Pharmacokinetic Analysis of Enhancement-Constrained Acceleration (ECA) reconstruction-based high temporal resolution breast DCE-MRI

Zhen Ren; Ty O. Easley; Federico D. Pineda; Xiaodong Guo; Rina F. Barber; Gregory S. Karczmar

doi:10.1371/journal.pone.0286123

Peer Review History

Original SubmissionAugust 19, 2022
7 Feb 2023 Decision Letter - Zhentian Wang, Editor PONE-D-22-23285Enhancement-Constrained Acceleration (ECA) reconstruction-based high temporal resolution DCE-MRI for pharmacokinetic of breast MRI dataPLOS ONE Dear Dr. Ren, 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. As pointed by both reviewers, please reformulate the Introduction section and improve the overall quality and style following the reviewers' comments. One weakness of this work is the lack of the comparsion with peer techniques, please add new supporting materials and comment on this point. Please submit your revised manuscript by Mar 24 2023 11:59PM. 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Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice. Additional Editor Comments (if provided): [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: I found this paper interesting. Also the presented technique ECA seems promising compared to the conventional methods of accerelating image acquisition. There are some points needing clarification. #1 Introduction: Interesting, yet a bit length for original paper. It is not a review paper on image reconstruction of UF-DCE MRI and therefore the contents are better to be summarized. #2 Methodology 2.1 Simulation Phantoms Table 1 right column"Temporal resolution range 2.8-7 I am just wondering why there are wide variations in temporal resolution. #3 Considering that non-technically-oriented readers are there, mathematical parts might be better put into the appendix. #4 Fgure 5 all of the upper row and all of the lower row looks quite similar. Can you magnify parts of the graph to enhance their differece? Reviewer #2: This is a follow-up study of the performance of the previously proposed temporally constrained reconstruction with different sampling trajectories, SNRs, and acceleration rates in estimating contrast media kinetics in lesions and arteries. The evaluation was performed in simulation and controlled phantom studies. The original publication demonstrated an initial promise of the method, and the current method adds further substantial knowledge on the practical utility of the developments. Overall, the body of knowledge introduced in the manuscript is substantial and may be of interest to PLOS ONE readership. However, there are several moderate-to-minor concerns about the work outlined below: 1. The main weakness of the manuscript is the lack of comparison of the ECA method with peer techniques. Given that the presented results relate to rather artificial situations (simulations and phantom studies), it is important to study if the method actually provides benefits compared to existing state of art. Please pick a related established temporal regularization method and study ECA performance with respect to the benchmark in some relevant experiment(s). 2. Overall quality and style: Introduction is too long and contains many rationalizations and reviews related to the method which was already published. Instead, it should take into account that the method was already presented and concentrate on the importance of validating the method in controlled conditions. I envision a significant redesign of the Introduction. Similarly, “Image reconstruction” section contains a very detailed description of the ECA method, which was already described in the supplemental material of the previous paper. I don’t think such detailed duplication is necessary. The title of the previous paper was “Enhancement constrained acceleration: A robust reconstruction framework in breast DCE-MRI” and the title of the manuscript under review is virtually the same. Instead, it should reflect the essence of the efforts attempted in the manuscript (validation, evaluation, etc). 3. Please cite prior art on the use of the first and second differences in the temporal dimension (e.g., use most recent MRM 2023, 89(1):112-127 to track the relevant references). ****** 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". 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Revision 1
29 Mar 2023 Author Response RESPONSE TO DECISION LETTER Dear Editor and Reviewers, Thank you so much for your consideration of our paper. We are grateful to receive the valuable comments from reviewers, which are very helpful in improving our paper. We have followed your instructions to modify our paper and would like to submit a revised version. The major changes we have made are (1) shortening the introduction by summarizing the acceleration methods; (2) removing the mathematical description of ECA method; (3) replacing Figure 5; (4) adding introduction and discussion of the regularization methods. We believe that the manuscript has been improved and hope it has reached the standard of the journal. We have addressed each comment as below. In the revised manuscript, we have colored the changes related to Reviewer #1’s comments in green, related to Reviewer #2’s comments in blue, and related both in yellow. Reviewer #1: I found this paper interesting. Also the presented technique ECA seems promising compared to the conventional methods of accelerating image acquisition. There are some points needing clarification. #1 Introduction: Interesting, yet a bit length for original paper. It is not a review paper on image reconstruction of UF-DCE MRI and therefore the contents are better to be summarized. Authors’ response: Thank you for this suggestion. We have shortened the introduction and summarized acceleration methods. The changes are highlighted in yellow. #2 Methodology 2.1 Simulation Phantoms Table 1 right column"Temporal resolution range 2.8-7 I am just wondering why there are wide variations in temporal resolution. Authors’ response: Thank you for your question. The variations in temporal resolution come from the ultrafast DCE-MRI on different scanners. A higher temporal resolution – approx. 3 seconds per image – was on a 3T MRI scanner. The 7 seconds per image scans were on a 1.5 T scanner. #3 Considering that non-technically-oriented readers are there, mathematical parts might be better put into the appendix. Authors’ response: Thank you for your suggestion. We have removed the detailed description of the ECA method and cited a reference that provides a detailed description of ECA reconstruction. The changes are highlighted in yellow. #4 Figure 5 all of the upper row and all of the lower row looks quite similar. Can you magnify parts of the graph to enhance their difference? Authors’ response: Thank you for your suggestion. Figure 5 has been changed. We have magnified the part of graph to enhance the difference, but for the two UnWRAP sampling trajectories, the difference is small. The changes are highlighted in green. Reviewer #2: This is a follow-up study of the performance of the previously proposed temporally constrained reconstruction with different sampling trajectories, SNRs, and acceleration rates in estimating contrast media kinetics in lesions and arteries. The evaluation was performed in simulation and controlled phantom studies. The original publication demonstrated an initial promise of the method, and the current method adds further substantial knowledge on the practical utility of the developments. Overall, the body of knowledge introduced in the manuscript is substantial and may be of interest to PLOS ONE readership. However, there are several moderate-to-minor concerns about the work outlined below: 1. The main weakness of the manuscript is the lack of comparison of the ECA method with peer techniques. Given that the presented results relate to rather artificial situations (simulations and phantom studies), it is important to study if the method actually provides benefits compared to existing state of art. Please pick a related established temporal regularization method and study ECA performance with respect to the benchmark in some relevant experiment(s). Authors’ response: We appreciate your questions and comments. We believe that the current ECA method and the application proposed here are very different from existing regularization methods. A useful comparison of the ECA with other regularization methods would require significant modifications and many experiments. Therefore we respectfully suggest that comparison with of the ECA with other regularization method should be left to our next paper. Our goal here is simply to demonstrate that the ECA is effective and has potential to improve clinical MRI. We did not intent to suggest that the ECA is better than other acceleration method. It is likely that different methods may be preferable in different contexts. We point out that we DID compare the ECA with interpolation which is one of the simplest regularization methods. In this revision, rather than adding additional simulations, we briefly compared the ECA with other published regularization methods. Most of the existing state-of-the-art methods for image acceleration (which we believe this point refers to) are based on non-Cartesian sampling schemes and in some cases (i.e., compressed sensing approaches) incoherent sampling is required. While we agree that a comparison with other methods would be valuable to benchmark the performance of the proposed method, our purpose in this manuscript and in developing the ECA approach is to introduce a method that does not rely on a specific sampling scheme and is therefore applicable to data acquired under varying conditions. In this manuscript, we opted for testing Cartesian-based sampling trajectories given that these are universally available regardless of vendor or software packages available at different sites. Because the ECA does not require a specific sampling scheme, we do plan to test it under non-Cartesian sampling conditions in future work. At that point hope to benchmark its performance in those experiments against other existing methods. We have added a paragraph in the Introduction and Discussion to further explain the difference between the ECA and other existing regularization methods. We also point out in the discussion that we have not yet tested the ECA for real breast scans and have not compared the ECA with other reconstruction methods. In the revised manuscript, the changes are marked in blue. 2. Overall quality and style: Introduction is too long and contains many rationalizations and reviews related to the method which was already published. Instead, it should take into account that the method was already presented and concentrate on the importance of validating the method in controlled conditions. I envision a significant redesign of the Introduction. Authors’ response: Thank you for your suggestion. We have shortened the introduction and summarized the review on the acceleration methods. The changes are highlighted in yellow. Similarly, “Image reconstruction” section contains a very detailed description of the ECA method, which was already described in the supplemental material of the previous paper. I don’t think such detailed duplication is necessary. Authors’ response: Thank you. We have removed the introduction of the ECA method and cited a reference of the detailed description of ECA reconstruction. The changes are highlighted in yellow. The title of the previous paper was “Enhancement constrained acceleration: A robust reconstruction framework in breast DCE-MRI” and the title of the manuscript under review is virtually the same. Instead, it should reflect the essence of the efforts attempted in the manuscript (validation, evaluation, etc). Authors’ response: Thank you for your suggestion. We have changed the title to “Pharmacokinetic Analysis of Enhancement-Constrained Acceleration (ECA) reconstruction-based high temporal resolution breast DCE-MRI” and highlighted in blue. 3. Please cite prior art on the use of the first and second differences in the temporal dimension (e.g., use most recent MRM 2023, 89(1):112-127 to track the relevant references). Author’s response: Thank you for this suggestion. We added a paragraph in the Introduction to summarize those works, which is highlighted in blue. We would like to thank you for all the comments and suggestions. We look forward to the outcome of your assessment. Yours Sincerely, Zhen Ren, Ph.D. Department of Radiology The University of Chicago zren1@uchicago.edu Attachments Attachment Submitted filename: Response to reviewers.docx https://doi.org/10.1371/journal.pone.0286123.r002
10 May 2023 Decision Letter - Zhentian Wang, Editor Pharmacokinetic Analysis of Enhancement-Constrained Acceleration (ECA) reconstruction-based high temporal resolution breast DCE-MRI PONE-D-22-23285R1 Dear Dr. Ren, 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. 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If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation. Reviewer #1: All comments have been addressed Reviewer #2: All comments have been addressed ******** 2. Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented. Reviewer #1: Yes Reviewer #2: Yes ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #2: Yes ****** 4. Have the authors made all data underlying the findings in their manuscript fully available? The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified. Reviewer #1: Yes Reviewer #2: Yes ****** 5. Is the manuscript presented in an intelligible fashion and written in standard English? PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here. Reviewer #1: Yes Reviewer #2: 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: I think the author responded to my previous queries and the new revised paper becomes easier to follow. Reviewer #2: The manuscript was significantly improved. Most of my previous comments were addressed except for comparison with existing techniques. While the arguments of not doing such comparison are weak, I think the manuscript is generally in good shape. ****** 7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files. If you choose “no”, your identity will remain anonymous but your review may still be made public. Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy. Reviewer #1: No Reviewer #2: No ******** https://doi.org/10.1371/journal.pone.0286123.r003
Formally Accepted
7 Jun 2023 Acceptance Letter - Zhentian Wang, Editor PONE-D-22-23285R1 Pharmacokinetic Analysis of Enhancement-Constrained Acceleration (ECA) reconstruction-based high temporal resolution breast DCE-MRI Dear Dr. Ren: 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 Prof. Zhentian Wang Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0286123.r004

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