Higher number of steps is related to lower endogenous progesterone but not estradiol levels in women

Kinga Słojewska; Andrzej Galbarczyk; Magdalena Klimek; Anna Tubek-Krokosz; Karolina Krzych-Miłkowska; Joanna Szklarczyk; Magdalena Mijas; Monika Ścibor; Grazyna Jasienska

doi:10.1371/journal.pone.0299580

Peer Review History

Original SubmissionOctober 3, 2023
28 Nov 2023 Decision Letter - Sandar Tin Tin, Editor PONE-D-23-31898Higher number of steps is related to lower endogenous progesterone but not estradiol levels in womenPLOS ONE Dear Dr. Galbarczyk, Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. Please submit your revised manuscript by Jan 12 2024 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file. 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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 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: In the study entitled "Higher number of steps is related to lower endogenous progesterone but not estradiol levels in women," the authors investigate the association between physical activity and the levels of sex hormones in premenopausal women. The importance of the study is driven by the paucity of data on the mechanism by which physical activity reduces the risk of breast cancer. The paper is well-written, the methodology and design of the study are clear, but there should be clarification regarding other physical activities the participants might have done during the study period. Comments that should be acknowledged: • Although mentioned in the limitation, please clarify if you asked about other physical activities unrelated to steps. For example, the Fitbit Alta HR wristband accelerometers cannot track biking in the step count. If women performed other activities not monitored by the device, it could significantly change the results • Table 1 should be in the results section • Statistical analysis: “multiple regression models were used to test the effects of exercise (expressed as number of steps) on estradiol and progesterone levels.” I would consider changing it to “… (expressed as the average number of steps per day)...” • Table 2 – linear association between daily number of steps and estradiol level: I think the p-value should be 0.688 or 0.69 and not 0.60. • The reference to Feehan et al on page 19 should be changed to [49]. Reviewer #2: The manuscript studied the relationship between female sex hormone levels and the level of physical activity in women. The topic is of high importance since the level of physical activity is very low in adults in the modern societies, and the prevalence of sex-hormone related cancers is increasing in women. The aims are well defined, however the methods that is used to estimate the influence of physical activity on sex hormone levels is not appropriate. The aims are well defined, however the methods are not appropriate. I suggest the manuscript for publication after a major revision. The reasons for this suggestion are the following: 1) Two subgroups of women were formed on the basis of the level of physical activity, however, the two subgroups are not described by age and the other studied biological parameters (height, weight, BMI, the description is given only for the whole sample (Table 1). Since the age-group is ranged between 20.4 and 35.4 years, this is important to describe. Sex hormone levels change by ageing, a decrease can be seen after 30 years of age in the level of estradiol and progesterone. The mean steps per day is 10319 in the whole sample, this value is rather high in this age-group, it should be important to see the mean value of steps per day also for the subgroups. The recommendation for the studied age group for steps per day is 7-10000 according to the literature (e.g. DOI: https://doi.org/10.1016/S2468-2667(21)00302-9). By considering the mean steps of the 2 subgroups could help in the understanding of the research results. It is my impression that the cut-off value (10 000 steps/day) too high in the studied sample, or not only two but 3 subgroups should be formed (low, average, high level of physical activity) to analyse the relationship between the level of physical activity and sex hormone levels. 2) It is not clear why it is of high importance to ‘reduce’ the sex hormone levels in premenopausal women (this is emphasized by the Authors in the Abstract and in the main part of the manuscript, too). They are in the reproductive stage of their lives, decreased sex hormone levels can influence menstrual cycle, reproductive activity, bone health etc. It must be emphasized that the level of physical activity decreased very dramatically in the last decades, so increased level of physical activity means in this case that women have sufficient level of physical activity. 3) Why only body weight measured by Tanita was analysed in the manuscript? This device estimate body mass components as well, why the relationship of sex hormone levels with body fat mass and muscle mass were not analysed? Increased body fatness is evidenced to be related with sex hormone levels in women. ****** 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: Yes: Annamaria Zsakai ******** [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. 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Revision 1
11 Jan 2024 Author Response Dear Editors, We would like to thank the Reviewers and Editors for their insightful assessment of the manuscript. We have tried to adequately answer all reviewers’ comments. We believe that our work has improved significantly, and we hope our manuscript will be considered suitable for publication. Reviewer #1: Although mentioned in the limitation, please clarify if you asked about other physical activities unrelated to steps. For example, the Fitbit Alta HR wristband accelerometers cannot track biking in the step count. If women performed other activities not monitored by the device, it could significantly change the results. -Response: We asked participants about other activities but decided not to take them into account in this publication. Due to the fact that there are official recommendations on how many steps a day should be taken to maintain health, we have decided to include only the average number of steps taken per day in this publication. Information about other activities was self-reported by participants and thus not very reliable and difficult to quantify. In addition, the purpose of this study was to assess if number of steps per day correlates with levels of ovarian hormones. This approach allows to formulate conclusions that are useful for individual women and important in the context of public health in the area of breast cancer prevention. Table 1 should be in the results section -Response: Thank you. Agreed. We moved Table 1 to the results section. Statistical analysis: “multiple regression models were used to test the effects of exercise (expressed as number of steps) on estradiol and progesterone levels.” I would consider changing it to “… (expressed as the average number of steps per day)” -Response: Thank you for pointing out this shortcut. As suggested, we changed "expressed as number of steps" to "expressed as average number of steps per day". Table 2 – linear association between daily number of steps and estradiol level: I think the p-value should be 0.688 or 0.69 and not 0.60. -Response: Thank you very much for spotting this mistake. We changed the p-value to 0.69. The reference to Feehan et al on page 19 should be changed to [49]. -Response: We are not entirely sure if our interpretation of the Reviewer’s suggestion is correct. We have found an incorrect style of the reference “Feehan et al., 2018” on page 12. We have now changed it to the Vancouver style. We would be grateful if the Reviewer could confirm if this was the suggested issue. Reviewer #2 Two subgroups of women were formed on the basis of the level of physical activity, however, the two subgroups are not described by age and the other studied biological parameters (height, weight, BMI) the description is given only for the whole sample (Table 1). Since the age-group is ranged between 20.4 and 35.4 years, this is important to describe. Sex hormone levels change by ageing, a decrease can be seen after 30 years of age in the level of estradiol and progesterone. The mean steps per day is 10319 in the whole sample, this value is rather high in this age-group, it should be important to see the mean value of steps per day also for the subgroups. The recommendation for the studied age group for steps per day is 7-10000 according to the literature (e.g. DOI: https://doi.org/10.1016/S2468-2667(21)00302-9). By considering the mean steps of the 2 subgroups could help in the understanding of the research results. -Response: Thank you for pointing this out. We have supplemented Table 1 with descriptive characteristics of the subgroups. We agree, that the mean steps per day is rather high in this age-group. This is a result of the study's design. At the beginning of the observation, each woman received a fitness club pass which allowed for unlimited training sessions and was asked to perform no less than 180 minutes/week of moderate to vigorous physical activity of her choice. We have clarified this in the methods section. It is my impression that the cut-off value (10 000 steps/day) too high in the studied sample, or not only two but 3 subgroups should be formed (low, average, high level of physical activity) to analyse the relationship between the level of physical activity and sex hormone levels. Response: We decided to set a cut-off of 10,000 steps a day due to the widespread recommendations of this value as necessary to maintain health. However, we realize that there is evidence in the literature that health benefits are observed at rates lower than 10,000 steps per day. Therefore, we also divided the study group into 3 subgroups (tertiles: low = 8,209; medium = 10,450; high = 12,274) according to the average daily number of steps. These results are presented in Table 2. It is not clear why it is of high importance to ‘reduce’ the sex hormone levels in premenopausal women (this is emphasized by the Authors in the Abstract and in the main part of the manuscript, too). They are in the reproductive stage of their lives, decreased sex hormone levels can influence menstrual cycle, reproductive activity, bone health etc. It must be emphasized that the level of physical activity decreased very dramatically in the last decades, so increased level of physical activity means in this case that women have sufficient level of physical activity. -Response: Indeed, this issue was not sufficiently explained in our original manuscript. We have added the following in the discussion: It should be also emphasized that sex hormones, while related to the increased risk of breast cancer, are crucial for many aspects of healthy physiology [63,64]. Their beneficial role is well established for fertility, cardiovascular function, bone health and mental health. However, insufficient levels of physical activity may lead to changes in the body’s delicate hormonal balance contributing to altered hormone levels and adverse health outcomes. Thus, it is important for physically active women to discuss these issues with their physicians. Why only body weight measured by Tanita was analysed in the manuscript? This device estimate body mass components as well, why the relationship of sex hormone levels with body fat mass and muscle mass were not analysed? Increased body fatness is evidenced to be related with sex hormone levels in women. -Response: Although the role of body mass index on sex hormone levels and the development of breast cancer in premenopausal women is not clear, body mass index has been shown to be associated with sex hormone binding [Ingram, D M et al. 1990; doi:10.1038/bjc.1990.57]. Thus, we decided to perform statistical analyzes using BMI because it is a parameter that anyone can easily calculate. We wanted our research to be understandable to people outside the scientific community and to be easily conveyed in conversation. This is important in the context of public health. Additionally, in response to the Reviewer’s comment we rerun our analyses replacing BMI with the percentage of body fat or muscle mass. Attachments Attachment Submitted filename: Response to Reviewers.docx https://doi.org/10.1371/journal.pone.0299580.r002
6 Feb 2024 Decision Letter - Sandar Tin Tin, Editor PONE-D-23-31898R1Higher number of steps is related to lower endogenous progesterone but not estradiol levels in womenPLOS ONE Dear Dr. Galbarczyk, Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. Please submit your revised manuscript by Mar 22 2024 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file. Please include the following items when submitting your revised manuscript: A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'. A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'. An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'. If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter. If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. 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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 ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: 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 ****** 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 ****** 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: Thank you for revising the manuscript based on the Reviewers comments. I have one more comments that should be addressed: Please describe in table 1 if there is a significant difference in any of the parameters between the groups (<10000 steps per day and > 10 days per day). It is clear there is a difference in the number of steps, but other parameters should be compared. ****** 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.0299580.r003
Revision 2
8 Feb 2024 Author Response As suggested by the Reviewer #1, we have added results of independent samples t-tests to the Table 1. We have also stated in the Results section that: "There was no statistically significant differences between the groups of women who took less than 10,000 steps and more than 10,000 steps in mean age, cycle length, body height, body weight and BMI." We also made sure that we did not cite papers that have been retracted. Attachments Attachment Submitted filename: Response to Reviewers.docx https://doi.org/10.1371/journal.pone.0299580.r004
13 Feb 2024 Decision Letter - Sandar Tin Tin, Editor Higher number of steps is related to lower endogenous progesterone but not estradiol levels in women PONE-D-23-31898R2 Dear Dr. Galbarczyk, 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, Sandar Tin Tin Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0299580.r005
Formally Accepted
26 Mar 2024 Acceptance Letter - Sandar Tin Tin, Editor PONE-D-23-31898R2 PLOS ONE Dear Dr. Galbarczyk, I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now being handed over to our production team. At this stage, our production department will prepare your paper for publication. This includes ensuring the following: * All references, tables, and figures are properly cited * All relevant supporting information is included in the manuscript submission, * There are no issues that prevent the paper from being properly typeset If revisions are needed, the production department will contact you directly to resolve them. If no revisions are needed, you will receive an email when the publication date has been set. At this time, we do not offer pre-publication proofs to authors during production of the accepted work. Please keep in mind that we are working through a large volume of accepted articles, so please give us a few weeks to review your paper and let you know the next and final steps. Lastly, if your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org. If we can help with anything else, please email us at customercare@plos.org. Thank you for submitting your work to PLOS ONE and supporting open access. Kind regards, PLOS ONE Editorial Office Staff on behalf of Dr. Sandar Tin Tin Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0299580.r006

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