dgkh000462
10.3205/dgkh000462
urn:nbn:de:0183-dgkh0004621
Research Article
Can the adenosine triphosphate (ATP) bioluminescence assay be used as an indicator for hospital cleaning? – A pilot study
Kann die Adenosintriphosphat (ATP)-Biolumineszenzmethode als Reinigungsindikator im Krankenhaus eingesetzt werden? – Eine Pilotstudie
Niephaus
Niephaus
Valerie
V
Dr. med.
Evang. Kliniken Essen-Mitte, Henricistr. 92, 45136 Essen, GermanyPhone: +49 201 174 25020Evang. Kliniken Essen-Mitte, Essen, Germany
valerieniephaus@gmx.de
author
Parohl
Parohl
Nina
N
HyKoMed GmbH, Dortmund, Germany
author
Heiligtag
Heiligtag
Sabine
S
3M Deutschland GmbH, Neuss, Germany
author
Reuter
Reuter
Henning
H
3M Deutschland GmbH, Neuss, Germany
author
Hackler
Hackler
Reiner
R
3M Deutschland GmbH, Neuss, Germany
author
Popp
Popp
Walter
W
HyKoMed GmbH, Dortmund, Germany
author
German Medical Science GMS Publishing House
Düsseldorf
610
ATP
adenosine triphosphate bioluminescence
hospital cleaning
cleaning monitoring
healthcare-associated infections
ATP
Adenosintriphosphat Biolumineszenz-Methode
Krankenhausreinigung
nosokomiale Infektionen
Reinigungsüberwachung
20240221
engl
This is an Open Access article distributed under the terms of the Creative Commons Attribution 4.0 License.
Dieser Artikel ist ein Open-Access-Artikel und steht unter den Lizenzbedingungen der Creative Commons Attribution 4.0 License (Namensnennung).
2196-5226
19
GMS Hygiene and Infection Control
GMS Hyg Infect Control
07
Hintergrund: In der Krankenhausreinigung gibt es weder in Deutschland noch international derzeit einen Standard für ein einheitliches Monitoring der Flächenreinigung. Eine Möglichkeit der objektiven Kontrolle ist der Einsatz sog. objektiver Methoden zur Überprüfung der Reinigungsleistung, z.B. mit der Fluoreszenz- oder Adenosintriphosphat (ATP)-Methode.Zielsetzung: Ziel der Studie war die Implementierung der ATP-Biolumineszenz-Methode als Reinigungsindikator im Krankenhausalltag und die Bewertung deren Aussagekraft. Methoden: In 3 Phasen wurden 5 häufig angefasste Oberflächen zu verschiedenen Zeitpunkten untersucht. In Phase 1 wurden 846 Messungen auf der dermatologischen Station einer Universitätsklinik, in Phase 2 1.350 Messungen auf fünf verschiedenen Stationen der Universitätsklinik und in Phase 3 1.044 Messungen auf 5 Stationen eines anderen großen Krankenhauses durchgeführt. Für Phase 2 und 3 wurden jeweils eine baulich alte und neue Station sowie eine Intensivstation, Ambulanz und Röntgenabteilung ausgewählt.Ergebnisse: Die ATP-Biolumineszenz-Methode konnte eine Reduktion der Werte nach der Reinigung (vor der Reinigung ATP-Mittelwert (M) 907 RLU; 95% Konfidenzintervall (CI) 777; 1.038, nach der Reinigung M=286 RLU; CI=233; 495) (Phase 1) nachweisen sowie durch die Intervention 5 h nach der täglichen Reinigung (M=360 RLU (CI=303; 428); 5 h nach täglicher Reinigung und zweimaliger zusätzlicher Reinigung M=128 RLU, CI=107; 152) (Phase 3). Die ATP-Werte stiegen 5 h (Phase 1 und 2) bzw. 8 h nach der Reinigung wieder an (Phase 3). Die baulich alten Stationen wiesen den höchsten ATP-Gehalt auf, die Intensivstationen und die Röntgenabteilungen u.a. den niedrigsten. Die Türklinke wies in allen Phasen sowohl eine Reduktion nach Reinigung bzw. Intervention als auch einen nachfolgenden Anstieg der ATP-Werte auf. Die Stuhlarmlehne, die Ambulanzliege und der Türgriff wiesen insgesamt hohe ATP-Werte auf.Fazit: Die Studie kann Stationsunterschiede sowohl für Reinigungseffekte als auch für die Verschmutzung von Oberflächen im Tagesverlauf aufzeigen. Darüber hinaus weist sie den positiven Nutzen einer zweimaligen Zwischenreinigung nach. Auffallend ist, dass baulich alte Stationen und älteres Inventar stärker verschmutzen und zum Teil schwieriger zu reinigen sind. Die Ergebnisse zeigen, dass die ATP-Biolumineszenz-Methode zum Nachweis von Reinigungseffekten geeignet ist und im Klinikalltag zur einfachen Reinigungskontrolle eingesetzt werden kann. Darüber hinaus ermöglicht sie die Bestimmung von Risikoflächen bzw. leicht zu reinigenden Flächen mit erheblicher Wiederverschmutzung.
Background: In hospital cleaning, there is currently no standard for uniform monitoring of surface cleaning, either in Germany or internationally. One possibility for monitoring is the use of so-called objective methods for checking cleaning performance (e.g. fluorescence or adenosine triphosphate (ATP) method).Aim: The aim of the study was to monitor and evaluate the implementation of the adenosine triphosphate (ATP) bioluminescence assay as a cleaning indicator in everyday hospital cleaning, in order to verify its utility and effectiveness.Methods: In three phases, five frequently touched surfaces were examined with the ATP bioluminescence assay at different time points. 846 measurements were performed on the dermatology ward of <![CDATA[a u</PlainText></TextGroup>niversity hospital (phase 1), 1,350 measurements were performed on five different wards of the university hospital (phase 2), and 1,04<TextGroup><PlainText>4 m</PlainText></TextGroup>easurements were performed on five wards of another large hospital (phase 3). For this purpose, one structurally old and one structurally new ward as well as an intensive care unit (ICU), an outpatient clinic and a radiology department were selected for phases 2 and 3.</Pgraph><Pgraph><Mark1>Results:</Mark1> With the ATP bioluminescence method, we were able to demonstrate a reduction in values after cleaning: before cleaning mean of ATP, 907 relative light units (RLU) (95% confidence interval [CI] 77<TextGroup><PlainText>7; 1</PlainText></TextGroup>,038); after cleaning mean=286 RLU (CI=233; 495) (phase 1) and by intervention (five hours after daily cleaning mean=360 RLU (CI=303; 428); five hours after daily cleaning and two additional cleanings mean=128 RLU (CI=107; 152) (phase 3). The ATP values increased five hours after cleaning in phases 1 and 2, and eight hours after cleaning in phase 3. The structurally old wards had the highest ATP content, the ICU and the radiology department, among others, the lowest. In all phases, door handles showed both a reduction after cleaning or intervention and a subsequent increase in ATP values. Chair armrests, examination tables and door handles had high ATP values overall.</Pgraph><Pgraph><Mark1>Conclusion:</Mark1> The study shows ward differences both for cleaning effects and for the soiling characteristics of surfaces during the course of the day. In addition, it demonstrates the benefit of intermediate cleaning twice a day. It is noteworthy that structurally old stations and older inventory were more heavily soiled and, in some cases, more difficult to clean. </Pgraph><Pgraph>The results show that the ATP bioluminescence method is suitable for detecting cleaning effects and can be used in everyday clinical practice for simple cleaning monitoring. Furthermore, it enables the detection of risk surfaces and easy-to-clean surfaces with significant re-soiling. </Pgraph></Abstract>
<TextBlock linked="yes" name="Introduction">
<MainHeadline>Introduction</MainHeadline><Pgraph>Nosocomial infections with multidrug-resistant pathogens (MDRO) are a major problem for many hospitals, due to the more complicated therapy, the increased length of stay and high costs for the healthcare system <TextLink reference="1"></TextLink>. Environmental cleaning, especially of surfaces close to patients, is of great importance for the prevention of nosocomial infections <TextLink reference="2"></TextLink>, <TextLink reference="3"></TextLink>. In addition to direct personal contact, contaminated objects are also vectors for pathogens <TextLink reference="4"></TextLink>. There are already many interventions to reduce nosocomial infections, such as hand antisepsis campaigns and standardised procedures <TextLink reference="5"></TextLink>, <TextLink reference="6"></TextLink>, <TextLink reference="7"></TextLink>.</Pgraph><Pgraph>However, surface disinfection is still given too little importance in the daily routine of many hospitals, although recent studies show that hospital-acquired infections can result from contaminated surfaces, especially close to patients <TextLink reference="8"></TextLink>, <TextLink reference="9"></TextLink>, <TextLink reference="10"></TextLink>. Therefore, it is necessary to implement objective methods for cleaning monitoring in hospitals. One of these is the adenosine triphosphate (ATP) bioluminescence assay, which has been established in hygiene research for many years. It should be mentioned that guidelines and recommendations for cleaning monitoring have been published in the meantime. For this purpose, DIN 13063 and the Commission for Hospital Hygiene and Vaccination Prevention (KRINKO for short) specify the use of objective methods <TextLink reference="10"></TextLink>, <TextLink reference="11"></TextLink>. Based on this, the present study reviews the applicability of the ATP bioluminescence method as cleaning monitoring in daily hospital practice.</Pgraph></TextBlock>
<TextBlock linked="yes" name="Method">
<MainHeadline>Method</MainHeadline><Pgraph>In 3 phases, frequently touched surfaces were examined by means of ATP measurements from January 2015 to August 2016 in two different hospitals in a German city. Prior to this, these surfaces were selected by inspection of the wards, provided they had been cleaned by the cleaning staff. Different disinfectants were used for surface disinfection, such as Perform<Superscript>®</Superscript> 0.5% (Schülke & Mayr GmbH, active agent: active oxygen, spectrum of activity: bactericidal, levurocidal, fungicidal, virucidal, sporicidal), Incidin™ Plus 0.5% (Ecolab Deutschland GmbH, active agent: Glucoprotamin™, spectrum of activity: bactericidal, levurocidal, virucidal, tuberculocidal, mycobactericidal) (phase 1 and 2) and Terralin<Superscript>®</Superscript> Protect 0.5% (Schülke & Mayr GmbH, active agent: quaternary ammonium compounds; spectrum of activity: bactericidal, levurocidal, tuberculocidal and virucidal at low load) (phase 3). The exposure time may be varied for the respective cleaning effect. The disinfectants have shown an influence on the results of the ATP measurements <TextLink reference="12"></TextLink>, <TextLink reference="13"></TextLink>, <TextLink reference="14"></TextLink>. Sampling was done only after the surface was completely dry to eliminate the influence of disinfectant residues.</Pgraph><Pgraph>The cleaning staff was informed about the study. Each sampled room was occupied by at least one patient. The aim was to determine the cleaning effect and factors influencing soiling development during the course of the day by ATP measurement.</Pgraph><SubHeadline>Phase 1</SubHeadline><Pgraph>On each of four days, six frequently touched surfaces were examined in 10 rooms of the dermatology ward of a university hospital. Samples were taken before, immediately after and five hours after daily cleaning. A total of 846 measurements were taken by two samplers.</Pgraph><SubHeadline>Phase 2</SubHeadline><Pgraph>The focus was on surface measurements from five wards with different requirements. On five days, on five frequently touched surfaces, a total of 1,350 measurements were taken by a sampler 15 minutes after daily cleaning and five hours afterwards. A structurally old ward (urology), a structurally new ward (trauma surgery), an outpatient clinic (trauma surgery outpatient clinic), a radiology department and an intensive care unit were selected. The order of the surface measurements per room was randomised.</Pgraph><SubHeadline>Phase 3</SubHeadline><Pgraph>The focus was to prove the effect of an intervention and the applicability of the ATP bioluminescence method on five wards in another large hospital in Essen. For this purpose, a total of 1,044 measurements were taken weekly by one sampler on a control day and an intervention day. On intervention days, an additional intermediate cleaning of the surfaces took place 1.5 hours and three hours after the daily cleaning. </Pgraph><Pgraph>There was always a rest day between the control day and the intervention day. Therefore, the surfaces were examined immediately after cleaning and five and eight hours afterwards. </Pgraph><Pgraph>Two rooms each in the oncology ward as a structurally old ward, the private ward as a structurally new ward, and the multidisciplinary emergency unit as an outpatient department, were studied in three weeks. The intensive care unit with three rooms was also examined for three weeks. The radiology’s only X-ray room was assessed for six weeks.</Pgraph><SubHeadline>Samplings</SubHeadline><Pgraph>For sampling, 3M™ Clean-Trace™ ATP surface tests and the 3M™ Clean-Trace™ NGi luminometer were used according to the manufacturer’s instructions. The samplers also received training from a 3M™ Deutschland GmbH employee on the proper use of the surface tests and the luminometer. Templates of 4x4 cm and 8x2 cm were used for sampling to obtain a standardised area of 1<TextGroup><PlainText>6 c</PlainText></TextGroup>m².</Pgraph><SubHeadline>Statistical analysis</SubHeadline><Pgraph>Statistical analysis was performed using Minitab 17 (Minitab Inc., State College, Pennsylvania, USA). Descriptive statistics were presented using box-plot and interval plots. Inductive statistics were performed using generalised linear mixed models (GLM) to determine significant differences between means of ATP content (dependent variable) for fixed factors (e.g., time, surface, ward, room, intervention). p<0.1 was considered statistically significant, as determined by the overall F-test and t-distribution. The raw data were not normally distributed, so they were transformed using log-normal distribution. The analysis was based on replacing outliers that were three standard deviations away from the expected value µ, calculated by the model. Only significant terms were used for the model <TextLink reference="15"></TextLink>.</Pgraph></TextBlock>
<TextBlock linked="yes" name="Results">
<MainHeadline>Results</MainHeadline><SubHeadline>Phase 1</SubHeadline><Pgraph>The factor “time” had the greatest influence on the ATP content, with a decrease after cleaning and an increase five hours afterwards (afternoon) (Table 1 <ImgLink imgNo="1" imgType="table"/>). Table 2 <ImgLink imgNo="2" imgType="table"/> and Figure 1 <ImgLink imgNo="1" imgType="figure"/> give an overview of ATP values for the point of time and surfaces. Chair armrests had the highest average ATP content. The greatest reduction in ATP values was found for door handles. Five hours after cleaning, the greatest increase over the course of the day was also found for door handles; these changes were significantly different. There was a significant difference between the investigators. This effect was only significant for the time before cleaning, but not after cleaning. The analysis showed no significant difference between the cleaners. The factor “room number” showed a large range of mean values. </Pgraph><SubHeadline>Phase 2</SubHeadline><Pgraph>The ATP content increased five hours after cleaning. There were clear ward differences. The structurally old urology ward had the highest ATP content. The outpatient department and the structurally new trauma surgery ward had a significantly lower ATP content. The lowest values were found for the ICU and radiology department (Figure 2 <ImgLink imgNo="2" imgType="figure"/>). </Pgraph><Pgraph>For all wards, an increase in values was found five hours after cleaning. This increase varied and was highest for the outpatient department and lowest for the radiology department (Table 3 <ImgLink imgNo="3" imgType="table"/>).</Pgraph><Pgraph>In phase 2, there were surfaces with high ATP values, such as door handles, chair armrests (trauma surgery and urology ward) and examination tables (outpatient clinic). Overall, door handles also exhibited a high increase in values five hours after cleaning. </Pgraph><SubHeadline>Phase 3</SubHeadline><Pgraph>The intervention group had a significantly reduced ATP content compared to the control group (Table 4 <ImgLink imgNo="4" imgType="table"/>). On control days, the values increased continuously, in contrast to the values on intervention days. There, a significant reduction of the ATP content with a subsequent increase observed after the intervention. Figure 3 <ImgLink imgNo="3" imgType="figure"/> illustrates the difference between control and intervention group for the point of time.</Pgraph><Pgraph>In the intervention group, the ATP values of the wards converged, and the value differences decreased. Compared to the control group, a reduction of the standard deviations and standard errors was noticeable in the intervention group. </Pgraph><Pgraph>The structurally old oncology ward and the outpatient clinic had significantly higher ATP values than the other wards. In particular, chair surfaces and table tops (oncology) as well as examination couch (outpatient department) had high ATP values. For door handles, the ATP content increased most significantly after the intervention, up to 8 hours after daily cleaning.</Pgraph></TextBlock>
<TextBlock linked="yes" name="Discussion">
<MainHeadline>Discussion</MainHeadline><Pgraph>Like other studies, we were able to demonstrate the positive effect of both daily cleaning <TextLink reference="16"></TextLink>, <TextLink reference="17"></TextLink>, <TextLink reference="18"></TextLink>, <TextLink reference="19"></TextLink> and an intervention <TextLink reference="20"></TextLink>, <TextLink reference="21"></TextLink>, <TextLink reference="22"></TextLink> on surface contamination using the ATP bioluminescence method. An interesting aspect is offered by Smith et al. <TextLink reference="23"></TextLink>, who were able to demonstrate a post-intervention effect even after a washout phase. Their results show not only the short-term, but also and especially the long-term effect of an intervention program. In our study, there was no longer-term follow-up. However, it does show the lasting effect of the intervention over the course of the day. Furthermore, as in our case, there is a reduction in variability due to the intervention <TextLink reference="24"></TextLink>. Thus, the method may serve to improve and monitor existing cleaning practices in terms of reducing nosocomial infections as a continuing health risk <TextLink reference="25"></TextLink>.</Pgraph><Pgraph>Moreover, we were able to identify risk surfaces with different cleaning requirements. On the one hand, door handles, cupboard handles and chair surfaces were easy to clean. Other authors also describe an ATP reduction for door handles after cleaning <TextLink reference="3"></TextLink> or through an intervention (3 periods, cleaning monitoring by fluorescence markers, additional UV cleaning and enhanced cleaning after the use of ATP bioluminescence measurements) <TextLink reference="26"></TextLink>. In addition, we found a significant increase in contamination over the course of the day for door handles in all three phases. An unrealistic option is more frequent intermediate cleaning of such surfaces. If the 5 WHO moments of hand antisepsis are followed, these potential infection routes for staff can be interrupted. On the other hand, there were surfaces with more difficult cleaning characteristics and overall high contamination. Other authors also documented such surfaces <TextLink reference="3"></TextLink>, <TextLink reference="17"></TextLink>, <TextLink reference="19"></TextLink>, <TextLink reference="27"></TextLink>. These can have a considerable influence on the ward level. For the oncology chair surface, there is hardly any effect of the intervention, despite correctly performed cleaning. This may be due to potentially porous, scratched and long-stressed surface materials <TextLink reference="28"></TextLink>. For surfaces with structurally demanding cleaning characteristics, the choice of disinfectant and detergent <TextLink reference="29"></TextLink>, cleaning cloth and application of mechanical force is important <TextLink reference="22"></TextLink>, <TextLink reference="30"></TextLink>. However, one should not draw conclusions from one surface contamination to the contamination of other surfaces of a whole room or ward <TextLink reference="21"></TextLink>. In particular, heavily contaminated surfaces should be investigated as to their nature and cleaning method. To ensure the cleaning or disinfecting cleaning of surfaces, the Commission for Hospital Hygiene and Infection Prevention (KRINKO) at the Robert Koch Institute Berlin recommends that hygienically relevant surfaces are to be cleaned and disinfected safely and that no material damage be caused by the cleaning or disinfecting surface cleaning. Before purchasing new items, e.g., floor coverings and furniture, it is recommended that the manufacturer confirm the material compatibility regarding disinfectability <TextLink reference="10"></TextLink>. The KRINKO and its voluntary work are legitimised by the mandate according to § 23 of the German Infection Protection Act to establish binding principles and standards for prevention measures. Adjustments in cleaning procedures, especially mechanics and duration, may need to be made and surface material may need to be replaced. It is also important to sensitize cleaning, nursing and medical staff to the cleaning of such surfaces.</Pgraph><Pgraph>In phases 2 and 3, the structurally old wards (urology ward, oncology ward) with the comparatively oldest inventory had the highest ATP values. The intensive care units and radiology departments, on the other hand, had the lowest ATP values. Possible reasons could be a fixed room allocation, greater motivation <TextLink reference="21"></TextLink> of the nursing staff, as well as more frequent intermediate cleaning. Other authors also found lower ATP values for intensive care units <TextLink reference="22"></TextLink>, <TextLink reference="31"></TextLink>. In our study, there were clear differences between the wards during the course of the day, which also have different levels of contamination due to full occupancy and increased patient turnover, among other factors <TextLink reference="6"></TextLink>. For example, the outpatient department in phase 2 showed the greatest increase in contamination, while ATP values in phase 3 decreased on control days. It should be noted that due to different work structures and differing ward requirements, a direct comparison between wards, hospitals, countries and even surfaces is difficult <TextLink reference="32"></TextLink>. Furthermore, we have not determined any benchmark for the purity classification, as no generally applicable benchmark has been found so far <TextLink reference="27"></TextLink>, <TextLink reference="33"></TextLink>, <TextLink reference="34"></TextLink>. Therefore, like other authors, we recommend determining the internal limits for each hospital individually <TextLink reference="22"></TextLink>, <TextLink reference="35"></TextLink>.</Pgraph><Pgraph>We found that at least before cleaning, the sampling persons showed a significant difference (phase 1). Therefore, we conducted the further measurements with only one sampler, as Knape et al. <TextLink reference="21"></TextLink> did, to reduce the systematic error. Moreover, we found that all cleaners had similar cleaning efficiencies. This indicates a standardised cleaning protocol. Its application and adaptation contribute significantly to the improvement of surface cleaning <TextLink reference="36"></TextLink>, <TextLink reference="37"></TextLink>. Another reason is the Hawthorne effect, as all cleaners were informed about the study in advance.</Pgraph><Pgraph>We did not conduct microbiological examinations of the surfaces, as many previous studies have shown little or no correlation with the ATP bioluminescence assay <TextLink reference="17"></TextLink>, <TextLink reference="18"></TextLink>, <TextLink reference="19"></TextLink>, <TextLink reference="38"></TextLink>, <TextLink reference="39"></TextLink>. It should be noted that the determination of ATP only quantitatively measures organic material without any differentiation, even between viable and non-viable organisms <TextLink reference="40"></TextLink>. It can be concluded that the measurement of ATP can verify the effectiveness of purification, but not determine the prevailing microbial load.</Pgraph><Pgraph>In addition to many non-detectable influencing factors on surface purity in the hospital, however, there are also various influencing factors as a limitation of the ATP bioluminescence method. Among other things, this results in high variability, which we as well as other authors documented <TextLink reference="19"></TextLink>, <TextLink reference="27"></TextLink>, <TextLink reference="28"></TextLink>, <TextLink reference="37"></TextLink>, <TextLink reference="41"></TextLink>. The choice of disinfectant can also influence the ATP results <TextLink reference="12"></TextLink>, <TextLink reference="25"></TextLink>, <TextLink reference="32"></TextLink>. Therefore, one should not use different disinfectants in comparisons <TextLink reference="13"></TextLink>. However, in addition to detergent and disinfectant residues, ATP measurements can also be influenced by worn surfaces, softeners, microfiber cloths and ammonium compounds in detergents <TextLink reference="42"></TextLink>. Considering various factors, comparability between studies and hospitals is difficult, also due to significant differences in study designs, diverse hospital structures and requirements <TextLink reference="25"></TextLink>.</Pgraph></TextBlock>
<TextBlock linked="yes" name="Conclusion">
<MainHeadline>Conclusion</MainHeadline><Pgraph>Our results allow the evaluation of the ATP bioluminescence method for routine monitoring of cleaning in different hospitals. It is fast, cost-effective and useful for assessing interventions, but high readings do not indicate a risk of infection for patients <TextLink reference="42"></TextLink>. ATP measurements offer a major advantage in their ease of use and they can provide quick feedback through self-application, highlight potential cleaning deficits and thus increase cleaning performance and staff motivation. In addition, risk surfaces are highlighted and can be examined more closely for their condition and cleaning requirements. However, before implementing the ATP bioluminescence assay, we recommend that each hospital establish its own reference values to determine individual contamination levels and associated benchmarks. </Pgraph><Pgraph>In summary, our study confirms the use of the ATP bioluminescence method for cleaning assessment in hospitals, in accordance with current studies <TextLink reference="34"></TextLink>, <TextLink reference="35"></TextLink>. The efficiency of a cleaning process, surface-specific effects and the evaluation of existing cleaning protocols can be shown by ATP measurements and allow direct interpretation considering various influencing factors.</Pgraph><Pgraph>According to Ferreira et al. <TextLink reference="43"></TextLink>, the fluorescence method and the optical control are well suited for monitoring compliance with the cleaning specifications, while methods that check the microbiological load give a better indication of an actual risk of infection and the effectiveness of the disinfection. Irrespective of the use of a measuring method, the observation of process sequences by means of a checklist is necessary to assess the quality of disinfecting surface cleaning. The repeat intervals must be set according to the results of the audit. If monitoring is used specifically to improve quality, the choice of method is secondary <TextLink reference="10"></TextLink>.</Pgraph></TextBlock>
<TextBlock linked="yes" name="Notes">
<MainHeadline>Notes</MainHeadline><SubHeadline>Author’s ORCID</SubHeadline><Pgraph><UnorderedList><ListItem level="1">Valerie Niephaus: <Hyperlink href="https://orcid.org/0009-0005-5526-2539">0009-0005-5526-2539</Hyperlink></ListItem></UnorderedList></Pgraph><SubHeadline>Competing interests</SubHeadline><Pgraph>The study was financially supported by 3M Germany, Neuss, Germany. Three authors are employed by 3M Germany, Neuss, Germany.</Pgraph></TextBlock>
<References linked="yes">
<Reference refNo="1">
<RefAuthor>Oberdörfer H</RefAuthor>
<RefAuthor>Hübner C</RefAuthor>
<RefAuthor>Linder R</RefAuthor>
<RefAuthor>Fleßa S</RefAuthor>
<RefTitle>Mehrkosten bei der Versorgung von Patienten mit multiresistenten Erregern--Eine Analyse aus Sicht einer gesetzlichen Krankenversicherung</RefTitle>
<RefYear>2015</RefYear>
<RefJournal>Gesundheitswesen</RefJournal>
<RefPage>854-60</RefPage>
<RefTotal>Oberdörfer H, Hübner C, Linder R, Fleßa S. Mehrkosten bei der Versorgung von Patienten mit multiresistenten Erregern--Eine Analyse aus Sicht einer gesetzlichen Krankenversicherung [Additional Costs for Care of Patients with Multi-Resistant Pathogens--An Analysis from the Perspective of a Statutory Health Insurance]. Gesundheitswesen. 2015 Nov;77(11):854-60. German. DOI: 10.1055/s-0034-1387709</RefTotal>
<RefLink>https://doi.org/10.1055/s-0034-1387709</RefLink>
</Reference>
<Reference refNo="2">
<RefAuthor>Han JH</RefAuthor>
<RefAuthor>Sullivan N</RefAuthor>
<RefAuthor>Leas BF</RefAuthor>
<RefAuthor>Pegues DA</RefAuthor>
<RefAuthor>Kaczmarek JL</RefAuthor>
<RefAuthor>Umscheid CA</RefAuthor>
<RefTitle>Cleaning Hospital Room Surfaces to Prevent Health Care-Associated Infections: A Technical Brief</RefTitle>
<RefYear>2015</RefYear>
<RefJournal>Ann Intern Med</RefJournal>
<RefPage>598-607</RefPage>
<RefTotal>Han JH, Sullivan N, Leas BF, Pegues DA, Kaczmarek JL, Umscheid CA. Cleaning Hospital Room Surfaces to Prevent Health Care-Associated Infections: A Technical Brief. Ann Intern Med. 2015 Oct 20;163(8):598-607. DOI: 10.7326/M15-1192</RefTotal>
<RefLink>https://doi.org/10.7326/M15-1192</RefLink>
</Reference>
<Reference refNo="3">
<RefAuthor>Al-Hamad A</RefAuthor>
<RefAuthor>Maxwell S</RefAuthor>
<RefTitle>How clean is clean? Proposed methods for hospital cleaning assessment</RefTitle>
<RefYear>2008</RefYear>
<RefJournal>J Hosp Infect</RefJournal>
<RefPage>328-34</RefPage>
<RefTotal>Al-Hamad A, Maxwell S. How clean is clean? Proposed methods for hospital cleaning assessment. J Hosp Infect. 2008 Dec;70(4):328-34. DOI: 10.1016/j.jhin.2008.08.006</RefTotal>
<RefLink>https://doi.org/10.1016/j.jhin.2008.08.006</RefLink>
</Reference>
<Reference refNo="4">
<RefAuthor>Russotto V</RefAuthor>
<RefAuthor>Cortegiani A</RefAuthor>
<RefAuthor>Raineri SM</RefAuthor>
<RefAuthor>Giarratano A</RefAuthor>
<RefTitle>Bacterial contamination of inanimate surfaces and equipment in the intensive care unit</RefTitle>
<RefYear>2015</RefYear>
<RefJournal>J Intensive Care</RefJournal>
<RefPage>54</RefPage>
<RefTotal>Russotto V, Cortegiani A, Raineri SM, Giarratano A. Bacterial contamination of inanimate surfaces and equipment in the intensive care unit. J Intensive Care. 2015 Dec 10;3:54. DOI: 10.1186/s40560-015-0120-5</RefTotal>
<RefLink>https://doi.org/10.1186/s40560-015-0120-5</RefLink>
</Reference>
<Reference refNo="5">
<RefAuthor>Kampf G</RefAuthor>
<RefAuthor>Löffler H</RefAuthor>
<RefAuthor>Gastmeier P</RefAuthor>
<RefTitle>Hand hygiene for the prevention of nosocomial infections</RefTitle>
<RefYear>2009</RefYear>
<RefJournal>Dtsch Arztebl Int</RefJournal>
<RefPage>649-55</RefPage>
<RefTotal>Kampf G, Löffler H, Gastmeier P. Hand hygiene for the prevention of nosocomial infections. Dtsch Arztebl Int. 2009 Oct;106(40):649-55. DOI: 10.3238/arztebl.2009.0649</RefTotal>
<RefLink>https://doi.org/10.3238/arztebl.2009.0649</RefLink>
</Reference>
<Reference refNo="6">
<RefAuthor>Mielke M</RefAuthor>
<RefAuthor>Werner G</RefAuthor>
<RefAuthor>Pfeiffer Y</RefAuthor>
<RefAuthor>Witte W</RefAuthor>
<RefTitle></RefTitle>
<RefYear>2011</RefYear>
<RefBookTitle>Das Problem der nosokomialen Infektionen und Antibiotikaresistenz</RefBookTitle>
<RefPage></RefPage>
<RefTotal>Mielke M, Werner G, Pfeiffer Y, Witte W. Das Problem der nosokomialen Infektionen und Antibiotikaresistenz. Robert Koch-Institut; 2011 Mar. Available from: https://www.rki.de/DE/Content/Infekt/Krankenhaushygiene/Nosokomiale_Infektionen/Downloads/Uebersicht_NI.pdf?__blob=publicationFile</RefTotal>
<RefLink>https://www.rki.de/DE/Content/Infekt/Krankenhaushygiene/Nosokomiale_Infektionen/Downloads/Uebersicht_NI.pdf?__blob=publicationFile</RefLink>
</Reference>
<Reference refNo="7">
<RefAuthor>Geffers C</RefAuthor>
<RefTitle>Änderungen bei den Definitionen für nosokomiale Infektionen im Krankenhaus-Infektions-Surveillance-System (KISS)</RefTitle>
<RefYear>2017</RefYear>
<RefJournal>Epid Bull</RefJournal>
<RefPage>207–12</RefPage>
<RefTotal>Geffers C. Änderungen bei den Definitionen für nosokomiale Infektionen im Krankenhaus-Infektions-Surveillance-System (KISS). Epid Bull. 2017 Jun 8;23:207–12. DOI: 10.17886/EpiBull-2017-031</RefTotal>
<RefLink>https://doi.org/10.17886/EpiBull-2017-031</RefLink>
</Reference>
<Reference refNo="8">
<RefAuthor>Geffers C</RefAuthor>
<RefAuthor>Gastmeier P</RefAuthor>
<RefAuthor>Rüden H</RefAuthor>
<RefTitle></RefTitle>
<RefYear>2002</RefYear>
<RefBookTitle>Nosokomiale Infektionen</RefBookTitle>
<RefPage></RefPage>
<RefTotal>Geffers C, Gastmeier P, Rüden H. Nosokomiale Infektionen. Berlin: Robert-Koch-Institut; 2002. (Gesundheitsberichterstattung des Bundes, Heft 8). Available from: https://edoc.rki.de/bitstream/handle/176904/3157/26TzxAg9BtuM_65.pdf?sequence=1&isAllowed=y</RefTotal>
<RefLink>https://edoc.rki.de/bitstream/handle/176904/3157/26TzxAg9BtuM_65.pdf?sequence=1&isAllowed=y</RefLink>
</Reference>
<Reference refNo="9">
<RefAuthor>Hayden MK</RefAuthor>
<RefAuthor>Bonten MJ</RefAuthor>
<RefAuthor>Blom DW</RefAuthor>
<RefAuthor>Lyle EA</RefAuthor>
<RefAuthor>van de Vijver DA</RefAuthor>
<RefAuthor>Weinstein RA</RefAuthor>
<RefTitle>Reduction in acquisition of vancomycin-resistant enterococcus after enforcement of routine environmental cleaning measures</RefTitle>
<RefYear>2006</RefYear>
<RefJournal>Clin Infect Dis</RefJournal>
<RefPage>1552-60</RefPage>
<RefTotal>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 Jun 1;42(11):1552-60. DOI: 10.1086/503845</RefTotal>
<RefLink>https://doi.org/10.1086/503845</RefLink>
</Reference>
<Reference refNo="10">
<RefAuthor>Anonym</RefAuthor>
<RefTitle>Anforderungen an die Hygiene bei der Reinigung und Desinfektion von Flächen: Empfehlung der Kommission für Krankenhaushygiene und Infektionsprävention (KRINKO) beim Robert Koch-Institut</RefTitle>
<RefYear>2022</RefYear>
<RefJournal>Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz</RefJournal>
<RefPage>1074-115</RefPage>
<RefTotal>Anforderungen an die Hygiene bei der Reinigung und Desinfektion von Flächen: Empfehlung der Kommission für Krankenhaushygiene und Infektionsprävention (KRINKO) beim Robert Koch-Institut. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz. 2022 Oct;65(10):1074-1115. DOI: 10.1007/s00103-022-03576-1</RefTotal>
<RefLink>https://doi.org/10.1007/s00103-022-03576-1</RefLink>
</Reference>
<Reference refNo="11">
<RefAuthor>Anonym</RefAuthor>
<RefTitle>Hospital cleaning - Requirements for cleaning and disinfection cleaning in hospitals and other health care facilities</RefTitle>
<RefYear>2021</RefYear>
<RefBookTitle>DIN 13063:2021-05: Hospital cleaning - Requirements for cleaning and disinfection cleaning in hospitals and other health care facilities</RefBookTitle>
<RefPage></RefPage>
<RefTotal>DIN 13063:2021-05: Hospital cleaning - Requirements for cleaning and disinfection cleaning in hospitals and other health care facilities. Berlin: Beuth; 2021. DOI: 10.31030/3280849</RefTotal>
<RefLink>https://doi.org/10.31030/3280849</RefLink>
</Reference>
<Reference refNo="12">
<RefAuthor>Guh A</RefAuthor>
<RefAuthor>Carling P</RefAuthor>
<RefAuthor> Environmental Evaluation Workgroup</RefAuthor>
<RefTitle></RefTitle>
<RefYear>2010</RefYear>
<RefBookTitle>Options for evaluating environmental cleaning</RefBookTitle>
<RefPage></RefPage>
<RefTotal>Guh A, Carling P; Environmental Evaluation Workgroup. Options for evaluating environmental cleaning. 2010. Available from: https://www.cdc.gov/hai/toolkits/evaluating-environmental-cleaning.html</RefTotal>
<RefLink>https://www.cdc.gov/hai/toolkits/evaluating-environmental-cleaning.html</RefLink>
</Reference>
<Reference refNo="13">
<RefAuthor>Omidbakhsh N</RefAuthor>
<RefAuthor>Ahmadpour F</RefAuthor>
<RefAuthor>Kenny N</RefAuthor>
<RefTitle>How reliable are ATP bioluminescence meters in assessing decontamination of environmental surfaces in healthcare settings? PLoS One</RefTitle>
<RefYear>2014</RefYear>
<RefTotal>Omidbakhsh N, Ahmadpour F, Kenny N. How reliable are ATP bioluminescence meters in assessing decontamination of environmental surfaces in healthcare settings? PLoS One. 2014 Jun 18;9(6):e99951. DOI: 10.1371/journal.pone.0099951</RefTotal>
<RefLink>https://doi.org/10.1371/journal.pone.0099951</RefLink>
</Reference>
<Reference refNo="14">
<RefAuthor>Lappalainen J</RefAuthor>
<RefAuthor>Loikkanen S</RefAuthor>
<RefAuthor>Havana M</RefAuthor>
<RefAuthor>Karp M</RefAuthor>
<RefAuthor>Sjöberg AM</RefAuthor>
<RefAuthor>Wirtanen G</RefAuthor>
<RefTitle>Microbial testing methods for detection of residual cleaning agents and disinfectants-prevention of ATP bioluminescence measurement errors in the food industry</RefTitle>
<RefYear>2000</RefYear>
<RefJournal>J Food Prot</RefJournal>
<RefPage>210-5</RefPage>
<RefTotal>Lappalainen J, Loikkanen S, Havana M, Karp M, Sjöberg AM, Wirtanen G. Microbial testing methods for detection of residual cleaning agents and disinfectants-prevention of ATP bioluminescence measurement errors in the food industry. J Food Prot. 2000 Feb;63(2):210-5. DOI: 10.4315/0362-028x-63.2.210</RefTotal>
<RefLink>https://doi.org/10.4315/0362-028x-63.2.210</RefLink>
</Reference>
<Reference refNo="15">
<RefAuthor>Niephaus V</RefAuthor>
<RefTitle></RefTitle>
<RefYear>2016</RefYear>
<RefBookTitle>Kann ATP als Reinigungsindikator eingesetzt werden? – Eine Pilotstudie [Dissertation]</RefBookTitle>
<RefPage></RefPage>
<RefTotal>Niephaus V. Kann ATP als Reinigungsindikator eingesetzt werden? – Eine Pilotstudie [Dissertation]. Duisburg-Essen: Universität Duisburg-Essen; 2016.</RefTotal>
</Reference>
<Reference refNo="16">
<RefAuthor>Luick L</RefAuthor>
<RefAuthor>Thompson PA</RefAuthor>
<RefAuthor>Loock MH</RefAuthor>
<RefAuthor>Vetter SL</RefAuthor>
<RefAuthor>Cook J</RefAuthor>
<RefAuthor>Guerrero DM</RefAuthor>
<RefTitle>Diagnostic assessment of different environmental cleaning monitoring methods</RefTitle>
<RefYear>2013</RefYear>
<RefJournal>Am J Infect Control</RefJournal>
<RefPage>751-2</RefPage>
<RefTotal>Luick L, Thompson PA, Loock MH, Vetter SL, Cook J, Guerrero DM. Diagnostic assessment of different environmental cleaning monitoring methods. Am J Infect Control. 2013 Aug;41(8):751-2. DOI: 10.1016/j.ajic.2012.09.019</RefTotal>
<RefLink>https://doi.org/10.1016/j.ajic.2012.09.019</RefLink>
</Reference>
<Reference refNo="17">
<RefAuthor>Smith PW</RefAuthor>
<RefAuthor>Sayles H</RefAuthor>
<RefAuthor>Hewlett A</RefAuthor>
<RefAuthor>Cavalieri RJ</RefAuthor>
<RefAuthor>Gibbs S</RefAuthor>
<RefAuthor>Rupp ME</RefAuthor>
<RefTitle>A study of three methods for assessment of hospital environmental cleaning</RefTitle>
<RefYear>2013</RefYear>
<RefJournal>Healthc Infect</RefJournal>
<RefPage>80–5</RefPage>
<RefTotal>Smith PW, Sayles H, Hewlett A, Cavalieri RJ, Gibbs S, Rupp ME. A study of three methods for assessment of hospital environmental cleaning. Healthc Infect. 2013;18(2):80–5. DOI: 10.1071/HI13001</RefTotal>
<RefLink>https://doi.org/10.1071/HI13001</RefLink>
</Reference>
<Reference refNo="18">
<RefAuthor>Mulvey D</RefAuthor>
<RefAuthor>Redding P</RefAuthor>
<RefAuthor>Robertson C</RefAuthor>
<RefAuthor>Woodall C</RefAuthor>
<RefAuthor>Kingsmore P</RefAuthor>
<RefAuthor>Bedwell D</RefAuthor>
<RefAuthor>Dancer SJ</RefAuthor>
<RefTitle>Finding a benchmark for monitoring hospital cleanliness</RefTitle>
<RefYear>2011</RefYear>
<RefJournal>J Hosp Infect</RefJournal>
<RefPage>25-30</RefPage>
<RefTotal>Mulvey D, Redding P, Robertson C, Woodall C, Kingsmore P, Bedwell D, Dancer SJ. Finding a benchmark for monitoring hospital cleanliness. J Hosp Infect. 2011 Jan;77(1):25-30. DOI: 10.1016/j.jhin.2010.08.006</RefTotal>
<RefLink>https://doi.org/10.1016/j.jhin.2010.08.006</RefLink>
</Reference>
<Reference refNo="19">
<RefAuthor>Sherlock O</RefAuthor>
<RefAuthor>O'Connell N</RefAuthor>
<RefAuthor>Creamer E</RefAuthor>
<RefAuthor>Humphreys H</RefAuthor>
<RefTitle>Is it really clean? An evaluation of the efficacy of four methods for determining hospital cleanliness</RefTitle>
<RefYear>2009</RefYear>
<RefJournal>J Hosp Infect</RefJournal>
<RefPage>140-6</RefPage>
<RefTotal>Sherlock O, O'Connell N, Creamer E, Humphreys H. Is it really clean? An evaluation of the efficacy of four methods for determining hospital cleanliness. J Hosp Infect. 2009 Jun;72(2):140-6. DOI: 10.1016/j.jhin.2009.02.013</RefTotal>
<RefLink>https://doi.org/10.1016/j.jhin.2009.02.013</RefLink>
</Reference>
<Reference refNo="20">
<RefAuthor>Chan MC</RefAuthor>
<RefAuthor>Lin TY</RefAuthor>
<RefAuthor>Chiu YH</RefAuthor>
<RefAuthor>Huang TF</RefAuthor>
<RefAuthor>Chiu SK</RefAuthor>
<RefAuthor>Liu TL</RefAuthor>
<RefAuthor>Hung PS</RefAuthor>
<RefAuthor>Chang CM</RefAuthor>
<RefAuthor>Lin JC</RefAuthor>
<RefTitle>Applying ATP bioluminescence to design and evaluate a successful new intensive care unit cleaning programme</RefTitle>
<RefYear>2015</RefYear>
<RefJournal>J Hosp Infect</RefJournal>
<RefPage>344-6</RefPage>
<RefTotal>Chan MC, Lin TY, Chiu YH, Huang TF, Chiu SK, Liu TL, Hung PS, Chang CM, Lin JC. Applying ATP bioluminescence to design and evaluate a successful new intensive care unit cleaning programme. J Hosp Infect. 2015 Aug;90(4):344-6. DOI: 10.1016/j.jhin.2015.04.008</RefTotal>
<RefLink>https://doi.org/10.1016/j.jhin.2015.04.008</RefLink>
</Reference>
<Reference refNo="21">
<RefAuthor>Knape L</RefAuthor>
<RefAuthor>Hambraeus A</RefAuthor>
<RefAuthor>Lytsy B</RefAuthor>
<RefTitle>The adenosine triphosphate method as a quality control tool to assess ‘cleanliness’ of frequently touched hospital surfaces</RefTitle>
<RefYear>2015</RefYear>
<RefJournal>J Hosp Infect</RefJournal>
<RefPage>166-70</RefPage>
<RefTotal>Knape L, Hambraeus A, Lytsy B. The adenosine triphosphate method as a quality control tool to assess ‘cleanliness’ of frequently touched hospital surfaces. J Hosp Infect. 2015 Oct;91(2):166-70. DOI: 10.1016/j.jhin.2015.06.011</RefTotal>
<RefLink>https://doi.org/10.1016/j.jhin.2015.06.011</RefLink>
</Reference>
<Reference refNo="22">
<RefAuthor>Moore G</RefAuthor>
<RefAuthor>Smyth D</RefAuthor>
<RefAuthor>Singleton J</RefAuthor>
<RefAuthor>Wilson P</RefAuthor>
<RefTitle>The use of adenosine triphosphate bioluminescence to assess the efficacy of a modified cleaning program implemented within an intensive care setting</RefTitle>
<RefYear>2010</RefYear>
<RefJournal>Am J Infect Control</RefJournal>
<RefPage>617-22</RefPage>
<RefTotal>Moore G, Smyth D, Singleton J, Wilson P. The use of adenosine triphosphate bioluminescence to assess the efficacy of a modified cleaning program implemented within an intensive care setting. Am J Infect Control. 2010 Oct;38(8):617-22. DOI: 10.1016/j.ajic.2010.02.011</RefTotal>
<RefLink>https://doi.org/10.1016/j.ajic.2010.02.011</RefLink>
</Reference>
<Reference refNo="23">
<RefAuthor>Smith PW</RefAuthor>
<RefAuthor>Beam E</RefAuthor>
<RefAuthor>Sayles H</RefAuthor>
<RefAuthor>Rupp ME</RefAuthor>
<RefAuthor>Cavalieri RJ</RefAuthor>
<RefAuthor>Gibbs S</RefAuthor>
<RefAuthor>Hewlett A</RefAuthor>
<RefTitle>Impact of adenosine triphosphate detection and feedback on hospital room cleaning</RefTitle>
<RefYear>2014</RefYear>
<RefJournal>Infect Control Hosp Epidemiol</RefJournal>
<RefPage>564-9</RefPage>
<RefTotal>Smith PW, Beam E, Sayles H, Rupp ME, Cavalieri RJ, Gibbs S, Hewlett A. Impact of adenosine triphosphate detection and feedback on hospital room cleaning. Infect Control Hosp Epidemiol. 2014 May;35(5):564-9. DOI: 10.1086/675839</RefTotal>
<RefLink>https://doi.org/10.1086/675839</RefLink>
</Reference>
<Reference refNo="24">
<RefAuthor>Griffith CJ</RefAuthor>
<RefAuthor>Obee P</RefAuthor>
<RefAuthor>Cooper RA</RefAuthor>
<RefAuthor>Burton NF</RefAuthor>
<RefAuthor>Lewis M</RefAuthor>
<RefTitle>The effectiveness of existing and modified cleaning regimens in a Welsh hospital</RefTitle>
<RefYear>2007</RefYear>
<RefJournal>J Hosp Infect</RefJournal>
<RefPage>352-9</RefPage>
<RefTotal>Griffith CJ, Obee P, Cooper RA, Burton NF, Lewis M. The effectiveness of existing and modified cleaning regimens in a Welsh hospital. J Hosp Infect. 2007 Aug;66(4):352-9. DOI: 10.1016/j.jhin.2007.05.016</RefTotal>
<RefLink>https://doi.org/10.1016/j.jhin.2007.05.016</RefLink>
</Reference>
<Reference refNo="25">
<RefAuthor>Shama G</RefAuthor>
<RefAuthor>Malik DJ</RefAuthor>
<RefTitle>The uses and abuses of rapid bioluminescence-based ATP assays</RefTitle>
<RefYear>2013</RefYear>
<RefJournal>Int J Hyg Environ Health</RefJournal>
<RefPage>115-25</RefPage>
<RefTotal>Shama G, Malik DJ. The uses and abuses of rapid bioluminescence-based ATP assays. Int J Hyg Environ Health. 2013 Mar;216(2):115-25. DOI: 10.1016/j.ijheh.2012.03.009</RefTotal>
<RefLink>https://doi.org/10.1016/j.ijheh.2012.03.009</RefLink>
</Reference>
<Reference refNo="26">
<RefAuthor>Sitzlar B</RefAuthor>
<RefAuthor>Deshpande A</RefAuthor>
<RefAuthor>Fertelli D</RefAuthor>
<RefAuthor>Kundrapu S</RefAuthor>
<RefAuthor>Sethi AK</RefAuthor>
<RefAuthor>Donskey CJ</RefAuthor>
<RefTitle>An environmental disinfection odyssey: evaluation of sequential interventions to improve disinfection of Clostridium difficile isolation rooms</RefTitle>
<RefYear>2013</RefYear>
<RefJournal>Infect Control Hosp Epidemiol</RefJournal>
<RefPage>459-65</RefPage>
<RefTotal>Sitzlar B, Deshpande A, Fertelli D, Kundrapu S, Sethi AK, Donskey CJ. An environmental disinfection odyssey: evaluation of sequential interventions to improve disinfection of Clostridium difficile isolation rooms. Infect Control Hosp Epidemiol. 2013 May;34(5):459-65. DOI: 10.1086/670217</RefTotal>
<RefLink>https://doi.org/10.1086/670217</RefLink>
</Reference>
<Reference refNo="27">
<RefAuthor>Willis C</RefAuthor>
<RefAuthor>Morley R</RefAuthor>
<RefAuthor>Westbury J</RefAuthor>
<RefAuthor>Greenwood M</RefAuthor>
<RefAuthor>Pallett A</RefAuthor>
<RefTitle>Evaluation of ATP bioluminescence swabbing as a monitoring and training tool for effective hospital cleaning</RefTitle>
<RefYear>2007</RefYear>
<RefJournal>Brit J Infect Contr</RefJournal>
<RefPage>17–21</RefPage>
<RefTotal>Willis C, Morley R, Westbury J, Greenwood M, Pallett A. Evaluation of ATP bioluminescence swabbing as a monitoring and training tool for effective hospital cleaning. Brit J Infect Contr. 2007;8(5):17–21. DOI: 10.1177/1469044607083604</RefTotal>
<RefLink>https://doi.org/10.1177/1469044607083604</RefLink>
</Reference>
<Reference refNo="28">
<RefAuthor>Griffith CJ</RefAuthor>
<RefAuthor>Cooper RA</RefAuthor>
<RefAuthor>Gilmore J</RefAuthor>
<RefAuthor>Davies C</RefAuthor>
<RefAuthor>Lewis M</RefAuthor>
<RefTitle>An evaluation of hospital cleaning regimes and standards</RefTitle>
<RefYear>2000</RefYear>
<RefJournal>J Hosp Infect</RefJournal>
<RefPage>19-28</RefPage>
<RefTotal>Griffith CJ, Cooper RA, Gilmore J, Davies C, Lewis M. An evaluation of hospital cleaning regimes and standards. J Hosp Infect. 2000 May;45(1):19-28. DOI: 10.1053/jhin.1999.0717</RefTotal>
<RefLink>https://doi.org/10.1053/jhin.1999.0717</RefLink>
</Reference>
<Reference refNo="29">
<RefAuthor>Ali S</RefAuthor>
<RefAuthor>Moore G</RefAuthor>
<RefAuthor>Wilson AP</RefAuthor>
<RefTitle>Spread and persistence of Clostridium difficile spores during and after cleaning with sporicidal disinfectants</RefTitle>
<RefYear>2011</RefYear>
<RefJournal>J Hosp Infect</RefJournal>
<RefPage>97-8</RefPage>
<RefTotal>Ali S, Moore G, Wilson AP. Spread and persistence of Clostridium difficile spores during and after cleaning with sporicidal disinfectants. J Hosp Infect. 2011 Sep;79(1):97-8. DOI: 10.1016/j.jhin.2011.06.010</RefTotal>
<RefLink>https://doi.org/10.1016/j.jhin.2011.06.010</RefLink>
</Reference>
<Reference refNo="30">
<RefAuthor>Sattar SA</RefAuthor>
<RefAuthor>Maillard JY</RefAuthor>
<RefTitle>The crucial role of wiping in decontamination of high-touch environmental surfaces: review of current status and directions for the future</RefTitle>
<RefYear>2013</RefYear>
<RefJournal>Am J Infect Control</RefJournal>
<RefPage>S97-104</RefPage>
<RefTotal>Sattar SA, Maillard JY. The crucial role of wiping in decontamination of high-touch environmental surfaces: review of current status and directions for the future. Am J Infect Control. 2013 May;41(5 Suppl):S97-104. DOI: 10.1016/j.ajic.2012.10.032</RefTotal>
<RefLink>https://doi.org/10.1016/j.ajic.2012.10.032</RefLink>
</Reference>
<Reference refNo="31">
<RefAuthor>Huang YS</RefAuthor>
<RefAuthor>Chen YC</RefAuthor>
<RefAuthor>Chen ML</RefAuthor>
<RefAuthor>Cheng A</RefAuthor>
<RefAuthor>Hung IC</RefAuthor>
<RefAuthor>Wang JT</RefAuthor>
<RefAuthor>Sheng WH</RefAuthor>
<RefAuthor>Chang SC</RefAuthor>
<RefTitle>Comparing visual inspection, aerobic colony counts, and adenosine triphosphate bioluminescence assay for evaluating surface cleanliness at a medical center</RefTitle>
<RefYear>2015</RefYear>
<RefJournal>Am J Infect Control</RefJournal>
<RefPage>882-6</RefPage>
<RefTotal>Huang YS, Chen YC, Chen ML, Cheng A, Hung IC, Wang JT, Sheng WH, Chang SC. Comparing visual inspection, aerobic colony counts, and adenosine triphosphate bioluminescence assay for evaluating surface cleanliness at a medical center. Am J Infect Control. 2015 Aug;43(8):882-6. DOI: 10.1016/j.ajic.2015.03.027</RefTotal>
<RefLink>https://doi.org/10.1016/j.ajic.2015.03.027</RefLink>
</Reference>
<Reference refNo="32">
<RefAuthor>van Arkel A</RefAuthor>
<RefAuthor>Willemsen I</RefAuthor>
<RefAuthor>Kilsdonk-Bode L</RefAuthor>
<RefAuthor>Vlamings-Wagenaars S</RefAuthor>
<RefAuthor>van Oudheusden A</RefAuthor>
<RefAuthor>Waegemaeker P</RefAuthor>
<RefAuthor>Leroux-Roels I</RefAuthor>
<RefAuthor>Verelst M</RefAuthor>
<RefAuthor>Maas E</RefAuthor>
<RefAuthor>van Oosten A</RefAuthor>
<RefAuthor>Willemse P</RefAuthor>
<RefAuthor>van Asselen E</RefAuthor>
<RefAuthor>Klomp-Berens E</RefAuthor>
<RefAuthor>Franssen K</RefAuthor>
<RefAuthor>Van Cauwenberg E</RefAuthor>
<RefAuthor>Kluytmans J</RefAuthor>
<RefAuthor> i-4-1-Health Study Group</RefAuthor>
<RefTitle>ATP measurement as an objective method to measure environmental contamination in 9 hospitals in the Dutch/Belgian border area</RefTitle>
<RefYear>2020</RefYear>
<RefJournal>Antimicrob Resist Infect Control</RefJournal>
<RefPage>77</RefPage>
<RefTotal>van Arkel A, Willemsen I, Kilsdonk-Bode L, Vlamings-Wagenaars S, van Oudheusden A, Waegemaeker P, Leroux-Roels I, Verelst M, Maas E, van Oosten A, Willemse P, van Asselen E, Klomp-Berens E, Franssen K, Van Cauwenberg E, Kluytmans J; i-4-1-Health Study Group. ATP measurement as an objective method to measure environmental contamination in 9 hospitals in the Dutch/Belgian border area. Antimicrob Resist Infect Control. 2020 May 28;9(1):77. DOI: 10.1186/s13756-020-00730-9</RefTotal>
<RefLink>https://doi.org/10.1186/s13756-020-00730-9</RefLink>
</Reference>
<Reference refNo="33">
<RefAuthor>Whiteley GS</RefAuthor>
<RefAuthor>Derry C</RefAuthor>
<RefAuthor>Glasbey T</RefAuthor>
<RefTitle>Reliability testing for portable adenosine triphosphate bioluminometers</RefTitle>
<RefYear>2013</RefYear>
<RefJournal>Infect Control Hosp Epidemiol</RefJournal>
<RefPage>538-40</RefPage>
<RefTotal>Whiteley GS, Derry C, Glasbey T. Reliability testing for portable adenosine triphosphate bioluminometers. Infect Control Hosp Epidemiol. 2013 May;34(5):538-40. DOI: 10.1086/670208</RefTotal>
<RefLink>https://doi.org/10.1086/670208</RefLink>
</Reference>
<Reference refNo="34">
<RefAuthor>Nante N</RefAuthor>
<RefAuthor>Ceriale E</RefAuthor>
<RefAuthor>Messina G</RefAuthor>
<RefAuthor>Lenzi D</RefAuthor>
<RefAuthor>Manzi P</RefAuthor>
<RefTitle>Effectiveness of ATP bioluminescence to assess hospital cleaning: a review</RefTitle>
<RefYear>2017</RefYear>
<RefJournal>J Prev Med Hyg</RefJournal>
<RefPage>E177-E183</RefPage>
<RefTotal>Nante N, Ceriale E, Messina G, Lenzi D, Manzi P. Effectiveness of ATP bioluminescence to assess hospital cleaning: a review. J Prev Med Hyg. 2017 Jun;58(2):E177-E183. </RefTotal>
</Reference>
<Reference refNo="35">
<RefAuthor>Sanna T</RefAuthor>
<RefAuthor>Dallolio L</RefAuthor>
<RefAuthor>Raggi A</RefAuthor>
<RefAuthor>Mazzetti M</RefAuthor>
<RefAuthor>Lorusso G</RefAuthor>
<RefAuthor>Zanni A</RefAuthor>
<RefAuthor>Farruggia P</RefAuthor>
<RefAuthor>Leoni E</RefAuthor>
<RefTitle>ATP bioluminescence assay for evaluating cleaning practices in operating theatres: applicability and limitations</RefTitle>
<RefYear>2018</RefYear>
<RefJournal>BMC Infect Dis</RefJournal>
<RefPage>583</RefPage>
<RefTotal>Sanna T, Dallolio L, Raggi A, Mazzetti M, Lorusso G, Zanni A, Farruggia P, Leoni E. ATP bioluminescence assay for evaluating cleaning practices in operating theatres: applicability and limitations. BMC Infect Dis. 2018 Nov 19;18(1):583. DOI: 10.1186/s12879-018-3505-y</RefTotal>
<RefLink>https://doi.org/10.1186/s12879-018-3505-y</RefLink>
</Reference>
<Reference refNo="36">
<RefAuthor>Rupp ME</RefAuthor>
<RefAuthor>Huerta T</RefAuthor>
<RefAuthor>Cavalieri RJ</RefAuthor>
<RefAuthor>Lyden E</RefAuthor>
<RefAuthor>Van Schooneveld T</RefAuthor>
<RefAuthor>Carling P</RefAuthor>
<RefAuthor>Smith PW</RefAuthor>
<RefTitle>Optimum outlier model for potential improvement of environmental cleaning and disinfection</RefTitle>
<RefYear>2014</RefYear>
<RefJournal>Infect Control Hosp Epidemiol</RefJournal>
<RefPage>721-3</RefPage>
<RefTotal>Rupp ME, Huerta T, Cavalieri RJ, Lyden E, Van Schooneveld T, Carling P, Smith PW. Optimum outlier model for potential improvement of environmental cleaning and disinfection. Infect Control Hosp Epidemiol. 2014 Jun;35(6):721-3. DOI: 10.1086/676431</RefTotal>
<RefLink>https://doi.org/10.1086/676431</RefLink>
</Reference>
<Reference refNo="37">
<RefAuthor>Boyce JM</RefAuthor>
<RefAuthor>Havill NL</RefAuthor>
<RefAuthor>Lipka A</RefAuthor>
<RefAuthor>Havill H</RefAuthor>
<RefAuthor>Rizvani R</RefAuthor>
<RefTitle>Variations in hospital daily cleaning practices</RefTitle>
<RefYear>2010</RefYear>
<RefJournal>Infect Control Hosp Epidemiol</RefJournal>
<RefPage>99-101</RefPage>
<RefTotal>Boyce JM, Havill NL, Lipka A, Havill H, Rizvani R. Variations in hospital daily cleaning practices. Infect Control Hosp Epidemiol. 2010 Jan;31(1):99-101. DOI: 10.1086/649225</RefTotal>
<RefLink>https://doi.org/10.1086/649225</RefLink>
</Reference>
<Reference refNo="38">
<RefAuthor>Larson EA</RefAuthor>
<RefAuthor>Aiello AE</RefAuthor>
<RefAuthor>Gomez-Duartec C</RefAuthor>
<RefAuthor>Lin SX</RefAuthor>
<RefAuthor>Lee L</RefAuthor>
<RefAuthor>Della-Latta P</RefAuthor>
<RefAuthor>Lindhardt Bioluminescence C</RefAuthor>
<RefTitle>ATP monitoring as a surrogate marker for microbial load on hands and surfaces in the home</RefTitle>
<RefYear>2003</RefYear>
<RefJournal>Food Microbiol</RefJournal>
<RefPage>735–9</RefPage>
<RefTotal>Larson EA, Aiello AE, Gomez-Duartec C, Lin SX, Lee L, Della-Latta P, Lindhardt Bioluminescence C. ATP monitoring as a surrogate marker for microbial load on hands and surfaces in the home. Food Microbiol. 2003;20(6):735–9. DOI: 10.1016/S0740-0020(03)00041-8</RefTotal>
<RefLink>https://doi.org/10.1016/S0740-0020(03)00041-8</RefLink>
</Reference>
<Reference refNo="39">
<RefAuthor>O’Neill C</RefAuthor>
<RefAuthor>Speziale P</RefAuthor>
<RefAuthor>Blue J</RefAuthor>
<RefAuthor>Ballantyne L</RefAuthor>
<RefAuthor>DiSimoni D</RefAuthor>
<RefTitle>Evaluation of ATP biolluminescence measuring system for monitoring hospital discharge cleaning</RefTitle>
<RefYear>2013</RefYear>
<RefJournal>Canad J Infect Contr</RefJournal>
<RefPage>9–11</RefPage>
<RefTotal>O’Neill C, Speziale P, Blue J, Ballantyne L, DiSimoni D. Evaluation of ATP biolluminescence measuring system for monitoring hospital discharge cleaning. Canad J Infect Contr. 2013;28(1):9–11. </RefTotal>
</Reference>
<Reference refNo="40">
<RefAuthor>Colbert EM</RefAuthor>
<RefAuthor>Sayles H</RefAuthor>
<RefAuthor>Lowe JJ</RefAuthor>
<RefAuthor>Chaika O</RefAuthor>
<RefAuthor>Smith PW</RefAuthor>
<RefAuthor>Gibbs SG</RefAuthor>
<RefTitle>Time series evaluation of the 3MTM Clean-TraceTM ATP detection device to confirm swab effectiveness</RefTitle>
<RefYear>2015</RefYear>
<RefJournal>Healthc Infect</RefJournal>
<RefPage>108–14</RefPage>
<RefTotal>Colbert EM, Sayles H, Lowe JJ, Chaika O, Smith PW, Gibbs SG. Time series evaluation of the 3MTM Clean-TraceTM ATP detection device to confirm swab effectiveness. Healthc Infect. 2015;20(4):108–14. DOI: 10.1071/HI15011</RefTotal>
<RefLink>https://doi.org/10.1071/HI15011</RefLink>
</Reference>
<Reference refNo="41">
<RefAuthor>Cooper RA</RefAuthor>
<RefAuthor>Griffith CJ</RefAuthor>
<RefAuthor>Malik RE</RefAuthor>
<RefAuthor>Obee P</RefAuthor>
<RefAuthor>Looker N</RefAuthor>
<RefTitle>Monitoring the effectiveness of cleaning in four British hospitals</RefTitle>
<RefYear>2007</RefYear>
<RefJournal>Am J Infect Control</RefJournal>
<RefPage>338-41</RefPage>
<RefTotal>Cooper RA, Griffith CJ, Malik RE, Obee P, Looker N. Monitoring the effectiveness of cleaning in four British hospitals. Am J Infect Control. 2007 Jun;35(5):338-41. DOI: 10.1016/j.ajic.2006.07.015</RefTotal>
<RefLink>https://doi.org/10.1016/j.ajic.2006.07.015</RefLink>
</Reference>
<Reference refNo="42">
<RefAuthor>Mitchell BG</RefAuthor>
<RefAuthor>Wilson F</RefAuthor>
<RefAuthor>Dancer SJ</RefAuthor>
<RefAuthor>McGregor A</RefAuthor>
<RefTitle>Methods to evaluate environmental cleanliness in healthcare facilities</RefTitle>
<RefYear>2013</RefYear>
<RefJournal>Health Infect</RefJournal>
<RefPage>23-30</RefPage>
<RefTotal>Mitchell BG, Wilson F, Dancer SJ, McGregor A. Methods to evaluate environmental cleanliness in healthcare facilities. Health Infect. 2013;18:23-30. DOI: 10.1071/HI12047</RefTotal>
<RefLink>https://doi.org/10.1071/HI12047</RefLink>
</Reference>
<Reference refNo="43">
<RefAuthor>Ferreira AM</RefAuthor>
<RefAuthor>de Andrade D</RefAuthor>
<RefAuthor>Rigotti MA</RefAuthor>
<RefAuthor>de Almeida MT</RefAuthor>
<RefAuthor>Guerra OG</RefAuthor>
<RefAuthor>dos Santos Junior AG</RefAuthor>
<RefTitle>Assessment of disinfection of hospital surfaces using different monitoring methods</RefTitle>
<RefYear>2015</RefYear>
<RefJournal>Rev Lat Am Enfermagem</RefJournal>
<RefPage>466-74</RefPage>
<RefTotal>Ferreira AM, de Andrade D, Rigotti MA, de Almeida MT, Guerra OG, dos Santos Junior AG. Assessment of disinfection of hospital surfaces using different monitoring methods. Rev Lat Am Enfermagem. 2015 May-Jun;23(3):466-74. DOI: 10.1590/0104-1169.0094.2577</RefTotal>
<RefLink>https://doi.org/10.1590/0104-1169.0094.2577</RefLink>
</Reference>
</References>
<Media>
<Tables>
<Table format="png">
<MediaNo>1</MediaNo>
<MediaID>1</MediaID>
<Caption><Pgraph><Mark1>Table 1: Mean value of relative light units (RLU) with 95%-confidence interval (CI) of timepoint, phase 1.</Mark1></Pgraph></Caption>
</Table>
<Table format="png">
<MediaNo>2</MediaNo>
<MediaID>2</MediaID>
<Caption><Pgraph><Mark1>Table 2: Mean value of relative light units (RLU) with 95%-confidence interval (CI) of location with highest and lowest contamination.</Mark1></Pgraph></Caption>
</Table>
<Table format="png">
<MediaNo>3</MediaNo>
<MediaID>3</MediaID>
<Caption><Pgraph><Mark1>Table 3: Mean values and 95%-confidence interval (CI) of relative light units (RLU) in different wards.</Mark1><LineBreak></LineBreak><LineBreak></LineBreak></Pgraph></Caption>
</Table>
<Table format="png">
<MediaNo>4</MediaNo>
<MediaID>4</MediaID>
<Caption><Pgraph><Mark1>Table 4: Mean values and 95%-confidence interval (CI) of ATP in relative light units (RLU) for group and timepoint.</Mark1><LineBreak></LineBreak><LineBreak></LineBreak><LineBreak></LineBreak></Pgraph></Caption>
</Table>
<NoOfTables>4</NoOfTables>
</Tables>
<Figures>
<Figure format="png" height="488" width="727">
<MediaNo>1</MediaNo>
<MediaID>1</MediaID>
<Caption><Pgraph><Mark1>Figure 1: Interaction plot for relative light units (RLU), timepoint and location, phase 1.</Mark1></Pgraph></Caption>
</Figure>
<Figure format="png" height="531" width="766">
<MediaNo>2</MediaNo>
<MediaID>2</MediaID>
<Caption><Pgraph><Mark1>Figure 2: Interaction plot for means of ATP in relative light units (RLU), phase 2.</Mark1></Pgraph></Caption>
</Figure>
<Figure format="png" height="524" width="730">
<MediaNo>3</MediaNo>
<MediaID>3</MediaID>
<Caption><Pgraph><Mark1>Figure 3: Interaction diagrams for mean of ATP in relative light units (RLU), phase 3.</Mark1></Pgraph></Caption>
</Figure>
<NoOfPictures>3</NoOfPictures>
</Figures>
<InlineFigures>
<NoOfPictures>0</NoOfPictures>
</InlineFigures>
<Attachments>
<NoOfAttachments>0</NoOfAttachments>
</Attachments>
</Media>
</OrigData>
</GmsArticle>]]></plaintext></textgroup></pgraph></abstract></origdata></gmsarticle>