozone for microorganisms. 05/12/why-is-there-a-shortage-of-disinfectants-during-the-covid-19-crisis/ AIHA J. (2003) 64:533–7. doi: 10.1080/15428110308984851 (accessed December 16, 2020). 32. Piskin N, Celebi G, Kulah C, Mengeloglu Z, Yumusak M. Activity of a dry mist-generated hydrogen peroxide disinfection system against methicillin- Conflict of Interest: BK and JK received a travel grant from INFUSER Germany resistant Staphylococcus aureus and Acinetobacter baumannii. Am J Infect GmbH, Mannheim, Deutschland. Control. (2011) 39:757–62. doi: 10.1016/j.ajic.2010.12.003 33. Steindl G, Fiedler A, Huhulescu S, Wewalka G, Allerberger F. Effect The remaining authors declare that the research was conducted in the absence of of airborne hydrogen peroxide on spores of Clostridium difficile. any commercial or financial relationships that could be construed as a potential Wien Klin Wochenschr. (2015) 127:421–6. doi: 10.1007/s00508-014- conflict of interest. 0682-6 34. Ali S, Muzslay M, Bruce M, Jeanes A, Moore G, Wilson APR. Efficacy of Copyright © 2021 Knobling, Franke, Klupp, Belmar Campos and Knobloch. This two hydrogen peroxide vapour aerial decontamination systems for enhanced is an open-access article distributed under the terms of the Creative Commons disinfection of meticillin-resistant Staphylococcus aureus, Klebsiella Attribution License (CC BY). The use, distribution or reproduction in other forums pneumoniae and Clostridium difficile in single isolation rooms. J Hosp is permitted, provided the original author(s) and the copyright owner(s) are credited Infect. (2016) 93:70–7. doi: 10.1016/j.jhin.2016.01.016 and that the original publication in this journal is cited, in accordance with accepted 35. Diederich BPS. Why is there a shortage of disinfectants during the covid-19 academic practice. No use, distribution or reproduction is permitted which does not crisis? (2020). Available online at: https://oecd-environment-focus.blog/2020/ comply with these terms. Frontiers in Public Health | www.frontiersin.org 7 February 2021 | Volume 9 | Article 618263 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Frontiers in Public Health Pubmed Central

Evaluation of the Effectiveness of Two Automated Room Decontamination Devices Under Real-Life Conditions

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ORIGINAL RESEARCH published: 23 February 2021 doi: 10.3389/fpubh.2021.618263 Evaluation of the Effectiveness of Two Automated Room Decontamination Devices Under Real-Life Conditions Birte Knobling, Gefion Franke, Eva M. Klupp, Cristina Belmar Campos and Johannes K. Knobloch* Institute for Medical Microbiology, Virology and Hygiene, University Medical Center Hamburg-Eppendorf, Hamburg, Germany To evaluate the effectiveness of automated room decontamination devices, a common aerosolized hydrogen peroxide (aHP) as well as a recent gaseous ozone-based device, which produces the disinfectant reagent without the need of consumables, were tested under real-life conditions. Twenty-two contaminated surfaces were positioned in different areas in a patient room with adjacent bathroom and anteroom. Following the decontamination process bacteria were recovered and reduction factors were calculated after performing quantitative culture. Following the manufactures instructions, Edited by: the ozone-based device displayed a bactericidal effect (log > 5), whereas the aHP Ruixue Huang, Central South University, China system failed for a high bacterial burden and achieves only a complete elimination of Reviewed by: a realistic bioburden (log 2). After increasing the exposure time to 30 min, the aHP M. Jahangir Alam, device also reached a bactericidal effect. Nevertheless, our results indicate, that further University of Houston, United States research and development is necessary, to get knowledge about toxicity, efficacy and David Paige Gilkey, Colorado State University, safety by using in complex hospital conditions and achieve meaningful integration in United States cleaning procedures, to reach positive effects on disinfection performance. *Correspondence: Johannes K. Knobloch Keywords: automated room disinfection, hydrogen peroxide, ozone, real-life condition, terminal cleaning and j.knobloch@uke.de disinfection, non-touch room decontamination Specialty section: This article was submitted to INTRODUCTION Environmental health and Exposome, a section of the journal Pathogens associated with common nosocomial infections like methicillin resistant Staphylococcus Frontiers in Public Health aureus, vancomycin-resistant enterococci or Clostridioides difficile can survive on dry surfaces Received: 27 October 2020 for several weeks to month (1). Furthermore, these pathogens are often detected in patient’s Accepted: 02 February 2021 environment, if patients are colonized or infected (2–5). Contaminated surfaces might be an Published: 23 February 2021 important source for transmission and acquisition of healthcare associated pathogens (5–8). This Citation: recognition is supported by recent studies, which pointed out an increased risk of acquiring these Knobling B, Franke G, Klupp EM, pathogens with possible subsequent healthcare associated infections, if prior room occupants had Belmar Campos C and Knobloch JK already been infected (9–12). (2021) Evaluation of the Effectiveness Regular cleaning such as terminal cleaning and disinfection of surfaces, have been implemented of Two Automated Room in hospitals in the past to reduce the risk of transmission by contact to inanimate surfaces (13, 14). Decontamination Devices Under However, various studies have demonstrated that adequate disinfection from routine daily cleaning Real-Life Conditions. Front. Public Health 9:618263. was not achieved. Using a fluorescence method, Carling et al. showed that only an average of doi: 10.3389/fpubh.2021.618263 48% of examined surfaces were cleaned successfully (15). In addition, another study demonstrates Frontiers in Public Health | www.frontiersin.org 1 February 2021 | Volume 9 | Article 618263 Knobling et al. Effectiveness of Automatic Room Decontamination a terminal cleaning thoroughness of average 57% for frequently Mettlach, Germany) to generate high and primary contaminated touched surfaces after patients discharge (16). surfaces (HCS & PCS). The high contaminated surfaces serve Routine disinfection depends on several human factors, such to prove a bactericidal reduction capacity of log10 > 5 (24). as the selection of suitable substances, complete application to all Furthermore, surfaces with low contamination were generated relevant surfaces, compliance with the required exposure time, by a touch transfer assay, to demonstrate efficacy against a and correct implementation of cleaning protocols. Moreover, realistic bioburden (25). In brief, dried E. faecium was picked the complex hospital environment contains areas, which up by touching the PCS with one finger covered with a sterile are unattainable and difficult to clean (17). Furthermore, cotton glove after moistening on Columbia Agar with Sheep unclarified responsibilities for cleaning of special sites such as Blood (COLS+, OXOID Deutschland GmbH, Wesel, Germany) medical equipment negatively affects cleaning and disinfection and bacteria were transferred to another sterile ceramic tile to success (18). produce the secondary contaminated surface (SCS). Only SCS 2 3 To achieve more effective results automated room disinfection that met an initial surface load of 5 × 10 -5 × 10 cfu were systems were developed to address vulnerabilities associated with included in the final analysis. manual cleaning and improve patient safety. In hospital settings The HCS were placed at 22 certain positions locations in the automated room disinfection devices could be an additional complex room structure to represent both vertical and horizontal method of disinfection, to prevent environmental-borne surfaces in different heights and positions [close to patients (n = transmission. Currently, aerosolized and vapored hydrogen 4); distant from patients (n = 10); bathroom (n = 3); anteroom peroxide, chlorine dioxide and ultraviolet germicidal radiation (n = 5)]. Four SCS were placed close to the patient area, while are disinfectants, which were used for room decontamination two were positioned in furnishings within the patient room and (18, 19). Different studies had shown the effectiveness of these bathroom (Figure 1). Also, one HCS and one SCS were placed agents in experimental settings (18–21). The efficacy of hydrogen outside the test room as controls. peroxide has also been demonstrated in hospital settings, e.g., Both systems for automatic room disinfection were during outbreak situations but also in routine use (19–21). In investigated at least in four independent experiments with contrast, gaseous ozone is not a common reagent, because of identical placement of contaminated surfaces. The disinfection the need of permanent moisture to achieve effectiveness (22). devices were employed according to manufactures instructions. Consequently, only a few studies reported using ozone for For the ozone-based device, a normal cycle with 70–80 ppm decontamination but not yet for hospital room decontamination ozone concentration was applied for a holding time of 15 min (21, 23). and 80–90% relative humidity. For the aHP unit a fogging In our study, the disinfection performance of a recently time of 20 min was used in accordance with the manufacturer’s developed, fully automated system for generating ozone from specifications depending on the volume of the test room. atmospheric oxygen in combination with an integrated nebulizer After insufficient decontamination performance according to for controlled increase of room humidity, was compared with manufactures instructions (n = 3), we increased fogging time a commercial nebulizer for generation of aerosolized hydrogen to 30 min (n = 4). Before application, doors and ventilation peroxide (aHP) under realistic conditions. diffusers as well as smoke detectors were sealed. After each decontamination process bacteria were recovered from both, treated and untreated ceramic tiles, by using flocked TM nylon swabs (eSwab Standard, Copan; Brescia, Italien). After MATERIALS AND METHODS moistening the swab with transport medium, the ceramic tiles The efficacy of aHP and ozone-based devices for automated were wiped in horizontal, vertical and diagonal direction while room disinfection were evaluated in a typical patient room the swab was rotated continuously. The bacteria were eluted into (31.89 m²) with adjacent bathroom (6.63 m²) and anteroom (7.11 the transport medium by vortexing for 30 s and subsequently m²) as displayed in Figure 1. Aerosolized hydrogen peroxide quantitative cultures were performed in double determination (aHP) was produced by the Sentinel H O Fogger system (IC (detection limit 5 cfu/25 cm²) by spreading 100 μl of the Amies 2 2 Solutions Leipzig, Germany) and ozone as well as the required Medium on COLS+, using a Drigalski spatula. Agar plates TM ◦ humidity were generated by the STERISAFE Pro system were incubated for 18–24 h at 37 C. The reduction factors were (STERISAFE Pro version 1.0, STERISAFE ApS, Ole Maaløe’s calculated by subtracting the log10 of the control and the log10 TM vej 5, DK – 2200 Copenhagen). The STERISAFE Pro has an after disinfection. Statistical analysis was performed in R (26) by integrated measuring device to monitor and document the ozone using a Bonferroni corrected pairwise t-test. concentration as well as humidity. A successful disinfection cycle is only confirmed, if the permissible limit value is exceeded. In addition, at the end of disinfection procedure an active RESULTS purification phase is included to remove existing ozone by degradation to oxygen and removal of fine dust by filtration. Evaluation of quantitative cultures of untreated high To prepare standardized contaminated surfaces a suspension contaminated surfaces (HCS) showed a mean of 7.4 × 10 7 8 2 of E. faecium ATCC 6057 with 5.0 × 10 -1.2 × 10 colony cfu/25 cm for all tested devices (Figure 2A). This surface load is forming units (cfu)/mL was produced. 20 μL of this suspension suitable for demonstrating a reduction of >5 log10 and was able was dried on ceramic tiles (5 × 5 cm, #3709PN00, Villeroy&Boch, to designate a product as a bactericidal disinfectant. The bacterial Frontiers in Public Health | www.frontiersin.org 2 February 2021 | Volume 9 | Article 618263 Knobling et al. Effectiveness of Automatic Room Decontamination FIGURE 1 | Illustration of test room with depiction of target positions and location of automated room decontamination devices. Both test devices (A: Sentinel TM H O -Fogger; B: STERISAFE Pro Ozone) were positioned at different spots in patient room according to manufactures instructions. The different symbols [O: high 2 2 contaminated surfaces (HCS); X: HCS into furnishings; 1: secondary contaminated surfaces (SCS)] represent the kind of contaminated surface used at particular positions. In addition, superscript numbers display the position heights into the room (1 on the ground; 2 middle level; 3 at the top). load of untreated SCS revealed an average of 2.1 × 10 cfu/25 Furthermore, no bacteria could be recovered from the SCS cm modeling a worst case contamination of frequent touched after automated room disinfection, regardless of the device used surfaces (25, 27). and the amount of nebulized H O . This results in a log10 2 2 The ozone-based STERISAFE Pro achieved a log10 reduction reduction factor of average >3. The reduction factors of the factor of >5 in all parts of test room, regardless of the placement different devices are only varying in dependence of bacterial load of the HCS. The total cycle time needed for one decontamination of untreated SCS (Figure 2C). Therefore, a statistical evaluation process was ∼3 h. The Sentinel H O Fogger needed about of these results was omitted. 2 2 2 h for one cycle, but did not achieve the reduction rate required for disinfectants, taking into account the manufacturer’s instructions. Under these conditions only a mean reduction of DISCUSSION 2 log10 was observed. Strikingly, different reduction rates were Manual cleaning is not standardized and often refuses to remove achieved in the three connected rooms under these conditions. Despite the direction of the device spray into the patient’s bioburden on frequently touched surfaces, because of different personal-related reasons (17, 18, 22). Therefore, automated room room, non-significantly lower reduction rates were observed in the patient’s room with a mean reduction rate of log10 decontamination systems could be a suitable method to enhance the success of cleaning and disinfection processes in hospitals. 1.73 compared to the anteroom (mean = 2.31, p > 0.05) and the bathroom (mean = 1.86, p > 0.05). Because of this, The efficacy of a procedure, the ease and safety of use, rapid availability and ability to be integrated into routine processes after three experiments the exposure time was increased to 30 min for four additional experiments. After this adaption, are important for using new standardized procedures for final the Sentinel H O Fogger achieved a log10 reduction rate of disinfection (18). Therefore, studies characterizing such devices 2 2 are essential to ensure effectivity as well as safe operation >5 at all test positions equally (Figure 2B). The reduction factors determined for the Sentinel H O Fogger at 20 min in hospitals. 2 2 The efficacy of the established aerosolized hydrogen were significantly less effective compared to the reductions TM achieved by Sterisafe Pro and Sentinel H O Fogger at 30 min peroxide (aHP) process was investigated in comparison to 2 2 a recently developed fully automated device for disinfection exposure (p < 0.01). Frontiers in Public Health | www.frontiersin.org 3 February 2021 | Volume 9 | Article 618263 Knobling et al. Effectiveness of Automatic Room Decontamination FIGURE 2 | Initial contamination of HCS and SCS surfaces (A) and reduction factors achieved by two different automated room decontamination devices (B,C). The distribution of contamination used for the experiments (A) are shown separately as boxplot for the HCS and the SCS for the equipment and processes performed. (Continued) Frontiers in Public Health | www.frontiersin.org 4 February 2021 | Volume 9 | Article 618263 Knobling et al. Effectiveness of Automatic Room Decontamination 2 3 FIGURE 2 | Only SCS that met an initial surface load of 5 × 10 -5 ×10 cfu were included (dashed lines). The effectiveness of the disinfection processes was TM determined in several independent experiments with quantification of recoverable bacterial load in duplicate (STERISAFE Pro [n = 4], Sentinel 20 min [n = 3], Sentinel 30 min [n = 4]). The distribution of the calculated reduction factors for the HCS (B) and the SCS (C) is shown separately as a boxplot for the patient room, the TM bathroom and the anteroom. Disinfection using STERISAFE Pro as well as a 30-min nebulization of H O , achieved the mean reduction rate of 5 log10 (B, dashed 2 2 line) required for a process recognized as disinfection. Both disinfection processes were superior to a 20-min nebulization of H O , as confirmed with the HCS 2 2 (p < 0.01 paired t-test with Bonferroni correction). Realistic bacterial contamination was completely eliminated (C) for both processes (for aHP regardless of nebulization time). The differences in the distribution of the reduction rates displayed in the boxplots, results exclusively from the differences in the contamination used (A, right side). using ozone under conditions as close to reality as possible. These data indicate that experimental dose finding for an aHP All decontamination experiments were carried out in a fully system is required before routine use. furnished patient room with two adjacent rooms using highly Both systems require a process time of more than 2 h and contaminated surfaces according to the European Committee of also require time-consuming preparation (e.g., sealing doors, air Standardization (24) as well as surfaces with a realistic bioburden. diffusers, and smoke detectors with adhesive tape) and therefore Both devices were used according to the manufacturer’s cannot be used at all times. Occupational safety aspects are well- TM specifications. The ozone-based device showed the required taken into account with the STERISAFE Pro device, since bactericidal effect with a reduction of >5 log10, while aHP did at the end of the process the active substance is completely not meet the requirement with an average reduction of only 2 degraded and the concentration of ozone prevailing in the log10 for the high contamination. However, a realistic surface room is continuously displayed on a mobile tablet computer contamination, which was modeled with touch transfer, could and recorded in a standardized manner. In contrast, there is be completely eliminated by both devices. By extending the no possibility of monitoring or logging process parameters for fogging time of the aHP device and thus increasing the amount the simple aHP nebulizer. For such devices, it is recommended of hydrogen peroxide applied, the full disinfecting efficacy could to use additional measurement equipment to verify sufficient be achieved. concentration and ensure adherence to safety exposure limits The obtained results show a bactericidal effectiveness of the afterwards (18). Both principles of action are based on reactive ozone device independent of the position in the room. Previous oxygen species that inactivate pathogens, so that sensitive studies demonstrated a reduction of bacteria known to cause materials could be attacked. However, many medical device hospital-acquired infections by only >3 log10 (28, 29). Here, manufacturers allow wipe disinfection with hydrogen peroxide, an ozone concentration of 25 ppm was applied over different so material compatibility data is available for many materials. exposure times and a relative humidity of 75–95%. However, Ozone is a highly reactive and corrosive gas (22, 23) and in the a reduction of >3 log10 does not meet the requirements for future further investigations on material compatibility have to bactericidal disinfection performance (24). Moat et al. assume take place. that an increase in the ozone concentration might led to The following limitations of present study should be noted: the achievement of disinfecting efficacy (29). Zoutman et al. The microbiocidal efficiency has only been tested for one showed that a reduction >6 log10 for MRSA could only be pathogen, which is known to be environmentally-resistant. achieved at 500 ppm ozone concentration (90 min exposure To make a general statement on the effectiveness of such time) at a relative humidity of 80%, which was produced devices in routine use, further investigations with other by a separate humidifier (30). However, enterococci were not healthcare associated pathogens such as S. aureus, C. difficile, or sufficiently reduced under these conditions. Only the addition Acinetobacter baumannii should be performed. Furthermore, the of 1% hydrogen peroxide instead of water nebulized to increase influence of soiling and organic load, which have contributed to the room humidity resulted in a high efficacy with a 30 min the reduction in efficacy of automated room decontamination exposure time (30). It was shown that an increased humidity devices in other studies (17, 32), has not yet been included in level enhances microbiocidal efficiency (31), our results with full our study. Additionally, tests should be carried out on various bactericidal efficacy are consistent with these previous data as surface materials to assess the impact of different surface texture the new system combines a controlled high relative humidity on disinfection performance. with a continuous ozone level above 70 ppm for 60 min. These In conclusion, both ozone-based as well as hydrogen data indicate, that full activity can be reached without the use peroxide automated room decontamination systems can of additional consumables (e.g., HP) if the process is controlled achieve bactericidal effectiveness and might have a high during the whole disinfection cycle. potential to improve disinfection performance in hospitals by The aHP system, only reaches full bactericidal effectiveness standardization of the process. The fact that no consumables after extending the fogging time to 30 min. This is in agreement are needed to generate ozone, could be a decisive advantage with observations that aHP shows varying antimicrobial activity especially in pandemic situations like current Covid-19, depending on the location of contaminated surfaces in the which, was in part characterized by supply bottlenecks also of room (17, 32–34). Consistent with Fu et al. (17), we did not disinfectants (35). However, currently unknown aspects of safety observe full efficacy for aHP at all positions when following the and material compatibility as well as long decontamination cycles manufacturer’s instructions, while full efficacy was observed at might restrain a routine use in terminal cleaning procedures. all positions with an increased amount of nebulized disinfectant. Therefore, additional research under real-life conditions is Frontiers in Public Health | www.frontiersin.org 5 February 2021 | Volume 9 | Article 618263 Knobling et al. Effectiveness of Automatic Room Decontamination needed to confirm effectiveness against a wide variety of AUTHOR CONTRIBUTIONS pathogens as well as for various environmental conditions BK and JK conceived and planned the experiments. BK and GF and surfaces. carried out the experiments. BK, GF, EK, CB, and JK contributed to the experiments and the interpretation of the results. BK DATA AVAILABILITY STATEMENT and JK performed the statistical analyses. BK, GF, and JK wrote the manuscript in consultation with EK and CB. All authors The original contributions presented in the study are included in the article/supplementary material, further inquiries can be discussed the results and critically revised and approved the final version of manuscript. directed to the corresponding author. REFERENCES 15. Carling PC, Parry MM, Rupp ME, Po JL, Dick B, von Beheren S. Improving cleaning of the environment surrounding patients in 36 acute care hospitals. 1. Kramer A, Schwebke I, Kampf G. 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Surface germicidal effects of ozone for microorganisms. 05/12/why-is-there-a-shortage-of-disinfectants-during-the-covid-19-crisis/ AIHA J. (2003) 64:533–7. doi: 10.1080/15428110308984851 (accessed December 16, 2020). 32. Piskin N, Celebi G, Kulah C, Mengeloglu Z, Yumusak M. Activity of a dry mist-generated hydrogen peroxide disinfection system against methicillin- Conflict of Interest: BK and JK received a travel grant from INFUSER Germany resistant Staphylococcus aureus and Acinetobacter baumannii. Am J Infect GmbH, Mannheim, Deutschland. Control. (2011) 39:757–62. doi: 10.1016/j.ajic.2010.12.003 33. Steindl G, Fiedler A, Huhulescu S, Wewalka G, Allerberger F. Effect The remaining authors declare that the research was conducted in the absence of of airborne hydrogen peroxide on spores of Clostridium difficile. any commercial or financial relationships that could be construed as a potential Wien Klin Wochenschr. (2015) 127:421–6. doi: 10.1007/s00508-014- conflict of interest. 0682-6 34. Ali S, Muzslay M, Bruce M, Jeanes A, Moore G, Wilson APR. Efficacy of Copyright © 2021 Knobling, Franke, Klupp, Belmar Campos and Knobloch. This two hydrogen peroxide vapour aerial decontamination systems for enhanced is an open-access article distributed under the terms of the Creative Commons disinfection of meticillin-resistant Staphylococcus aureus, Klebsiella Attribution License (CC BY). The use, distribution or reproduction in other forums pneumoniae and Clostridium difficile in single isolation rooms. J Hosp is permitted, provided the original author(s) and the copyright owner(s) are credited Infect. (2016) 93:70–7. doi: 10.1016/j.jhin.2016.01.016 and that the original publication in this journal is cited, in accordance with accepted 35. Diederich BPS. Why is there a shortage of disinfectants during the covid-19 academic practice. No use, distribution or reproduction is permitted which does not crisis? (2020). Available online at: https://oecd-environment-focus.blog/2020/ comply with these terms. Frontiers in Public Health | www.frontiersin.org 7 February 2021 | Volume 9 | Article 618263

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