Correlation of a commercial platform’s results with post-vaccination SARS-CoV-2 neutralizing antibody response and clinical host factors

Rebecca Slotkin; Tassos C. Kyriakides; Anupam Kundu; Gary Stack; Richard E. Sutton; Shaili Gupta

doi:10.1371/journal.pone.0289713

Peer Review History

Original SubmissionMarch 30, 2023
27 Apr 2023 Decision Letter - Harapan Harapan, Editor PONE-D-23-08631Correlation of a Commercial Platform’s Results with Post-vaccine SARS-CoV-2 Neutralizing Antibody Response and Clinical Host FactorsPLOS ONE Dear Dr. Gupta, Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. Please submit your revised manuscript by Jun 11 2023 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file. 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The PLOS ONE style templates can be found at https://journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and https://journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf 2.Thank you for stating the following financial disclosure: "Funding for this study was provided by the National Institutes of Health (awards R01 AI150334 to RES). The analysis was supported by Global Health Equity Scholars (FIC D43TW010540 to RS)." Please state what role the funders took in the study. If the funders had no role, please state: "The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript." If this statement is not correct you must amend it as needed. Please include this amended Role of Funder statement in your cover letter; we will change the online submission form on your behalf. 3. In your Data Availability statement, you have not specified where the minimal data set underlying the results described in your manuscript can be found. PLOS defines a study's minimal data set as the underlying data used to reach the conclusions drawn in the manuscript and any additional data required to replicate the reported study findings in their entirety. All PLOS journals require that the minimal data set be made fully available. For more information about our data policy, please see http://journals.plos.org/plosone/s/data-availability. "Upon re-submitting your revised manuscript, please upload your study’s minimal underlying data set as either Supporting Information files or to a stable, public repository and include the relevant URLs, DOIs, or accession numbers within your revised cover letter. For a list of acceptable repositories, please see http://journals.plos.org/plosone/s/data-availability#loc-recommended-repositories. Any potentially identifying patient information must be fully anonymized. Important: If there are ethical or legal restrictions to sharing your data publicly, please explain these restrictions in detail. Please see our guidelines for more information on what we consider unacceptable restrictions to publicly sharing data: http://journals.plos.org/plosone/s/data-availability#loc-unacceptable-data-access-restrictions. Note that it is not acceptable for the authors to be the sole named individuals responsible for ensuring data access. We will update your Data Availability statement to reflect the information you provide in your cover letter. 4. We note that you have stated that you will provide repository information for your data at acceptance. Should your manuscript be accepted for publication, we will hold it until you provide the relevant accession numbers or DOIs necessary to access your data. If you wish to make changes to your Data Availability statement, please describe these changes in your cover letter and we will update your Data Availability statement to reflect the information you provide. 5. Please amend either the title on the online submission form (via Edit Submission) or the title in the manuscript so that they are identical. 6. Please include your full ethics statement in the ‘Methods’ section of your manuscript file. In your statement, please include the full name of the IRB or ethics committee who approved or waived your study, as well as whether or not you obtained informed written or verbal consent. If consent was waived for your study, please include this information in your statement as well. [Note: HTML markup is below. Please do not edit.] 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 ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #2: Yes ****** 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: Yes Reviewer #2: Yes ****** 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 ****** 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: This manuscript is an interesting topic, however, the data is not new and the content is suitable for publishing as a letter or short communication that extended the result from the previous publications. I suggest adding more data and text to make it suitable for the original article. Major concerns. 1. Please add the IRB/EC approval number to the Methods. 2. Why you over emphasised the CMIA technique of the Abbott AdviseDx SARS-CoV-2 IgG II? The CMIA is only the technique, but the target of the antibody is more important than the technique of commercial diagnostic assays. Suggest using "IgG anti-S1/RBD" or "IgG anti-RBD" instead of "IgG-II CMIA" to make it more specific. See more: https://www.fda.gov/media/146371/download 3. Suggest creating a Demographic table including the clinical and COVID-19 vaccine used to delineate the participant's demographic data. Minor concerns. 1. Methods, suggest being divided into subtitles, such as Participants, Immunologic assessment, and Statistical analysis. 2. Suggest adding the conversion factor of the Abbott AdviseDx to the introduction, the real result from this instrument report is in the AU/mL but BAU/mL is converted. Some readers may don't understand where the BAU/mL came from. Comments. 1. Suggest using subscript of the "50" in the term "IC₅₀". Reviewer #2: Reviewer Suggestions 1. As it is known, antibody titers spontaneously decrease over time, and also may increase due to COVID-19 or vaccination. For this reason, to evaluate the correlations of the neutralizing antibody IC50 measurement and the anti-RBD-S1-IgG (IgG) antibody measurement, they must be studied from the sera samples taken at the same time-point. In order to indicate that the study was designed in this way and to make the study workflow easier to understand, it would be beneficial to use a visual abstract showing at which time-points, how many people in which groups (prior COVID infection/or not, etc.), and which tests were studied. 2. Could you explain the term 'intercept' and its purpose of usage in Table-1? What do the obtained values mean and how are they interpreted? ****** 6. 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. If you choose “no”, your identity will remain anonymous but your review may still be made public. 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: No Reviewer #2: Yes: Yeşim Tuyji Tok, MD ******** [NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.] While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step. Attachments Attachment Submitted filename: PONE-D-23-08631 review.docx https://doi.org/10.1371/journal.pone.0289713.r001
Revision 1
11 Jun 2023 Author Response Dear Dr. Harapan Harapan and Reviewers, Thank you for your consideration of this paper (PONE-D-23-08631) and the time you have taken to review it. We appreciate your thoughts and suggestions. Please see the responses below to see how we have incorporated your feedback into this new version. Journal Requirements: When submitting your revision, we need you to address these additional requirements. 1. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at https://journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and https://journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf Authors: Thank you for this reminder. We have ensured that both the manuscript and the file naming meet the journal style requirements. 2. Please state what role the funders took in the study. If the funders had no role, please state: "The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript." If this statement is not correct you must amend it as needed. Please include this amended Role of Funder statement in your cover letter; we will change the online submission form on your behalf. Authors: The funding statement has been amended to: "Funding for this study was provided by the National Institutes of Health (awards R01 AI150334 to RES). The analysis was supported by Global Health Equity Scholars and the National Institutes of Health (FIC D43TW010540 and T32AR007107 to RS). The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.” It has also been included in the attached cover letter, thank you. 3. In your Data Availability statement, you have not specified where the minimal data set underlying the results described in your manuscript can be found. PLOS defines a study's minimal data set as the underlying data used to reach the conclusions drawn in the manuscript and any additional data required to replicate the reported study findings in their entirety. All PLOS journals require that the minimal data set be made fully available. For more information about our data policy, please see http://journals.plos.org/plosone/s/data-availability. "Upon re-submitting your revised manuscript, please upload your study’s minimal underlying data set as either Supporting Information files or to a stable, public repository and include the relevant URLs, DOIs, or accession numbers within your revised cover letter. For a list of acceptable repositories, please see http://journals.plos.org/plosone/s/data-availability#loc-recommended-repositories. Any potentially identifying patient information must be fully anonymized. Important: If there are ethical or legal restrictions to sharing your data publicly, please explain these restrictions in detail. Please see our guidelines for more information on what we consider unacceptable restrictions to publicly sharing data: http://journals.plos.org/plosone/s/data-availability#loc-unacceptable-data-access-restrictions. Note that it is not acceptable for the authors to be the sole named individuals responsible for ensuring data access. We will update your Data Availability statement to reflect the information you provide in your cover letter. Authors: We have shared our de-identified dataset as a supplemental excel file, “S1 File”. 3. We note that you have stated that you will provide repository information for your data at acceptance. Should your manuscript be accepted for publication, we will hold it until you provide the relevant accession numbers or DOIs necessary to access your data. If you wish to make changes to your Data Availability statement, please describe these changes in your cover letter and we will update your Data Availability statement to reflect the information you provide. Authors: The de-identified data is being shared as a supplemental excel file, “S1 File” with this submission. 4. Please amend either the title on the online submission form (via Edit Submission) or the title in the manuscript so that they are identical. Authors: Thank you for noting the difference in title (Vaccine vs vaccination). We have corrected the online submission form and the title is identical now at both places: “Correlation of a Commercial Platform’s Results with Post-vaccination SARS-CoV-2 Neutralizing Antibody Response and Clinical Host Factors”. 6. Please include your full ethics statement in the ‘Methods’ section of your manuscript file. In your statement, please include the full name of the IRB or ethics committee who approved or waived your study, as well as whether or not you obtained informed written or verbal consent. If consent was waived for your study, please include this information in your statement as well. [Note: HTML markup is below. Please do not edit.] Authors: Thank you for this comment. We have updated the Methods section to include the following statement: “Approval for this study (SARS-CoV-2 Vaccine and You, Protocol #1599488) was obtained from the Veterans Affairs Connecticut Healthcare System (VACHS) Institutional Review Board (IRB) in December 2020. Written informed consent was obtained from willing participants recruited from COVID-vaccination clinics set up by VACHS beginning in December 2020.” Reviewers' comments: Reviewer #1: This manuscript is an interesting topic, however, the data is not new and the content is suitable for publishing as a letter or short communication that extended the result from the previous publications. I suggest adding more data and text to make it suitable for the original article. Authors: Thank you for this suggestion. We have added a Table 1 of demographics and comorbidities. We have incorporated more detail throughout our manuscript now, and feel that this made the manuscript clearer. We have elaborated on the ‘Methods’ section, including more details of statistical analysis. We redid the linear correlation to add an adjusted R-square value and tested it in several models to ensure it will be replicable in the field (linear model is in the body of the paper, the non-linear loess model is in the appendix. Although the loess model performed even better, it is harder to follow mathematically and less applicable to the clinical audience of PLOS, therefore we provide that in supplemental material). We also did a sensitivity analysis looking at the correlation if we removed any values that were above the limit of detection (read as >25,000 AU/mL) on the commercial platform we used. This sensitivity analysis demonstrated an improvement in the adjusted R-squared value of the correlation to 0.80. We can therefore conclude that the linear model we included in the body of this paper is the most conservative estimate of the true correlation between IgG and nAb IC50. This has been included in the ‘Results’ section. We thank the reviewer for encouraging us to add more data, and believe that this additional work has strengthened the conclusions while also providing more insight into the methodology. Major concerns. 1. Please add the IRB/EC approval number to the Methods. Authors: The ‘Methods’ section has been updated as noted above with the approved protocol number. 2. Why you over emphasised the CMIA technique of the Abbott AdviseDx SARS-CoV-2 IgG II? The CMIA is only the technique, but the target of the antibody is more important than the technique of commercial diagnostic assays. Suggest using "IgG anti-S1/RBD" or "IgG anti-RBD" instead of "IgG-II CMIA" to make it more specific. See more: https://www.fda.gov/media/146371/download Authors: We agree. It was not our intention to specifically highlight a single type of commercial test, but rather offer an example of how commercial IgG anti-S1/RBD testing may be used. We have updated the language throughout the manuscript with the exception of when describing the methodology used to measure the IgG anti-S1/RBD. Thank you for suggesting this. 3. Suggest creating a Demographic table including the clinical and COVID-19 vaccine used to delineate the participant's demographic data. Authors: We have added a demographics table, named Table 1 as you suggested. Minor concerns. 1. Methods, suggest being divided into subtitles, such as Participants, Immunologic assessment, and Statistical analysis. Authors: Thank you for the suggestion, the manuscript has been updated with the ‘Methods’ section broken into the following categories: ‘Participants’, ‘Variable collection’, and ‘Statistical analysis’. 2. Suggest adding the conversion factor of the Abbott AdviseDx to the introduction, the real result from this instrument report is in the AU/mL but BAU/mL is converted. Some readers may don't understand where the BAU/mL came from. Authors: Thank you for this suggestion. We have added the AU/mL to BAU/mL conversion and interpretation factor to the ‘Methods’ section in the manuscript, which reads as follows. “IgG anti-S1/RBD were measured in AU/ml, a unit specific to the commercial platform used. One Abbott platform AU/ml converts to 7.04 BAU/ml, the standard World Health Organization (WHO) units used as a standard for commercial antibody platform result interpretation [8, 9].” The following have been added as references: 8. Müller L, Kannenberg J, Biemann R, Hönemann M, Ackermann G, Jassoy C. Comparison of the measured values of quantitative SARS-CoV-2 spike antibody assays. J Clin Virol. 2022;155:105269. doi:10.1016/j.jcv.2022.105269 9. Perkmann T, Perkmann-Nagele N, Koller T, et al. Anti-Spike Protein Assays to Determine SARS-CoV-2 Antibody Levels: a Head-to-Head Comparison of Five Quantitative Assays. Microbiol Spectr. 2021;9(1):e0024721. doi:10.1128/Spectrum.00247-21 Our aim is to share this work with the field to illustrate that using a commercial platform can cost-effectively predict neutralizing ability of an individual’s serum against SARS-CoV-2. Since WHO has provided a standardization in BAU/mL, it helps the interpretation of results from various platforms, including the one we used, and adding this clarification strengthens the manuscript. We thank the reviewer for helping us specify this. Comments. 1. Suggest using subscript of the "50" in the term "IC₅₀". Authors: The formatting of IC50 is often investigator and journal dependent, and we have incorporated the suggested change now throughout the manuscript and figures. Reviewer #2: Reviewer Suggestions 1. As it is known, antibody titers spontaneously decrease over time, and also may increase due to COVID-19 or vaccination. For this reason, to evaluate the correlations of the neutralizing antibody IC50 measurement and the anti-RBD-S1-IgG (IgG) antibody measurement, they must be studied from the sera samples taken at the same time-point. In order to indicate that the study was designed in this way and to make the study workflow easier to understand, it would be beneficial to use a visual abstract showing at which time-points, how many people in which groups (prior COVID infection/or not, etc.), and which tests were studied. Authors: Thank you for this suggestion. Each sample was measured for IgG and IC50 at the same collection time point. We have clarified this in the ‘Methods’ section with the sentence: “Each measurement of IgG and IC50 was done on serum from the same collection time point to avoid any errors in measurement due to antibody fluctuation over time.” We have also added a supplemental visual abstract (S2 Fig) to illustrate how many samples at each time-point were from subjects that had COVID before that collection. We will defer to the journal to decide whether this new supplemental figure will be included in the publication. S2 Fig. Distribution of Subjects by Collection Time-point and COVID-status. COVID-positivity was defined as RT-PCR COVID- diagnosis at any time prior to collection. 2. Could you explain the term 'intercept' and its purpose of usage in Table-1? What do the obtained values mean and how are they interpreted? Authors: Thanks for this question. Each of the models in Table-1 (now Table-2) illustrates a formula that may be used to predict IC50. For example, Model 1 predicts IC50 from the variables IgG, COVID positive status, and renal function. With multiple datapoints, this model creates a line when graphed. The point at which that line intercepts the y axis, is the intercept. Attachments Attachment Submitted filename: PLOS reviewer response .docx https://doi.org/10.1371/journal.pone.0289713.r002
25 Jul 2023 Decision Letter - Harapan Harapan, Editor Correlation of a Commercial Platform’s Results with Post-vaccination SARS-CoV-2 Neutralizing Antibody Response and Clinical Host Factors PONE-D-23-08631R1 Dear Dr. Gupta, 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. Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication. An invoice for payment will follow shortly after the formal acceptance. To ensure an efficient process, please log into Editorial Manager at http://www.editorialmanager.com/pone/, click the 'Update My Information' link at the top of the page, and double check that your user information is up-to-date. If you have any billing related questions, please contact our Author Billing department directly at authorbilling@plos.org. If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org. Kind regards, Harapan Harapan, MD, PhD Academic Editor PLOS ONE Additional Editor Comments (optional): 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: (No Response) Reviewer #2: All comments have been addressed ******** 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 ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #2: Yes ****** 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 ****** 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 ****** 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: Thank you for your improvement in the quality and information in the revised manuscript. Have good luck. Reviewer #2: Although the subject is out of date, it is a well-designed and valuable study. Comments have been adressed and explained sufficiently. ****** 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. If you choose “no”, your identity will remain anonymous but your review may still be made public. 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: No Reviewer #2: Yes: Yeşim Tuyji Tok ******** https://doi.org/10.1371/journal.pone.0289713.r003
Formally Accepted
21 Aug 2023 Acceptance Letter - Harapan Harapan, Editor PONE-D-23-08631R1 Correlation of a Commercial Platform’s Results with Post-vaccination SARS-CoV-2 Neutralizing Antibody Response and Clinical Host Factors Dear Dr. Gupta: I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department. If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org. If we can help with anything else, please email us at plosone@plos.org. Thank you for submitting your work to PLOS ONE and supporting open access. Kind regards, PLOS ONE Editorial Office Staff on behalf of Dr. Harapan Harapan Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0289713.r004

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