Post-acute sequelae of COVID-19 among hospitalized patients in Estonia: Nationwide matched cohort study

Anna Tisler; Oliver Stirrup; Heti Pisarev; Ruth Kalda; Tatjana Meister; Kadri Suija; Raivo Kolde; Marko Piirsoo; Anneli Uusküla

doi:10.1371/journal.pone.0278057

Peer Review History

Original SubmissionJuly 14, 2022
1 Aug 2022 Decision Letter - Aqeel M Alenazi, 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-22-19899Post-acute sequelae of COVID-19 among hospitalized patients in Estonia: nationwide matched cohort studyPLOS ONE Dear Dr. tisler, 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. ============================== In addition to the reviewers' comments and suggestions, more clarifications should be written regarding the methods and diagnostic codes (ICD-10) using 1 or 2 codes to confirm the diagnosis of diseases. ============================== Please submit your revised manuscript by Sep 15 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. 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. Please include the following items when submitting your revised manuscript: A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). 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Should your manuscript be accepted for publication, we will hold it until you provide the relevant accession numbers or DOIs necessary to access your data. If you wish to make changes to your Data Availability statement, please describe these changes in your cover letter and we will update your Data Availability statement to reflect the information you provide. 4. Please include captions for your Supporting Information files at the end of your manuscript, and update any in-text citations to match accordingly. Please see our Supporting Information guidelines for more information: http://journals.plos.org/plosone/s/supporting-information. Additional Editor Comments: Reviewers indicated limitations in the selection of the cohorts and unbalanced diseases with some suggestions to improve such as propensity score matching. In addition, more clarifications should be written regarding the methods and diagnostic codes (ICD-10). For example, have you used one or 2 codes to confirm the diagnosis of diseases? This will improve the validity and accuracy of the results. [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: Partly ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: I Don't Know Reviewer #2: Yes ****** 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 ****** 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 ****** 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: The paper submitted by Anna Tisler et al analyzes clinical outcomes of patients hospitalized and surviving after COVID-19 disease in a nationwide study (Estonia) during the pre-vaccine era. They used a matched control population by age, sex, and Charlson’s comorbidity index (CCI). This kind of studies are relevant for health systems to design policies of surveillance after patients are discharged. The main objectives and the methods employed are clearly described in the manuscript. However, I have some concerns to address to the authors: 1. Despite cases and controls were matched by age, sex and CCI, the prevalence of relevant comorbidities was higher in the cohort of patients with COVID-19 (e.g., arterial hypertension, neoplasms, type 2 diabetes, ischemic and non-ischemic heart disease, etc). I wonder whether it is possible to do another approach taking into consideration for matching conditions with a high prevalence (for example, > 5%) in both cohorts. 2. In table 2 it is presented the incidence of outcomes among COVID-19 and control patients. Two different measures are presented: person-time and rate (both by 10.000 person-years). Despite I cannot repeat your calculations, rate was higher in COVID-19 patients than in controls (for example, in the case of death from all cause the figures were 1332 and 467, respectively). Conversely, when the same results are presented as person time the figure is higher in controls (1.19 vs. 0.29 for all cause mortality). Can you explain me this discrepancy? Reviewer #2: Authors wanted to examine post-acute sequelae of Covid-19 disease with a matched cohort study in Estonia. Data came from nationwide healthcare registry. Two patient groups were matched according to age, gender, and CCI score; Covid-19 and others. Although, these three features (age, gender and CCI score) were used for matching, it is obvious that Covid-19 patients had higher rate of pre-existing comorbidities than those of counter parts. So, it is expected that Covid-19 patients could have higher rates of hazard ratios or mortality, and results could be overestimated. Propensity score matching could be more appropriate to reduce these differences in the analysis. If it is not possible to do this test, this limitation should be added to the paper. Other concern is that how does this paper give contribution to the literature, as nearly all the population was vaccinated in Europe. Also, we still don’t know whether vaccination changed long term disease effects. Or, how long time should these patients will be watched for sequelae? These are topics that should be discussed in the paper. Other recommendations; Line 135: “all-cause” rather than “all cause”. Line 189: It is stated that “At baseline compared to general population cases were more likely to have a comorbid condition (most notably obesity …” Is there any information regarding obesity in the paper? Discussion; It was used that “age, gender and co-morbidities matched general population.” in a few sentences. Actually, it wasn’t a fully matched cohort. It can be used “CCI score” rather than “co-morbidities”. Abstract; The results may not provide “robust” estimates for post disease morbidity because the groups were not fully matched. This statement needs 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: Yes: Francesc Moreso Reviewer #2: Yes: Mehmet Ali Aslaner ******** [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. 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Revision 1
15 Sep 2022 Author Response RESPONSE TO REVIEWERS General comment: In addition to the reviewers' comments and suggestions, more clarifications should be written regarding the methods and diagnostic codes (ICD-10) using 1 or 2 codes to confirm the diagnosis of diseases. Response: Thank you for the comment. We have edited Methods section to clarify the use of ICD-10 codes. Reviewer #1: 1. Despite cases and controls were matched by age, sex and CCI, the prevalence of relevant comorbidities was higher in the cohort of patients with COVID-19 (e.g., arterial hypertension, neoplasms, type 2 diabetes, ischemic and non-ischemic heart disease, etc). I wonder whether it is possible to do another approach taking into consideration for matching conditions with a high prevalence (for example, > 5%) in both cohorts. Response: Thank you for pointing that out. In the addition to the matching for age, sex, Charlson Comorbidity Index the final Cox survival model was adjusted for comorbidities with prevalence of ≥5%, health care utilization and previous hospitalization that we believe removed confounding if imbalance existed after matching. 2. In table 2 it is presented the incidence of outcomes among COVID-19 and control patients. Two different measures are presented: person-time and rate (both by 10.000 person-years). Despite I cannot repeat your calculations, rate was higher in COVID-19 patients than in controls (for example, in the case of death from all cause the figures were 1332 and 467, respectively). Conversely, when the same results are presented as person time the figure is higher in controls (1.19 vs. 0.29 for all cause mortality). Can you explain me this discrepancy? Response: Cases were matched to a random subset of individuals insured by the EHIF who at the date of the first positive SARS-CoV-2 test of the COVID-19 case were alive and had no evidence of COVID-19 using a case to control ratio of 1:4 and that is the reason for person time being 4 times higher for controls (controls 1.19 versus cases 0.29 x 10 000 person years). Reviewer #2: 1. Authors wanted to examine post-acute sequelae of Covid-19 disease with a matched cohort study in Estonia. Data came from nationwide healthcare registry. Two patient groups were matched according to age, gender, and CCI score; Covid-19 and others. Although, these three features (age, gender and CCI score) were used for matching, it is obvious that Covid-19 patients had higher rate of pre-existing comorbidities than those of counter parts. So, it is expected that Covid-19 patients could have higher rates of hazard ratios or mortality, and results could be overestimated. Propensity score matching could be more appropriate to reduce these differences in the analysis. If it is not possible to do this test, this limitation should be added to the paper. Thank you for your comment, we do agree that the propensity score matching would be also another appropriate way to balance exposed groups on the confounding factors, but we believe that matching for for age, sex, Charlson Comorbidity Index and adjusting final Cox survival model for comorbidities with prevalence of ≥5%, health care utilization and previous hospitalization has removed confounding as imbalance existed after matching. 2. Other concern is that how does this paper give contribution to the literature, as nearly all the population was vaccinated in Europe. Also, we still don’t know whether vaccination changed long term disease effects. Or, how long time should these patients will be watched for sequelae? These are topics that should be discussed in the paper. Our findings are consistent with emerging evidence from early studies suggesting that a subset of people infected with SARS-CoV-2 can experience health problems several months after the acute phase of their infection; however, epidemiological characterisation of such sequelae has been limited. Only a few other studies to date have compared post-COVID risks with a control group in using nationwide data. The present study helps to contextualise these observations by adding explicit comparison with risks experienced by the general population. In addition we believe that our results can be generalised to those countries with similar population structure with lower vaccination coverage. We also believe that our results are relevant in terms of future and present pandemics as we note in the manuscript that the post-infectious sequelae have been documented following infection by other viral infections (Ebola, influenza, dengue) and only 63.2% of European population is fully vaccinated 1. 1 https://ourworldindata.org/covid-vaccinations?country=OWID_WRL Ongoing monitoring will be important to investigate whether these patterns persist in the light of new variants and increasing levels of vaccination. 3. Line 135: “all-cause” rather than “all cause” Response: corrected 4. Line 189: It is stated that “At baseline compared to general population cases were more likely to have a comorbid condition (most notably obesity …” Is there any information regarding obesity in the paper? Response: Thank you for pointing that out. We have now included it in the Tabel 1, we double- checked and it was already included in the final model. 5. It was used that “age, gender and co-morbidities matched general population.” in a few sentences. Actually, it wasn’t a fully matched cohort. It can be used “CCI score” rather than “co-morbidities” Response: corrected 6. The results may not provide “robust” estimates for post disease morbidity because the groups were not fully matched. This statement needs revision. Response: The reviewed statement is now included. Attachments Attachment Submitted filename: Response to Reviewers.rtf https://doi.org/10.1371/journal.pone.0278057.r002
18 Oct 2022 Decision Letter - Aqeel M Alenazi, Editor PONE-D-22-19899R1Post-acute sequelae of COVID-19 among hospitalized patients in Estonia: nationwide matched cohort studyPLOS ONE Dear Dr. tisler, 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, revise your manuscript or provide explanation to the reviewer's comments Please submit your revised manuscript by Dec 02 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. 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. Please include the following items when submitting your revised manuscript: A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'. A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'. An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'. If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter. If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: https://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols. We look forward to receiving your revised manuscript. Kind regards, Aqeel M Alenazi Academic Editor PLOS ONE Journal Requirements: Please review your reference list to ensure that it is complete and correct. 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. 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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 Response) ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: I Don't Know Reviewer #2: (No Response) ****** 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 #2: (No Response) ****** 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 #2: (No Response) ****** 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: The limitation that both reviewers have raised about the matching procedure of both cohorts is not fully addressed. Is it possible to match both populations by the baseline comorbidities (for example by a propensity socre)? Reviewer #2: (No Response) ****** 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: Yes: Francesc Moreso Reviewer #2: Yes: Mehmet Ali Aslaner ******** [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. https://doi.org/10.1371/journal.pone.0278057.r003
Revision 2
25 Oct 2022 Author Response RESPONSE TO REVIEWERS Reviewer #1: The limitation that both reviewers have raised about the matching procedure of both cohorts is not fully addressed. Is it possible to match both populations by the baseline comorbidities (for example by a propensity score)? Response: We are sorry that the matching procedure was not presented clearly. In the analysis presented both populations are matched by the baseline comorbidities burden (Charlson Comorbidity Index). In our analysis, we matched our cohorts for age, sex, and Charlson Comorbidity Index and adjusted the final Cox survival model for a rich set of covariates to remove confounding as imbalance existed after matching. Adjustment for preexisting comorbidities with a prevalence of ≥5%, health care utilization, and previous hospitalization was made. We believe that this was sufficient to balance the cohorts out. We do agree with the reviewer, that the propensity score matching would be also another appropriate way to balance exposed groups on the confounding factors. We have addressed this comment by adding an explanation in the Discussion section on page 20 line 359. Attachments Attachment Submitted filename: Response to Reviewers2.docx https://doi.org/10.1371/journal.pone.0278057.r004
9 Nov 2022 Decision Letter - Aqeel M Alenazi, Editor Post-acute sequelae of COVID-19 among hospitalized patients in Estonia: nationwide matched cohort study PONE-D-22-19899R2 Dear Dr. tisler, 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. 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If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation. Reviewer #1: All comments have been addressed Reviewer #2: All comments have been addressed ******** 2. 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 Response) ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: I Don't Know Reviewer #2: (No Response) ****** 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: No Reviewer #2: (No Response) ****** 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 #2: (No Response) ****** 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: The authors have answer my concerns appropriately. I suggest to the Editor to ask for an statistician to evaluate whether the analysis done in the present paper are correct. Reviewer #2: (No Response) ****** 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: Yes: Francesc Moreso Reviewer #2: Yes: Mehmet Ali Aslaner ******** https://doi.org/10.1371/journal.pone.0278057.r005
Formally Accepted
14 Nov 2022 Acceptance Letter - Aqeel M Alenazi, Editor PONE-D-22-19899R2 Post-acute sequelae of COVID-19 among hospitalized patients in Estonia: nationwide matched cohort study Dear Dr. Tisler: 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. Aqeel M Alenazi Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0278057.r006

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