Rapid diagnosis of periprosthetic joint infection from synovial fluid in blood culture bottles by direct matrix-assisted laser desorption ionization time-of-flight mass spectrometry

Feng-Chih Kuo; Chun-Chih Chien; Mel S. Lee; Jun-Wen Wang; Po-Chun Lin; Chen-Hsiang Lee

doi:10.1371/journal.pone.0239290

Peer Review History

Original SubmissionMay 20, 2020
25 Jun 2020 Decision Letter - Adriana Calderaro, Editor PONE-D-20-14441 Rapid diagnosis of periprosthetic joint infection from synovial fluid in blood culture bottles by direct matrix-assisted laser desorption ionization time-of-flight mass spectrometry PLOS ONE Dear Dr. Lee, 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 needs to be improved resolving the criticisms reported by the Authors. In particular the study design should be better clarified. Please submit your revised manuscript by Aug 09 2020 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: http://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols We look forward to receiving your revised manuscript. Kind regards, Adriana Calderaro Academic Editor PLOS ONE Journal Requirements: When submitting your revision, we need you to address these additional requirements. 1. 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. Please amend your current ethics statement to address the following concerns: a) Did participants provide their written or verbal informed consent to participate in this study? b) If consent was verbal, please explain i) why written consent was not obtained, ii) how you documented participant consent, and iii) whether the ethics committees/IRB approved this consent procedure. 3. Please update the title page within your main document to list all authors and all affiliations as per our author instructions and clearly indicate the corresponding author. 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 [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: Partly ******** 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: 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: The authors collect data from 77 patients to evaluate a direct matrix-assisted laser desorption ionization time-of-flight mass spectrometry (MALDI-TOF MS) in compared with the current laboratory practices. The results showed that the new technique shortens the time to microorganism identification and has superior results. The manuscript was well prepared. 1. Line 143. “80 SF samples were taken from 77 patients…” In other words, some samples were taken from the same patients and were correlated. However, the analysis doesn’t discuss how the correlated data were accounted. 2. Line 195. “All pairwise were significant differences …..”. Please report ANOVA results first. Also, what multiple testing procedure was applied? Reviewer #2: The paper entitled "Rapid diagnosis of periprosthetic joint infection from synovial fluid in blood culture bottles by direct matrix-assisted laser desorption ionization time-of-flight mass spectrometry" aimed to investigate the clinical practice for integrating a direct MALDI-TOF MS identification for rapid diagnosis of PJI. The study was a strict prospective design, but there are several major limitations. 1: The numbers of the patients included in the study is not big enough, there is still needed for the more samples to further verify the conclusion. 2: The presentation of the study is unclear and lacks rigor. 3: The authors argue that the purpose of the study was to evaluate whether direct MALDI-TOF MS can shorten the time to preliminary strain identification as compare with routine methods (Page 4, Line 61-62). Direct MALDI-TOF MS of course can shorten the time to preliminary strain identification, as subculture is not needed. Thus the argument is meaningless. 4: The Material and Methods section has several mistakes and detailed information is lacked. Page 6, line 116, where is the ethanol come from? Line 116-120, to my knowledge, it should be “μL” instead of “mL”, etc….. 5: The results section is badly structure and the description is confusing, major improvement is needed. ****** 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.0239290.r001
Revision 1
23 Jul 2020 Author Response Response to Reviewers Re: Rapid diagnosis of periprosthetic joint infection from synovial fluid in blood culture bottles by direct matrix-assisted laser desorption ionization time-of-flight mass spectrometry Dear Editors, Thank you for the comprehensive review of our manuscript. We appreciate the opportunity to submit a revised version and found the reviewers' comments to be very insightful and contribute considerably to the improvement of our manuscript. Below we provide our point-by-point responses to all of the reviewers’ comments. We also send this manuscript for English editing. We hope you will find our revised manuscript suitable for publication in PLOS ONE. Sincerely, Chen-Hsiang Lee Reviewer#1 1. Line 143. “80 SF samples were taken from 77 patients...” In other words, some samples were taken from the same patients and were correlated. However, the analysis doesn’t discuss how the correlated data were accounted. Ans: Thank you for this and all of your comments. We have rewritten this in page 13, line 158-159: “Two patients had recurrent infections after a two-stage exchange protocol. One patient had bilateral staged knee PJIs at different time points during the study period. Therefore, 80 SF samples were taken and analyzed from 77 patients who fulfilled the MSIS criteria (Table 1).” 2. Line 195. “All pairwise were significant differences .....”. Please report ANOVA results first. Also, what multiple testing procedure was applied? Ans: We used the Bonferroni post hoc test for multiple comparisons between groups. We have added this to page 12, line 149-151: “In order to fully understand group differences, the Bonferroni post hoc test was used for multiple comparisons when the Kruskal-Wallis test was significant.” We reported the overall results and group differences on page 20, line 211-226: “The overall difference between the three groups was significant (p < 0.0001). Significant Bonferroni-adjusted post hoc interactions are shown in Fig 2. In pairwise comparisons, there were significant differences in the time of microorganism identification between direct MALDI-TOF MS and routine MALDI-TOF MS (p < 0.0001) or swab culture (p < 0.0001). There was no significant difference between routine MALDI-TOF MS and swab culture (p = 0.0268).” Reviewer #2 1. The numbers of the patients included in the study is not big enough, there is still needed for the more samples to further verify the conclusion. Ans: Thank you for this and all of your comments. We have added this to address the power analysis on page 12, line 152-154: “Post hoc power analysis showed that a sample size of 80 was sufficient to achieve 89% power to detect an effect size of 0.23 with a significance level of 0.05 using a 2-sided one-way ANOVA test (G Power v3.1, Baden-Württemberg, Germany).” We have also added this in the conclusion on page 26, line 287-288: “Further large-scale studies are required to verify the clinical impact and the value of this testing method.” 2. The presentation of the study is unclear and lacks rigor. Ans: We calculated group differences using the Bonferroni post hoc test for multiple comparisons (page 12, line 149-151): “In order to fully understand group differences, the Bonferroni post hoc test was used for multiple comparisons when the Kruskal-Wallis test was significant.” We reported the overall results and group differences on page 20, line 211-216: “The overall difference between the three groups was significant (p < 0.0001). Significant Bonferroni-adjusted post hoc interactions are shown in Fig 2. In pairwise comparisons, there were significant differences in the time of microorganism identification between direct MALDI-TOF MS and routine MALDI-TOF MS (p < 0.0001) or swab culture (p < 0.0001). There was no significant difference between routine MALDI-TOF MS and swab culture (p = 0.0268).” 3. The authors argue that the purpose of the study was to evaluate whether direct MALDI-TOF MS can shorten the time to preliminary strain identification as compare with routine methods (Page 4, Line 61-62). Direct MALDI-TOF MS of course can shorten the time to preliminary strain identification, as subculture is not needed. Thus the argument is meaningless. Ans: Thank you for your valuable opinion. We have rewritten this part of the introduction on page 6, line 52-59: “Theoretically, direct MALDI-TOF MS can decrease the time to preliminary strain identification, as a subculture is not required in this process. This rapid microbial identification method has been used in many infection fields, such as bloodstream infections [8,11,12] meningitis [13,14] and urinary traction infections [15,16]. This method has been shown to have high accuracy for Gram-negative organisms but relatively low accuracy for Gram-positive bacteria [17]. However, Gram-positive bacteria are the most common organisms that cause PJIs [18,19]. However, whether the direct identification method can be efficiently applied in patients with PJIs by culturing SF in BCBs for a rapid and accurate diagnosis has yet to be elucidated.” 4. The Material and Methods section has several mistakes and detailed information is lacked. Page 6, line 116, where is the ethanol come from? Ans: We have rewritten the section of Material and Methods (line 89 on page 8 to line 143 on page 11) and changed a reference [Yonetani S, Ohnishi H, Ohkusu K, Matsumoto T, Watanabe T. Direct identification of microorganisms from positive blood cultures by MALDI-TOF MS using an in-house saponin method. Int J Infect Dis. 2016;52: 37–42. doi:10.1016/j.ijid.2016.09.014]. 5. Line 116-120, to my knowledge, it should be “μL” instead of “mL”, etc..... Ans: Thank you. The unit has been changed to μL. 6. The results section is badly structure and the description is confusing, major improvement is needed. Ans: The results section describes direct versus routine MALDI-TOF MS, followed by direct MALDI-TOF MS versus swabs, then routine swab culture versus swab. We have also added the group difference in the time to microorganism identification on page 20, line 211-216: “The overall difference between the three groups was significant (p < 0.0001). Significant Bonferroni-adjusted post hoc interactions are shown in Fig 2. In pairwise comparisons, there were significant differences in the time of microorganism identification between direct MALDI-TOF MS and routine MALDI-TOF MS (p < 0.0001) or swab culture (p < 0.0001). There was no significant difference between routine MALDI-TOF MS and swab culture (p = 0.0268).” We also added a paragraph in the discussion section to describe our finding in page 22 and 23, line 232-244 “Interestingly, direct MALDI-TOF MS identified 85.3% of Gram-positive organisms and 92.3% of Gram-negative organisms in SF samples in BCBs. Our results are consistent with previous studies which showed that direct MALDI-TOF MS had high accuracy for Gram-negative bacteria but moderate accuracy for Gram-positive organisms [17,22,23]. Zhou et al. demonstrated a higher accuracy for Gram-negative bacteria than for Gram-positive bacteria (92.8 vs. 82.4%) in their in-house protocol for direct MALDI-TOF MS in positive BCBs [8]. In addition, French et al reported an identification rate of 53% for Gram-positive organisms and 89% for Gram-negative organisms [12]. A recent systemic review and meta-analysis of 32 studies reported an overall correct identification rate of 72% for Gram-positive bacteria compared to 92% for Gram-negative bacteria with direct bacterial identification from positive BCBs using MALDI-TOF MS [24]. A possible reason for the lower identification rate of Gram-positive bacteria with MALDI-TOF MS analysis is because Gram-positive bacteria require pre-processing steps due to their more robust cell wall, which decreases the protein extraction rate [25].” Attachments Attachment Submitted filename: Response to Reviewers.docx https://doi.org/10.1371/journal.pone.0239290.r002
6 Aug 2020 Decision Letter - Adriana Calderaro, Editor PONE-D-20-14441R1 Rapid diagnosis of periprosthetic joint infection from synovial fluid in blood culture bottles by direct matrix-assisted laser desorption ionization time-of-flight mass spectrometry PLOS ONE Dear Dr. Lee, 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 was improved, however it requires again a revision. In particular, a language and editing revsion is needed especially for the sentences newly added. Furthermore, the Authors should be more cautious affirming that a subculturing is not needed when the direct identification by MALDI-TOF MS is performed. Please submit your revised manuscript by Sep 20 2020 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: http://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols We look forward to receiving your revised manuscript. Kind regards, Adriana Calderaro Academic Editor PLOS ONE [Note: HTML markup is below. Please do not edit.] Reviewers' comments: Reviewer's Responses to Questions Comments to the Author 1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation. Reviewer #1: All comments have been addressed ******** 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: (No Response) ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: (No Response) ****** 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: (No Response) ****** 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: (No Response) ****** 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: (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 #1: 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.0239290.r003
Revision 2
17 Aug 2020 Author Response Editor comment The manuscript was improved, however it requires again a revision. In particular, a language and editing revsion is needed especially for the sentences newly added. Furthermore, the Authors should be more cautious affirming that a subculturing is not needed when the direct identification by MALDI-TOF MS is performed. Ans: Thank you for this and all of your comments. The revised edition has been edited by an English native speaker to improve the language writing. Thanks for your reminder. The most time-intensive process using routine MALDI-TOF MS is the time required for the subculture of specimens before identification. Theoretically, direct MALDI-TOF MS can decrease the time to preliminary strain identification. We have clarified the issue of performing a subculture in the revised version of the manuscript. Attachments Attachment Submitted filename: Response to Reviewers.doc https://doi.org/10.1371/journal.pone.0239290.r004
3 Sep 2020 Decision Letter - Adriana Calderaro, Editor Rapid diagnosis of periprosthetic joint infection from synovial fluid in blood culture bottles by direct matrix-assisted laser desorption ionization time-of-flight mass spectrometry PONE-D-20-14441R2 Dear Dr. Lee, 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, Adriana Calderaro Academic Editor PLOS ONE Additional Editor Comments (optional): Reviewers' comments: Reviewer's Responses to Questions Comments to the Author 1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation. Reviewer #1: 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: (No Response) ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: (No Response) ****** 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: (No Response) ****** 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: (No Response) ****** 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: (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 #1: No https://doi.org/10.1371/journal.pone.0239290.r005
Formally Accepted
11 Sep 2020 Acceptance Letter - Adriana Calderaro, Editor PONE-D-20-14441R2 Rapid diagnosis of periprosthetic joint infection from synovial fluid in blood culture bottles by direct matrix-assisted laser desorption ionization time-of-flight mass spectrometry Dear Dr. Lee: 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 MD, PhD, Associate Professor Adriana Calderaro Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0239290.r006

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