Clinical characteristics and risk factors for rebleeding in uremic patients with obscure gastrointestinal bleeding undergoing deep enteroscopy: A multi-center retrospective study in Taiwan

Hsuan-Jen Hung; Chen-Shuan Chung; Chi-Ming Tai; Chen-Wang Chang; Chao-Ming Tseng; Go-Shine Huang; Meng-Chiung Lin; Tien-Yu Huang

doi:10.1371/journal.pone.0277434

Peer Review History

Original SubmissionJune 4, 2022
19 Jul 2022 Decision Letter - Hsu-Heng Yen, Editor PONE-D-22-16076Clinical characteristics and risk factors for rebleeding in uremic patients with obscure gastrointestinal bleeding undergoing deep enteroscopy: a multi-center retrospective study in TaiwanPLOS ONE Dear Dr. Huang, 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. The manuscript has been evaluated by two experts in the filed and significant improvement is required. Please submit your revised manuscript by Sep 02 2022 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. 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Please remove any funding-related text from the manuscript and let us know how you would like to update your Funding Statement. Currently, your Funding Statement reads as follows: The authors received no specific financial funding for this work. Please include your amended statements within your cover letter; we will change the online submission form on your behalf. [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: Partly ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: No Reviewer #2: I Don't Know ****** 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: 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: Authors proposed clinical characteristics and risk factors for rebleeding in uremic patients with obscure gastrointestinal bleeding undergoing deep enteroscopy. It would give another point of view for clinical daily practice. I have several questions as below. 1. In statistical analysis, continuous variables should be analyzed using the Mann–Whitney U test. Therefore, I suggest authors may recheck the P value for continuous variables in table 4 and 5. 2. In table 4 and 5, authors presented the characteristics and "factors" between subgroups with/without rebleeding or with/without angiodysplsia. Moreover, authors should calculate the odds ratios for these risk factors which were determined through univariate and multivariate logistic regression analyses in another tables. 3. In table 4, I don't know the meaning (no data) about "location of bleeding" between subgroups with/without rebleeding. Reviewer #2: Appreciate the authors providing us about the risk factors for rebleeding in uremic patients with obscure GI bleeding My comment: 1. There is no clear mention about definition of "rebleeding" in the article. There is no detailed statements about lesions with rebleeding. What is the most common lesion type of rebleeding, angiodysplasia or ulcer? 2. Eight patients with VHD and 4 of then with severe aortic stenosis and 4 patient were non-AS patients. Have you performed subgroup analysis for the relationship between OGIB and non-AS patients ? Many patients with VHD take antiplatelet or anticoagulation for prevention of thrombotic events. Have you analyze the effect of OGIB in anti-thrombotic agent for patient with VHD ? Your statistical analysis should manage the possible confounding factors of rebleeding. 3. No “Age” included in the clinical characteristics in table 1. 4. Table 1: What is the details of anti-thrombotic agents (antiplatelet ? warfarin ? DOAC ? ) Dose each subtype of anti-thrombotic agent have effect on OGIB? 5. Table 3: Endoscopic intervention for what kinds of bleeder ? Four patient received surgery or TAE and what is the cause of bleeding ? Different etiology of bleeding may be one of the risk factor of rebleeding. 6. You did not mention the endoscopic appearance of angiodysplasia. There are different types of angiodysplasia (Yano –Yamamoto classification) and each had different rebleeding rate. You should analyze the rebleeding risk between different subtype of angiodysplasia. 7. There are multiple grammatical mistakes throughout the manuscript, I would recommend the authors revise the manuscript and consult English editing. ****** 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. 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.0277434.r001
Revision 1
20 Sep 2022 Author Response Responses to Reviewers’ comments: Reviewer #1: Authors proposed clinical characteristics and risk factors for rebleeding in uremic patients with obscure gastrointestinal bleeding undergoing deep enteroscopy. It would give another point of view for clinical daily practice. I have several questions as below. 1. In statistical analysis, continuous variables should be analyzed using the Mann–Whitney U test. Therefore, I suggest authors may recheck the P value for continuous variables in table 4 and 5. A: Thank you for your reminder. We rechecked the statistical analysis in detail and revised the manuscript in the “Materials and Methods” section and in Tables 4 and 5. 2. In table 4 and 5, authors presented the characteristics and "factors" between subgroups with/without rebleeding or with/without angiodysplsia. Moreover, authors should calculate the odds ratios for these risk factors which were determined through univariate and multivariate logistic regression analyses in another tables. A: Thank you for your comments. We reperformed the statistical analysis and added the odds ratios from univariate and multivariate analyses in Tables 4 and 5. In Table 4, two factors (valvular heart disease and use of anti-thrombotic agents—correlated with VHD in clinical use) were entered into the multivariate logistical regression model. In Table 5, only the P-value of “rebleeding” was significant on univariate analysis, which was then entered into the multivariate logistical regression model. 3. In table 4, I don't know the meaning (no data) about "location of bleeding" between subgroups with/without rebleeding. A: Thank you for your question. The location of bleeding refers to the location of bleeder. We revised Table 4 and performed statistical analysis further in different locations. Reviewer #2: Appreciate the authors providing us about the risk factors for rebleeding in uremic patients with obscure GI bleeding 1. There is no clear mention about definition of "rebleeding" in the article. There is no detailed statements about lesions with rebleeding. What is the most common lesion type of rebleeding, angiodysplasia or ulcer? A: Thanks for your comment. The definition of rebleeding was described in “Materials and Methods” in the revised manuscript. However, not all patients with rebleeding underwent repeat deep enteroscopy; the actual etiology of rebleeding could thus not be clarified clearly. However, referring to the past literature and our indirect data (in the patients with different bleeding types, the rebleeding rate of angiodysplasia type vs. non-angiodysplasia type was 34% vs. 6.7%), the most common type of re-bleeding was likely to have been angiodysplasia. We put this issue into the “Discussion” section. 2. Eight patients with VHD and 4 of then with severe aortic stenosis and 4 patient were non-AS patients. Have you performed subgroup analysis for the relationship between OGIB and non-AS patients ? Many patients with VHD take antiplatelet or anticoagulation for prevention of thrombotic events. Have you analyze the effect of OGIB in anti-thrombotic agent for patient with VHD ? Your statistical analysis should manage the possible confounding factors of rebleeding. A: Given that only four patients had non-AS VHD, we did not further determine the relationship between OGIB and non-AS patients. As for the confounding effect of anti-thrombotic agents in patients with VHD, we adjusted for this factor using multivariate logistical regression analysis, and VHD still showed a statistically significant difference between the rebleeding and non-rebleeding groups (p=0.047). 3. No “Age” included in the clinical characteristics in table 1. A: Thank you for pointing this out. The age has been included in the top row of Table 1 (marked in Red). 4. Table 1: What is the details of anti-thrombotic agents (antiplatelet? warfarin? DOAC?) Dose each subtype of anti-thrombotic agent have effect on OGIB? A: In 25 patients who received antithrombotic agents (32.1%), 16 received aspirin and 9 received clopidogrel. We revised Table 1 accordingly. In our statistical analysis, the diffent types of anti-thrombotic agents showed no significalnt differences between the rebleeding and no rebleeding-groups (data no shown). 5. Table 3: Endoscopic intervention for what kinds of bleeder? Four patient received surgery or TAE and what is the cause of bleeding? Different etiology of bleeding may be one of the risk factor of rebleeding. A: Thank you for your comments. In our study, three patients underwent segmental bowel resection (two cases of jejunual angiodysplasia and one of ileal varices), and one patient with jejunal multiple angiodysplasia underwent transarterial embolization after failure of endoscopic intervention. This point was added to the “Results” section of the revised manuscript. 6. You did not mention the endoscopic appearance of angiodysplasia. There are different types of angiodysplasia (Yano –Yamamoto classification) and each had different rebleeding rate. You should analyze the rebleeding risk between different subtype of angiodysplasia. A: Thank you for your constructive comment. As per the Yano-Yamamoto classification, angiodysplasia was classified as type I (type Ia and Ib). Dieurofoy’s lesion was classified as type 2, AVM was classed as type 3, and unclassified lesion was classed as type 4. Therefore, our enrolled patients with angiodysplasia had type 1 vascular lesion and we did not determine the effect of different subtypes of angiodysplasia (type Ia and Ib) on rebleeding. However, whether the different types of vascular lesions in the small bowel can affect the rebleeding rate in uremic patients with OGIB needs further determination. We discussed this concern in the “Discussion” section. 7. There are multiple grammatical mistakes throughout the manuscript, I would recommend the authors revise the manuscript and consult English editing. A: Thanks for your positive comment. We have gotten the manuscript edited by a professional English language-editing service. Attachments Attachment Submitted filename: Reviewer_PLOS_N.docx https://doi.org/10.1371/journal.pone.0277434.r002
17 Oct 2022 Decision Letter - Hsu-Heng Yen, Editor PONE-D-22-16076R1Clinical characteristics and risk factors for rebleeding in uremic patients with obscure gastrointestinal bleeding undergoing deep enteroscopy: a multi-center retrospective study in TaiwanPLOS ONE Dear Dr. Huang, 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 01 2022 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, Hsu-Heng Yen 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 #2: (No Response) Reviewer #3: 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 #2: Partly Reviewer #3: Yes ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #2: I Don't Know Reviewer #3: 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 #2: Yes Reviewer #3: 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 #2: No Reviewer #3: 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 #2: Appreciate the authors revising the manuscripts with efforts. #1 Page 7 line 92-95 The sentence can be deleted “After being informed of the needs and potential complications of SBE, all patients signed an informed consent form. The requirement for patient consent for publication was waived because the patient information was anonymized and de-identified prior to analysis.”. You have repeated the same words in page 7, line 106-108. # 2 Page 7 line 104 Why the definition of rebleeding is “ the evidence of recurrent overt gastrointestinal bleeding with recent negative EGD and colonoscopy and/or a drop in the Hb level…..” ? Why not enteroscopy (SBE)? The purpose of manuscript as you mentioned was to “identify the clinical characteristics of uremic patients receiving SBE for OGIB and analyze the risk factors “ #3 Figure 1: I suggest that the author try to simplify the figure and remove redundant words. Otherwise this picture looks unnecessary. #4 Page 17 line 194-196 ?? “As lesions in the small intestine are similar to those in other gastrointestinal areas such as the stomach or large intestine, they can be diagnosed and treated by traditional EGD or colonoscopy. “ Does the author really express what you want to express correctly? #5 There are multiple grammatical mistakes throughout the manuscript, I strongly recommend the author revise the manuscript and consult English editing again. Reviewer #3: The authors purpose to identify the clinical characteristics of uremic patients undergoing deep enteroscopy for OGIB and analyze the risk factors for rebleeding after deep enteroscopy. Authors concluded that uremic patients with angiodysplasia-related bleeding appear to have a higher rebleeding rate and VHD is an independent risk factor associated with rebleeding after deep enteroscopy in uremic patients with OGIB. I think this article might give us an alternative point of view in our clinical management in uremic patients with OGIB. ****** 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 #2: No Reviewer #3: Yes: Wei-Chen Tai ******** [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.0277434.r003
Revision 2
26 Oct 2022 Author Response Responses to Reviewers’ comments: Reviewer #2: Appreciate the authors revising the manuscripts with efforts. #1 Page 7 line 92-95 The sentence can be deleted “After being informed of the needs and potential complications of SBE, all patients signed an informed consent form. The requirement for patient consent for publication was waived because the patient information was anonymized and de-identified prior to analysis.”. You have repeated the same words in page 7, line 106-108. A: Thank you for your comment. We have revised the manuscript. # 2 Page 7 line 104 Why the definition of rebleeding is “ the evidence of recurrent overt gastrointestinal bleeding with recent negative EGD and colonoscopy and/or a drop in the Hb level…..” ? Why not enteroscopy (SBE)? The purpose of manuscript as you mentioned was to “identify the clinical characteristics of uremic patients receiving SBE for OGIB and analyze the risk factors “ A: Thank you for your comment. Among the 78 uremic patients with OGIB receiving SBE, not all patients with recurrent GI bleeding underwent repeat EGD, colonoscopy, or SBE. Therefore, we defined rebleeding as the evidence of recurrent overt gastrointestinal bleeding (melena or hematochezia) with recent negative EGD and colonoscopy and/or a drop in the hemoglobin level by >2 g/dl. #3 Figure 1: I suggest that the author try to simplify the figure and remove redundant words. Otherwise this picture looks unnecessary. A: As suggested, we have simplified Figure 1 in the revised manuscript. #4 Page 17 line 194-196 ?? “As lesions in the small intestine are similar to those in other gastrointestinal areas such as the stomach or large intestine, they can be diagnosed and treated by traditional EGD or colonoscopy. “ Does the author really express what you want to express correctly? A: Thank you for your kind comment. We have revised the content of this paragraph to express our meaning correctly. #5 There are multiple grammatical mistakes throughout the manuscript, I strongly recommend the author revise the manuscript and consult English editing again. A: Thank you for pointing it out. I have further consulted an English editing service and revised this manuscript. Attachments Attachment Submitted filename: Reviewer_POLS_20221024.docx https://doi.org/10.1371/journal.pone.0277434.r004
27 Oct 2022 Decision Letter - Hsu-Heng Yen, Editor Clinical characteristics and risk factors for rebleeding in uremic patients with obscure gastrointestinal bleeding undergoing deep enteroscopy: a multi-center retrospective study in Taiwan PONE-D-22-16076R2 Dear Dr. Huang, 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, Hsu-Heng Yen Academic Editor PLOS ONE Additional Editor Comments (optional): Reviewers' comments: https://doi.org/10.1371/journal.pone.0277434.r005
Formally Accepted
18 Nov 2022 Acceptance Letter - Hsu-Heng Yen, Editor PONE-D-22-16076R2 Clinical characteristics and risk factors for rebleeding in uremic patients with obscure gastrointestinal bleeding undergoing deep enteroscopy: a multi-center retrospective study in Taiwan Dear Dr. Huang: 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. Hsu-Heng Yen Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0277434.r006

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