Performance of COVID-19 associated symptoms and temperature checking as a screening tool for SARS-CoV-2 infection

Benjamin Demah Nuertey; Kwame Ekremet; Abdul-Rashid Haidallah; Kareem Mumuni; Joyce Addai; Rosemary Ivy E. Attibu; Michael C. Damah; Elvis Duorinaa; Anwar Sadat Seidu; Victor C. Adongo; Richard Kujo Adatsi; Hisyovi Caedenas Suri; Abass Abdul-Karim Komei; Braimah Baba Abubakari; Enoch Weyori; Emmanuel Allegye-Cudjoe; Augustina Sylverken; Michael Owusu; Richard O. Phillips

doi:10.1371/journal.pone.0257450

Peer Review History

Original SubmissionMay 1, 2021
23 Jun 2021 Decision Letter - Martin Chtolongo Simuunza, Editor PONE-D-21-14457 Performance of COVID-19 associated symptoms and temperature checking as a screening tool for SARS-CoV-2 infection PLOS ONE Dear Dr. Nuertey, 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. The reviewer recommends that you make minor revisions to your work. Please ensure that previously published work in the same field are well acknowledged in the background of your manuscript and comparisons made. Please submit your revised manuscript by Aug 07 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. 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If patients provided informed written consent to have data from their medical records used in research, please include this information. [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 ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: 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 ****** 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 ****** 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 manuscript submitted by Dr. B. Demah Nuertey et al. aims to determine the usefulness of clinical symptoms in accurately predicting a final diagnosis of COVID-19. The manuscript is clear, well organized, and well written. Authors used a dataset of ~2,000 participants, from Tamale teaching hospital, Ghana. The study is generally sound, authors assess associations between symptoms and PCR positive test result using a multivariate logistic framework, considering the possible correlation between symptoms. Authors further performed a ROC analysis. Authors' conclusion is that "The use of fever alone or other symptoms individually as a screening tool for SARS-CoV-2 infection is not worthwhile based on ROC analysis." Major comments: - While the usefulness of temperature and other symptoms in COVID-19 screening is a key question, it is important acknowledge that other studies have been conducted, and replace the study in the context of the current literature (e.g. among others, a study in Australia https://onlinelibrary.wiley.com/doi/10.1111/1742-6723.13578 for temperature check, and a meta-analysis https://gut.bmj.com/content/70/4/806#ref-1 for loss of smell/taste). - A more in-depth exploration of the dataset could strengthen the manuscript. For example: is the temperature screening performing differently given the age of the patient? Would other symptoms be interesting to consider in the screening? Would a screening of a combination of symptoms perform better than individual ones? Also, it would be further interesting to place this study in a global context and see if there are any key differences in terms of disease presentation and/or prevalence of different symptoms. Minor comments: - In the abstract, the sentence: ‘The likelihood of a positive test result for SARS-CoV-2 was 5.9 [3.9 – 8.8] for loss of sense of smell and 5.9 [3.8 – 9.3] for loss of sense of taste.’ is unclear. A likelihood should be a probability, here it seems to be a relative risk of presenting with the symptoms when being positive, compared to when being negative. It would be better to use the formulation from page 10, which is well written. - In the methods, page 6, it would be useful to see the CT threshold used to declare the RT-PCR as positive. - In the methods, page 6, the term ‘Real-time RT-PCR’ is redundant. - The reporting of the ROC analysis from Table 4 is inaccurate: 4.8% sensitivity corresponds to a temperature cut-point of 37.7, and not 37.8. ****** 6. 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Revision 1
2 Jul 2021 Author Response 30th June, 2021 The editor PLOS one Dear Editor, Response to Reviewers: Performance of COVID-19 associated symptoms and temperature checking as a screening tool for SARS-CoV-2 infection Thank you for the opportunity and improving the quality of this manuscript. Below is how we addressed the comments of the reviewers. Journal/Editorial requirement • The data set has been made public and can be found here https://osf.io/fz82k/ • Also the map was changed using suggested resources Reviewer #1: comment - While the usefulness of temperature and other symptoms in COVID-19 screening is a key question, it is important acknowledge that other studies have been conducted, and replace the study in the context of the current literature (e.g. among others, a study in Australia https://onlinelibrary.wiley.com/doi/10.1111/1742-6723.13578 for temperature check, and a meta-analysis https://gut.bmj.com/content/70/4/806#ref-1 for loss of smell/taste). Response Thank you for the suggestions which significantly improved the manuscript. The abstract and introduction were updated with findings from current literature including the suggested literature to reflect the context comments - A more in-depth exploration of the dataset could strengthen the manuscript. For example: is the temperature screening performing differently given the age of the patient? Would other symptoms be interesting to consider in the screening? Would a screening of a combination of symptoms perform better than individual ones? Also, it would be further interesting to place this study in a global context and see if there are any key differences in terms of disease presentation and/or prevalence of different symptoms. Response Thank you very much, suggestions were carried out and a more in-depth exploration of the dataset was carried out. The performance of the temperature check at varying age groups were carried out and shown in supplement table 1. Also, a combination of symptoms such as the case definition used for screening in the Tamale teaching Hospital, Ghana attached as supplement table 2 was explored. A section on the combination of symptoms was added to the results and the performance of the combination of symptoms added as table 5. Minor comments: comment - In the abstract, the sentence: ‘The likelihood of a positive test result for SARS-CoV-2 was 5.9 [3.9 – 8.8] for loss of sense of smell and 5.9 [3.8 – 9.3] for loss of sense of taste.’ is unclear. A likelihood should be a probability, here it seems to be a relative risk of presenting with the symptoms when being positive, compared to when being negative. It would be better to use the formulation from page 10, which is well written. Response: Thank you very much, your suggestion was accepted and the formulation in page 10 was used as shown in the abstract, results section lines 56-57 Comment - In the methods, page 6, it would be useful to see the CT threshold used to declare the RT-PCR as positive. Response: The following was included in the method section of the manuscript to address your suggestion. “Samples with SARS-CoV-2 RT PCR cycle threshold (CT) value under 40 were considered positive” Comment - In the methods, page 6, the term ‘Real-time RT-PCR’ is redundant. Response: Thank you, “Real-time” was deleted Comment - The reporting of the ROC analysis from Table 4 is inaccurate: 4.8% sensitivity corresponds to a temperature cut-point of 37.7, and not 37.8. Response Thank you, the error was corrected; 4.8% was changed to 4.2%. the sentence now reads; “For example, using a temperature cut off of 37.8 would only pick 4.2% of positive SARS-CoV-2 infected patients” Once again thank you for the suggestions which greatly improved the manuscript Yours faithfully, Dr. Benjamin Nuertey Attachments Attachment Submitted filename: response to reviewer comment.docx https://doi.org/10.1371/journal.pone.0257450.r002
26 Jul 2021 Decision Letter - Martin Chtolongo Simuunza, Editor PONE-D-21-14457R1 Performance of COVID-19 associated symptoms and temperature checking as a screening tool for SARS-CoV-2 infection PLOS ONE Dear Dr. Nuertey, 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. The reviewer recommends that you include some discussion for the analysis that you added in the manuscript. Please attend to the concerns that have been raised and then return the revised manuscript as advised in this letter. Please submit your revised manuscript by Sep 09 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. 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: http://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, Martin Chtolongo Simuunza, PhD 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. 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. [Note: HTML markup is below. Please do not edit.] Reviewers' comments: Reviewer's Responses to Questions Comments to the Author 1. 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: (No Response) ******** 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 ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes ****** 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 ****** 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 ****** 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 paper has been greatly improved with more information on the context of the study and additional analyses, I thank the authors for their response. However, some minor issues remain, mainly on the discussion. I will mention some further below for the authors to consider. Comments: - The analysis of the performance on the temperature screening by age is a nice add-on, but it is not discussed at all. Also, the ‘desirable’ performance is not defined in the main text, and in Supplementary Table 1 the number of patients considered in each age group is not given. - The analysis of the performance of the combination of symptoms is very interesting. However, I would consider rephrasing the paragraph ‘Combination of symptoms’, as it is not clearly written. Some key figures would improve the reading. Further, these results are not discussed either. Discussing these results, side by side with the temperature check would improve the paper and strengthen the authors’ result that “The use of fever alone or other symptoms individually [or in combination] as a screening tool for SARS-CoV-2 infection is not worthwhile based on ROC analysis”. Also, it could be noted that the case definition of the Tamale hospital (criteria 1 or 2) led to quite a lot of missed cases. ****** 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: 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. https://doi.org/10.1371/journal.pone.0257450.r003
Revision 2
10 Aug 2021 Author Response RE: PONE-D-21-14457R1: Performance of COVID-19 associated symptoms and temperature checking as a screening tool for SARS-CoV-2 infection. Thank you for the opportunity to provide a revision to this work. Response to reviewer We are grateful to the editor and the reviewer for your determination to improve this manuscript. This kind gesture is well appreciated. We are privileged to have you review this manuscript. Below is how we address your comment; Comments: The paper has been greatly improved with more information on the context of the study and additional analyses, I thank the authors for their response. However, some minor issues remain, mainly on the discussion. I will mention some further below for the authors to consider. - The analysis of the performance on the temperature screening by age is a nice add-on, but it is not discussed at all. Also, the ‘desirable’ performance is not defined in the main text, and in Supplementary Table 1 the number of patients considered in each age group is not given. Response Discussion on temperature screening by age has been included in the discussion now. We are grateful for pointing this out to us. Desirable performance defined: the following was added to the method, statistical analysis, page 8, lines 200-202 “ The performance of a screening test is deemed to be desirable if Area Under Curve (AUC) is 0.7 � AUC � 0.8, excellent if 0.8 < AUC � 0.9 and outstanding if AUC is > 90 [37].” In Supplementary table 1, the number of patients considered and corresponding percentage in each age group has been provided now. Comment - The analysis of the performance of the combination of symptoms is very interesting. However, I would consider rephrasing the paragraph ‘Combination of symptoms’, as it is not clearly written. Some key figures would improve the reading. Further, these results are not discussed either. Discussing these results, side by side with the temperature check would improve the paper and strengthen the authors’ result that “The use of fever alone or other symptoms individually [or in combination] as a screening tool for SARS-CoV-2 infection is not worthwhile based on ROC analysis”. Also, it could be noted that the case definition of the Tamale hospital (criteria 1 or 2) led to quite a lot of missed cases Response Paragraph on combination of symptoms was rephrased and re-written. Some key figures were included to improve the reading. Page 14 to 15, lines 268 - 293 shows this modification. Some key figures to improve reading: supplemental figures 1 and 2 had been moved to main manuscript and named Figures 3 and 4 respectively. Also, a new figure displaying the three ROC curves for clinical criteria 1, 2 and combination of 1 or 2 had been included as supplemental figure 1. Also, it was noted in the results section, page 15, lines 291 – 293 that, the case definition of the Tamale hospital (criteria 1 or 2) led to quite a lot of missed cases. “The combination of symptoms as exemplified by clinical criteria 1 or 2 missed 66.3% of all positive cases.” Discussion section has been updated to include reviewer suggestions. As part of the update on the discussions and to address reviewer comment, the following publications were cited and referenced appropriately. • Mandrekar JN. Receiver operating characteristic curve in diagnostic test assessment. Journal of Thoracic Oncology. 2010;5:1315–6. • Bielecki M, Crameri GAG, Schlagenhauf P, Buehrer TW, Deuel JW. Body temperature screening to identify SARS-CoV-2 infected young adult travellers is ineffective. Travel Med Infect Dis. 2020;37:101832. doi:10.1016/j.tmaid.2020.101832. • Wright WF, Mackowiak PA. Why Temperature Screening for Coronavirus Disease 2019 With Noncontact Infrared Thermometers Does Not Work. Open Forum Infectious Diseases. 2021;8. doi:10.1093/ofid/ofaa603. • Roland LT, Gurrola JG, Loftus PA, Cheung SW, Chang JL. Smell and taste symptom-based predictive model for COVID-19 diagnosis. International Forum of Allergy & Rhinology. 2020;10:832–8. doi:10.1002/alr.22602. Attachments Attachment Submitted filename: Response to reviewer.docx https://doi.org/10.1371/journal.pone.0257450.r004
2 Sep 2021 Decision Letter - Martin Chtolongo Simuunza, Editor Performance of COVID-19 associated symptoms and temperature checking as a screening tool for SARS-CoV-2 infection PONE-D-21-14457R2 Dear Dr. Nuertey, 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, Martin Chtolongo Simuunza, PhD Academic Editor PLOS ONE Additional Editor Comments (optional): Reviewers' comments: Reviewer's Responses to Questions Comments to the Author 1. 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 ******** 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 ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes ****** 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 ****** 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 ****** 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 suitably addressed my comments. I believe the changes made a substantial improvement to the paper, so I recommend publication. ****** 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: No https://doi.org/10.1371/journal.pone.0257450.r005
Formally Accepted
8 Sep 2021 Acceptance Letter - Martin Chtolongo Simuunza, Editor PONE-D-21-14457R2 Performance of COVID-19 associated symptoms and temperature checking as a screening tool for SARS-CoV-2 infection Dear Dr. Nuertey: 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. Martin Chtolongo Simuunza Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0257450.r006

Open letter on the publication of peer review reports

PLOS recognizes the benefits of transparency in the peer review process. Therefore, we enable the publication of all of the content of peer review and author responses alongside final, published articles. Reviewers remain anonymous, unless they choose to reveal their names.

We encourage other journals to join us in this initiative. We hope that our action inspires the community, including researchers, research funders, and research institutions, to recognize the benefits of published peer review reports for all parts of the research system.

Learn more at ASAPbio .