Anatomical analysis of antebrachial cutaneous nerve distribution pattern and its clinical implications for sensory reconstruction

Hui Li; Weiwei Zhu; Shouwen Wu; Zairong Wei; Shengbo Yang

doi:10.1371/journal.pone.0222335

Peer Review History

Original SubmissionJune 22, 2019
10 Jul 2019 Decision Letter - Leila Harhaus, Editor PONE-D-19-16142 Anatomical Analysis of Antebrachial Cutaneous Nerve Distribution Pattern and Its Clinical Implications for Sensory Reconstruction PLOS ONE Dear Dr Yang, 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. We would appreciate receiving your revised manuscript by Aug 24 2019 11:59PM. When you are 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. If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. 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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 Reviewer #3: Yes ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: N/A Reviewer #2: Yes Reviewer #3: 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 Reviewer #3: 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 Reviewer #3: 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: The paper is original and adds to the knowledge base in this area using a novel approach to staining and defining the branching anatomy. The paper is well written and no substantial revisions are required. In line 73 the “A” should be non capital and in line 173 there should be a space between “Fig” and “3”. Reviewer #2: DEAR AUTHOR, THIS STUDY IS A VERY GOOD CADAVERIC WORK, DISPLAYING FOREARM SENSITIVE DISTRUBUTION WITH SOME LIMITATIONS CONCERNING RACE DIFFERENCES. HOWEVER CLINICAL USE OF THIS KNOWLEDGE ( YOUR FINDINGS ) IS DEBATABLE SINCE, FLAP ELEVATION STILL DEPENDS ON VASCULAR (PERFORATOR VESSEL) DISTRIBUTION. I HAVE SOME DOUBTS REGARDING DONOR AREA SENSITIVE NERVE THICKNESS IS DIRECTLY CORRELATED WITH BETTER SENSITIVE OUTCOME, YOU WOULD RATHER SMOOTHEN YOUR IDEAS OR SUPPORT WTH MORE DATA. Reviewer #3: This study describes distribution of forearm cutaneous nerves including gross anatomy, main and minor branches, interconnections and density. One of the aims is to give clinical suggestions to improve flap design in a matter or sensory reconstruction at recipient site and possible sensory loss at donor site. The study is well designed and appropriate methods were used including application of modified Sihler's staining to reveal and analyze cutaneous distribution. Advantages: - novel data about branches distribution, density and interconnections between major antebrachial nerves Disadvantages: - the process of pictures conversion and further image processing is not well described - although authors describe the results thickness, area and nerve branch density of each region (p.10) they provide only general ANOVA result (p. 11) without post-hoc analysis - clinical implications are hard to drawn due to big amount of data in multiple regions - most suitable donor sites could be marked on separate figure In the summary the study gives relevant and precise anatomical information but clinical implications are not so clear to me at this moment. ****** 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: Yes: Piotr Czarnecki [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 to be viewed.] 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 us at figures@plos.org. Please note that Supporting Information files do not need this step. https://doi.org/10.1371/journal.pone.0222335.r001
Revision 1
25 Jul 2019 Author Response Jul 25, 2019 Academic Editor, PLoS One PONE-D-19-16142 Dear Editor: Thank you for your letter on Jul 25, 2019 regarding this manuscript. We would also like to thank the reviewers for their helpful comments. We are now submitting a revised version as detailed below that addresses these comments (original comments from reviewers and the editor are in italics). All changes have been indicated in red in the revised manuscript. Response to Reviewer#1: The paper is original and adds to the knowledge base in this area using a novel approach to staining and defining the branching anatomy. The paper is well written and no substantial revisions are required. In line 73 the “A” should be non capital and in line 173 there should be a space between “Fig” and “3” Response: Thank you for your positive comments. As for the two errors you pointed out, we have revised the text accordingly. Response to Reviewer #2: 1. THIS STUDY IS A VERY GOOD CADAVERIC WORK, DISPLAYING FOREARM SENSITIVE DISTRUBUTION WITH SOME LIMITATIONS CONCERNING RACE DIFFERENCES. Response: (1) Thank you for your positive comment. (2) Because of the restrictions specimen resource, Our study could not answer racial differences indeed. (3) However, we did the following literature search about the current understanding of the “SENSITIVE DISTRUBUTION” in different races: ① Antebrachial Cutaneous Nerve trunk and its main branches’ distribution have been reported by authors in American, China, Austria, and Korea [1-8]. The nerve distributions described in these studies are essentially consistent. There are variations between individual samples but none mentioned racial differences. ② Studies by Lauria et al show that there are racial differences in cutaneous innervation of the leg among European, American and Asian populations [9]. However, Collongues et al. found that no racial difference showed in clinical correlations [10]. ③ Tenny et al [11] in 1984 used the lateral antebrachial cutaneous nerve graft for traumatic digital nerve defects where they found that “age” was a more important prognostic factor for sensibility. However, The study did not mention racial differences. ④ Our study is about the overall display and comparison of the forearm nerve distribution density in each region. As far as we know, neurosensitivity cannot be equated with nerve density, and sensitivity may be affected by gender, age, personal living conditions, etc. In general, we hope that further research in the future will confirm whether there are racial differences in the forearm nerve distribution. 1. Finneran JJ, Sandhu N. Ultrasound-Guided Posterior Antebrachial Cutaneous Nerve Block: Technical Description and Block Distribution in Healthy Volunteers. J Ultrasound Med. 2019; 38: 239-242. doi: 10.1002/jum.14678. PMID: 29732596. 2. Singhal S, Rao VV, Ravindranath R. Variations in brachial plexus and the relationship of median nerve with the axillary artery: A case report. J Brachial Plex Peripher Nerve Inj. 2007; 2: 21. doi: 10.1186/1749-7221-2-21. PMID: 17915015. 3. Race CM, Saldana MJ. Anatomic course of the medial cutaneous nerves of the arm. J Hand Surg Am. 1991; 16: 48–52. PMID: 1995693. 4. Zhang FH, Topp SG, Zhang WJ, Zheng HP, Zhang F. Anatomic study of distally based pedicle compound flaps with nutrient vessels of the cutaneousnerves and superficial veins of the forearm. Microsurgery. 2006; 26: 373-85. doi: 10.1002/micr.20255. PMID: 16783807. 5. Benedikt S, Parvizi D, Feigl G, Koch H. Anatomy of the medial antebrachial cutaneous nerve and its significance in ulnar nerve surgery: An anatomical study. J Plast Reconstr Aesthet Surg. 2017 Nov; 70: 1582-1588. doi: 10.1016/j.bjps.2017.06.025. PMID: 28756975. 6. Moritz T, Prosch H, Pivec CH, et al. High-resolution ultrasound visualization of the subcutaneous nerves of the forearm: A feasibility study in anatomic specimens. Muscle Nerve. 2014; 49: 676-679. doi: 10.1002/mus.24064. PMID: 24038104. 7. Im HS, Im JY, Kim KH,Kim DH, Park BK. Ultrasonographic Study of the Anatomical Relationship Between the Lateral Antebrachial Cutaneous Nerve and the Cephalic Vein. Ann Rehabil Med. 2017; 41: 421-425. doi: 10.5535/arm.2017.41.3.421. PMID: 28758079. 8. Oh CH, Park NS, Kim JM, Kim MW. Determination of an ideal stimulation site of the medial antebrachial cutaneous nerve using ultrasound and investigation of the efficiency. Ann Rehabil Med. 2014; 38: 836–842. doi: 10.5535/arm.2014.38.6.836. PMID: 25566484. 9. Lauria G, Bakkers M, Schmitz C, Lombardi R, Penza P, Devigili G, et al. Intraepidermal nerve fiber density at the distal leg: a worldwide normative reference study. J Peripher Nerv Syst. 2010; 15: 202–207. doi: 10.1111/j.1529-8027.2010.00271.x. PMID: 21040142. 10. Collongues N, Samama B, Schmidt-Mutter C, Chamard-Witkowski L, Debouverie M, Chanson JB. et al. Quantitative and qualitative normativedataset for intraepidermal nerve fibers usingskin biopsy. PLOS ONE. 2018; 13: e0191614. doi: 10.1371/journal.pone.0191614. PMID: 29370274. 11. Tenny JR, Lewis RC. Digital nerve-grafting for traumatic defects. Use of the lateral antebrachial cutaneous nerve.JBone Joint Surg Am. 1984; 66: 1375–1379. PMID: 6501333. 2. CLINICAL USE OF THIS KNOWLEDGE ( YOUR FINDINGS ) IS DEBATABLE SINCE, FLAP ELEVATION STILL DEPENDS ON VASCULAR (PERFORATOR VESSEL) DISTRIBUTION. I HAVE SOME DOUBTS REGARDING DONOR AREA SENSITIVE NERVE THICKNESS IS DIRECTLY CORRELATED WITH BETTER SENSITIVE OUTCOME, YOU WOULD RATHER SMOOTHEN YOUR IDEAS OR SUPPORT WTH MORE DATA. Response: We completely agree with you: “FLAP ELEVATION STILL DEPENDS ON VASCULAR (PERFORATOR VESSEL) DISTRIBUTION”. Our study aimed at improving the quality of the flaps by considering the recipient sensory recovery so that the clinicians can use this knowledge to guide the design of the flaps. We have also expressed these views in " Introduction, Paragraph 2 ". The theoretical design of this study is based on references 28-30 listed in this paper. Please also refer to the “Discussion section, paragraph 5”. “Sensory reconstruction primarily occurs as follows: the reception area and surrounding nerve fibers grow into the flap through the scar tissue (peripheral manner), or the recipient nerves are anastomosed with the main innervating nerve of the flap (central manner). The direction of nerve regeneration can be guided by the alignment of nerve tissues, so that Schwann cells at both ends can directly restore material communication channels, and the regenerated nerve fibers can grow smoothly into the distal neurotubules [28]. However, the important factors for flap recovery are distribution of sensory nerves in the donor site of the flap, the choice of the cutaneous nerve, and its anastomotic site [29, 30]. Therefore, if the recipient nerve is rich, a rich donor nerve should be matched to increase the probability of nerve contact.” We hope that this reviewer will accept our views. 28. Ide C, Tohyama K, Yokota R, Nitatori T, Onodera S. Schwann cell basal lamina and nerve regeneration. Brain Res. 1983; 288: 61-75. doi: 10.1016/0006-8993(83)90081-1. PMID: 6661636. 29. Feng SM, Wang AG, Zhang ZY, Sun QQ, Tao YL, Zhou MM, et al. Repair and sensory reconstruction of the children's finger pulp defects with perforator pedicled propeller flap in proper digital artery. Eur Rev Med Pharmacol Sci. 2017; 21: 3533-3537. PMID: 28925493. 30. Zhu L, Zhang J, Song X, Hou W, Wu S, Chen W, et al. Sensory recovery of non-innervated free flaps and nasolabial island flaps used for tongue reconstruction of oncological defects. J Oral Rehabil. 2017; 44: 736-748. doi: 10.1111/joor.12510. PMID: 28370156. Response to Reviewer #3: 1. Advantages：omit. 2. Disadvantages: - the process of pictures conversion and further image processing is not well described. - although authors describe the results thickness, area and nerve branch density of each region (p.10) they provide only general ANOVA result (p. 11) without post-hoc analysis - clinical implications are hard to drawn due to big amount of data in multiple regions - most suitable donor sites could be marked on separate figure. Response: In order to better intuitively understand the ideal donor sites, we have marked in Figs 4A and 4B. We did not add new figures for the concern of reducing the pages of the manuscript. About the clinical significance of this study: We analyzed the clinical application of three cutaneous nerves in the forearm based on the experimental results. These descriptions are in the fourth paragraph of the discussion section. We added post-hoc analysis in statistical processing (see revised text). Response to Editor Thank you for your consideration of this revision. The editing of the text is based on the template of your journal. Sincerely, Shengbo Yang Department of Anatomy Zunyi Medical University Attachments Attachment Submitted filename: Response to Reviewers.doc https://doi.org/10.1371/journal.pone.0222335.r002
22 Aug 2019 Decision Letter - Leila Harhaus, Editor PONE-D-19-16142R1 Anatomical Analysis of Antebrachial Cutaneous Nerve Distribution Pattern and Its Clinical Implications for Sensory Reconstruction PLOS ONE Dear Dr Yang, 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. We would appreciate receiving your revised manuscript by Oct 06 2019 11:59PM. When you are 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. If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. To enhance the reproducibility of your results, we recommend that if applicable you deposit your laboratory protocols in protocols.io, where a protocol can be assigned its own identifier (DOI) such that it can be cited independently in the future. For instructions see: http://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols 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). This letter should be uploaded as separate file and labeled 'Response to Reviewers'. A marked-up copy of your manuscript that highlights changes made to the original version. This file should be uploaded as separate file and labeled 'Revised Manuscript with Track Changes'. An unmarked version of your revised paper without tracked changes. This file should be uploaded as separate file and labeled 'Manuscript'. Please note while forming your response, if your article is accepted, you may have the opportunity to make the peer review history publicly available. The record will include editor decision letters (with reviews) and your responses to reviewer comments. If eligible, we will contact you to opt in or out. We look forward to receiving your revised manuscript. Kind regards, Leila Harhaus Academic Editor PLOS ONE 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: All comments have been addressed 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: Yes Reviewer #3: Yes ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #2: Yes 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: Yes 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: Forearm sensitive nerve distrubution is important in terms of donor area selection and flap choices so I think your manuscript will be usefull for the scientists dealing with this subject.However terminology is important as well so all "anastomosis" words must be replaced with coaptation or neuroraphy. Reviewer #3: (No Response) ****** 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: Yes: ATAKAN AYDIN Reviewer #3: Yes: Piotr Czarnecki [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 to be viewed.] 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 us at figures@plos.org. Please note that Supporting Information files do not need this step. https://doi.org/10.1371/journal.pone.0222335.r003
Revision 2
25 Aug 2019 Author Response Aug 25, 2019 Academic Editor, PLOS ONE PONE-D-19-16142R1 Dear Editor: Thank you for your letter on Aug 23, 2019 regarding this manuscript. We would also like to thank the reviewers for their helpful comments. We are now submitting a revised version as detailed below that addresses these comments (original comments from reviewers and the editor are in italics). All changes have been indicated in red in the revised manuscript. Response to Reviewer#2: Forearm sensitive nerve distrubution is important in terms of donor area selection and flap choices so I think your manuscript will be usefull for the scientists dealing with this subject. However terminology is important as well so all "anastomosis" words must be replaced with coaptation or neuroraphy. Response: Thank you for your positive comment. According to your comments, we have replaced "anastomosis" with coaptation. Response to Editor: We have revised the text in accordance with the comments of the reviewers. Sincerely, Shengbo Yang Department of Anatomy Zunyi Medical University Attachments Attachment Submitted filename: Response to Reviewers.doc https://doi.org/10.1371/journal.pone.0222335.r004
28 Aug 2019 Decision Letter - Leila Harhaus, Editor Anatomical Analysis of Antebrachial Cutaneous Nerve Distribution Pattern and Its Clinical Implications for Sensory Reconstruction PONE-D-19-16142R2 Dear Dr. Yang, We are pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it complies with all outstanding technical requirements. Within one week, you will receive an e-mail containing information on the amendments required prior to publication. When all required modifications have been addressed, you will receive a formal acceptance letter and your manuscript will proceed to our production department and be scheduled for publication. Shortly after the formal acceptance letter is sent, an invoice for payment will follow. To ensure an efficient production and billing process, please log into Editorial Manager at https://www.editorialmanager.com/pone/, click the "Update My Information" link at the top of the page, and update your user information. 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 enable them to help maximize its impact. If they will be preparing press materials for this manuscript, you must inform our press team as soon as possible and 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. With kind regards, Leila Harhaus Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0222335.r005
Formally Accepted
4 Sep 2019 Acceptance Letter - Leila Harhaus, Editor PONE-D-19-16142R2 Anatomical Analysis of Antebrachial Cutaneous Nerve Distribution Pattern and Its Clinical Implications for Sensory Reconstruction Dear Dr. Yang: I am 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 notify them about your upcoming paper at this point, to enable them to help maximize its impact. If they will be preparing press materials for this manuscript, 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. For any other questions or concerns, please email plosone@plos.org. Thank you for submitting your work to PLOS ONE. With kind regards, PLOS ONE Editorial Office Staff on behalf of Prof. Dr. med. Leila Harhaus Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0222335.r006

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