PONE-D-23-27473Impact of terminal cleaning in rooms previously occupied by patients with healthcare-associated infectionsPLOS ONE

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Additional Editor Comments:

Sorry for the delay in review. The original reviewer went out on parental leave and there was difficulty securing another reviewer. I agree with the reviewers that the paper is useful and adds to the literature on room cleaning, but that it needs some work. Some of the issues are methodological (e.g., why no negative control) some were questions on the statistical choices, and some were just comments on the readability. A major issue was a description of the surfaces. It appears this may have been in a citation, but that citation shows up as an error. Perhaps add some details about the surfaces here as well as correcting the citation. The other issue noted was the concern about increases at certain hospitals either in whole or part. There was confusion about what increased and how significant was that increases. There was particular concern around the tables which are not always clear.

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Partly

Reviewer #2: Yes

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2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

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3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: No

Reviewer #2: Yes

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4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

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5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: Summary

This study highlights the impact of terminal room cleaning on removing pathogens from high-touch surfaces. This is an absolutely important subject, particularly with potential implications for the role of environment in transmission of HAIs.

The study includes the collection and analysis of environmental samples from 36 patient rooms at 3 major hospitals located in 3 different US states. The findings suggest that while complete eradication of pathogens to undetectable levels, which is the goal of most terminal cleaning protocols, was not consistently achieved, concentration levels of Acinetobacter baumannii, MRSA, VRE, and C diff. were moderately to significantly reduced after the cleaning procedure across different surface types. One interesting finding was the increase in VRE concentration on nurse call buttons after cleaning in one of the hospitals, which the authors argued to be potentially due to cross contamination. Another interesting finding, which agrees with other studies, was that using only ATP measurement was shown to be insufficient for assessing hospital surface cleanliness. The authors have provided suggestions about amending and standardizing current terminal cleaning protocols to protect patients from exposure to residual pathogens on surfaces left by previous patients, with a particular focus on MRSA and VRE as the most frequently found pathogens on hospital surfaces after terminal cleaning. In light of uncertainties regarding the effectiveness of terminal cleaning, the study suggests transitioning to a risk-based framework that can link terminal cleaning protocols to expected HAI outcomes.

I found the study interesting and suitable for publication in PLOS ONE, though I have a few questions that I would like to be addressed before publication.

Major comments/questions

1. The authors have provided a brief discussion of the potential impacts of the differences in cleaning protocols and compliance across the three sites on their findings, in addition to other limitation of their study (which is shared with other similar studies). I think it would help to make a more comprehensive discussion if other factors that may contribute to variabilities and rare but significant discrepancies (such as VRE increase in one of the hospitals) were also incorporated, factors such as differences in cleaning staff diligence, patient colonization rates, admission prevalence rate, average length of stay, frequency of HCW visits, and other factors that affect pathogen shedding and transfer and may differ across rooms, wards, and hospitals.

2. Discussion, Paragraph 2: “on at least one occasion, detections and/or concentrations increased from pre-cleaning to post-cleaning sampling. This occurred for C. difficile on chair handrail, MRSA on bed handrail…” While the “one” occasion was covered in the results section for VRE on nurse call buttons, other instances of such observations, where pathogen concentration was increased after terminal cleaning, was not explained neither could be interpreted from the results (Tables 2 and 3), for example C. difficile on chair handrail. I am not sure if these other instances were isolated cases in one or just a few rooms, or if the findings were not reliable due to below-detectable concentrations. What could be the reason? Please elaborate.

3. The one occasion where VRE concentration was increased after terminal cleaning is interesting. While the authors have provided their interpretation of the potential causes, it would make it easier for readers to objectively interpret such a rare but impactful case if more information was provided, for example, was this observed for all nurse call buttons (all rooms), if not how many of the rooms, and whether there could be anything different about those specific rooms or their occupying patients. This deserves a little deeper investigation.

4. Statistical analysis: what method was used for multiple hypothesis tests (detections) to correct for family-wise type I errors? If such a consideration was not necessary, please justify by explaining in the paper the scale of detection tests (i.e., whether detection tests were done on a surface-, room-, or hospital-level) in relation to the comparison scale which is surface type at each hospital.

Minor comments

1. Abstract: Please spell out what ATP stands for, the first time it is used.

2. Abstract: Incomplete sentence: “Surfaces from 36 occupied … and Clostridioides difficile (C. difficile)).”

3. Abstract: Missing comma before “desk surface” in the following statement: “Six nonporous, high touch surfaces (i.e., chair handrail, bed handrail, nurse call button desk surface, bathroom counter near the sink, and a grab bar near the toilet) ...”

4. Introduction, Paragraph 1: “ATP as a biochemical indicator of biological material.” Incomplete sentence. Please complete or merge with the previous or next sentence.

5. Methods, Sample Site Selection, Paragraph 2: Missing comma before “desk surface” in the following statement: “The six surfaces (i.e., chair handrail, bed handrail, nurse call button desk surface, bathroom counter near the sink, and a grab bar near the toilet) ...”

6. Methods, Sample Site Selection, Paragraph 2: Please address the cross-referencing error.

7. Methods, Sample Site Selection, Paragraph 2: “If a pre-selected item was not present …” An example or two for the replacements could help clarify, also how often this was the case?

8. Methods, Sample Site Selection, Table 1: To improve readability, please align cells, preferably to the top left corner of the cells, or use borders.

9. Methods, Detections, below Figure 1: “At hospital 2, VRE was the only organism detected and confirmed (n nurse call button) pre-cleaning…” Please correct the typo inside the parentheses.

10. Discussion, Paragraph 4: “Other studies, however, have shown poor relationship relationships [38–41] …” Please remove the extra “relationship.”

Reviewer #2: Thank you for this informative paper in this important area of infection prevention and control in the hospital setting. I have some comments that revolve primarily around making the paper clearer, and easier for the reader to understand and contextualize. It includes using a denominator to give context to the numbers you are referrring to.

-The abstract needs to include the number of rooms being evaluated for each in order to make sense of these results.

-The statement "ATP detections did not correlate with any pathogen concentration and thus are not recommended for assessing cleanliness or safety." is too conclusive based on the data shown. ATP measures organic matter, and would be better correlated with overall aerobic colony counts, it is not specific to multidrug resistant organisms.

-In methods, there is an error: "Descriptions of the surfaces are presented in Error!Reference source not found.."

-Include use of negative control in the micro methods section if used, or if not used explain why.

- Presumptive and confirmed concentrations needs to be explained in the methods. From my reading/understanding only AB isolates from wet surfaces were confirmed as these may be non-baumanii. But then it seems to apply to all and is very unclear. Table 2 is also very unclear.

- Detections needs a denominator to put the “51” and “12” on the first line in context. The rest of the section is unclear, and does not seem to align with the methods.

-Discussion: needs to be clearer - Other studies, however, have shown poor relationship relationships [38–41] or significant

relationships [42–47] between ATP and pathogen presence.

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Reviewer #1: Yes: Fardad Haghpanah

Reviewer #2: No

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Impact of terminal cleaning in rooms previously occupied by patients with healthcare-associated infections

PONE-D-23-27473R1

Dear Dr. Verhougstraete,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

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Eili Y. Klein, PhD

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Thank you for your diligence in responding to all the comments and your patience in the process

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #2: All comments have been addressed

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2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

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3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

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4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

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5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

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6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: (No Response)

Reviewer #2: Thank you for addressing the reviewer comments. I do not have any further comments or edits to suggest.

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7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

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Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: Yes: Fardad Haghpanah

Reviewer #2: No

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