Associations between physical activity types and multi-domain cognitive decline in older adults from the Three-city cohort

Caroline Dupré; Catherine Helmer; Bienvenu Bongue; Jean François Dartigues; Frédéric Roche; Claudine Berr; Isabelle Carrière

doi:10.1371/journal.pone.0252500

Peer Review History

Original SubmissionJanuary 28, 2021
26 Mar 2021 Decision Letter - Masaki Mogi, Editor PONE-D-21-03103 Household- and transportation-related physical activities are prospectively associated with preserved executive functions and verbal fluency in older people from the Three-city cohort. PLOS ONE Dear Dr. Carriere, 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. ============================== Two Reviewers well assessed this manuscript. However, several major revisions are needed in the present form. See the Reviewers’ comments and respond them appropriately. ============================== Please submit your revised manuscript by May 10 2021 11:59PM. 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In your revised cover letter, please address the following prompts: a) If there are ethical or legal restrictions on sharing a de-identified data set, please explain them in detail (e.g., data contain potentially identifying or sensitive patient information) and who has imposed them (e.g., an ethics committee). Please also provide contact information for a data access committee, ethics committee, or other institutional body to which data requests may be sent. b) If there are no restrictions, please upload the minimal anonymized data set necessary to replicate your study findings as either Supporting Information files or to a stable, public repository and provide us with the relevant URLs, DOIs, or accession numbers. Please see http://www.bmj.com/content/340/bmj.c181.long for guidelines on how to de-identify and prepare clinical data for publication. For a list of acceptable repositories, please see http://journals.plos.org/plosone/s/data-availability#loc-recommended-repositories. We will update your Data Availability statement on your behalf to reflect the information you provide. 3. Thank you for stating the following in the Acknowledgments Section of your manuscript: "The Three-city study is conducted under a partnership agreement between the Institut National de la Santé et de la Recherche Médicale (INSERM), Victor-Segalen Bordeaux¬ II University, and Sanofi- Aventis. The Three-city study was also supported by the Caisse Nationale d'Assurance Maladie des Travailleurs Salariés, Direction Générale de la Santé, MGEN, the Institut de la Longévité, Agence Française de Sécurité Sanitaire des Produits de Santé, the Regional Governments of Aquitaine, Bourgogne and Languedoc-Roussillon, the Fondation de France, the Ministry of Research-Inserm Programme 'Cohorts and collection of biological material', Novartis, the Fondation Plan Alzheimer, the Agence Nationale de la Recherche ANR PNR 2006 (ANR/DEDD/PNRA/PROJ/200206-01-01) and Longvie 2007 (LVIE- 003-01), the Caisse Nationale de Solidarité pour l'Autonomie (CNSA) and the Roche Pharma. This work was supported by the Chaire Santé des aînés et Ingénierie de la prévention, Université Jean Monnet, Saint-Etienne, France The funders had no role in study design, data collection and analysis, or preparation of the manuscript." We note that you have provided funding information that is not currently declared in your Funding Statement. However, funding information should not appear in the Acknowledgments section or other areas of your manuscript. We will only publish funding information present in the Funding Statement section of the online submission form. Please remove any funding-related text from the manuscript and let us know how you would like to update your Funding Statement. Currently, your Funding Statement reads as follows: "The authors received no specific funding for this work." Please include your amended statements within your cover letter; we will change the online submission form on your behalf. [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: 1. The title of the article can not cover the research content. The title is “Household- and transportation-related physical activities are prospectively associated with preserved executive functions and verbal fluency in older people from the Three-city cohort”, but this article investigates the effects of household/transportation activities, leisure time activities, and sport activities on the cognitive function of the elderly. And the cognitive domain is more than executive function and language fluency. 2. Introduction part should be further organized to make it clearer, more logical, and hierarchical. 3.The Voorrips questionnaire includes three parts: household/transportation activities, leisure time activities, and sport activities. Why do you divide the physical activity into two categories( household/transportation activities, leisure/sport activities) in your paper? What is the theoretical basis for this classification? 4. In the paper, you used the Mini-Mental State Examination (MMSE). Although the Mini-Mental State Examination (MMSE) was widely available from 1975 it is under copyright and since 2001 the authors have licensed Psychological Assessment Resources (PAR) to enforce this and payment to use this scale is required. As you used MMSE in the research reported in your submission you need to provide us with evidence of the payment/license. 5. On page 5, the word "Wave" is not clearly explained. Can you provide the raw data in the supplementary document? 6.The discussion part is too superficial, it is only a repetition of the research results, and there is no further analysis and explanation of the results. 7. The subjects of this study are about 80 years old, their level of leisure and sports activities was relatively low(research limitation 1). They can not represent the whole elderly population. Therefore, the expression of the conclusion in this paper should be adjusted. Reviewer #2: This article is of great scientific and clinical use value. Overall the manuscript, from the Introduction to the Conclusion, is easy to read, the text is well written, concise and logical and, conceptually and methodologically, relevant and correct. Results, discussion and conclusions are very well organized and written, supported by recent and relevant scientific literature. The manuscript, however, suffers from minor errors, that authors can improve. I outlined some (terminology) and I suggested to make some changes (please, see comments). In discussion, if possible, introduce the sociocultural factors to explain some differences from the other studies once it was conducted with French older adults, probably different from Northern European or anglossaxonic populations. ****** 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:** Xing WANG 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. Attachments Attachment Submitted filename: reviewer comments.docx Attachment Submitted filename: PONE-D-21-03103_reviewer_ACM.pdf https://doi.org/10.1371/journal.pone.0252500.r001
Revision 1
28 Apr 2021 Author Response Academic editor's comments: 1. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The author list, affiliations and the section headings were revised. The naming of supplemental tables and files was also changed. 2. We note that you have indicated that data from this study are available upon request. PLOS only allows data to be available upon request if there are legal or ethical restrictions on sharing data publicly. For information on unacceptable data access restrictions, please see http://journals.plos.org/plosone/s/data-availability#loc-unacceptable-data-access-restrictions. In your revised cover letter, please address the following prompts: a) If there are ethical or legal restrictions on sharing a de-identified data set, please explain them in detail (e.g., data contain potentially identifying or sensitive patient information) and who has imposed them (e.g., an ethics committee). Please also provide contact information for a data access committee, ethics committee, or other institutional body to which data requests may be sent. Our database includes information, such as age, sex, city of residence (study center), education levels, that are considered as personal data according to French and European laws. In the interest of participant confidentiality and in keeping with the data sharing guidelines imposed by the French national data protection agency (Commission Nationale de l’Informatique et des Libertés, CNIL), the data from the 3C cohort used in this study are available upon request. Interested researchers may contact e3c.coordinatingcenter@gmail.com for access. We modified the statement as follows: " In the interest of participant confidentiality and to comply with the data sharing guidelines imposed by the French national data protection agency (Commission Nationale de l’Informatique et des Libertés, CNIL), data are available upon request to the 3C data access committee. Please email requests to: e3c.coordinatingcenter@gmail.com" 3. We note that you have provided funding information that is not currently declared in your Funding Statement. However, funding information should not appear in the Acknowledgments section or other areas of your manuscript. We will only publish funding information present in the Funding Statement section of the online submission form. Please remove any funding-related text from the manuscript and let us know how you would like to update your Funding Statement. The Funding statement was removed from the manuscript text and the online Funding statement was replaced by: "The Three-city study is carried out under a partnership agreement between the Institut National de la Santé et de la Recherche Médicale (INSERM), Victor-Segalen Bordeaux II University, and Sanofi-Aventis. The Three-city study was also supported by the Caisse Nationale d'Assurance Maladie des Travailleurs Salariés, Direction Générale de la Santé, MGEN, the Institut de la Longévité, Agence Française de Sécurité Sanitaire des Produits de Santé, the Regional Governments of Aquitaine, Bourgogne and Languedoc-Roussillon, the Fondation de France, the Ministry of Research-Inserm Programme 'Cohorts and collection of biological material', Novartis, the Fondation Plan Alzheimer, the Agence Nationale de la Recherche ANR PNR 2006 (ANR/DEDD/PNRA/PROJ/200206-01-01), Longvie 2007 (LVIE-003-01), the Caisse Nationale de Solidarité pour l'Autonomie (CNSA), and Roche Pharma. This work was supported by the Chaire Santé des aînés et Ingénierie de la prévention, Université Jean Monnet, Saint-Etienne, France. The funders had no role in the study design, data collection and analysis, or preparation of the manuscript." Reviewer #1: 1. The title of the article cannot cover the research content. The title is “Household- and transportation-related physical activities are prospectively associated with preserved executive functions and verbal fluency in older people from the Three-city cohort”, but this article investigates the effects of household/transportation activities, leisure time activities, and sport activities on the cognitive function of the elderly. And the cognitive domain is more than executive function and language fluency. We thank the reviewer for this comment. We changed the title as follows: "Associations between physical activity types and multi-domain cognitive decline in older adults from the Three-city cohort." 2. Introduction part should be further organized to make it clearer, more logical, and hierarchical. We added a transition sentence before the focus on the protective effect of physical activity and we now better define the objective. 3.The Voorrips questionnaire includes three parts: household/transportation activities, leisure time activities, and sport activities. Why do you divide the physical activity into two categories( household/transportation activities, leisure/sport activities) in your paper? What is the theoretical basis for this classification? The Voorrips questionnaire collects data in two ways: - For household and transportation activities, the questionnaire includes 10 multiple-choice questions about housework, size of the house, cooking and use of transport. Each question has 3 or 4 possible answers. This first part of the questionnaire was used to calculate the household/transportation score. - For leisure and sport activities, two open-ended questions ask the participants to give their activities and then the frequencies. Thus, the same activity can be cited as leisure or sport activity. For example, several participants cited cycling in the sport part and others in the leisure part of the questionnaire. We could not reclassify leisure and sport activities according to their intensity because the Voorrisp questionnaire does not collect this information. In addition, in French older adults (≥72 years of age), intense sport activities are unusual. Therefore, we considered that the classification as sport or leisure activities by the participants was not accurate, and we pooled the two parts of the questionnaire into a single score. 4. In the paper, you used the Mini-Mental State Examination (MMSE). Although the Mini-Mental State Examination (MMSE) was widely available from 1975 it is under copyright and since 2001 the authors have licensed Psychological Assessment Resources (PAR) to enforce this and payment to use this scale is required. As you used MMSE in the research reported in your submission you need to provide us with evidence of the payment/license. We used the original French version of the questionnaire that is unlicensed. 5. On page 5, the word "Wave" is not clearly explained. Can you provide the raw data in the supplementary document? To clarify the 3C cohort design, we now provide in a supplemental table, for each wave and each center, the number of participants still in the cohort and the observed time since inclusion. For practical reasons and also because the sample was aged, the examination time varies from one participant to another in the same wave. However, we used continuous-time statistical models to take into account this variation. 6.The discussion part is too superficial, it is only a repetition of the research results, and there is no further analysis and explanation of the results. This comment seems to contradict the analysis by reviewer #2 who wrote that "Results, discussion and conclusions are very well organized and written, supported by recent and relevant scientific literature." In the Discussion we compared our results with the abundant literature in the field and suggested possible explanations for conflicting results. The inconsistencies can be due to inadequate methods, analysis of different physical activity types, and assessment of cognitive abilities related to different domains. We extensively discussed the limits and the strengths of our study. We also added in the new version a paragraph at the end of the Discussion section that mentions the differences in both prevalence and type of physical activities in different world regions, between rural and urban societies, and between genders. This may lead to differences in the statistical power of the studies and explain some inconsistent previous findings. We also highlighted that the physical activity types are changing with a decrease of domestic activities and increase of leisure time, and that these changes are not uniform across countries. We added two references and concluded on the need to confirm our results in other older populations. 7. The subjects of this study are about 80 years old, their level of leisure and sports activities was relatively low (research limitation 1). They cannot represent the whole elderly population. Therefore, the expression of the conclusion in this paper should be adjusted. We agree that our results only apply to people older than 72 years, and we clarified this point in the conclusion. Reviewer #2: 1- This article is of great scientific and clinical use value. Overall the manuscript, from the Introduction to the Conclusion, is easy to read, the text is well written, concise and logical and, conceptually and methodologically, relevant and correct. Results, discussion and conclusions are very well organized and written, supported by recent and relevant scientific literature. We thank the reviewer for his/her very positive comments on our manuscript. 2- The manuscript, however, suffers from minor errors, that authors can improve. I outlined some (terminology) and I suggested to make some changes (please, see comments). The errors have been corrected in the new version. 3- In discussion, if possible, introduce the sociocultural factors to explain some differences from the other studies once it was conducted with French older adults, probably different from Northern European or anglossaxonic populations. We thank the reviewer for this suggestion. We have written an additional paragraph at the end of the Discussion section that mentions the differences in both prevalence and type of physical activities in different world regions, between rural and urban societies, and between genders. This may lead to differences in the statistical power of the studies and explain some inconsistent previous findings. We also highlighted that the physical activity types are changing with a decrease of domestic activities and increase of leisure time, and that these changes are not uniform across countries. We added two references and concluded on the need to confirm our results in other older populations. Attachments Attachment Submitted filename: Response to Reviewers.docx https://doi.org/10.1371/journal.pone.0252500.r002
18 May 2021 Decision Letter - Masaki Mogi, Editor Associations between physical activity types and multi-domain cognitive decline in older adults from the Three-city cohort. PONE-D-21-03103R1 Dear Dr. Carriere, 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, 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: All comments have been addressed Reviewer #2: (No Response) ******** 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: (No Response) ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #2: (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: Yes Reviewer #2: (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: Yes Reviewer #2: (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) Reviewer #2: (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 Reviewer #2: No https://doi.org/10.1371/journal.pone.0252500.r003
Formally Accepted
21 May 2021 Acceptance Letter - Masaki Mogi, Editor PONE-D-21-03103R1 Associations between physical activity types and multi-domain cognitive decline in older adults from the Three-city cohort. Dear Dr. Carrière: 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 Dr. Masaki Mogi Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0252500.r004

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