Maternal body composition and gestational weight gain in relation to asthma control during pregnancy

Danielle R. Stevens; Matthew C. H. Rohn; Stefanie N. Hinkle; Andrew D. Williams; Rajesh Kumar; Leah M. Lipsky; William Grobman; Seth Sherman; Jenna Kanner; Zhen Chen; Pauline Mendola

doi:10.1371/journal.pone.0267122

Peer Review History

Original SubmissionJuly 1, 2021
5 Nov 2021 Decision Letter - Kelli K Ryckman, Editor PONE-D-21-21560Maternal body composition and gestational weight gain in relation to asthma control during pregnancyPLOS ONE Dear Dr. Mendola, 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 Dec 20 2021 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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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: This is a well written paper, and novel study examining body composition and gestational weight gain and their relationship with asthma control during pregnancy. What was the rationale for examining FEV6? Reviewer #2: This is a prospective cohort of 299 women examining the associations between body composition and weight gain with asthma during pregnancy. The manuscript is well written and shows that increased weight and exessive weight gain in the first trimester were associated woth lung function during pregnancy. I only have some minor comments. Materials and Methods In regards to the population; did you account for women twins or triplets? Were they included in the cohort? In the last paragraph on page 7 (rows 145-148) you state that women reported asthma attacks and medical encounters from the past year; did you also have medical records to confirm this or was it just by participants recall? Results Do you have any explanation for the improved PEF in women with exessive weight gain? (Table S3) Dicsussion The FEV1/FVC seems to be unaltered during pregnancy regardless of weight gain. Still, women tend to have more asthma symptoms with increased weight. Do you have any comments on this? Is the symptomology reflecting asthma? Or something else? The conclusion is not very clear. Now it includes parts that should be in the introduction (background) as well as parts that should be in the first paragraph of the discussion. I suggest you leave those things out and instead include something more similar to what you have in the abstract. ****** 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. 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Revision 1
25 Mar 2022 Author Response RESPONSE TO REVIEWERS Reviewer #1: This is a well written paper, and novel study examining body composition and gestational weight gain and their relationship with asthma control during pregnancy. What was the rationale for examining FEV6? Response: FEV6 was included as part of the original study protocol based on prior studies in pregnant populations finding FEV6 to be highly correlated with FVC whilst being easier, more achievable, more reproducible, and less physically demanding1. Its inclusion in the analysis was to completely represent all measures from spirometry. 1. Zairina E, Abramson MJ, McDonald CF, et al. A prospective cohort study of pulmonary function during pregnancy in women with and without asthma. J Asthma. 2016;53(2):155-63. doi:10.3109/02770903.2015.1080268 Reviewer #2: This is a prospective cohort of 299 women examining the associations between body composition and weight gain with asthma during pregnancy. The manuscript is well written and shows that increased weight and excessive weight gain in the first trimester were associated with lung function during pregnancy. I only have some minor comments. Materials and Methods In regards to the population; did you account for women twins or triplets? Were they included in the cohort? Response: To be eligible for study participation, participants had to have a singleton pregnancy. We have added study eligibility criteria to our supplement as S1 Table and reference this table on page 6, line 108 of the revised manuscript: “Medical record review was used to identify potentially eligible participants, who were then screened for eligibility (S1 Table) and consent”. In the last paragraph on page 7 (rows 145-148) you state that women reported asthma attacks and medical encounters from the past year; did you also have medical records to confirm this or was it just by participants recall? Response: A chart abstraction was completed for participants during their time in the study and included encounters within a given hospital system. Thus, chart abstractions were unfortunately not able to detail a complete history of asthma attacks and/or medical encounters. However, you bring up a good point about the limitations of this measure. We have thus added additional language to the limitations section (page 21, lines 389-402) on self-reported measurement error. This section now reads, “This study was limited by a small sample size which precluded our ability to conduct subgroup analyses by asthma phenotypes. Participant self-report of certain exposure (pre-pregnancy BMI) or outcome (symptomology, exacerbations) may be subject to measurement error. Self-reported pre-pregnancy weights were highly correlated with first measured pregnancy weights (n=343, r=0.98) as well as chart-abstracted pre-pregnancy weights (n=118, r=0.94) in our cohort, and missing data imputation for pre-pregnancy BMI allowed us to produce unbiased and efficient estimates for our associations[41]. Symptomology was self-reported in daily diaries, which have been shown to provide more sensitive estimates of asthma control than retrospective questionnaires[42]. Exacerbations – especially for the first trimester, which encompassed a one-year timeframe – were subject to recall bias. However, given the severity of asthma exacerbations and disruption that they would cause, any recall bias of exacerbations is likely limited. Finally, though we account for chronic mediation use at baseline, we did not assess how changes in medication use may have impacted our associations[43].” Results Do you have any explanation for the improved PEF in women with excessive weight gain? (Table S3) Response: We agree that this is a curious finding. These associations are present only for the excessive second trimester gestational weight gain; though not significant, first and third trimester excessive gestational weight gain were associated with reduced PEF. In childhood, weight gain is associated with greater lung volumes due to lung growth via IGF-1 and other factors. In adult women, this would not make too much sense. From the pregnancy literature (which is admittedly limited), there is no strong explanation. More notable, our clinical authors do not see a reason for the finding, and we are hesitant to speculate. We have added some additional language to the discussion on page 19, lines 344-346 clarifying this: “Unexpectedly, we observed few associations between gestational weight gain and lung function other than improved percent predicted peak flow with excessive second trimester gestational weight gain. Given the lack of biologic plausibility, this finding may be due to chance.” Discussion The FEV1/FVC seems to be unaltered during pregnancy regardless of weight gain. Still, women tend to have more asthma symptoms with increased weight. Do you have any comments on this? Is the symptomology reflecting asthma? Or something else? Response: Our findings are present only among participants with asthma, suggesting that the mechanisms driving this association are asthma-specific. Further, the main symptoms influenced were activity limitation, night symptoms, and rescue inhaler use; respiratory symptoms – which may be more obviously linked to lung function – were unaffected. Several potential mechanisms may explain our findings. The means by which participants regulate weight changes (e.g., exercise, diet) may differ by asthma status, and this may be the true factor influencing symptomology in participants with asthma. Asthma may be co-occurring with weight gain-related pregnancy complications (e.g., hypertensive disorders of pregnancy) to influence symptomology. Along the lines of your suggestion, symptomology may be reflecting something other than asthma (e.g., increased perception of dyspnea and fatigue associated with pregnancy-related weight gain, which may be felt more keenly among participants with asthma). We have discussed lifestyle factors (page 20, lines 355-359), pregnancy-related dyspnea and fatigue (page 19, lines 345-347), and now briefly reference weight gain-related pregnancy complications on page 20, lines 358-359. The conclusion is not very clear. Now it includes parts that should be in the introduction (background) as well as parts that should be in the first paragraph of the discussion. I suggest you leave those things out and instead include something more similar to what you have in the abstract. Response: We have modified the Conclusions (Page 22, lines 407-422) to now read, “Poor asthma control affects 57-80% of patients [44] and is modified for more than half of women during pregnancy[7], making identification of risk factors a priority. In this prospective pregnancy cohort of women with and without asthma, we observed asthma-specific associations between higher pre-pregnancy BMI, early pregnancy skinfolds, and excessive first trimester gestational weight gain associated with restrictive changes in lung function and poor asthma control during pregnancy. Despite experiencing decrements in lung function and asthma control, women with an obese asthma phenotype had fewer asthma-related doctor’s visits, suggesting less active management of asthma in this high-risk group. Active asthma management is key to the control of asthma and mitigation of adverse outcomes in pregnancies complicated by asthma[6]. While prenatal care visits are unrelated to asthma, they may provide an opportunity to help pregnant persons with asthma – particularly high-risk individuals with obesity or excess first trimester gestational weight gain – achieve better asthma control." Attachments Attachment Submitted filename: Response to Reviewers.docx https://doi.org/10.1371/journal.pone.0267122.r002
4 Apr 2022 Decision Letter - Kelli K Ryckman, Editor Maternal body composition and gestational weight gain in relation to asthma control during pregnancy PONE-D-21-21560R1 Dear Dr. Mendola, 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, Kelli K Ryckman Academic Editor PLOS ONE Additional Editor Comments (optional): Reviewers' comments: https://doi.org/10.1371/journal.pone.0267122.r003
Formally Accepted
7 Apr 2022 Acceptance Letter - Kelli K Ryckman, Editor PONE-D-21-21560R1 Maternal body composition and gestational weight gain in relation to asthma control during pregnancy Dear Dr. Mendola: I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department. If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org. If we can help with anything else, please email us at plosone@plos.org. Thank you for submitting your work to PLOS ONE and supporting open access. Kind regards, PLOS ONE Editorial Office Staff on behalf of Dr. Kelli K Ryckman Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0267122.r004

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