Effectiveness of a combined UV-C and ozone treatment in reducing healthcare-associated infections in hospital facilities

 

Source: The entire contents of this page refer to the related article posted by The Journal of Hospital Infection. We have quoted it in its entirety
Authors:
C. Sottani - G. Favorido Barraza - F. Frigerio - G. Corica - F.S. Robustelli della Cuna - D. Cottica - E. Grignani

 

SUMMARY

Background

Hospital-acquired infections pose an ongoing threat to patient safety due to the presence of multi-drug-resistant organisms (MDROs) and other pathogens such as Clostridioides difficile which are dependent on thorough and effective cleaning and disinfection by personnel.

Methods

This study evaluated the influence of UV-C air treatment: the air in the room was sanitized by UV-C and redirected into the room. In addition, ozone was released into the room to treat actual surfaces in low-risk areas such as hospital gyms, and high- to medium-risk areas such as hospital rooms. To this aim, a portable device designed for treating the environment air was tested against nine bacterial strains including Aspergillus spp. and Clostridioides spp.

Results

The use of UV-C air treatment during daily operations and ozone treatment achieved at least a 2-log10 pathogen reduction except for Clostridioides spp

Conclusion

Effective prevention of C. difficile normally requires the use of combined approaches that include chemical compounds and disinfection agents whose toxicity can be harmful not only to patients but also to healthcare personnel. Thus, the proposed no-touch device may be evaluated in future research to assess the needed requirements for its possible and full implementation in hospitals.

 

INTRODUCTION

Biological standards for surface hygiene in hospitals are still an open debate within the scientific community of microbiolo-gists. Hospital-acquired infections (HAIs) can cause diseases because some pathogens such as meticillin-resistant Staphylococcus aureus (MRSA), vancomycin-resistant Enterococcus (VRE), Klebsiella pneumoniaePseudomonas aeruginosaAcinetobacter baumannii, and Clostridioides difficile may persist in hospital environments [,]. Because a general increase in morbidity and mortality worldwide in hospital settings has been reported by the European Antimicrobial Resistance Surveillance System Network (EARS-Net), European guidelines have recently been issued [].

They are focused on the transmission of infection and its reduction in hospitalized patients mainly colonized by Gram-negative bacteria such as Escherichia coli, Klebsiella spp. and P. aeruginosa. Conversely, there is some evidence that Gram-positive pathogens such as MRSA or C. difficile may contribute to HAIs []. 

To control HAIs in hospital environments, many methods for both manual and automated cleaning have been described in recent literature [,,6,7].

The most commonly used approaches to control HAIs include traditional cleaning methods based on detergents and disinfectants []. However, to date, there is great concern regarding the effectiveness of terminal cleaning (disinfection of a room between occupying patients) and disinfection with germicides because, if not correctly used, they may leave environmental surfaces contaminated with significant nosocomial pathogens []. Consequently, other disinfection systems such as steam vapour, hydrogen peroxide, ultraviolet germicidal irradiation (UV-C), Pulsed Xenon Ultraviolet (PX-UV), ozone, photocatalytic oxidation (PCO), and combination of these have been investigated [,11,12,13,14,15,16].

Although steam vapour machines are effective against a wide range of pathogens, notably VRE, MRSA, and Gram-negative bacilli, steam vapour is not frequently used in hospitals. In fact, its cleaning effect depends on a longer period of time during which steam turns into water []. 

Nowadays, there is a growing interest in other decontamination systems such as gaseous disinfectants like hydrogen peroxide and ozone [[,19,20].

The latter is a potent oxidizing agent, which is highly effective against C. difficile spores and E. coli [,22]].
In the literature, strategies based on the use of no-touch systems in combination with hypochlorite-containing disinfectant (bleach) are reported in several studies and summarized in recent original papers and reviews [[10],[12],[23],[24],[25].
 
The study by Nerandzic et al. [] highlighted the usefulness of combining UV-C radiation at 254 nm with bleach for terminal room disinfection and suggested that the removal of debris from surfaces before using UV-C lowered the number of room infections. In a recent publication by Bong et al., the use of ozone delivered in a sealed chamber against broad-spectrum bacteria (i.e., VRE, carbapenem-resistant K. pneumoniae, carbapenem-resistant P. aeruginosa, carbapenem-resistant A. baumannii (CRAB) and C. difficile spores was evaluated). The authors demonstrated that gaseous disinfectants can be as active as antimicrobial agents. In addition, the authors featured the future use of no-touch devices (NTDs) because gases can reach places and objects inaccessible to conventional manual methods. Thus, much has been achieved in the study of NTDs and ozone-based systems during recent years [,].

 

In light of these considerations, we investigated the effectiveness of air treatment by means of UV-C irradiation and ozone delivery to disinfect surfaces following patient discharge. Limiting UV-C irradiation to the air avoids the implementation of technical and organizational measures against the release of air pollutants and contaminants from the UV irradiation of materials. In particular, the formation of toxic chemical compounds such as volatile organic compounds is described in the literature []. For this reason, we chose the UV-C irradiation of air instead of other techniques such as photocatalytic oxidation []. To our knowledge, this is the first time that an UV–ozone device has been designed as a modular, scalable ozone generator to decrease the bioburden on actual hospital surfaces. The system, whose functioning was previously reported [], was tested in two areas at different risks of infection to assess the efficacy of the combination of UV-C and ozone treatment. This study aims to compare the reduction of pathogens obtained by manual cleaning versus the reduction obtained by using UV-C irradiation of the air combined with gaseous ozone in a portable system.

 

METHODS

OZY AIR+LIGHT device

The different environments were treated with the OZY AIR+LIGHT device, supplied by O3ZY SA, Stabio, Switzerland. The device is a wheel-mounted portable ozone generator, coupled with UVC sanitizer, connected to the internet via WiFi, and remotely controlled and operated by a smartphone application. The ozone generator produces up to 60 g/h of ozone through dielectric barrier discharge (corona effect) from ambient air. An ozone detector measures in real time the ozone concentration such that a built-in controller maintains a continuous ozone generation until a desired environment concentration is achieved and kept for a preset time. After this treatment time, the air in the environment is circulated by a fan through a catalytic converter to hasten the recombination of ozone back into oxygen. The system automatically shuts off the generator and starts the cleaning procedure if a movement is detected in the environment. The UV-C sanitizer provides a flux of 80 m3/h of air taken from the environment and treated by UV-C radiation at 254 nm. The UV-C sanitization can be maintained without any constraint because the UV-C radiation does not leak outside the device. An illustration of the mechanism of action is reported in Figure 1.

Figure 1 - View of OZY AIR+LIGHT device with inlets and outlets for ozone and ultraviolet (UV-C)-treated air.

This figure shows OZY AIR+LIGHT device with separated inlets for UV-C air treatment and ozone production. After the end of the ozone production phase, the air is emitted from the ozone outlet. Room air is taken from the environment and passed through a converter in order to hasten the reduction of ozone back into oxygen. Any sequence of UV Light and ozone treatments can be programmed and controlled by the application that also stores a log of each treatment.

Sampling method

The sampling procedure was carried out according to the Italian guideline entitled: Linea guida sulla valutazione del processo di sanificazione ambientale nelle strutture ospedaliere e territoriali per il controllo delle Infezioni Correlate all’Assistenza []. Because hospital settings are classified as low-risk (LR) infection areas and high- to medium-risk (HR) infection areas, these locations were investigated. Because our laboratory met the requirements of the International Organization for Standardization ISO 17025, RODAC plates (Scharlab, S.L., supplier Biogenetics), swabs/sponges were used throughout the study. Moreover, according to EN ISO 17141:2021 standard 2, samples were taken using dry or pre-moistened swabs and sponges (SRK® Copan, supplier Biogenetics). In particular, for small and non-flat surfaces, samples were collected using Rodac plates. For curved surfaces, swabs were used. Flat areas of 20 × 20 cm (400 cm2) were also sampled by means of swabs. As a sampling error is seen as one of the most important causes of confounding, the measurement of sampling areas was carried out by means of swab kits and sampling masks. To avoid an error caused by the growth-productivity of the Rodac plates, ready-to-use plates were used (UNI EN ISO 11333). In HR areas, the sampling was scheduled during the day and ozone was working in the absence of patients. Because the patient rooms had an approximate volume of 60 m3, one OZY AIR+LIGHT device was sufficient. Relative humidity and temperature were recorded by a portable Sensor (Delta OHM HD 21AB17 supplier Delta OHM, PD, Selvazzano Dentro, Italy).
Gyms have a volume of 1200 m3, and hence two devices were used to warrant the efficacy of both UV-C and ozone. The changing rooms were directly connected to the gym's open space needed another device. For both LH and HR areas, a concentration of 6 ppm ozone was maintained by the sensor's device and kept stable for an hour. The sampling procedure was carried out once a week for three consecutive weeks for each hospital.

Analysis method

The sampled swabs were immersed in 10 mL 1% buffered peptone water (recovery solution), from SRK® Copan (Biogenetics, Brescia, Italy). Each sample was vortexed for 2 min to ensure that pathogens were suspended. A 100-/200-μL aliquot of the recovery solution was inoculated in appropriate selective and differential solid culture media. To reduce the possibility of false negatives, each sample was inoculated in duplicate to observe the mean colony-forming unit (cfu) value. Once the mean number of colonies per pathogen was established, the number of plates was obtained. That allowed for a good representation of the sample distribution according to ISO 19458:2006. In this study, pathogens were: Aspergillus spp. and Candida spp. required spore count by lactophenol staining and the subsequent observation under an optical microscope. Then, the vegetative sowing on Sabourand agar with chloramphenicol was needed to complete the analysis.
According to UNI EN ISO 9308-1 and UNI EN ISO 9308-2, for Enterobacterales, a selective and differential seeding method was carried out on MacConckey AGAR medium (Biolife, Milano, Italy). To differentiate E. coli from Klebsiella spp., biochemical tests (EnteroPluri-Test supplied by SECURLAB, Roma, Italy) were used. For S. aureus, the seeding was carried out in a selective and differential medium (Baird Parker RPF Agar, Biolife Milano, Italy), following ISO 6888-1:2021. The confirmed colonies were sub-cultured to sheep blood agar (5% blood agar sheep Biolife, Milano, Italy) to ensure β-haemolysis. Non-β-haemolytic staphylococci were analysed by sowing in Baird Parker and in blood agar sheep, whereas colony counting was performed without agglutination halos. Confirmation was established by Gram staining. The staphylococci colonies were sub-cultured to 5% blood agar sheep also to confirm the absence of β-haemolysis. For P. aeruginosa, the analyses were carried out by inoculating them in P. aeruginosa selective agar according to UNI EN ISO 16266. Finally, Clostridium spp. was analysed using C. difficile selective agar (Biolife, Milano, Italy) and the Schaeffer–Fulton (Millipore, Darmstadt, Germany) staining method (UNI EN ISO 14189).

Uncertainty assessment

Swab release errors were investigated using pure lyophilized strains of E. coli ATCC™ 8739™ and Enterococcus faecalis ATCC™ 29212™. Both strains were supplied by manufacturer Microbiologics™ (Biogenetics, Saint Cloud, MN, USA). The tests were carried out using Ringers solution 1:4 strength tablets purchased from Merck (Darmstadt, Germany). A total of 50 discs were used (25 E. coli and 25 Enterococcus). Each sample was collected by means of a swab (SRK® Copan, supplier Biogenetics). In order to ensure the quality of the data, 50 swabs of the same batch were examined and the swab batches were used throughout the sampling campaign. Expanded uncertainty (U) was estimated according to ISO 29201. This standard requires the calculation of the error as a combination of several factors. In this study, the uncertainty derives mainly from dilutions (u2rel: 0.0065), volume withdrawals (u2rel 100 μL: 0.00888 and u2rel 200 μL: 0.00831), the incubation (u2rel: 0.000315778), confirmation of suspicious colonies (u2rel change in the base of total cfu) and cell count (u2rel: 0.000196). All values obtained from the same swab were averaged and each value was evaluated using the chi-squared parameter with α = 0.005. The values showed a tabulated confidence interval (CI) of 99%, with a tabulated P-value less than 0.01.

Study design

The study was conducted in three Italian hospitals. In Table I, locations and types of rooms are described including sampling points, the number of samples taken on surfaces, and plate numbers. Thus, for nine strains we obtained 240 samples in LR and 144 samples in HR areas. In this study, a multi-treatment approach was set to evaluate the efficacy of cleaning procedures combined with UV-C and ozone treatment. In Figure 2, the whole process is depicted. The procedure was undertaken over 3 weeks numbered as zero, one, and two. The schematic process was set to be performed in three cycles. Dots represent the sampling that was performed on a targeted day (on Tuesday) each week. In this experimental setting, UV-C treatment was applied continuously for a total of 10 h (starting from 8 a.m.) each day. Ozone treatment was delivered at 6 ppm for 1 h when UV-C was off (Figure 2). In locations such as gyms and changing rooms, ozone was used in the absence of patients. In hospital rooms, ozone treatment started after discharging patients and routine cleaning (Figure 3). For patient safety, ozone gaseous was used at the patient discharge, whereas UV-C radiation remained on from around 8 a.m. to 6 p.m.
Table I - Summary of the sampling procedure
Figure 2 - Scheme of the sampling programme, the dots represent the samples taken before cleaning, after cleaning, and after ozone treatment.
Figure 3 - Data storage and final report from the OZY AIR+LIGHT device. The system records the gaseous treatment at a 6-ppm ozone level.
To investigate the level of environmental surface contamination in HR areas, 48 hospital-care rooms were monitored. The sampling strategy was the same as that for LR areas. In detail, six sampling points before, after cleaning, and after ozone treatment (three times per week) on the same day of the week (Tuesday) were monitored.
Benzalkonium chloride solutions (Saniquat®, Nuova Farmec S.r.L., Settimo, Verona, Italy) was used as detergent and disinfectant. Because the sampling points were repeated three times, the measurements allowed reproducible and reliable data to be achieved and used for the subsequent statistical analysis.
In both LR and HR areas, according to this process, basal values of infection were determined at week 0 utilizing the sampling method previously described and applied before cleaning procedures. This work did not address the quantity of volatile organic compounds and other toxic chemicals incidentally generated by the use of the device because the ozone concentration was monitored by the device itself and our local regulation does not allow the complete air recirculation using HVAC (heating, ventilation and air conditioning). UV-C irradiation being limited to the air taken from the room, the quantification of any other chemical pollutants would have required methods beyond the scope of this study [].

Study design

The antimicrobial activity of ozone and the UV-C air treatment in combination with a disinfection cleaning procedure based on the use of quaternary ammonium compounds was investigated over three consecutive weeks. The results for experiments conducted in LR areas and HR areas are presented in Table IITable III, respectively. To evaluate the pathogen reduction, the mean concentration values are expressed as log10 and detailed for Gram-positive (S. aureus, non-β-haemolytic staphylococci, Clostridioides spp.), Gram-negative (Enterobacterales, E. coli, Klebsiella spp., P. aeruginosa), mould and yeasts (Candida spp., Aspergillus spp.).
Table II - Results obtained from ordinary cleaning and the sanitizing OZY AIR+LIGHT device against Gram+ bacteria, Gram− bacteria, and against mould and yeasts over three cycles of the disinfection process in low-risk areas
Table III - Results obtained from ordinary cleaning and the sanitizing OZY AIR+LIGHT device against Gram-positive bacteria, Gram-negative bacteria, and against mould and yeasts over three cycles of the disinfection process in High-Medium risk areas
In LR areas, while UV-C irradiation of the air was working continuously during the normally performed activities, the ozone was used in gyms and changing rooms not occupied by patients. Generally, the admission to gyms occurs in the morning to allow the subsequent cleaning procedures to be carried out in the evening. The investigated hospitals housed four gyms and four changing rooms. Because the sampling points were five (Table I) for each location and the sampling procedure was carried out three times, the comprehensive number was 6480 plate counts for nine bacterial strains over the entire period of the study. Relative humidity ranged from 50% to 60% approximately, at 25 °C.
In Table II, the results underline the effectiveness of the combined use of UV-C and ozone. In particular, for Gram-negative bacteria, the percentage of reduction after ozone plus UV-C air treatment was more than 99%. However, for Clostridioides spp. and Aspergillus spp., the percentage reduction of C. difficile spores varied from 41% (week 0) to 79% (week 2). Whereas, for Aspergillus spp. the percentage reduction was between 44% and 97%. Notably, the reduction of the mean concentration value depended on the number of treatments carried out during weeks 0, 1, and 2. The reduction was more than the 2-log10 of the mean concentration value.
In HR areas, 3888 plate counts were obtained over the entire study (Table I). The overall results are reported in Table III. The combined treatments showed effectiveness against Gram-positive bacteria (S. aureus and non-β-hemolytic staphylococci), Gram-negative bacteria, and Candida spp. Similarly, Clostridioides spp. and Aspergillus spp. were found to be less susceptible to the combined use of UV-C and ozone. As an example, Clostridioides spp. accounted for 29% and 40% of reduction at weeks 0 and 2, respectively. Aspergillus spp. achieved a significant reduction (99%) only after 3 weeks of treatment.
For LR and HR areas, the log10 reduction is reported in Figure 4Figure 5, respectively. In each figure, panels a and b depict the reduction rates after UV-C air treatment after weeks 1 and 2, respectively; panel c shows the log10 reduction after ozone and UV-C treatment.
Figure 4 - Log10 mean reduction values obtained in low-risk areas.
Figure 5 - Log10 mean reduction values obtained in high- to medium-risk areas.
The results in Figure 4Figure 5 show the ability of UV-C air sanitization to reduce microbial contamination even on the surfaces. In this context, Aspergillus spp. showed a significant reduction rate of a 1.88-log10 after 1 week and, a 2.83-log10 after 2 weeks of UV-C treatment. Conversely, the ozone as a disinfection system applied in unoccupied locations after UVC air treatment appeared to be effective (panel c) against all the studied pathogens with values ranging from 1.15-log10 for C. difficile to 3.78-log10 for S. aureus.
The log10 reduction values are reported for HR areas in Figure 5. Because the hospital rooms hosted the same patient, the basal concentration levels were homogeneously distributed. This allowed us to determine how a decrease of more than 2-log10 was consistently obtained by applying the ozone sanitation system after UV-C air treatment. The reduction rate for C. difficile was found to be 1.51-log10 and 2.03-log10 for Aspergillus.

Discussion

In recent years, room disinfection in healthcare facilities has been focusing on automated technologies used in combination with standard cleaning procedures. In particular, the UV-C irradiation of the surfaces has been proven to be effective against pathogens infecting hospital environments [8]. The Commission Internationale d’Eclarage (CIE) established the dependence of the germicidal effect on wavelength [] with a peak effectiveness at 270 nm. To date, the most widely used wavelength is the 254 nm peak obtained from mercury discharge lamps. However, it is well established that the lethal UV dose for most pathogens is higher than the energy level to which humans can be safely exposed [29] thus requiring special precautions to avoid human irradiation.
In our study, the irradiation was limited to air in the room that was circulated between the UV-C sources. The filtered air was then reintroduced as cleaned air into the room. Little is known about the dose of UV necessary to achieve at least a 2-log10 reduction when surfaces are directly irradiated [24]. In a randomized clinical trial, Anderson et al., [30]
confirmed that UV light was able to decrease the environmental bioburden of MRSA, VRE, C. difficile, and Acinetobacter spp. However, hospital rooms with complicated surfaces, which included a variety of items (i.e., doors, shelves, radiators, ceilings and walls) or surfaces that were frequently touched, such as handles, buttons, switches and computer keyboards, required specific treatments. In the direct irradiation of these items, it was very difficult to assess the actual energy delivered. Therefore, the use of UV alone for disinfection remains uncertain. As a result, there has been interest in decontamination systems, such as gaseous disinfectants like hydrogen peroxide and ozone. The latter is a potent oxidizing agent, which is highly effective against C. difficile spores. Ozone treatment and its use has been previously discussed to overcome challenges emerging during the COVID-19 pandemic []. Sharma et al. demonstrated that a wide range of Gram-positive and Gram-negative bacteria, including spores and Mycobacterium species were susceptible to ozone when it was used at a level of 25 ppm for 20 min in a controlled humidity condition [18].
In a recent 2022 study from Bong et al., the efficacy of ozone was tested against VRE and CRAB when this agent was used at 500 ppm for 15 min 
[]. In our study, the decrease in the number of pathogens and the effectiveness of air treatment using UV-C in combination with ozone in actual hospital environments (gyms and rooms) was evaluated. The combination of UV light and ozone was also studied to assess the ozone level that could kill bacterial strains, yeast and moulds. We determined that a 6-ppm ozone level delivered for 1 h in combination with UV-C air sanitization after the daily cleaning procedures with detergents was effective against the most common pathogens. Furthermore, this level did not pose as a hazard for damaging fabrics and surfaces. Because laboratory testing performed in test chambers does not necessarily predict what actually happens on real hospital surfaces, the results obtained here are useful to confirm the results previously reported in test chambers. These studies [18][20] described the capability of ozone of killing CRAB and C. difficile spores using this oxidizing agent at higher doses (25 and 500 ppm) for shorter times than those used in our study.
For MRSA, Klebsiella spp., P. aeruginosaC. difficile and Acinetobacter spp., we obtained more than a 2-log10 reduction using ozone at a 6-ppm level for 1 h. Thus, in order to decrease contamination and reduce healthcare-associated infections, after the removing of soil contamination, ozone was shown to be applicable in both hospital settings and clinical environments. Moreover, we observed that the addition of chemical compounds (i.e., disinfectants), whose toxicity may be harmful not only to patients but also to healthcare personnel, was not crucial to obtaining a significant HAI reduction.
However, there are limitations to this study. We evaluated UV-C air treatment combined with ozone antiseptic effect over an experimental time of 3 weeks. This might result in preliminary outcomes that are difficult to generalize to all hospital settings. A more prolonged study design is in progress to define whether the reduction of pathogen concentrations is possibly related to the incidence of HAIs. Moreover, in agreement with Otter et al. [31], further data are needed to evaluate not only the applicability but also the cost-effectiveness of NTD systems in comparison with conventional cleaning procedures.
In conclusion, the present study showed the effectiveness of ozone in a synergistic combination with UV-C air treatment because this oxidative process was shown to decrease the concentration of the most common healthcare-associated pathogens in LR and HR areas. Furthermore, the results underlined that manual cleaning methods had a limited efficacy in reducing the bioburden of pathogens in healthcare environments. Combining air sanitization with UV-C and ozone diffusion, the OZY AIR+LIGHT device provided more than the necessary 2-log10 reduction of pathogens. This no-touch system of a new generation has been shown to be superior to other disinfectants in terms of practicability and safety for hospital personnel in different settings previously occupied by colonized patients, with not only common pathogens but also C. difficile spores and multi-drug-resistant Pseudomonas spp.
 
 

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Article info

Conflict of interest statement:
The authors declare no conflicts of interest

Funding:
this work was partially supported by the Ricerca Corrente funding scheme of the Italian Ministry of Health, Italy

Publication history:
Published online: July 19, 2023
Accepted: June 25, 2023
Received: April 27, 2023

Identification:
DOI: https://doi.org/10.1016/j.jhin.2023.06.029

Copyright: © 2023 The Authors. Published by Elsevier Ltd on behalf of The Healthcare Infection Society.

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