Clinical correlates of sarcopenia and falls in Parkinson’s disease

Danielle Pessoa Lima; Samuel Brito de Almeida; Janine de Carvalho Bonfadini; João Rafael Gomes de Luna; Madeleine Sales de Alencar; Edilberto Barreira Pinheiro-Neto; Antonio Brazil Viana-Júnior; Samuel Ranieri Oliveira Veras; Manoel Alves Sobreira-Neto; Jarbas de Sá Roriz-Filho; Pedro Braga-Neto

doi:10.1371/journal.pone.0227238

Peer Review History

Original SubmissionDecember 13, 2019
20 Jan 2020 Decision Letter - Masaki Mogi, Editor PONE-D-19-34534 Clinical correlates of sarcopenia and falls in Parkinson’s disease PLOS ONE Dear Dr. Lima, 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. Major revisions are needed in the present form. See the Reviewers' comments carefully and respond them appropriately. We would appreciate receiving your revised manuscript by Mar 05 2020 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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Please ensure that references have been provided for all the scales and questionnaires used in this study. 4. PLOS requires an ORCID iD for the corresponding author in Editorial Manager on papers submitted after December 6th, 2016. Please ensure that you have an ORCID iD and that it is validated in Editorial Manager. To do this, go to ‘Update my Information’ (in the upper left-hand corner of the main menu), and click on the Fetch/Validate link next to the ORCID field. This will take you to the ORCID site and allow you to create a new iD or authenticate a pre-existing iD in Editorial Manager. Please see the following video for instructions on linking an ORCID iD to your Editorial Manager account: https://www.youtube.com/watch?v=_xcclfuvtxQ [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: No ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #2: No ****** 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 have read the tex with great interest. SARC-F works well in PD patients. Study is well organized. Clinical confaunders are comprehensively evaluated. I have some suggestions in the content of minör revision. Abstract Falls are mentioned in the method section as ‘’in the six months prior to their medical visit’’. This description is sufficient throughout the abstract section. Please remove this description after each ‘’falls’’ from result section. Introduction Line 68: Despite its importance, few studies have assessed the prevalence and characteristics of sarcopenia in this population (references?). Please add refrences. Line 80: on the quality of life ‘’of’’ PD patients. Please write ‘’in’’ instead of ‘’of’’. Materials and Metods Please define how you diagnosed dementia and osteoporosis. Line 137:’’ lower extremity strength (SARC-F) and strength during on phases.’’ Please change as ’’lower extremity strength (FTSTS) and hand grip strength during on phases.’’ Line 142: Information ‘’on the number’’ of falls. Please remove ‘’on the number’’ because you did not evaluate the recurrent falls. Falls are mentioned in the method section as ‘’in the six months prior to their medical visit’’. This description is sufficient throughout the text. Please remove this description after each ‘’falls’’ from result and discussion sections. Results Line 164: Before defining Table 1 please give the number (%) of patients with low muscle strenght according to both hand grip strenght and FTSTS. Line 190: Why did you not include depression or GDS scores and number of medications in logistic regression models because p <0.05 in these values? Also please define depression cut off point according to GDS scale in method section. In Table 1 and 3 both median and mean±standart deviation are not necessary, please only give mean±standart for normally distributed data and give median (25th-75th) for not normally distributed. In Table 1 and 3 total number of participants for each independent variable is not necessary. You can remove them. (Example: SARC-F+ a ‘’(n = 218)’’ is not necessary) Table 4: Instead of ‘’time’’ please write ‘’duration’’ of disease Discussion Line 305: Disease duration was associated ‘’to’’ falls. Please write ‘’with’’ instead of ‘’to’’. Line 307: ‘’compared falling versus non-falling’’ please change the statement as ‘’compared fallers versus non-fallers’’ Line 310: Disease duration has also been correlated ‘’to’’ the occurrence of falls in other studies. Please write ‘’with’’ instead of ‘’to’’. References There is a duplication of references. 6th and 15th are same. Reviewer #2: Dear Authors the main problem with the manuscript is regarding the diagnosis and definition of sarcopenia. Using the time to rise from a chair in Parkinsonian patients the main limitation is that time is related to the brakinesia and not to the muscle function. Other tests should be used in this case for the diagnosis of sarcopenia ****** 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: Firuzan Fırat Ozer Reviewer #2: Yes: Fulvio Lauretani [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.0227238.r001
Revision 1
17 Feb 2020 Author Response Reviewer #1: I have read the text with great interest. SARC-F works well in PD patients. Study is well organized. Clinical confounders are comprehensively evaluated. I have some suggestions in the content of minor revision. Response: We thank the reviewer for the comments. Abstract Falls are mentioned in the method section as ‘’in the six months prior to their medical visit’’. This description is sufficient throughout the abstract section. Please remove this description after each ‘’falls’’ from result section. Response: The description was further removed throughout the abstract section, as suggested. Introduction Line 68: Despite its importance, few studies have assessed the prevalence and characteristics of sarcopenia in this population (references?). Please add references. Response: References are now added to this sentence. Line 80: on the quality of life ‘’of’’ PD patients. Please write ‘’in’’ instead of ‘’of’’. Materials and Metods Response: We agree with the reviewer. The sentence was modified in accordance with the recommendations. Please define how you diagnosed dementia and osteoporosis Response: Dementia was diagnosed following the Diagnostic and Statistical Manual of Mental Disorders (DSM-V) criteria (called major neurocognitive disorder). The diagnostic assessment for osteoporosis was conducted according to National Osteoporosis Foundation recommendations. This information was included in Methods section. Line 137:’’ lower extremity strength (SARC-F) and strength during on phases.’’ Please change as ’’lower extremity strength (FTSTS) and hand grip strength during on phases.’’ Line 142: Information ‘’on the number’’ of falls. Please remove ‘’on the number’’ because you did not evaluate the recurrent falls. Falls are mentioned in the method section as ‘’in the six months prior to their medical visit’’. This description is sufficient throughout the text. Please remove this description after each ‘’falls’’ from result and discussion sections. Response: We thank the reviewer for the suggestions. All modifications were performed according to the reviewer suggestions. Results Line 164: Before defining Table 1 please give the number (%) of patients with low muscle strenght according to both hand grip strenght and FTSTS. Response: Among patients with probable sarcopenia, 61 (59.2%) and 87 (84.4%) had low muscle strength according to hand grip strength and FTSTS respectively. We included this information in Results section. Line 190: Why did you not include depression or GDS scores and number of medications in logistic regression models because p <0.05 in these values? Depression, GDS score and number of medications were in fact included in logistic regression models. This information is now included in Results section. Also please define depression cut off point according to GDS scale in method section. Response: Although GDS was applied in this study, it was not used in order to establish a diagnosis of depression, which was defined according to DSM-V criteria. In this sense, a cut off point for GDS was not adopted in this study. In Table 1 and 3 both median and mean ± standart deviation are not necessary, please only give mean±standart for normally distributed data and give median (25th-75th) for not normally distributed. In Table 1 and 3 total number of participants for each independent variable is not necessary. You can remove them. (Example: SARC-F+ a ‘’(n = 218)’’ is not necessary) Table 4: Instead of ‘’time’’ please write ‘’duration’’ of disease Discussion Line 305: Disease duration was associated ‘’to’’ falls. Please write ‘’with’’ instead of ‘’to’’. Line 307: ‘’compared falling versus non-falling’’ please change the statement as ‘’compared fallers versus non-fallers’’ Line 310: Disease duration has also been correlated ‘’to’’ the occurrence of falls in other studies. Please write ‘’with’’ instead of ‘’to’’. Response: We thank the reviewer for the suggestions. All modifications were performed according to the reviewer suggestions. References There is a duplication of references. 6th and 15th are same. Response: We apologize the reviewer for this mistake. All References section was changed considering that and also because new references were added. Reviewer #2: Dear Authors: The main problem with the manuscript is regarding the diagnosis and definition of sarcopenia. Using the time to rise from a chair in Parkinsonian patients the main limitation is that time is related to the bradykinesia and not to the muscle function. Other tests should be used in this case for the diagnosis of sarcopenia Response: The authors acknowledge the influence of bradykinesia on altered results in this test as a limitation of the study. The limitations regarding the Five Times Sit-to-Stand Test (FTSTS) are in the tenth paragraph of the discussion. Indeed, literature concerning diagnosis of sarcopenia in PD patients is extremely scarce. Nonetheless, the FTSTS is the only test recommended by the European Working Group on Sarcopenia in Older People (EWGSOP 2) to assess muscle strength of the lower limbs. In this sense, as a validated tool to assess probable sarcopenia due to reduced muscle strength in the lower limbs in PD patients is yet unavailable, and given the need to use a standardized approach, the authors decided to follow the most widely accepted recommendations. Moreover, in this study all patients were assessed during “on” phases in order to minimize this confounding factor. Cano-de-la-cuerda et al (2010) developed a systematic review with the objective of investigating whether muscle weakness exists in Parkinson's disease. Seventeen studies showed that the isokinetic muscle strength of patients with Parkinson's disease was reduced compared to age-matched controls. Interestingly, they concluded that muscle weakness was not specifically associated with tremor or stiffness. The specific etiology of this weakness requires further studies. It is necessary to establish better if this weakness is of central or peripheral origin, that is, if it is intrinsic to the disease or a secondary phenomenon. Duncan, Leddy and Earhart (2011) evaluated intra-rater and test-retest reliability of the FTSTS, the performance of patients in the test at different stages of the disease, its correlation to other measures and its ability to predict falls in 80 patients with PD. They concluded that the test-retest reliability of the FTSTS in PD is feasible and it is comparable to that of other populations. They recommended the use of the FTSTS as a quick and objective measure to determine the risk of fall. The FTSTS was correlated to worse quality of live, to lower balance confidence, to lower limbs strength, to slower movements of upper extremity in bivariate analysis. The lower limbs strength was not correlated to FTSTS in multiple regression analysis. To the best of our knowledge, it was the first trial to examine FTSTS performance in individuals with PD. The sample size of the study was small so that we need more studies that examine the FTSTS in individuals with PD to clarify its correlation with postural instability and bradykinesia. References Cano-de-la-Cuerda R, Pérez-de-Heredia M, Miangolarra-Page JC, Munoz-Hellín E, Fernández-de-las-Penas C. Is there muscular weakness in Parkinson's disease?. American Journal of Physical Medicine & Rehabilitation. 2010;89(1):70-6. doi: 10.1097/PHM.0b013e3181a9ed9b. Duncan RP, Leddy AL, Earhart GM. Five times sit-to-stand test performance in Parkinson's disease. Arch Phys Med Rehabil. 2011;92(9):1431-6. doi: 10.1016/j.apmr.2011.04.008. Attachments Attachment Submitted filename: Response to reviewers Plos 2.16.2020.docx https://doi.org/10.1371/journal.pone.0227238.r002
26 Feb 2020 Decision Letter - Masaki Mogi, Editor Clinical correlates of sarcopenia and falls in Parkinson’s disease PONE-D-19-34534R1 Dear Dr. Lima, 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, Masaki Mogi Academic Editor PLOS ONE Additional Editor Comments (optional): No further comment. 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: (No Response) 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: (No Response) Reviewer #2: The authors addressed all my comments. In particular, they reported the validity of using the time to reach from a chair in PD. ****** 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: Yes: Firuzan Fırat Ozer Reviewer #2: Yes: Fulvio Lauretani https://doi.org/10.1371/journal.pone.0227238.r003
Formally Accepted
5 Mar 2020 Acceptance Letter - Masaki Mogi, Editor PONE-D-19-34534R1 Clinical correlates of sarcopenia and falls in Parkinson’s disease Dear Dr. Lima: 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 Dr. Masaki Mogi Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0227238.r004

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