Second breast cancer following negative breast MRI: Analysis by interval from surgery and risk factors

Yohan Joo; Min Jung Kim; Jung Hyun Yoon; Miribi Rho; Vivian Youngjean Park

doi:10.1371/journal.pone.0306828

Peer Review History

Original SubmissionJanuary 12, 2024
8 Apr 2024 Decision Letter - Daniele Ugo Tari, Editor PONE-D-24-00795Second breast cancer following negative breast MRI: analysis by interval from surgery and risk factorsPLOS ONE Dear Dr. Park, 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 May 23 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, Daniele Ugo Tari, M.D. Academic Editor PLOS ONE Journal requirements: 1. When submitting your revision, we need you to address these additional requirements. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at https://journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and https://journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf. 2. We noticed you have some minor occurrence of overlapping text with the following previous publication(s), which needs to be addressed: Outcomes Following Negative Screening MRI Results in Korean Women with a Personal History of Breast Cancer: Implications for the Next MRI Interval - https://doi.org/10.1148/radiol.2021204217 In your revision ensure you cite all your sources (including your own works), and quote or rephrase any duplicated text outside the methods section. Further consideration is dependent on these concerns being addressed. 3. Please include your full ethics statement in the ‘Methods’ section of your manuscript file. In your statement, please include the full name of the IRB or ethics committee who approved or waived your study, as well as whether or not you obtained informed written or verbal consent. If consent was waived for your study, please include this information in your statement as well. 4. Please include captions for your Supporting Information files at the end of your manuscript, and update any in-text citations to match accordingly. Please see our Supporting Information guidelines for more information: http://journals.plos.org/plosone/s/supporting-information. 5. 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. Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented. Reviewer #1: Yes Reviewer #2: Yes ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #2: Yes ****** 3. Have the authors made all data underlying the findings in their manuscript fully available? The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified. Reviewer #1: Yes Reviewer #2: Yes ****** 4. Is the manuscript presented in an intelligible fashion and written in standard English? PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here. Reviewer #1: Yes Reviewer #2: Yes ****** 5. Review Comments to the Author Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters) Reviewer #1: Although it did not have any effect on my acceptance when I evaluated the current article, patients receiving neoadjuvant chemotherapy could have been excluded to ensure homogeneity when selecting the patients in the sample. I don't say that this should have been done because it would not affect its contribution to the literature when compared to similar articles in the literature. The subject is an area of my interest and in which I follow the literature, and it is written carefully and the data results are well-examined in the discussion. Therefore, I think there is no need for revision in the article. Reviewer #2: This retrospective study on second breast cancers following negative breast MRI examinations is well written and practical. 1. In Abstract Objectives, the first sentence needs clarification. 2. In Abstract Results, the second sentence needs re-writing. Second breast cancers is duplicated in that sentence. In that sentence, I suggest starting the sentence with The incidence. In the third sentence, I suggest starting the sentence with The median intervals. In the third sentence and throughout the paper, the two groups should be clearly defined. In the last sentence of Abstract Results, the authors should indicate that BRCA mutations, breast conservation therapy, and adjuvant chemotherapy were significant factors for developing a second breast cancer. 3. In Introduction, 1st paragraph, last sentence, years should be added after 50. 4. In Methods, MRI evaluation, 1st sentence, lexicon should be added after BI-RADS. In the last sentence, I suggest changing imaging to MRI. 5. In Methods, Statistical analysis, the second paragraph needs clarification and the sentence should start with The incidence. 6. In Results, Patient characteristics, last sentence, I suggest: and ductal carcinoma in situ (DCIS) in 225 (14.5%) patients. 7. In Results, Overall outcomes after surveillance MRI, 1st paragraph, 1st sentence, I suggest adding a before second 8. In Results, Overall outcomes after surveillance MRI, 2nd paragraph, last sentence, I suggest: after a negative MRI...before the MRI examinations. 9. In Results, Comparison of second breast cancers according to intervals (<3 years vs >3 years) following initial surgery, 1st and 2nd paragraphs, 1st sentence, each group should be defined. 10. In Discussion, 2nd paragraph, 1st sentence, I suggest: only two breast cancers were. 11. In Discussion, 3rd paragraph, 3rd sentence, the should be added before incidence and the two groups should be defined. In the 4th sentence, the should be added between of and period. In the last sentence of that paragraph, factor should be changed to factors. 12. The authors should check the journal's reference style. In references 3, 4, 8, and 12, I think that the first 3 authors should be listed, followed by et al. In references 6, 7, 11-13, 15, and 16, only the first word of the title of the article should be capitalized. 13. I suggest that the authors add a figure showing a second breast cancer identified on MRI. ****** 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: Yes: ONUR DÜLGEROĞLU 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.0306828.r001
Revision 1
11 Apr 2024 Author Response Response to Comments from the Reviewers; Reviewer #1: Although it did not have any effect on my acceptance when I evaluated the current article, patients receiving neoadjuvant chemotherapy could have been excluded to ensure homogeneity when selecting the patients in the sample. I don't say that this should have been done because it would not affect its contribution to the literature when compared to similar articles in the literature. The subject is an area of my interest and in which I follow the literature, and it is written carefully and the data results are well-examined in the discussion. Therefore, I think there is no need for revision in the article. : Response – Thank you for your kind comment. In our study, we did not exclude patients who underwent neoadjuvant chemotherapy, which comprised 16.4% (254 of 1552) of our study sample (Table 1). We agree that this would not have affected our outcomes, as there was no significant difference by surgery-MRI interval. Reviewer #2: This retrospective study on second breast cancers following negative breast MRI examinations is well written and practical. 1. In Abstract Objectives, the first sentence needs clarification. : Response – Thank you for your comment. In our initially submitted manuscript, we had included the first sentence to provide some background on why we performed this study. As the risk of local regional recurrence as a first event after breast cancer treatment decreases with increasing event-free years, outcomes following negative surveillance breast MRI results may differ according to interval from initial surgery. Therefore, the main objective of this study was to compare outcomes following a negative surveillance MRI study by surgery-MRI interval. Upon re-reviewing the manuscript, we acknowledge that this sentence can be confusing in the Abstract and is unnecessary. Therefore, we have deleted it in our revised manuscript. 2. In Abstract Results, the second sentence needs re-writing. Second breast cancers is duplicated in that sentence. In that sentence, I suggest starting the sentence with The incidence. In the third sentence, I suggest starting the sentence with The median intervals. In the third sentence and throughout the paper, the two groups should be clearly defined. In the last sentence of Abstract Results, the authors should indicate that BRCA mutations, breast conservation therapy, and adjuvant chemotherapy were significant factors for developing a second breast cancer. : Response – Thank you for your helpful comment. We have revised the Abstract Results section accordingly (Amended text) • Abstract Results: “The incidence of second breast cancers or local-regional recurrence did not significantly differ by surgery-MRI interval. The median intervals between MRI to second breast cancer detection showed no significant difference between the two groups (surgery-MRI interval <3 years vs. ≥ 3 years). Two node-positive second breast cancers were detected in the group with <3 years interval. BRCA mutation status, receipt of breast-conserving surgery, and adjuvant chemotherapy (all p < .05) were significant factors associated with the development of second breast cancers”, Page 2 in revised clean manuscript. 3. In Introduction, 1st paragraph, last sentence, years should be added after 50. : Response – Thank you for your helpful comment. We have revised the sentence accordingly. (Amended text) • Introduction: “Accordingly, the 2018 American College of Radiology recommendations now recommend annual surveillance with breast MRI for women with a PHBC and dense breast tissue, or those diagnosed before age 50 years [5]”, Page 4 in revised clean manuscript. 4. In Methods, MRI evaluation, 1st sentence, lexicon should be added after BI-RADS. In the last sentence, I suggest changing imaging to MRI. : Response – Thank you for your comment. We have revised the first sentence accordingly. Although follow-up MRI is primarily recommended for BI-RADS category 3 lesions, targeted ultrasound or follow-up ultrasound at 6 months is also performed at our institution. Physicians sometimes opt to order an additional MRI when there is no US correlate. Therefore, we did not change our last sentence. However, we are willing to make changes if necessary in future revisions, as this sentence regards recommendations. (Amended text) • Methods, MRI Evaluation: “One of four radiologists with 8-20 years of experience in breast MRI (including V.Y.P., J.H.Y., and M.J.K.) interpreted the MRI examinations, with findings reported according to the BI-RADS lexicon”, Page 6 of revised clean manuscript. 5. In Methods, Statistical analysis, the second paragraph needs clarification and the sentence should start with The incidence. : Response – Thank you for your comment. We have revised the sentence accordingly, and have added ‘the incidence’ in the middle of the sentence to make it clearer. (Amended text) • Methods, Statistical Analysis: “The incidence of second breast cancers and the incidence of second breast cancer or locoregional recurrence were compared based on intervals between initial surgery and negative surveillance breast MRI (less than 3 years vs. 3 years or more)”, Page 7 of revised clean manuscript. 6. In Results, Patient characteristics, last sentence, I suggest: and ductal carcinoma in situ (DCIS) in 225 (14.5%) patients. : Response – Thank you for your helpful comment. (Amended text) • Results, Patient Characteristics: “The original breast cancer diagnosis was invasive cancer in 1327 (85.5%) and ductal carcinoma in situ (DCIS) in 225 (14.5%) patients”, Page 8 of revised clean manuscript. 7. In Results, Overall outcomes after surveillance MRI, 1st paragraph, 1st sentence, I suggest adding a before second : Response – Thank you for your helpful comment. (Amended text) • Results, Overall outcomes after surveillance MRI: “Of the 1552 women, 38 (2.4%) developed a second breast cancer (1.6%, 25 of 1552) or local-regional recurrence (0.8%, 13 of 1552) during a median follow-up of 34.9 months after negative surveillance MRI (interquartile range [IQR], 24.8–50.7 months)”, Page 8 of revised clean manuscript. 8. In Results, Overall outcomes after surveillance MRI, 2nd paragraph, last sentence, I suggest: after a negative MRI...before the MRI examinations. : Response – Thank you for your helpful comment. We have revised the sentence accordingly. (Amended text) • Results, Overall outcomes after surveillance MRI: “Notably, 6 (24%) were detected only with subsequent surveillance breast MRI performed at a median of 33.2 months (range, 28.1–55.5 months) after a negative MRI, although mammography had been performed at a median of 10.5 months (range, 4.9–13.9 months) before the MRI examinations (Fig 2 and S1 Table)”, Page 10 of revised clean manuscript. 9. In Results, Comparison of second breast cancers according to intervals (<3 years vs >3 years) following initial surgery, 1st and 2nd paragraphs, 1st sentence, each group should be defined. : Response – Thank you for your helpful comment. We have clearly defined each group in the first sentence of both paragraphs in our revised manuscript. (Amended text) • Results, Comparison of second breast cancers according to intervals (<3 years vs ≥ 3 years) following initial surgery: “The median interval between initial surgery and surveillance MRI were 26.1 months (IQR, 24.2–31.5; surgery-MRI interval < 3 years group) and 55.6 months (IQR, 43.0–57.3; surgery-MRI interval ≥ 3 years group), respectively”, Page 11 of revised clean manuscript. “There was no significant difference in intervals between negative surveillance MRI and detection of second breast cancer (34.9 [IQR, 28.4–47.2] vs 50.6 [IQR, 32.7–55.5] months, p = .202) or intervals between negative surveillance MRI and detection of second breast cancer or local-regional occurrence (42.4 [IQR, 32.2–53.7] vs 33.1 [IQR, 18.0–42.4], p = .110) between the two groups (surgery-MRI interval <3 years vs ≥ 3 years)”, Page 12 of revised clean manuscript. 10. In Discussion, 2nd paragraph, 1st sentence, I suggest: only two breast cancers were. : Response – Thank you for your helpful comment. We have revised the above sentence. (Amended text) • Discussion, 2nd paragraph: “Similar to our previous report [7], we found that only two second breast cancers were detected within 24 months following a negative surveillance MRI”. Page 14 of revised clean manuscript. 11. In Discussion, 3rd paragraph, 3rd sentence, the should be added before incidence and the two groups should be defined. In the 4th sentence, the should be added between of and period. In the last sentence of that paragraph, factor should be changed to factors. : Response – Thank you for your helpful comment. We have revised the sentences accordingly. (Amended text) • Discussion, 3rd paragraph: “However, we found no significant difference in the incidence of second breast cancers or that of second breast cancers or local-regional recurrence following negative surveillance breast MRI between the two groups (surgery-MRI interval <3 years vs ≥ 3 years). This is likely because contralateral breast cancers accounted for 68% of second breast cancers, which risk is relatively constant regardless of the period from initial diagnosis.”, Page 15 in revised clean manuscript. “Nonetheless, longer imaging intervals for supplemental surveillance MRI may still be appropriate for most patients, especially for those without other high risk factors, as the overall second breast cancer rate following a negative surveillance breast MRI was low (1.6%, 25 of 1552)”, Page 15 in revised clean manuscript. 12. The authors should check the journal's reference style. In references 3, 4, 8, and 12, I think that the first 3 authors should be listed, followed by et al. In references 6, 7, 11-13, 15, and 16, only the first word of the title of the article should be capitalized. : Response – Thank you for your thorough comment. We have rechecked the submission guidelines for PLOS ONE, and the references guidelines state that “References with more than six authors should list the first six author names, followed by “et al.” Therefore, we did not change references 3, 4, 8 and 12. We failed to find specific guidelines regarding capitalization of letters, but have changed references 6, 7, 11-13 accordingly – only the first word of the title of the article has been capitalized, with the exception of abbreviations (MRI) and proper nouns. 13. I suggest that the authors add a figure showing a second breast cancer identified on MRI. : Response – Thank you for your helpful comment. In our revised manuscript, we have added Fig 2 showing a second breast cancer case identified on subsequent surveillance MRI. Attachments Attachment Submitted filename: Response to Reviewers.docx https://doi.org/10.1371/journal.pone.0306828.r002
24 Jun 2024 Decision Letter - Daniele Ugo Tari, Editor Second breast cancer following negative breast MRI: analysis by interval from surgery and risk factors PONE-D-24-00795R1 Dear Dr. Park, 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, Daniele Ugo Tari, M.D. Academic Editor PLOS ONE Additional Editor Comments (optional): Reviewers' comments: https://doi.org/10.1371/journal.pone.0306828.r003
Formally Accepted
6 Aug 2024 Acceptance Letter - Daniele Ugo Tari, Editor PONE-D-24-00795R1 PLOS ONE Dear Dr. Park, 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. Daniele Ugo Tari Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0306828.r004

Open letter on the publication of peer review reports

PLOS recognizes the benefits of transparency in the peer review process. Therefore, we enable the publication of all of the content of peer review and author responses alongside final, published articles. Reviewers remain anonymous, unless they choose to reveal their names.

We encourage other journals to join us in this initiative. We hope that our action inspires the community, including researchers, research funders, and research institutions, to recognize the benefits of published peer review reports for all parts of the research system.

Learn more at ASAPbio .