Tracking the incidence and risk factors for SARS-CoV-2 infection using historical maternal booking serum samples

Edward Mullins; Ruth McCabe; Sheila M. Bird; Paul Randell; Marcus J. Pond; Lesley Regan; Eleanor Parker; Myra McClure; Christl A. Donnelly

doi:10.1371/journal.pone.0273966

Peer Review History

Original SubmissionApril 25, 2022
12 Aug 2022 Decision Letter - Atalay Goshu Muluneh, Editor Transfer Alert This paper was transferred from another journal. As a result, its full editorial history (including decision letters, peer reviews and author responses) may not be present. PONE-D-22-11657Tracking the incidence and risk factors for SARS-CoV-2 infection using historical maternal booking serum samplesPLOS ONE Dear Author, 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 Sep 26 2022 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. 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Thank you for stating the following in the Acknowledgments Section of your manuscript: This research was partly funded by Community Jameel and the Imperial President’s Excellence Fund. EM was funded by an NIHR Academic Clinical Lecturer post until February 2021. RM and CAD acknowledge the NIHR HPRU in Emerging and Zoonotic Infections, a partnership between Public Health England (PHE), University of Oxford, University of Liverpool and Liverpool School of Tropical Medicine [grant number NIHR200907]. CAD also acknowledges the MRC Centre for Global Infectious Disease Analysis [grant number MR/R015600/1], which is jointly funded by the UK Medical Research Council (MRC) and the UK Foreign, Commonwealth & Development Office (FCDO), under the MRC/FCDO Concordat agreement and is also part of the EDCTP2 programme supported by the European Union (EU). EP, MM and RST acknowledge support from NIHR CV220-111: Serological detection of past SARS-CoV-2 infection by non-invasive sampling for field epidemiology and quantitative antibody detection and from departmental funds. Disclaimer: “The views expressed are those of the authors and not necessarily those of the United Kingdom (UK) Department of Health and Social Care, EU, FCDO, MRC, National Health Service, NIHR, or PHE. The funding bodies had no role in the design of the study, analysis and interpretation of data and in writing the manuscript.” However, funding information should not appear in the Acknowledgments section or other areas of your manuscript. We will only publish funding information present in the Funding Statement section of the online submission form. Please remove any funding-related text from the manuscript and let us know how you would like to update your Funding Statement. Currently, your Funding Statement reads as follows: This research was partly funded by Community Jameel and the Imperial President’s Excellence Fund. https://www.imperial.ac.uk/jameel-institute/ EM was funded by an NIHR Academic Clinical Lecturer post until February 2021. https://www.nihr.ac.uk/explore-nihr/academy-programmes/integrated-academic-training.htm RM and CAD acknowledge the NIHR HPRU in Emerging and Zoonotic Infections, a partnership between Public Health England (PHE), University of Oxford, University of Liverpool and Liverpool School of Tropical Medicine [grant number NIHR200907]. CAD also acknowledges the MRC Centre for Global Infectious Disease Analysis [grant number MR/R015600/1], which is jointly funded by the UK Medical Research Council (MRC) and the UK Foreign, Commonwealth & Development Office (FCDO), under the MRC/FCDO Concordat agreement and is also part of the EDCTP2 programme supported by the European Union (EU). EP, MM and RST acknowledge support from NIHR CV220-111: Serological detection of past SARS-CoV-2 infection by non-invasive sampling for field epidemiology and quantitative antibody detection and from departmental funds. Infrastructure support was provided by the NIHR Imperial College Biomedical Research Centre. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Please include your amended statements within your cover letter; we will change the online submission form on your behalf. 4. Thank you for stating the following in the Competing Interests section: EM is an academic editor at PLOS One. MM is listed as an inventor in IPR filings for the Imperial Hybrid DABA used in this analysis. Please see United Kingdom Patent Application No. 2011047.4 for “SARS-CoV-2 antibody detection assay”. SMB is member of both Royal Statistical Society’s COVID-19 Taskforce and Working Group on Diagnostic Tests. 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If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice. Additional Editor Comments: Title: Tracking the incidence and risk factors for SARS-CoV-2 infection using historical maternal booking serum samples Editor comment: 1. Please abide by the journal guideline 2. Check the grammar 3. Data availability is mandatory so please attach the data Reviewer 1 In this manuscript, Mullins and McCabe et al. have estimated the prevalence of seroreactivity of total antibodies to the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) receptor-binding domain (anti-RBD) in stored antenatal serum samples over time between COVID-19 pre-pandemic and pandemic periods. The authors reported a higher prevalence of seroreactivity to SARS-CoV-2 on Sept 2019 compared to mid-Feb 2020. Overall it is an interesting study representing a retrospective analysis of the prevalence of seroreactivity over time and its association with variables. My comments to the authors are: 1. In the method, in the logistic regression, have you controlled potential confounders (such as BMI, previous history of flu infections, flu vaccination status etc.) potentially affected the outcome variable in the analysis? 2. In the method ‘Defining seroreactivity’ section, please provide rationale and/or reference why the binding ratio (BR) ≥ 1 was considered as seroreactive for SARS-CoV-2 anti-RBD. 3. In the result, table 3, is it adjusted or unadjusted odds? 4. Some minor errors in the use of English throughout, i.e, missing/incorrect use of articles and prepositions - further proofreading required. Reviewer 2 First of all, I would like to thank all authors.... this manuscript titled “Tracking the incidence and risk factors for SARS-CoV-2 infection using historical maternal booking serum samples" is easy to follow and well written. However, I have only one comment: Could you please follow PLOS ONE guidelines, such as line number and reference style? Reviewer 3 comment 1. Would like to hear more about the choice of sample size prior to starting the study. Maybe mention the possible limitations of generalizability of maternal cohorts when pregnant women may be more susceptible to infection. [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: Yes Reviewer #3: Yes ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #2: Yes Reviewer #3: I Don't Know ****** 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: Yes 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: 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 this manuscript, Mullins and McCabe et al. have estimated the prevalence of seroreactivity of total antibodies to the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) receptor-binding domain (anti-RBD) in stored antenatal serum samples over time between COVID-19 pre-pandemic and pandemic periods. The authors reported a higher prevalence of seroreactivity to SARS-CoV-2 on Sept 2019 compared to mid-Feb 2020. Overall it is an interesting study representing a retrospective analysis of the prevalence of seroreactivity over time and its association with variables. My comments to the authors are: 1. In the method, in the logistic regression, have you controlled potential confounders (such as BMI, previous history of flu infections, flu vaccination status etc.) potentially affected the outcome variable in the analysis? 2. In the method ‘Defining seroreactivity’ section, please provide rationale and/or reference why the binding ratio (BR) ≥ 1 was considered as seroreactive for SARS-CoV-2 anti-RBD. 3. In the result, table 3, is it adjusted or unadjusted odds? 4. Some minor errors in the use of English throughout, i.e, missing/incorrect use of articles and prepositions - further proofreading required. Reviewer #2: First of all, I would like to thank all authors.... this manuscript titled “Tracking the incidence and risk factors for SARS-CoV-2 infection using historical maternal booking serum samples" is easy to follow and well written. However, I have only one comment: Could you please follow PLOS ONE guidelines, such as line number and reference style? Reviewer #3: Would like to hear more about the choice of sample size prior to starting the study. Maybe mention the possible limitations of generalizability of maternal cohorts when pregnant women may be more susceptible to infection. ****** 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: Yes: Md Jahangir Alam 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. 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. Attachments Attachment Submitted filename: tracking the incidence of COVID-19 reviers comment.docx https://doi.org/10.1371/journal.pone.0273966.r001
Revision 1
17 Aug 2022 Author Response Please see cover letter. Editor comments: 1. Please abide by the journal guideline Format adjusted in-line with journal guidance. 2. Check the grammar Thank you, I have re-read and I can’t see any further errors. I may be insensitive to my own mistakes. 3. Data availability is mandatory so please attach the data As per the manuscript, study data is available open access at https://github.com/ruthmccabe/historic_antenatal_serostudy Reviewer 1 In this manuscript, Mullins and McCabe et al. have estimated the prevalence of seroreactivity of total antibodies to the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) receptor-binding domain (anti-RBD) in stored antenatal serum samples over time between COVID-19 pre-pandemic and pandemic periods. The authors reported a higher prevalence of seroreactivity to SARS-CoV-2 on Sept 2019 compared to mid-Feb 2020. Overall it is an interesting study representing a retrospective analysis of the prevalence of seroreactivity over time and its association with variables. My comments to the authors are: 1. In the method, in the logistic regression, have you controlled potential confounders (such as BMI, previous history of flu infections, flu vaccination status etc.) potentially affected the outcome variable in the analysis? No, data used were unlinked and anonymous: we were only able to include data relating to deprivation, age, ethnicity and sample-period only. Please see Methods, line 100-106 for further detail on included data: ‘Prior to anonymization, samples were cross-classified by fortnight, age group (18-29 years, 30-34 years, 35-44 years), ethnicity (all white, all Asian, all Black, Other), and deprivation (most-deprived two IMD deciles 1-2, intermediate four deciles 3-6, least-deprived four deciles 7-10) ... We gave an undertaking not to report on any cross-classification for which the observed count was under 25. This undertaking was met by pooling across adjacent fortnights. ‘ 2. In the method ‘Defining seroreactivity’ section, please provide rationale and/or reference why the binding ratio (BR) ≥ 1 was considered as seroreactive for SARS-CoV-2 anti-RBD. Thank you, we describe our approach in using the standard formula to determine an ELISA cut-off in the, ‘Defining Seroreactivity section,’ lines 144-150: ‘Defining seroreactivity As set out in Rosadas et al.17, the cutoff for seroreactivity was established by adding 0.1 to the average of optical density (OD) obtained for three negative controls assayed in each run. The signal-to-cutoff value, known as the binding ratio (BR), for each sample was determined by dividing the sample OD by the cutoff OD. A sample was generally considered seroreactive for SARS-CoV-2 anti-RBD when the BR was greater than or equal to 1. BRs between 0.8 and 1.2 were considered to display a weak signal (borderline non-seroreactive; borderline seroreactive).’ 3. In the result, table 3, is it adjusted or unadjusted odds? The odds in table 3 are adjusted as based derived from regression analysis which legend states. Table 3 column title amended to read: ‘Adjusted Odds Ratio.’ 4. Some minor errors in the use of English throughout, i.e, missing/incorrect use of articles and prepositions - further proofreading required. Thank you, I have re-read and I can’t see any further errors. I may be insensitive to my own mistakes. Reviewer 2 First of all, I would like to thank all authors.... this manuscript titled “Tracking the incidence and risk factors for SARS-CoV-2 infection using historical maternal booking serum samples" is easy to follow and well written. However, I have only one comment: Could you please follow PLOS ONE guidelines, such as line number and reference style? Thank you, formatting adjusted in line with PLOS ONE guidance. Reviewer 3 comment 1. Would like to hear more about the choice of sample size prior to starting the study. Maybe mention the possible limitations of generalizability of maternal cohorts when pregnant women may be more susceptible to infection. Thank you. With regard to sample size, as noted in text, prior estimates based on population data on ethnicity did not fully reflect the ethnicity distribution for pregnant women but the chosen age-bands worked well. After high prevalence was attained, sample size was reduced to enable testing of samples further back in 2019. As described in lines 91-94 we had planned to analyse all available stored maternal serum samples from 4 NW London maternity centres from the period December 2019-May 2020. When seroreactive samples were found in the earliest time period and sufficiently narrow confidence were obtained with testing of 500 samples per fortnight, we adjusted our strategy as described in lines 107-116 to cover a wider time period in order to firstly test earlier samples to examine the onset of community transmission and secondly to test later samples to overlap with national serosurveillance studies for comparative purposes. This study was as pilot study to establish the testing period for a subsequent national study. With regards to generalisability and susceptibility, this is a good point and we have included the following in the discussion, lines 369-374: ‘Pregnant women’s increased susceptibility for some respiratory viruses make them a crucial group for surveillance, however the evidence for increased susceptibility to SARS-CoV-2 in pregnancy is mixed 31. Advice for pregnant women to shield may affect the generalisability of our data to other populations, however these samples were taken at around 10-12 weeks gestation when the majority of women would have only recently have become aware of pregnancy.’ https://doi.org/10.1371/journal.pone.0273966.r002
19 Aug 2022 Decision Letter - Atalay Goshu Muluneh, Editor Tracking the incidence and risk factors for SARS-CoV-2 infection using historical maternal booking serum samples PONE-D-22-11657R1 Dear Dr. Edward W. S. Mullins 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, Atalay Goshu Muluneh, MPH Academic Editor PLOS ONE Additional Editor Comments (optional): Reviewers' comments: https://doi.org/10.1371/journal.pone.0273966.r003
Formally Accepted
24 Aug 2022 Acceptance Letter - Atalay Goshu Muluneh, Editor PONE-D-22-11657R1 Tracking the incidence and risk factors for SARS-CoV-2 infection using historical maternal booking serum samples Dear Dr. Mullins: 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 Mr. Atalay Goshu Muluneh Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0273966.r004

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