Efficacy and safety of tranexamic acid on blood loss and seizures in patients undergoing meningioma resection: A systematic review and meta-analysis

Xiaoyuan Liu; Minying Liu; Shu Li; Yue Ren; Maoyao Zheng; Min Zeng; Yuming Peng

doi:10.1371/journal.pone.0308070

Peer Review History

Original SubmissionJanuary 22, 2024
30 May 2024 Decision Letter - Andreas K Demetriades, Editor PONE-D-24-02588Efficacy and safety of tranexamic acid on blood loss and seizures in patients undergoing meningioma resection: a systematic review and meta-analysisPLOS ONE Dear Dr. Peng, 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 Jul 14 2024 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. 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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. We note that the grant information you provided in the ‘Funding Information’ and ‘Financial Disclosure’ sections do not match. When you resubmit, please ensure that you provide the correct grant numbers for the awards you received for your study in the ‘Funding Information’ section. 3. Please include your tables as part of your main manuscript and remove the individual files. Please note that supplementary tables (should remain/ be uploaded) as separate ""supporting information"" files. Additional Editor Comments: Major review recommended [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: No Reviewer #2: Yes Reviewer #3: Yes Reviewer #4: Yes ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: No Reviewer #2: Yes Reviewer #3: I Don't Know Reviewer #4: 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: No Reviewer #2: Yes Reviewer #3: Yes Reviewer #4: 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: No Reviewer #2: Yes Reviewer #3: Yes Reviewer #4: 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: Dear Author, The search strategy is not clear/available. Literature suggests that Tranexamic acid can precipitate seizures in certain doses and there is controversy regarding the role of prevention of seizures. It is not clear whether the patients in either group were on anti-epileptics. Study needs to more elaborative. Reviewer #2: Comments for Manuscript Submission ID PONE-D-24-02588 Comments for the Authors I find it a well-designed paper. This study demonstrates that the administration of TXA could reduce blood loss (by 252 mL) in patients undergoing intracerebral meningioma resection. Meanwhile, TXA did not increase the risk of seizure, or other postoperative complications. I, however, have a few minor comments to make: Comment #1: Meningiomas are one of the most common intracranial tumors Line 232, on page 20, with null or hard-to-interpret outcomes may not be published; please, the author explicitly states the meaning of “hard-to-interpret outcomes.” Comment #2: Line 243-245, on page 21, This systematic review and meta-analysis suggests that the administration of TXA could reduce blood loss (by 252 mL) in patients undergoing intracerebral meningioma resection. The detailed blood loss (by 252) is inappropriate in the conclusion section. Reviewer #3: Thank you for this valuable research. The manuscript is presented in a very good, informative and organised way. It is also written in a standard English language. Only the differences between the studies you choose for your analysis are multiple. Reviewer #4: In their reponse letter, authors claim that recent study showed that TMZ did not add any benefit in the treatment of IDH wildtype glioblastoma compared with radiotherapy alone, regardless of MGMT promoter status (https://pubmed.ncbi.nlm.nih.gov/34000245/. This is simply a misinterpretation: Adjuvant temozolomide chemotherapy, but not concurrent temozolomide chemotherapy, was associated with a survival benefit in patients with 1p/19q non-co-deleted anaplastic gliomas. I suggest to change the passages in Discussion accordingly. I suggest to re-write the conclusion and state that the effects of the two drugs were shown in an in-vitro animal model under laboratory circumstances, and that it by no means suggest a positive clinical perspective for patients with necessity of further studies. ****** 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 Reviewer #3: No Reviewer #4: 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. 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Revision 1
2 Jul 2024 Author Response Response to Reviewers: Reviewer #1: The search strategy is not clear/available. Literature suggests that Tranexamic acid can precipitate seizures in certain doses and there is controversy regarding the role of prevention of seizures. It is not clear whether the patients in either group were on anti-epileptics. Study needs to more elaborative. Response: Thanks. The search strategy for this paper was: ((tranexamic acid) OR (TXA) OR (Tranexamic acid)) AND (meningioma) AND ((randomized controlled trial) OR (randomized)). Tranexamic acid can precipitate seizures in certain doses, and we found that tranexamic acid did not increase the incidence of seizure in our meta-analysis. Additionally, the meta-analysis included four studies, of which only one mentioned the prophylactic administration of antiepileptic drugs postoperatively, while the remaining three did not specify whether antiepileptic treatment was given. Author, year Whether to use postoperative antiepileptic drugs administration Hooda et al., 2017 None. Rebai et al., 2021 None. Ravi et al., 2021 None. Shu Li et al., 2023 Yes. Postoperative antiepileptic treatment includes intravenous or oral administration of valproic acid, oxcarbazepine, carbamazepine, levetiracetam, and phenobarbital. Rescue intramuscular phenobarbital or continuous infusion of midazolam was administered when seizure fit attacks. Related revised manuscript text: Only one study mentioned the prophylactic administration of antiepileptic drugs postoperatively, while the other studies did not specify this. Manuscript location: Page 9, line 19- and table 1 last column in the revised manuscript. Reviewer #2: I find it a well-designed paper. This study demonstrates that the administration of TXA could reduce blood loss (by 252 mL) in patients undergoing intracerebral meningioma resection. Meanwhile, TXA did not increase the risk of seizure, or other postoperative complications. I, however, have a few minor comments to make: Comment #1: Meningiomas are one of the most common intracranial tumors. Line 232, on page 20, with null or hard-to-interpret outcomes may not be published; please, the author explicitly states the meaning of “hard-to-interpret outcomes.” Response: Thanks. We acknowledge that the term “hard-to-interpret” is inappropriate and have removed it. Related revised manuscript text: In addition, we collected studies through systematically searching selected databases, nevertheless the potential for publication bias persists. Manuscript location: Page 12, line 14- in the revised manuscript. Comment #2: Line 243-245, on page 21, This systematic review and meta-analysis suggests that the administration of TXA could reduce blood loss (by 252 mL) in patients undergoing intracerebral meningioma resection. The detailed blood loss (by 252) is inappropriate in the conclusion section. Response: Thanks. We agree with you and have moved the data in the conclusion section. Related revised manuscript text: This systematic review and meta-analysis suggests that the administration of TXA could reduce blood loss in patients undergoing intracerebral meningioma resection. Manuscript location: Page 13, line 5- in the revised manuscript. Reviewer #3: Thank you for this valuable research. The manuscript is presented in a very good, informative and organised way. It is also written in a standard English language. Only the differences between the studies you choose for your analysis are multiple. Response: Thanks. We appreciate your positive comments on the manuscript. We acknowledge that the multiple analysis in the studies chose in the meta which also led to the high value of I2. We also discussed this in detail in the limitations section to clarify the impact of these factors on our results. Related revised manuscript text: The multiple analyses in the studies chose in the meta also led to the high value of I2. Manuscript location: Page 12, line 17- in the revised manuscript. Reviewer #4: In their response letter, authors claim that recent study showed that TMZ did not add any benefit in the treatment of IDH wildtype glioblastoma compared with radiotherapy alone, regardless of MGMT promoter status (https://pubmed.ncbi.nlm.nih.gov/34000245/. This is simply a misinterpretation: Adjuvant temozolomide chemotherapy, but not concurrent temozolomide chemotherapy, was associated with a survival benefit in patients with 1p/19q non-co-deleted anaplastic gliomas. I suggest to change the passages in Discussion accordingly. I suggest to re-write the conclusion and state that the effects of the two drugs were shown in an in-vitro animal model under laboratory circumstances, and that it by no means suggest a positive clinical perspective for patients with necessity of further studies. Response: Thanks. The reviewer’s comment appears to not correspond to our paper. Attachments Attachment Submitted filename: Response to reviewers_0701.docx https://doi.org/10.1371/journal.pone.0308070.r002
7 Jul 2024 Decision Letter - Andreas K Demetriades, Editor PONE-D-24-02588R1Efficacy and safety of tranexamic acid on blood loss and seizures in patients undergoing meningioma resection: a systematic review and meta-analysisPLOS ONE Dear Dr. Peng, 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 Aug 21 2024 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, Andreas K Demetriades, MBBChir, MPhil, FRCSEd, FEBNS. 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. [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 #4: 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 #4: Yes ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #4: 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 #4: 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 #4: 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: The authors have made suggested changes. Reviewer #4: Authors present a revised version of their manuscript -systematic review on role of transexamic acid in resection of meningiomas for prevention of postoperative bleeding as well as on prevention of seizures, where following anaylsis of four cohorts and more than 700 patients their main conclusion was that TXE reduces blood loss without increasing the risk of seizures. All limitations which were adressed, such as the fact that 3/4 cohort studies did not report use of anticonvulsive therapy - this needs to be adressed in the Conclusions and in Discussion. ****** 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 #4: 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. 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.0308070.r003
Revision 2
14 Jul 2024 Author Response Response to Reviewers: Reviewer #4: Authors present a revised version of their manuscript -systematic review on role of transexamic acid in resection of meningiomas for prevention of postoperative bleeding as well as on prevention of seizures, where following anaylsis of four cohorts and more than 700 patients their main conclusion was that TXA reduces blood loss without increasing the risk of seizures. All limitations which were adressed, such as the fact that 3/4 cohort studies did not report use of anticonvulsive therapy - this needs to be adressed in the Conclusions and in Discussion. Response: Thanks. We accepted your suggestion and added the limitation in the part of the conclusion and discussion. Related revised manuscript text: Last, though two of the four studies excluded patients with preoperative seizures, only one study reported the use of anticonvulsive therapy, leading to an inconclusive effect of TXA on postoperative seizure. However, due to the heterogeneity of studies, the impact of TXA on the risk of seizure or other postoperative complications remains inconclusive. Large multi-center clinical trials are needed to fully confirm the effect of TXA administration in saving blood loss and postoperative seizures in the neurosurgical population. Manuscript location: Page 13, line 6-8, line 13-16- in the revised manuscript. Attachments Attachment Submitted filename: LS-reviewer comments-0711.docx https://doi.org/10.1371/journal.pone.0308070.r004
17 Jul 2024 Decision Letter - Andreas K Demetriades, Editor Efficacy and safety of tranexamic acid on blood loss and seizures in patients undergoing meningioma resection: a systematic review and meta-analysis PONE-D-24-02588R2 Dear authors 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 will be generated when your article is formally accepted. Please note, if your institution has a publishing partnership with PLOS and your article meets the relevant criteria, all or part of your publication costs will be covered. Please make sure your user information is up-to-date by logging into Editorial Manager at Editorial Manager® and clicking the ‘Update My Information' link at the top of the page. If you have any questions relating to publication charges, 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, Andreas K Demetriades, MBBChir, MPhil, FRCSEd, FEBNS. 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 #4: 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 #4: Yes ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #4: 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 #4: 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 #4: 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 #4: Authors have sufficiently responded to reviewer remarks. I suggest this manuscirpt for publication. ****** 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 #4: No ******** https://doi.org/10.1371/journal.pone.0308070.r005
Formally Accepted
19 Jul 2024 Acceptance Letter - Andreas K Demetriades, Editor PONE-D-24-02588R2 PLOS ONE Dear Dr. Peng, I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now being handed over to our production team. At this stage, our production department will prepare your paper for publication. This includes ensuring the following: * All references, tables, and figures are properly cited * All relevant supporting information is included in the manuscript submission, * There are no issues that prevent the paper from being properly typeset If revisions are needed, the production department will contact you directly to resolve them. If no revisions are needed, you will receive an email when the publication date has been set. At this time, we do not offer pre-publication proofs to authors during production of the accepted work. Please keep in mind that we are working through a large volume of accepted articles, so please give us a few weeks to review your paper and let you know the next and final steps. Lastly, 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 Dr. Andreas K Demetriades Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0308070.r006

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