Title: Systematic review of lung function and COPD with peripheral blood DNA methylation in population based studies
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1 Author s response to reviews Title: Systematic review of lung function and COPD with peripheral blood DNA methylation in population based studies Authors: Matthew Machin (matthew.machin12@imperial.ac.uk) Andre Amaral (a.amaral@imperial.ac.uk) Matthias Wielscher (m.wielscher@imperial.ac.uk) Faisal Rezwan (F.Rezwan@soton.ac.uk) Medea Imboden (medea.imboden@unibas.ch) Marjo-Riitta Jarvelin (m.jarvelin@imperial.ac.uk) Ian Adcock (ian.adcock@imperial.ac.uk) Nicole Probst-Hensch (Nicole.Probst@unibas.ch) John Holloway (J.W.Holloway@soton.ac.uk) Deborah Jarvis (d.jarvis@imperial.ac.uk) Version: 1 Date: 30 Jan 2017 Author s response to reviews: We would like to thank the editor for this opportunity to present our revised manuscript. Reviewer #1 Machin and colleagues present a systematic review of lung function and COPD. The manuscript is well written and the methods in accordance with PRISMA. In general the work is a good contribution to summarize the growing literature in the field of epigenetics and respiratory health and disease. There are minor issues that need addressing that will improve the manuscript. C1. Update to literature.
2 I note one additional study in an African American cohort of subjects published after the last date of indexing. Busch PUBMED ID This could be considered for inclusion if not burdensome but the cutoff of literature searching is well referenced in the manuscript. R1. The paper by Busch et al. has only been made public on 5 November 2016, during the review process of our manuscript. However, we have mentioned this paper in the discussion. C2. Correction to comments about Qiu et al study. The authors suggest that different criteria were used to define COPD in the Qiu study. This is not the case. The enrollment to the parent study is as stated on page 17 but both ICGN and EOCOPD used cutoff on a ratio of 0.7 to define COPD (published manuscript main text methods). Therefore line 55 on page 17 should be corrected with regard to the suggestion that "there was little consistency in the definition of COPD even within the same report". Also relevant in line 33 page 9. R2. We have corrected it. C3. Minor-please be sure that the first authors last name is spelled correctly as Qiu. (Table 9 legend - Qui, line 24 page 16 Qui) R3. We have corrected it. C4. Minor-the reference for this paper #24 does not include a complete author list or et al). R4. We have corrected it. C5. Page 14 line 29-the focus of the published results was the overlap CpG for COPD and lung function. All of those data are in the supplement of the manuscript. R5. We have deleted this sentence. C6. Grey literature
3 It would be helpful to the reader to have a definition of "grey" literature. R6. We have added it to the text as grey literature (i.e. published in non-commercial form or that falls outside the mainstream of journal and monograph publications). C7. Word choice regarding topic of study. Since the focus of the review is cross sectional methylation the authors might swap out "Epigenetic chnage" with "epigenetic variation" to better convey that change is not being measured in the highlighted studies. R7. We have changed it to epigenetic variation. Reviewer #2 Machen and colleagues reviewed the current literature to identify biomarkers of COPD identified by epigenetic changes linked to lung function. From population-based studies, the authors examined previously published datasets of DNA methylation profiles in peripheral blood from COPD subjects. Of the 1155 articles identified, only 6 papers were further reviewed. Authors found no significant CpG sites were consistently observed following combining these studies. This manuscript addresses a clinically important disease that requires new biomarkers to determine key biological plays in disease. However, in its present state the manuscript is not a research article but a review of the current COPD blood DNA methylation literature. As a review article, the manuscript is descriptive and requires major editing to become a review article. There are several items that require addressing. These are itemized below, not in order of significance, but in order of presentation. Major: C8. The major problem with this article is that its presented as research but it's a review article. As a review article, the layout of the paper would require major editing. Therefore, a methods section would not be needed. This could be removed and condensed into each subsection of the paper. R8. Our manuscript has been prepared following the guidelines for a systematic review, which includes a methods section so that others can replicate our findings. BMC Pulmonary Medicine does not have a specific section for Systematic Reviews, but these have been frequently published under the section of Research Articles (e.g. Hawkins et al doi: /s ; McLean et al doi: /s ; Wang et al doi: /s y). However, we have shortened the methods and moved a table to the supplement.
4 C9. Since epigenetics is a relatively modern technic, why were conference abstracts excluded? R9. As many conference abstracts do not reflect the final conclusion, often require changes/corrections prior to publication, and the amount of information provided on the methods is limited, these are not commonly included in systematic reviews. C10. Many lung tissue epigenetic papers exist that may aid in the discussing of this review. Please discuss the finding from these 6 papers compared to lung tissue epigenetic data. Are any CpG sites relevant compared to the lung data? R10. We aimed to explore the relationship of DNA methylation with lung function and COPD using samples that could realistically be obtained in a usual clinical setting (i.e. peripheral blood). It is beyond the scope of our article to systematically review the lung tissue reports, but we believe that, to date, there are no consistent unambiguous evidence of association with any particular sites in such tissue samples. In addition, we feel that studies using lung tissue may not be comparable to those using peripheral blood. C11. Were there any differences in the adjustment for confounders from study to study? Or were any consistent biomarkers reported between these studies prior to adjusting data to confounders? R11. The adjustment for confounders varied considerably across studies. However, most adjusted for age and smoking, and a few for sex too. We have commented on this issue in the discussion. C12. Authors state that there was a lack of consistency in the definition of COPD. What are the ethnicity breakdown in each of these studies? Please discuss this in greater detail in this lack of consistency section. R12. While some studies reported the proportions of different races/ethnicities in their sample, others did not. Lepeule et al. and Lange et al. reported the proportions of white and non-white participants, and adjusted their analyses for race/ethnicity. Participants in the studies by Qiu et al. and Marioni et al. were all white. Bell et al. and Wieslscher et al. did not provide a race/ethnicity breakdown. We have added this information to the lack of consistency section.
5 C13. Smoking history is unavailable for several of the studies. The studies that do supply a smoking history vary hugely. Please discuss this important factor in greater detail. R13. We have discussed it in further detail. C14. Since the studies primarily focus on leukocytes, was any exacerbation data available for each study cohort? This would greatly alter these profiles. Please discuss in greater detail. R14. None of the studies provided information on whether the samples had been collected during an exacerbation episode or not. We have added this information to the discussion. C15. Expansion of identified CpG sites and genes would be helpful. Why are these sites only listed from 2 papers (Qiu and Wielscher et al)? The 4 other papers must have similar data associated with lung function R15. We have deleted tables 7 through to 9. Minor: C16. On page 5 line 58, remove "(authors DJ and MM)." And again, on page 8 line 2. R16. On page 5, we have changed this sentence to Titles and Abstracts of articles were screened by two authors (DJ and MM) against the predefined inclusion criteria (Table 2) to identify articles for full-text review. On page 8, we have deleted it. Reviewer #3 The authors performed a systematic literature review of studies on DNA methylation with lung outcomes. They did a good job in terms of the systematic review, which I believe was comprehensive. The overall conclusion is that there is too much heterogeneity across study designs and methods; combining the results is not possible. I think this is an important conclusion, not only for the pulmonary DNA methylation studies, but all methylation work in the future. Comments: Abstract:
6 C17. Please name the lung function test (FEV1, FEV1/FVC ratio) earlier in the abstract (methods). R17. We have done it. C18. First sentence of Conclusions is again introduction, please omit. R18. We have deleted this sentence. Introduction: C19. I wouldn t say CpG base-pairs are "rare" R19. We have deleted the word rare and changed the sentence to These CpG base-pairs are concentrated in relatively high densities in areas known as CpG islands (CGIs). Results: C20. When I do = =21, instead of 16. Please correct this (from the figure, I get 1139). R20. We have corrected the text. It now reads as This step excluded 1,139 articles, leaving 16 articles for full-text review. C21, Study approaches: page 8 line is equal to line Please omit the last sentence (Lepeule et al. [26] adopted a candidate-loci approach whereas Lange et al. [27] performed global methylation analysis.) R21. We have deleted it. C22. Cell type corrections: please state whether the cell counts were imputed using Houseman method, or directly measured. R22. We have clarified this in the text ( All other articles adjusting for differing white cells used relative proportions of the cell types, which were directly measured ).
7 C23. Page 17, line 12: the ")" is placed incorrectly. R23. We have corrected it. Discussion: C24. In the second paragraph the authors start with the lack of consistency across studies, which I agree is very important. However, the first example is the COPD definition, which I believe is not the most important inconsistency. I think cell count adjustment and replication of results is crucial. To stress this out, please omit the COPD definition difference from the start of the paragraph. R24. We have deleted it. C25. I believe that the discussion can be more focused on the pitfalls of the published methylation studies. Already in the first paragraph I would stress out the lacks of the prior studies (cell count correction, confounder adjustment, smoking problems, lack of replication (which we know from gwas is crucial!). Furthermore, I think that the discussion can be shortened, for instance the paragraphs on the specific genes are a bit too much, I assume this is also discussed in the individual papers. And the findings are based on suboptimal study designs. R25. We have discussed these points further, and have followed the suggestion of shortening the discussion by deleting the paragraphs on specific genes. Reviewer #4 In "Systematic review of lung function and COPD with peripheral blood DNA methylation in population based studies", Machin and colleagues perform a systematic review of the published literature on blood DNA methylation in relation with COPD and lung function, to evaluate if there are any evidence of common CpGs associated with these traits cross-publications. From their analyses they conclude that in the current body of work no consistent findings have been reported for these traits. However, they note that two of the studies report associations at genes in the same pathway. The aim of the study was well defined, however, there remain some issues to be addressed. The heterogeneous nature of the analyses and phenotypes in the included papers are obviously one of the concerns in drawing conclusions from the systemic review of the results.
8 C26. Did the authors try to get access to the full list of significantly associated CpGs for the ICGN cohort in the Qiu et al. paper? I think that it would be useful if you could provide the analysis across all significant CpGs, to be able to draw proper conclusions. R26. We have checked the 349 CpGs listed in the Qiu et al s online supplement and could not find any of the significant hits from the other studies on that list. C27. The authors state (page 12, 18 and Table 5) that batch correction in the three EWAS studies was performed using principle component analysis (should be principal component analysis). While Bell et al. used PCA in identification of technical factors that may be potential confounders, neither Marioni et al. nor Bell et al. used principal components to correct for known confounding factors but rather included these factors directly as covariates in the models. In the third paper by Qiu et al., the authors report that they include indicator variables for batch effects in the linear models. It is unclear what this mean, but they do not mention using PCA. Please clarify. R27. We have reworded these sentences and have deleted the column Batch correction from table 5 (now table 4). C28. In some of the included papers, CpG probes were excluded based on some criteria (not listed), which the authors refer to as a sensitivity analysis (page 12, line 26-27). Can you please explain further what the authors of the original work did, and how this constitutes as a sensitivity analysis? R28. This refers to quality control, rather than statistical sensitivity analysis we have reworded this part of the text. C29. In the candidate studies, are more than one CpG included per loci/genomic region? If you would do the analysis on genomic region/gene basis rather than exact CpG do you observe any overlap between candidate and EWAS studies? R29. We have checked whether the significant genes in the candidate studies overlapped with those of the EWAS, and they did not.
9 C30. Were the CpGs tested in the candidate studies all included on either the 27k (or 450k) array used in the EWAS studies? R30. The CpGs tested by Wielscher et al. are present in the 450k array. However, Lepeule et al. and Lange et al. did not examine CpG sites as in the arrays they examined positions in the promoter region of genes (Lepeule et al.) and repetitive elements (i.e. Alu and LINE1; Lange et al.), which are not comparable to the CpG sites tested in by Qiu et al., Marioni et al. and Bell et al. C31. The authors state that Bell et al. account for probes with a SNP (page 18, line 26). Please explain. R31. We have deleted this sentence. C32. Is blood the correct tissue for addressing questions of causality for these traits? Besides studies looking at longitudinal changes would it not also be useful with larger studies, using denser arrays/sequencing, of lung function and COPD? R32. The use of lung tissue may be more informative than peripheral blood in terms of assessing causality between a risk factor and COPD. However, our interest is in identifying markers of abnormal lung function and COPD in samples that can be collected easily in a clinical/primary care setting these may inform future studies evaluating temporal changes in these markers in relation to lung function decline and disease progression and even before clinical signs are evident. C33. Please add a list of the abbreviations to the manuscript (as per requirements). R33. We have added a list of abbreviations and acronyms. C34. What is Table 7 showing? Please clarify in the legend or footnote whether the p-values are from analysis in the ICGN or EOCOPD cohort, meta-analysis of both? R34. We have deleted this table. C35. The authors write that pack years "..varied widely between individuals and possibly between studies". Did pack year vary between studies or not?
10 R35. Smoking history varied across studies. We have corrected this sentence. C36. How many significant associations did Qiu et al report in models adjusted for confounding factors? R36. This information is not clear in Qiu et al. s paper. In their supplement, only the top 100 CpGs for model II (adjusted for confounders) in ICGN were listed. They also presented a list of 349 hits for both ICGN and EOCOPD for COPD and lung function, but these are from the unadjusted analyses. C37. Are the two CpG sites in the SERPINA1 gene (reported in Qiu et al.) in the same CGI or different CGIs? R37. Neither cg nor cg are part of a CGI. C38. As a different p-value threshold was used in the replication in Qui et al. (page 14, line 39-41) state both p-values in the text. R38. We have added these to the text. C39. When discussing Leupele et al study, please also state if any of these are associated in the other studies (page 17, line 23)? R39. Lepeule et al. examined the levels of methylation in several positions in the promoter region of a specific group of genes. Their sites were not coded as CpG sites and could not be compared to those of the other studies. We have modified the text to make this clear. Some minor comments/spelling mistakes C40. Include et al either as italic or as normal font (not both). R40. We have corrected it. C41. Page 3, line 55: Use defined abbreviation for CpG islands
11 R41. We have corrected it. C42. Page 14, line 22: Missing word. "Qiu et al. reported COPD was associated with" R42. We have corrected it. C43. Page 14, line 55: Missing full stop after "from the Qiu et al report" R43. We have corrected it. C44. Page 17, lines 1-14: parenthesis in the wrong place. If possible split the sentence to improve readability. R44. We have corrected it and made the sentence easier to read. C45. Page 17, line 19: two --> too R45. We have corrected it. C46. Additional File: Remove the duplicate entry for the paper by Barret et al. R46. We have corrected it.
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