More precise method of low-density lipoprotein cholesterol estimation for tobacco and electronic cigarette smokers: A cross-sectional study

Han-Joon Bae; Hae Won Jung; Seung-Pyo Hong

doi:10.1371/journal.pone.0309002

Peer Review History

Original SubmissionMarch 12, 2024
5 Jun 2024 Decision Letter - Shukri AlSaif, Editor PONE-D-24-08009More precise method of low-density lipoprotein cholesterol estimation for tobacco and electronic cigarette smokers: a cross-sectional studyPLOS ONE Dear Dr. Bae, 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 Jul 20 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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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: This work investigated the accuracy of three equations used for LDL-C calculation in smokers. Several points should be addressed before publication. 1. The rationale for this analysis should be elaborated more. Is calculated LDL-C really needed? Why don't you just measure LDL-C directly? If calculated LDL-C is needed, what is the rationale? Whether it is availability problem, technical difficulty of the test and/or cost problem, I think it should be described in the Introduction. 2. Why did you decide that analysis was done according to the smoking status? Was calculated LDL-C less accurate in smokers compared to non-smokers? 3. Related to #2, you described the relationship between smoking and lipid profile in the Discussion section (line 262-277). I think this may be moved to the Introduction, because it helps to justify why the analysis should be done according to the smoking status. 4. What is the novelty of the work? It seems that the Conclusion just confirms that the study finding is consistent with the pre-existing knowledge overall. Reviewer #2: 1. The tables S1, S2, and S3 should include posthoc test results for significant comparisons. Additionally, significant results should be highlighted in bold to enhance the readability and comprehension of the tables. 2. Given that the comparisons are made within the same sample, adjusted p-values (e.g., using the Benjamini-Hochberg method) should be provided to control for multiple testing. 3. The statement in line 110 should indicate that TG <150 is excluded. 4. The font sizes in the axes and titles of all figures should be increased to improve readability. 5. The definition of overall precision as the ratio of direct LDL-C (dLDL-C) to non-high-density lipoprotein (non-HDL-C) should be supported by a reference or a clear rationale, such as citing relevant studies or providing a logical explanation for why this ratio is an appropriate measure 6. In Figure 2, the LDL-C ranges should be explicitly labeled on the plots for better clarity. 7. Figure 2 currently presents TG <150 mg/dL and TG <1000 mg/dL. It should categorize as TG ≥150–TG <400 mg/dL and TG ≥400–TG <1000 mg/dL. Including TG <150 mg/dL in the <1000 mg/dL category can lead to complexity in comparisons. 8. In line 212, the comment on TG categories is confusing. Table 1 presents data for TG <150 mg/dL, Table S4 for <400 mg/dL, and Table S5 for <1000 mg/dL. However, the text mentions TG levels <150 mg/dL, 150–400 mg/dL, and 400–1000 mg/dL. The TG categories should be clarified consistently throughout the manuscript. 9. The issue of inconsistent TG categories appears in multiple places. The TG categories should be clearly defined and consistently used throughout the manuscript. 10. In Figure 3, the legend should be reordered to present TG <150, 150–400 mg/dL, and 400–1000 mg/dL sequentially to improve the clarity of the plot. 11. The statement in the results about the superiority of the Martin equation in Figure 3 should be moderated. The results suggest that the equations perform similarly. 12. The findings related to Figure 4 should be included in the manuscript to provide a complete interpretation of the results. 13. The performance of the equations in the category of LDL-C <70 mg/dL and TG >400 mg/dL should be evaluated. These results could provide valuable insights into the literature. 14. A more detailed discussion comparing the results with existing literature should be provided. Comparing these findings with studies conducted in different populations would help to understand the consistency and differences in the results. ****** 6. 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Revision 1
17 Jul 2024 Author Response Thank you for your thoughtful and thorough review of our manuscript. We have made every effort to fulfil the reviewers’ specific requests. We have provided a point-by-point response to all comments from the editorial committee and reviewers below and also indicated our revisions to the manuscript in response to each comment. 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: This work investigated the accuracy of three equations used for LDL-C calculation in smokers. Several points should be addressed before publication. 1. The rationale for this analysis should be elaborated more. Is calculated LDL-C really needed? Why don't you just measure LDL-C directly? If calculated LDL-C is needed, what is the rationale? Whether it is availability problem, technical difficulty of the test and/or cost problem, I think it should be described in the Introduction. ▶Response: We appreciate the reviewers’ comments. Accordingly, the following text has been added to the Introduction (3rd paragraph): “The best method for measuring LDL-C levels uses ultracentrifuged plasma, but this method is time-consuming and labor-intensive [11]. Therefore, several homogeneous direct methods to measure high-density lipoprotein cholesterol (HDL-C) and LDL-C levels have been developed. These methods use various surfactants, ionic polymers, and other components to measure cholesterol levels in specific classes of lipoproteins in the serum [12]; however, they can be expensive and are not available at all medical centers.” 2. Why did you decide that analysis was done according to the smoking status? Was calculated LDL-C less accurate in smokers compared to non-smokers? ▶Response: Thank you for your comment. We have added the following information to the Introduction (second paragraph) to clarify this aspect: “…, and both smoking and smoking cessation have been shown to be associated with changes in cholesterol levels [9, 10].” 3. Related to #2, you described the relationship between smoking and lipid profile in the Discussion section (line 262-277). I think this may be moved to the Introduction, because it helps to justify why the analysis should be done according to the smoking status. ▶Response: Thank you for your comment, which we agree with. As mentioned in the response to the previous comment, we have now referred to this aspect in the Introduction (third paragraph). “and both smoking and smoking cessation have been shown to be associated with changes in cholesterol levels [9, 10].” 4. What is the novelty of the work? It seems that the Conclusion just confirms that the study finding is consistent with the pre-existing knowledge overall. ▶Response: Thank you for pointing this out. We agree with your comment, and research on LDL validation has indeed been conducted in several countries and research institutes. However, research on validation according to smoking status, particularly for users of electronic cigarettes, is lacking. Accordingly, we have added the following text to the Introduction (third paragraph): “Moreover, the use of electronic cigarettes (ECs) has increased considerably recently, but there have been very few studies on LDL-C measurements in this context.” Reviewer #2: 1. The tables S1, S2, and S3 should include posthoc test results for significant comparisons. Additionally, significant results should be highlighted in bold to enhance the readability and comprehension of the tables. ▶Response: Thank you for your helpful comments. Accordingly, we have highlighted the significant results in bold in Tables S1, S2, and S3, and added adjusted p-values derived using the Benjamini–Hochberg post-hoc method to the tables. 2. Given that the comparisons are made within the same sample, adjusted p-values (e.g., using the Benjamini-Hochberg method) should be provided to control for multiple testing. ▶Response: Thank you for pointing this out. As mentioned in the response to the previous comment, the required changes have now been made to Tables S1, S2, and S3. S1 Table. Characteristics of the study population with triglyceride levels of ≥400 mg/dL and <1000 mg/dL Smoke status Adjusted p-values (Benjamini–Hochberg method) Never Never Never Former Former Current Former Current Electronic Current Electronic Electronic Age, years 0.037 0.001 <0.001 <0.001 <0.001 0.001 Male, % <0.001 <0.001 <0.001 0.101 0.658 0.244 Body mass index, kg/m2 0.602 0.602 0.768 0.602 0.602 0.602 Laboratory data 　　　　　 Fasting glucose, mg/dL 0.088 0.600 0.108 0.137 0.030 0.088 Blood urea nitrogen, mg/dL <0.001 0.691 0.691 <0.001 0.016 0.691 Creatinine, mg/dL <0.001 <0.001 <0.001 0.002 0.350 0.523 GFR_EPI 0.004 0.224 0.168 <0.001 <0.001 0.224 Cholesterol 　　　　　 Total cholesterol, mg/dL 0.998 0.998 0.998 0.998 0.998 0.998 Triglyceride, mg/dL 0.808 <0.001 0.492 0.006 0.530 0.492 HDL-C, mg/dL 0.971 0.971 0.971 0.971 0.971 0.971 Direct LDL-C, mg/dL 0.983 0.642 0.144 0.642 0.144 0.158 Non-HDL-C, mg/dL 0.978 0.978 0.978 0.978 0.978 0.978 Sampson, mg/dL 0.416 0.054 0.977 0.416 0.690 0.416 Martin, mg/dL 0.387 0.066 0.917 0.387 0.661 0.387 Friedewald, mg/dL 0.366 0.018 0.902 0.366 0.707 0.366 Positive absolute value Martin, mg/dL 0.877 0.006 0.030 0.006 0.024 0.364 Positive absolute value Sampson, mg/dL 0.217 <0.001 0.080 0.003 0.204 0.993 Positive absolute value Friedewald, mg/dL 0.181 <0.001 0.056 <0.001 0.181 0.740 S2 Table. Characteristics of the study population with triglyceride levels of ≥150 mg/dL and <400 mg/dL Smoke status adjusted p-values (Benjamini–Hochberg method) Never Never Never Former Former Current Former Current Electronic Current Electronic Electronic Age, years 0.001 <0.001 <0.001 <0.001 <0.001 <0.001 Male, % <0.001 <0.001 <0.001 0.021 0.901 0.5436 Body mass index, kg/m2 0.048 0.888 0.174 0.066 0.634 0.174 Laboratory data 　　　　　　 Fasting glucose, mg/dL <0.001 0.020 0.413 <0.001 <0.001 0.084 Blood urea nitrogen, mg/dL <0.001 0.517 0.396 <0.001 <0.001 0.478 Creatinine, mg/dL <0.001 <0.001 <0.001 <0.001 0.014 0.853 GFR_EPI <0.001 0.018 0.035 <0.001 <0.001 <0.001 Cholesterol 　　　　　　 Total cholesterol, mg/dL 0.006 0.201 0.709 0.201 0.201 0.378 Triglyceride, mg/dL <0.001 <0.001 <0.001 0.008 0.030 0.338 HDL-C, mg/dL 0.042 <0.001 0.219 0.219 0.719 0.719 Direct LDL-C, mg/dL 0.012 0.329 0.195 0.006 0.018 0.329 Non-HDL-C, mg/dL 0.024 0.547 0.518 0.100 0.100 0.500 Sampson, mg/dL <0.001 0.009 0.681 0.378 0.378 0.538 Martin, mg/dL <0.001 0.090 0.934 0.224 0.224 0.541 Friedewald, mg/dL <0.001 0.003 0.541 0.461 0.461 0.541 Positive absolute value Martin, mg/dL 0.605 <0.001 0.003 <0.001 0.002 0.149 Positive absolute value Sampson, mg/dL 0.003 <0.001 0.968 0.581 0.248 0.140 Positive absolute value Friedewald, mg/dL <0.001 <0.001 <0.001 <0.001 0.004 0.810 S3 Table. Characteristics of the study population with triglyceride levels of <150 mg/dL Smoke status Adjusted p-values (Benjamini–Hochberg method) Never Never Never Former Former Current Former Current Electronic Current Electronic Electronic Age, years <0.001 <0.001 0.026 <0.001 <0.001 <0.001 Male, % <0.001 <0.001 <0.001 0.2964 0.2385 0.49 Body mass index, kg/m2 <0.001 0.008 0.074 <0.001 0.253 0.454 Laboratory data 　　　　　　 Fasting glucose, mg/dL <0.001 0.021 0.302 <0.001 0.012 0.959 Blood urea nitrogen, mg/dL <0.001 <0.001 0.475 <0.001 <0.001 0.014 Creatinine, mg/dL <0.001 <0.001 <0.001 <0.001 0.024 0.845 GFR_EPI <0.001 <0.001 0.700 <0.001 <0.001 <0.001 Cholesterol 　　　　　　 Total cholesterol, mg/dL 0.904 0.369 0.904 0.369 0.904 0.904 Triglyceride, mg/dL <0.001 <0.001 0.004 0.611 0.857 0.857 HDL-C, mg/dL <0.001 <0.001 0.044 0.410 0.730 0.882 Direct LDL-C, mg/dL 0.555 0.779 0.863 0.546 0.906 0.779 Non-HDL-C, mg/dL 0.036 0.843 0.835 0.099 0.835 0.835 Sampson, mg/dL 0.297 0.340 0.886 0.120 0.678 0.784 Martin, mg/dL 0.159 0.548 0.972 0.126 0.692 0.797 Friedewald, mg/dL 0.282 0.282 0.818 0.096 0.656 0.784 Positive absolute value Martin, mg/dL 0.552 0.030 0.500 0.234 0.552 0.887 Positive absolute value Sampson, mg/dL 0.597 0.363 0.402 0.402 0.402 0.363 Positive absolute value Friedewald, mg/dL 0.600 0.600 0.805 0.988 0.600 0.600 3. The statement in line 110 should indicate that TG <150 is excluded. ▶Response: Thank you for pointing this out. Accordingly, the corresponding text has been modified as follows: “At each TG level, the current smoker group exhibited higher TG levels (except those with TG levels <150 mg/dL) and dLDL-C levels (except those with TG levels <150 mg/dL) than the never smoker group (except those with TG levels <150 mg/dL).” 4. The font sizes in the axes and titles of all figures should be increased to improve readability. ▶Response: Thank you for this helpful comment. Accordingly, we have increased the font sizes of all axes and titles in the figures. 5. The definition of overall precision as the ratio of direct LDL-C (dLDL-C) to non-high-density lipoprotein (non-HDL-C) should be supported by a reference or a clear rationale, such as citing relevant studies or providing a logical explanation for why this ratio is an appropriate measure ▶Response: Thank you for your insightful comments. Non-HDL-C, calculated by subtracting HDL-C from total cholesterol, includes all particles that cause cardiovascular disease, namely, LDL-C, very low-density lipoprotein (VLDL), intermediate density lipoprotein, and lipoprotein A cholesterol. Non-HDL-C does not distinguish between LDL-C and remnant cholesterol and is considered a comprehensive target for managing cardiovascular risk. Clinically, LDL-C levels are related to non-HDL-C values in most cases; however, some patients have significantly higher non-HDL-C levels than LDL-C levels. 1. Nordestgaard B.G. Quantifying atherogenic lipoproteins for lipid-lowering strategies: consensus-based recommendations from EAS and EFLM. Atherosclerosis. 2020; 294: 46-61 2. Nordestgaard B.G. Triglyceride-rich lipoproteins and atherosclerotic cardiovascular disease: new insights from epidemiology, genetics, and biology. Circ Res. 2016; 118: 547-563 Accordingly, the corresponding text has been modified as follows: Method statistical analyses 1st pararagh “Overall precision was defined as the ratio of direct LDL-C (dLDL-C) to estimated LDL-C and non-high-density lipoprotein (NHDL). (S2 Fig, S3 Fig and S4 Fig).” 6. In Figure 2, the LDL-C ranges should be explicitly labeled on the plots for better clarity. ▶Response: Thank you for pointing this out. We have now added labels for the LDL-C ranges and the axis indexes. 7. Figure 2 currently presents TG <150 mg/dL and TG <1000 mg/dL. It should categorize as TG ≥150–TG <400 mg/dL and TG ≥400–TG <1000 mg/dL. Including TG <150 mg/dL in the <1000 mg/dL category can lead to complexity in comparisons. ▶Response: Thank you for your insightful comment. To illustrate the LDL-C error ranges for TG <150 mg/dL and the more commonly used TG <1000 mg/dL, Figure 2 depicts the TG <150 and TG <1000 mg/dL ranges. Additional data for the TG ≥150 and <400 mg/dL and TG ≥400 and <1000 mg/dL groups have now been included in the supplementary material. 8. In line 212, the comment on TG categories is confusing. Table 1 presents data for TG <150 mg/dL, Table S4 for <400 mg/dL, and Table S5 for <1000 mg/dL. However, the text mentions TG levels <150 mg/dL, 150–400 mg/dL, and 400–1000 mg/dL. The TG categories should be clarified consistently throughout the manuscript. ▶Response: Thank you for your comment. In real-world applications, we divided the groups to show the error when TG levels are below 400 mg/dL and TG levels are 1000 mg/dL. In the real world, we classified the difference between TGs below 400 and 1000 differently from the existing categories to explain the variation by LDL level. It has been modified like this. The Friedewald equation demonstrated higher MADs and MeADs than the other equations for TG levels <150 mg/dL, <400 mg/dL, <1000 mg/d, and 400-1000 mg/dL according to smoking status (Tables 1, S4,S5 and S6). 9. The issue of inconsistent TG categories appears in multiple places. The TG categories should be clearly defined and consistently used throughout the manuscript. ▶Response: Thank you for your comment. As mentioned in the response to the previous comment, the relevant data has been added and changes have now been made to the text. 10. In Figure 3, the legend should be reordered to present TG <150, 150–400 mg/dL, and 400–1000 mg/dL sequentially to improve the clarity of the plot. ▶Response: Thank you for your comment. We have changed the sequence of the TG groups as follows: 11. The statement in the results about the superiority of the Martin equation in Figure 3 should be moderated. The results suggest that the equations perform similarly. ▶Response: Thank you for your comment. Accordingly, we have changed the text as follows (Results - Precision of estimated LDL-C for the group with daily smoker status): “The accuracies of the Martin and Sampson equations were similar to that of the Friedewald equation.” 12. The findings related to Figure 4 should be included in the manuscript to provide a complete interpretation of the results. ▶Response: Thank you for your comment. Accordingly, we have added the following text to the manuscript (Results - Precision of estimated LDL-C for the group with daily smoker status): “In the EC smoker group with TG levels <400 mg/dL and >400 mg/dL, the MADs, MeADs, and correlation coefficients for the Sampson and Martin equations were similar. The Friedewald equation exhibited a higher difference than the other equations.” 13. The performance of the equations in the category of LDL-C <70 mg/dL and TG >400 mg/dL should be evaluated. These results could provide valuable insights into the literature. ▶Response: Thank you for your valuable suggestions. Accordingly, we have provided the corresponding data in S6 Table and added the following text to the Discussion (Differences in LDL-C and dLDL-C in current smokers): “In case of LDL-C levels <70 mg/dL and TG levels >400 mg/dL, the MAD of the Sampson equation was lower than those of the other equations without never smokers. In case of LDL-C levels <70 mg/dL and TG levels > 400 mg/dL with never smokers, the Martin equation had a lower MAD than the other equations.” S6 Table. Mean and median absolute deviations with 95% confidence intervals of estimated low-density lipoprotein cholesterol stratified by dLDL-C in the group with TG levels >400 mg/dL and <1000 mg/dL Sampson equation Martin equation Friedewald equation MAD MeAD MAD MeAD MAD MeAD Never smoker 9.81 -2.52 (-11.16 to 6.12) 9.49 -1.78 (-10.29 to 6.74) 14.11 -10.06 (-20.09 to -0.04) Former smoker 9.91 -5.34 (-9.82 to -0.85) 10.36 -7.12 (-11.96 to -2.27) 16.99 -15.21 (-21.71 to -8.72) Current smoker 11.87 -9.34 (-13.88 to -4.80) 12.45 -7.56 (-11.66 to -3.47) 20.23 -17.49 (-23.57 to -11.42) Electronic smoker 12.83 -15.12 (-39.4 to 9.16) 13.00 -13.71 (-37.40 to 9.97) 17.05 -19.45 (-50.38 to 11.47) 14. A more detailed discussion comparing the results with existing literature should be provided. Comparing these findings with studies conducted in different populations would help to understand the consistency and differences in the results ▶Response: Thank you for your comment. However, although numerous reports on LDL validation have been published recently, it is difficult to make comparisons due to insufficient literature on validation according to smoking status. In fact, the lack of data in this context was the main motivation behind designing and conducting this study. Attachments Attachment Submitted filename: comment_EC-PLOS_-1.docx https://doi.org/10.1371/journal.pone.0309002.r002
5 Aug 2024 Decision Letter - Shukri AlSaif, Editor More precise method of low-density lipoprotein cholesterol estimation for tobacco and electronic cigarette smokers: a cross-sectional study PONE-D-24-08009R1 Dear Dr. Bae, 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. Please make sure your user information is up-to-date by logging into Editorial Manager at Editorial Manager® and clicking the ‘Update My Information' link at the top of the page. If you have any questions relating to publication charges, 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, Shukri AlSaif Academic Editor PLOS ONE Review Comments to the Author Reviewer #1: Comments from the reviewer has been properly addressed and the manuscript has been improved. Thanks for your effort. Reviewer #2: I would like to express my gratitude to the authors for their attention to and implementation of the suggested corrections. https://doi.org/10.1371/journal.pone.0309002.r003
Formally Accepted
12 Sep 2024 Acceptance Letter - Shukri AlSaif, Editor PONE-D-24-08009R1 PLOS ONE Dear Dr. Bae, 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. Shukri AlSaif Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0309002.r004

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