Association between lignan polyphenol bioavailability and enterotypes of isoflavone metabolism: A cross-sectional analysis

Tomoko Fujitani; Mariko Harada Sassa; Zhaoqing Lyu; Yukiko Fujii; Kouji H. Harada

doi:10.1371/journal.pone.0295185

Peer Review History

Original SubmissionJuly 5, 2023
11 Sep 2023 Decision Letter - Awatif Abid Al-Judaibi, Editor PONE-D-23-19702Lignan polyphenol metabolism is partially determined by isoflavone metabolism enterotypes: a cross-sectional analysisPLOS ONE Dear Dr. Harada, 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 Oct 26 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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Please ensure that your ethics statement is included in your manuscript, as the ethics statement entered into the online submission form will not be published alongside your manuscript. [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: Yes Reviewer #2: No ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #2: No ****** 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 ****** 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: No ****** 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: The manuscript aims at studying of lignan metabolism using modern analytical methods. I have the following questions, comments and remarks: Comments and suggestions: • Abstract. The experimental groups should be defined. • Experimental procedures/ Results and Discussion. Did the authors monitor the changes of the detected compounds in time, i.e. the time of storage? Conclusion I would suggest to response minor issues prior to further consideration of the work. Based on my concerns, minor revision is required. Reviewer #2: I have reviewed the manuscript titled Lignan polyphenol metabolism is partially determined by isoflavone metabolism enterotypes: a cross-sectional analysis, and I appreciate the authors' efforts in conducting this research. However, after careful evaluation, I regret to inform you that I cannot recommend this manuscript for publication in its current form due to “Lack of Significance”, “Weak Methodology”, “Less Clarity in Data Presentation”, and “Less Statistical Significance”. I encourage the authors to consider revising the manuscript, addressing the aforementioned concerns, and potentially exploring alternative avenues for publication. ****** 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: No ******** [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. 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Revision 1
18 Oct 2023 Author Response Responses for reviewers’ comments Dear Editor and reviewers, Thank you for valuable feedbacks to our manuscript. We revised our manuscript based on your suggestions. Please see following responses and revisions. In addition, according to the editorial instructions, ethical statements were moved from Acknowledgments section to Methods section (L74–78, L298–301). Data availability section was revised to state the reason for the restriction (L306–309). Reviewer #1: The manuscript aims at studying of lignan metabolism using modern analytical methods. I have the following questions, comments and remarks: Comments and suggestions: #1. Abstract. The experimental groups should be defined. (response) Thank you for your comments. We revised the manuscripts as suggested to include the definition of EQP and O-DMAP (L18–20 in changes-tracked manuscript). EQP was defined by urinary daidzein (DAI) and equol concentrations as log(equol/DAI) ≥ –1.42. O-DMAP was defined by urinary DAI and O-DMA concentrations as O-DMA/DAI > 0.018. #2. Experimental procedures/ Results and Discussion. Did the authors monitor the changes of the detected compounds in time, i.e. the time of storage? (response) Thank you for the valuable comment. Changes over time of the detected compounds were not measured in this study. But in our previous study, we evaluated the stability of isoflavones and lignans. We revised the manuscripts to include this information (L107–109 in changes-tracked manuscript). Changes over time in the target compounds during storage were not evaluated in this study, but in our previous study [17], the archived samples used from the same specimen bank showed similar average concentrations of isoflavones and lignans to fresh samples. #3. Conclusion I would suggest to response minor issues prior to further consideration of the work. Based on my concerns, minor revision is required. Thank you for your evaluation and kind comments. Reviewer #2: I have reviewed the manuscript titled Lignan polyphenol metabolism is partially determined by isoflavone metabolism enterotypes: a cross-sectional analysis, and I appreciate the authors' efforts in conducting this research. However, after careful evaluation, I regret to inform you that I cannot recommend this manuscript for publication in its current form due to “Lack of Significance”, “Weak Methodology”, “Less Clarity in Data Presentation”“Less Statistical　Significance”. I encourage the authors to consider revising the manuscript, addressing the aforementioned concerns, and potentially exploring alternative avenues for publication. (response) Thank you for your comments. We revised the manuscript regarding for “Lack of Significance”, “Weak Methodology”,“Less Clarity in Data Presentation”, “Less Statistical Significance”. “Lack of Significance” (response) We emphasized the significance of the study more in the discussion section. (L231–233 in changes-tracked manuscript) There have not been reported for determinants of availability of lignan polyphenols while inter-individual variability was found. In the present study, we examined individual differences in urinary END and ENL concentrations for enterotypes of isoflavone metabolisms. “Weak Methodology” (response) We have already written the limitation of the study in the Discussion section, but we also added it to the abstract as well. (L28–31 in changes-tracked manuscript) The variables and participants in this study was limited, which the possibility of confounding by other variables cannot be ruled out. However, there are no established determinants of lignan metabolism to date. Further research is needed to determine what factors should be considered, and to examine in different settings to confirm the external validity. “Less Clarity in Data Presentation” (response) Since the primary outcome is the relationship between gut microbiota types and urinary lignans, this is clearly indicated in the tables and figures. But we now clearly indicate it in the statistical analysis section (L112 in changes-tracked manuscript). The primary outcome is the relationship between four enterotypes and urinary lignans concentrations. “Less Statistical　Significance”. (response) The analysis of the primary outcome shows sufficient statistical significances (P<0.01 to P<0.001). The p-values have been added to the Abstract (L24–26) The urinary lignan concentration was significantly higher in the O-DMAP/EQP group (ENL: P<0.001, END: P<0.001), and this association remained significant after adjusting for several background variables (END:β=0.138 P=0.00607 for EQP, β=0.147 P= 0.00328 for O-DMAP; ENL:β=0.312, P<0.001 for EQP, β=0.210, P<0.001 for O-DMAP). Attachments Attachment Submitted filename: Reviewer1016.docx https://doi.org/10.1371/journal.pone.0295185.r002
31 Oct 2023 Decision Letter - Awatif Abid Al-Judaibi, Editor PONE-D-23-19702R1Lignan polyphenol metabolism is partially determined by isoflavone metabolism enterotypes: a cross-sectional analysisPLOS ONE Dear Dr. Harada, 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 Dec 15 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. Please include the following items when submitting your revised manuscript: A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'. A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'. An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'. If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter. If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: https://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols. We look forward to receiving your revised manuscript. Kind regards, Awatif Abid Al-Judaibi, PhD Academic Editor PLOS ONE Journal Requirements: Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice. Additional Editor Comments: Dear authors, Thank you for submitting your value work in PLOSONE, your positive response is appreciated. I agree with reviewer2 that the title need improving and I am suggesting "A cross-sectional analysis of Lignan polyphenol partially determination by isoflavone metabolism enterotypes", or you can improve it by yourself, the word metabolism is written twice, and this may confuse the readers. [Note: HTML markup is below. Please do not edit.] 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 ******** 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: Partly ****** 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: No ****** 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: The manuscript was corrected according to reviewers comments. Therefore, the manuscript may be accepted. Reviewer #2: Dear Authors, You've made good efforts to address the comments. I recommend a minor revision: Make the title more catchy and concise. For instance, consider "Cross-Sectional Analysis of Lignan Polyphenol Metabolism and Isoflavone Enterotypes." Ensure the conclusion is clear by summarizing the main findings, discussing their significance, addressing research questions and limitations, and providing data-based recommendations for future research. Best regards. ****** 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: Muhammad Zeeshan Ahmed ******** [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. https://doi.org/10.1371/journal.pone.0295185.r003
Revision 2
15 Nov 2023 Author Response Responses for comments Dear Editor and Reviewer, Thank you for valuable feedbacks to our manuscript. We revised our manuscript based on your suggestions. Please see following responses and revisions. Editor’s comment Thank you for submitting your value work in PLOS ONE, your positive response is appreciated. I agree with reviewer2 that the title need improving and I am suggesting "A cross-sectional analysis of Lignan polyphenol partially determination by isoflavone metabolism enterotypes", or you can improve it by yourself, the word metabolism is written twice, and this may confuse the readers. (response) Thank you for your comment. As the Editor and Reviewer 2 suggested, we revised the title to “Association between lignan polyphenol bioavailability and enterotypes of isoflavone metabolism: a cross-sectional analysis” (L1–2 in changes-tracked manuscript). In addition, we reviewed the manuscript and edits for typos. Reviewer #1: The manuscript was corrected according to reviewers comments. Therefore, the manuscript may be accepted. (response) We appreciate your efforts in this review and evaluation of our study. Reviewer #2: Dear Authors, You've made good efforts to address the comments. I recommend a minor revision: #1: Make the title more catchy and concise. For instance, consider "Cross-Sectional Analysis of Lignan Polyphenol Metabolism and Isoflavone Enterotypes." (response) Thank you for your comment. As the Editor and Reviewer 2 suggested, we revised the title to “Association between lignan polyphenol bioavailability and enterotypes of isoflavone metabolism: a cross-sectional analysis” (L1–2 in changes-tracked manuscript). #2: Ensure the conclusion is clear by summarizing the main findings, discussing their significance, addressing research questions and limitations, and providing data-based recommendations for future research. (response) Thank you for the suggestion. We revised the Conclusion section as suggested (L287–294 in the changes-tracked manuscript). In this study, the factors that are responsible for individual differences in the bioavailability of ENL and END were investigated in relation to enterotypes of isoflavone metabolism. Urinary END and ENL concentrations were 3.80- and 10.2-fold higher in the EQP/O-DMAP group than in the non-EQP/non-O-DMAP group, respectively. However urinary isoflavone concentrations were not associated with END and ENL concentrations. Dietary intake of lignan polyphenols may not represent precise bioavailable amounts and these enterotypes may provide better estimates. The possibility of biases and confounding cannot be ruled out due to the limitations in observed variables and participants. Further research to determine causative gut bacteria is needed. Also, the values of lignans are provided (L156–160). The geometric mean of the urinary log END (0.0473 μmol/g-Cr) value in non-O-DMAP/non-EQP was lower than for O-DMAP/EQP and O-DMAP/non-EQP (0.180 and 0.119 μmol/g-Cr; P < 0.001 and P = 0.0025, respectively). Also, urinary log ENL (0.0176 μmol/g-Cr) concentrations were lower in non-EQP/non-O-DMAP than in EQP/O-DMAP, non-EQP/O-DMAP, and non-O-DMAP/EQP (0.181, 0.0577 and 0.0943 μmol/g-Cr; P < 0.001, P < 0.001, and P = 0.0003, respectively). Attachments Attachment Submitted filename: responses20231115.docx https://doi.org/10.1371/journal.pone.0295185.r004
16 Nov 2023 Decision Letter - Awatif Abid Al-Judaibi, Editor Association between lignan polyphenol bioavailability and enterotypes of isoflavone metabolism: a cross-sectional analysis PONE-D-23-19702R2 Dear Dr. Kouji Harada, 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, Awatif Abid Al-Judaibi, PhD Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0295185.r005
Formally Accepted
24 Nov 2023 Acceptance Letter - Awatif Abid Al-Judaibi, Editor PONE-D-23-19702R2 Association between lignan polyphenol bioavailability and enterotypes of isoflavone metabolism: a cross-sectional analysis Dear Dr. Harada: 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 customercare@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 Professor Awatif Abid Al-Judaibi Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0295185.r006

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