Bone mineral density and related clinical and laboratory factors in peritoneal dialysis patients: Implications for bone health management

Rami Tamimi; Amjad Bdair; Ahmad Shratih; Mazen Abdalla; Alaa Sarsour; Zakaria Hamdan; Zaher Nazzal

doi:10.1371/journal.pone.0301814

Peer Review History

Original SubmissionSeptember 18, 2023
8 Jan 2024 Decision Letter - Ali B. Roomi, Editor PONE-D-23-30185Bone Mineral Density and Related Clinical and Laboratory Factors in Peritoneal Dialysis Patients: Implications for Bone Health ManagementPLOS ONE Dear Dr. Nazzal, 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 Feb 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. 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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 include your full ethics statement in the ‘Methods’ section of your manuscript file. In your statement, please include the full name of the IRB or ethics committee who approved or waived your study, as well as whether or not you obtained informed written or verbal consent. If consent was waived for your study, please include this information in your statement as well. Additional Editor Comments: General Comments: This is a single-center observational study that aims to determine the prevalence of osteoporosis in Peritoneal Dialysis patients using bone mineral density measurements obtained through dual-energy X-ray absorptiometry scans. The study also explores possible associations with clinical and biochemical factors. Specific Revision Comments: 1. In the Introduction, please discuss the association between vitamin D and BMD found in kidney transplant recipients (KTRs), emphasizing the importance of early identification and correction of low BDM in peritoneal treatment patients who are often candidates for kidney transplants, adding the reference (Nutrients 2022, 14, 323. https://doi.org/10.3390/nu14020323). 2. In the Methods section, please consider addressing patients undergoing calcimimetic treatment. If included, add calcimimetics to the current medication history and consider them as a confounding variable in statistical analysis. 3. In the Study Measures section, please provide more details regarding the dosage of the parathormone kit. 4. In the Analysis Plan, please explicitly mention the variables used in regression analysis. 5. In the Results section, address the very low level of 25-hydroxyvitamin D. Explain how the authors interpret this data. 6. In Table 1, please define the history of the type of transplant being referred to. 7. In Table 1, please include data regarding inactive vitamin D supplementation. 8. In Figure 1, please ensure that the groups are consistently divided into non-osteoporosis and osteoporosis, as the figure currently reports data categorized into three groups. Please, homogenize the data. 9. In the Background Characteristics of the Patients (line 157, page 8), pleae note that the figure 1 in the brackets (Bone Mineral Density Distribution) does not match with the text (vitamin D lab results). 10. Tables 2 and 3: Divide Univariate and Multivariate analyses into two separate tables. 11. In the Discussion, please highlight the strengths of this study. 12. Please perform an extensive English language revision. [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 Reviewer #3: Partly ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #2: Yes Reviewer #3: 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: No Reviewer #2: Yes Reviewer #3: 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 Reviewer #3: 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: Dear editor, thank you for alllwing me the opportunity to review this paper. Overal, it is nicely crafted and reads well. The findings are not novel although data on PD patients a relatively scanty. The reviewer has not special comments to make. Reviewer #2: This study evaluates end-stage renal disease (ESRD) patients and risk of bone loss. The authors claim that the patients have accelerated bone turnover, leading to osteoporosis and osteopenia. The authors enrolled 76 peritoneal dialysis patients and performed DXA scan to evaluate BMD 31 at classic sites. By multivariate analysis they describe the relationship between BMD and clinical and biochemical parameters. The authors observed about 50% of the patients had low bone mass i.e. BMD T-score below -2,5 and formulated as osteoporosis and not surprising with a higher prevalence among patients with low BMI. Due to higher bone turnover higher alkaline phosphatase levels were observed among patients with low bone mass and vitamin D deficiency was also prevalent affecting about 85% of patients. The authors conclude correctly that they have observed that a notable proportion of PD patients experience reduced BMD and high degree of low vitamin D and the low BMD was correlated to low BMI. I do not find these observations new or surprising. It is very well known that high bone turnover increased alkaline phosphatase. That low BMI increase the risk of low bone mass and that vitamin D deficiency leads to immature bone and low BMD. I dislike the use of the term osteoporosis in the group of patients described and prefer the use of T-scores/Z-scores when younger than 50 years of age. The patients are very heterogenous i.e. some have had fractures, some are in prednisolone, they are male and females and aged younger and older than 50 years of age. A significant amount of the patients are suffering of secondary/tertiary hyperparathyroidism and the authors do not describe or discuss the impact hereof. The low bone mass might be explained by the renal disease (osteomalcia, hyperparathyroidism and renal ostedystrophia). Due to that the use of the term osteoporosis are misleading although all of the above might lead to increased risk of fractures. The reported alkaline phosphatase values are just slightly increase (mean value) although correlates to low bone mass. What does than mean in a clinical setting of the use of biochemistry to pin-point the diagnosis of low bone mass – claimed by the authors themselves? The authors cannot conclude anything from the present study other than it seems that PD patients are also of risk of low bone mass for many reasons and thereby might have an increased risk of fractures. That sufficient care of keeping normal vitamin D among other recommendations are needed. However, it is unknown if this would decrease the risk of low BMD. Reviewer #3: General Comments: This is a single-center observational study that aims to determine the prevalence of osteoporosis in Peritoneal Dialysis patients using bone mineral density measurements obtained through dual-energy X-ray absorptiometry scans. The study also explores possible associations with clinical and biochemical factors. Specific Revision Comments: 1. In the Introduction, please discuss the association between vitamin D and BMD found in kidney transplant recipients (KTRs), emphasizing the importance of early identification and correction of low BDM in peritoneal treatment patients who are often candidates for kidney transplants, adding the reference (Nutrients 2022, 14, 323. https://doi.org/10.3390/nu14020323). 2. In the Methods section, please consider addressing patients undergoing calcimimetic treatment. If included, add calcimimetics to the current medication history and consider them as a confounding variable in statistical analysis. 3. In the Study Measures section, please provide more details regarding the dosage of the parathormone kit. 4. In the Analysis Plan, please explicitly mention the variables used in regression analysis. 5. In the Results section, address the very low level of 25-hydroxyvitamin D. Explain how the authors interpret this data. 6. In Table 1, please define the history of the type of transplant being referred to. 7. In Table 1, please include data regarding inactive vitamin D supplementation. 8. In Figure 1, please ensure that the groups are consistently divided into non-osteoporosis and osteoporosis, as the figure currently reports data categorized into three groups. Please, homogenize the data. 9. In the Background Characteristics of the Patients (line 157, page 8), pleae note that the figure 1 in the brackets (Bone Mineral Density Distribution) does not match with the text (vitamin D lab results). 10. Tables 2 and 3: Divide Univariate and Multivariate analyses into two separate tables. 11. In the Discussion, please highlight the strengths of this study. 12. Please perform an extensive English language revision. ****** 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 Reviewer #3: 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. 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Revision 1
2 Feb 2024 Author Response Reviewer 1 comments: Dear editor, thank you for allowing me the opportunity to review this paper. Overall, it is nicely crafted and reads well. The findings are not novel although data on PD patients a relatively scanty. The reviewer has not special comments to make. Authors’ Response: Thank you for your time reading and evaluating the manuscript. We agree with you that some findings within our study may not be deemed novel. However, our primary objective was to evaluate the precise extent of BMD reduction within this specific patient demographic, thereby laying a foundation for subsequent investigations. Moreover, the existing literature lacks consistency in detailing the correlations between clinical and biochemical factors and BMD, underscoring the significance of our efforts to contribute clarity and insight to this nuanced discussion. Reviewer 2 comments This study evaluates end-stage renal disease (ESRD) patients and risk of bone loss. The authors claim that the patients have accelerated bone turnover, leading to osteoporosis and osteopenia. The authors enrolled 76 peritoneal dialysis patients and performed DXA scan to evaluate BMD 31 at classic sites. By multivariate analysis they describe the relationship between BMD and clinical and biochemical parameters. The authors observed about 50% of the patients had low bone mass i.e. BMD T-score below -2,5 and formulated as osteoporosis and not surprising with a higher prevalence among patients with low BMI. Due to higher bone turnover higher alkaline phosphatase levels were observed among patients with low bone mass and vitamin D deficiency was also prevalent affecting about 85% of patients. The authors conclude correctly that they have observed that a notable proportion of PD patients experience reduced BMD and high degree of low vitamin D and the low BMD was correlated to low BMI. Authors’ Response: Thank you for your time reading and evaluating the manuscript. We appreciate your supportive comments, they were very helpful and we believe they enhanced the manuscript. We carefully addressed each comment individually and incorporated relevant adjustments accordingly. I do not find these observations new or surprising. It is very well known that high bone turnover increased alkaline phosphatase. That low BMI increase the risk of low bone mass and that vitamin D deficiency leads to immature bone and low BMD. Authors’ Response: We expected certain findings for some factors. For instance, we expected BMD to exhibit a low measure among PD patients. However, our primary objective was to evaluate the precise extent of BMD reduction as well as Vitamin D deficiency within this specific patient demographic, thereby laying a foundation for subsequent investigations. Moreover, the existing literature lacks consistency in detailing the correlations between clinical and biochemical factors and BMD. For example, we expected certain results and associations for some biochemical factors, but the data didn't match those expectations. I dislike the use of the term osteoporosis in the group of patients described and prefer the use of T-scores/Z-scores when younger than 50 years of age. The patients are very heterogenous i.e. some have had fractures, some are in prednisolone, they are male and females and aged younger and older than 50 years of age. Authors’ Response: We agree to your point of view. For simplicity and convenience, we used the term "osteoporosis" when T-scores fell below -2.5. However, we acknowledge in the study limitations that relying solely on DEXA scan results for diagnosing osteoporosis may not be applicable to all patients' categories. A significant amount of the patients are suffering of secondary/tertiary hyperparathyroidism and the authors do not describe or discuss the impact hereof. The low bone mass might be explained by the renal disease (osteomalcia, hyperparathyroidism and renal ostedystrophia). Due to that the use of the term osteoporosis are misleading although all of the above might lead to increased risk of fractures. Authors’ Response: Since we employed DEXA scans for bone assessment, we chose to categorize patients into osteoporosis and osteopenia based on T scores. While acknowledging renal osteodystrophy's precision, our choice aligns with the DEXA scan methodology for bone status evaluation. Despite a notable portion of patients experiencing secondary/tertiary hyperparathyroidism, our multivariate analysis, encompassing both parathyroid hormone (PTH) and calcium laboratory results, failed to discern any significant association between these factors and bone mineral density (BMD), as expressed by T-score measurements. We elaborated on this point in the discussion section. The reported alkaline phosphatase values are just slightly increase (mean value) although correlates to low bone mass. What does that mean in a clinical setting of the use of biochemistry to pin-point the diagnosis of low bone mass – claimed by the authors themselves? Authors’ Response: In this study we don’t claim that elevated alkaline phosphatase levels can be utilized as a means to diagnose low bone mass in PD patients. Rather, we claim that higher alkaline phosphatase levels were observed in patients with lower BMD, and this observation reached statistical significance. It's important to clarify that while the statistical significance is established, we do not claim it to be clinically significant. We elaborated on this point more detail in the discussion section. The authors cannot conclude anything from the present study other than it seems that PD patients are also of risk of low bone mass for many reasons and thereby might have an increased risk of fractures. That sufficient care of keeping normal vitamin D among other recommendations are needed. However, it is unknown if this would decrease the risk of low BMD. Authors’ Response: In this cross-sectional study, we determined the prevalence rates of osteoporosis and osteopenia among PD patients in the region, along with the prevalence of vitamin D deficiency. While PD patients are inherently at risk of low bone mass for various reasons, our findings revealed that certain factors expected to influence bone health, such as PTH levels, Ca levels, Vitamin D levels, age, and gender, did not exhibit a significant role, at least in this study. It is noteworthy that future studies exploring the change of these variables within this population may alter the prevalence of bone mineral density. For example, a future trial of Vitamin D treatment with a pre and post DEXA scan to evaluate the effect of vitamin D in BMD changes among PD patients. Reviewer 3 comments 1. In the Introduction, please discuss the association between vitamin D and BMD found in kidney transplant recipients (KTRs), emphasizing the importance of early identification and correction of low BDM in peritoneal treatment patients who are often candidates for kidney transplants, adding the reference (Nutrients 2022, 14, 323. https://doi.org/10.3390/nu14020323). Authors’ Response: Thank you for your suggestion. Case discussed in the introduction of the manuscript (line 66-68). 2. In the Methods section, please consider addressing patients undergoing calcimimetic treatment. If included, add calcimimetics to the current medication history and consider them as a confounding variable in statistical analysis Authors’ Response: Patients in this cross-sectional study were not on any calcimimetic treatment. 3. In the Study Measures section, please provide more details regarding the dosage of the parathormone kit Authors’ Response: The kit used to determine the levels of Parathyroid hormone was added 4. In the Analysis Plan, please explicitly mention the variables used in regression analysis Authors’ Response: Variables used in the regression analysis were added. 5. In the Results section, address the very low level of 25-hydroxyvitamin D. Explain how the authors interpret this data Authors’ Response: The findings on 25-hydroxyvitamin D are addressed in the results section and interpreted in the discussion section. 6. In Table 1, please define the history of the type of transplant being referred to. Authors’ Response: History of kidney transplant added. 7. In Table 1, please include data regarding inactive vitamin D supplementation. Authors’ Response: Patients in this study were only on active Vitamin D supplementation (alpha D3). None were on inactive Vit D (cholecalciferol). 8. In Figure 1, please ensure that the groups are consistently divided into non-osteoporosis and osteoporosis, as the figure currently reports data categorized into three groups. Please, homogenize the data. Authors’ Response: Thank you for noting this. The figure has been corrected. 9. In the Background Characteristics of the Patients (line 157, page 8), please note that the figure 1 in the brackets (Bone Mineral Density Distribution) does not match with the text (vitamin D lab results). Authors’ Response: This typo was unintentional, and it has been rectified. The figure 1 has been placed in its correct position. 10. Tables 2 and 3: Divide Univariate and Multivariate analyses into two separate tables Authors’ Response: We agree with your suggestion. We divided Univariate and Multivariate analyses into two separate tables; Tables 2, 3, 4, and 5. 11. In the Discussion, please highlight the strengths of this study. Authors’ Response: Strengths of the study were highlighted. 12. Please perform an extensive English language revision. Authors’ Response: Extensive English language revision was done. Attachments Attachment Submitted filename: Response to Reviewers.pdf https://doi.org/10.1371/journal.pone.0301814.r002
25 Mar 2024 Decision Letter - Patricia Khashayar, Editor Bone Mineral Density and Related Clinical and Laboratory Factors in Peritoneal Dialysis Patients: Implications for Bone Health Management PONE-D-23-30185R1 Dear Dr. Nazzal, 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 will be generated when your article is formally accepted. Please note, if your institution has a publishing partnership with PLOS and your article meets the relevant criteria, all or part of your publication costs will be covered. 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Reviewer #1: Yes Reviewer #3: 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 #3: 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 #3: 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 further comments. Authors have addressed all comments in an adequate manner. Reviewer #3: The authors have satisfactorily addressed all the concerns I had with the previous submission and made the necessary changes in the manuscript. ****** 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 #3: No ******** https://doi.org/10.1371/journal.pone.0301814.r003
Formally Accepted
3 May 2024 Acceptance Letter - Patricia Khashayar, Editor PONE-D-23-30185R1 PLOS ONE Dear Dr. Nazzal, 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. Patricia Khashayar Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0301814.r004

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